Comparative study of erythrocyte morphology and size in relation to ecophysiological adaptations in Rodentia species

Comparative study of erythrocyte morphology and size in relation to ecophysiological adaptations in Rodentia species

Kizhina A.G., Kalinina S.N., Uzenbaeva L.B., Panchenko D.V., Łapiński S., Ilyukha V.A., Pechorina E.F., Fokina V.O.

P. 161-171

The size of erythrocytes varies widely across mammals. Previously, deviations from allometric relationships and existence of factors regulating erythrocyte size other than body mass have been shown. The contribution of factors such as habitat and taxonomy are still under discussion. In the present study we examined the morphology of erythrocytes in rodent species and determined their diameter, and for Ondatra zibethicus and Sciurus vulgaris this was done for the first time. We discovered that erythrocyte diameter of the investigated rodent species ranged from 5.5 to 8.4 μm, varying by a factor of more than 1.5. We analyzed our own data obtained for 10 species as well as data from the literature for 22 species. We found that the size of erythrocytes depended on the phylogenetic position, environmental conditions and body mass.DOI: 10.15298/rusjtheriol.19.2.06

Литература
  • Aarts P.A., Bolhuis P.A., Sakariassen K.S., Heethaar R.M. & Sixma J.J. 1983. Red blood cell size is important for adherence of blood platelets to artery subendothelium // Blood. Vol.62. P.214–217.
  • Ahlers A.A., Mitchell M.A., Schooley R.L., Heske E.J. & Levengood J.M. 2011. Hematologic and blood chemistry reference values for free-ranging muskrats (Ondatra zibethicus) // Journal of Wildlife Diseases. Vol.47. P.685–689.
  • Baraquet M., Grenat P.R., Salas N.E. & Martino A.L. 2013. Intraspecific variationin erythrocyte size among populations of Hypsiboas cordobae (Anura: Hylidae) // Acta Herpetologica. Vol.8. P.93–97.
  • Benga G., Porutiu D., Ghiran I., Kuchel P.W., Gallagher C.H. & Cox G.C. 1992. Scanning electron microscopy of red blood cells from eleven species of marsupial // Comparative Haematology International. Vol.2. P.227–230.
  • Bolls N.J. & Perfect J.R. 1972. Summer resting metabolic rate of the gray squirrel // hysiological Zoology. Vol.45. No.1. P.54–59.
  • Bottaeva Z.K. 2017. [Comparative characteristic of eritron of two species of vole under the conditions of the subalpical zone of the Tersky variant of zonality in the central Caucasus] // Izvestiya Samarskogo Nauchnogo Tsentra Rossiiskoi Akademii Nauk. Vol.19. No.5. P.30–35 [in Russian].
  • Bottaeva Z.K., Tembotova F.A., Emkuzheva M.M., Bersekova Z.A. & Chapaev A.K. 2019. [Effect of ecogeographic factors along latitudinal–longitudinal gradient on the red blood system of the Caucasian snow vole (Chionomys gud), a species autochthonous to the Caucasus] // Ekologiya. Vol.50. P.34–42 [in Russian].
  • Bozinovic F. & Rosenmann M. 1988. Comparative energetics of South American cricetid rodents // Comparative Biochemistry and Physiology. Vol.91A. P.195–202.
  • Bullard R.W., Broumand C. & Meyer F.R. 1966. Blood characteristics and volume in two rodents native to high altitude // Journal of Applied Physiology. Vol.21. P.994–998.
  • Campbell T. 2015. Exotic animal hematology and cytology
  • Hoboken, New Jersey: John Wiley & Sons. 402 p. Canfield P.J. 1998. Comparative cell morphology in the peripheral blood film from exotic and native animals // Australian Veterinary Journal. Vol.76. P.793–800.
  • Chiacchio R.G., Prioste F.E., Vanstreels R.E., Knobl T., Kolber M., Miyashiro S.I. & Matushima E.R. 2014. Health Evaluation and Survey of Zoonotic Pathogens in Free-ranging Capybaras (Hydrochaeris hydrochaeris) // Journal of Wildlife Diseases. Vol.50. P.496–504.
  • Corazza G.R., Ginaldi L., Zoli G., Frisoni M., Lalli G., Gasbarrini G. & Quaglino D. 1990. Howell-Jolly body counting as a measure of splenic function. A reassessment // Clinical Laboratory Hematology. Vol.12. P.269–275.
  • Crait J.R., Prange H.D., Marshall N.A., Harlow H.J., Cotton C.J. & Ben-David M. 2012. High-altitude diving in river otters: coping with combined hypoxic stresses // Journal of Experimental Biology. Vol.215. No.2. P.256–263.
  • Donnelly T.M., Bergin I. & Melanie I. 2015. Biology and diseases of other rodents // Fox J.G. (ed.). Laboratory Animal Medicine. Amsterdam etc: Academic Press. P.285–349.
  • Drożdż A., Górecki A., Grodziński W. & Pelikán J. 1971. Bioenergetics of water voles (Arvicola terrestris L.) from southern Moravia // Annales Zoologici Fennici. Vol.8. P.97–103.
  • Ederstrom H.E., Akers T.K., Keefner K.R. & Thompson R.E. 1971. Comparison of tolerance to hypoxia and hyperoxia in chinchillas and guinea pigs // Space Life Sciences. Vol.3. No.2. P.171–173.
  • Foreman C.W. 1956. Notes and blood data on some small mammals of Durham Country, North Carolina // Journal of Mammalogy. Vol.37. P.427–428.
  • Frase B.A. 2002. Hematological parameters of high-elevation bushy-tailed woodrats // The Southwestern Naturalist. Vol.47. P.508–510.
  • Galantsev V.P. 1977. [Anatomical and physiological adaptations of muskrat and European water vole to semi-aquatic life and diving] // Trudy Nauchno-issledovatel’skogo Sel’sko-khozyaistvennogo Instituta Krainego Severa. Vol.14. P.97–106 [in Russian].
  • Girling S.J., Campbell-Palmer R., Pizzi1 R., Fraser M.A., Cracknell J., Arnemo J. & Rosell F. 2015. Haematology and serum biochemistry parameters and variations in the Eurasian beaver (Castor fiber) // PLoS ONE. Vol.10. No.6. e0128775.
  • Goodman R.M. & Heah T.P. 2010. Temperature-induced plasticity at cellular and organismal levels in the lizard Anolis carolinensis // Integrative Zoology. Vol.5. P.208–217.
  • Gregory T.R. 2000. Nucleotypic effects without nuclei: Genome size and erythrocyte size in mammals // Genome. Vol.43. P.895–901.
  • Gregory T.R. 2005. Cell size database. http://www.genomesize. com/cellsize
  • Guthrie D.R., Mosby H.S. & Osborne J.C. 1966. Hematological values for the eastern gray squirrel (Sciurus carolinensis) // Canadian Journal of Zoology. Vol.44. No.2. P.323–327.
  • Gulliver G. 1875. On the size and shape of red corpuscles of the blood of vertebrates, with drawings of them to a uniform scale, and extended and revised tables of measurement // Proceedings of the Zoological Society of London. P.474–495.
  • Hall F.G. 1966. Minimal utilizable oxygen and the oxygen dissociation curve of blood of rodents // Journal of Applied Physiology.Vol.21. P.375–378.
  • Harr K.E., Isaza R., Blue J.T., Weiss D.J. & Wardrop K.J. 2010. Hematology of elephants // Weiss D.G. & Wardrop K.J. (eds.) Schalm’s Veterinary Hematology. Ames: Wiley-Blackwell. P.942–949.
  • Harvey J.W., Harr K.E., Murphy D., Walsh M.T., Nolan E.C., Bonde R.K., Pate M.G., Deutsch C.J., Edwards H.H. & Clapp W.L. 2009. Hematology of healthy Florida manatees (Trichechus manatus) // Veterinary Clinical Pathology. Vol.38. P.183–193.
  • Hawkey C.M. 1975. Comparative Mammalian Haematology. London: Medical Books Ltd. 310 p.
  • Hawkey C.M. & Dennet T.B. 1989. Comparative Veterinary Haematology. Ipswich: W.S. Cowell Ltd. 192 p.
  • Heatley J.J. & Harris M.C. 2009. Hamsters and Gerbils // Mitchell M. & Tully T.N. (eds.). Manual of Exotic Pet Practice. Elsevier. P.406–432.
  • Jelínek P. 1984. Basic hematological indices in adult nutria (Myocastor coypus M.) males // Acta Veterinaria Brno. Vol.53. P.41–47.
  • Kalabukhova T.N. 2005. [The evaluation of the size of erythrocytes of the hibernating ground squirrel Citellus undulatus Pallas] // Biofizika. Vol.50. No2. P.346–347 [in Russian]. Katahira K. & Ohwada K. 1993. Hematological standard values in the cotton rat (Sigmodon hispidus) // Experimental Animals. Vol.42. No.4. P.653–656.
  • Kostelecka-Myrcha A. 1966. Hemoglobin, erythrocytes and hematocrit in the blood of some microtidae under laboratory conditions // Bulletin de l’Academie Polonaise des Sciences. Serie des Sciences Biologiques.Vol.14. P.343–349.
  • Kostelecka-Myrcha A. 1967. Variation of morpho-physiological indices of blood in Clethrionomys glareolus (Schreber, 1780) // Acta Theriologica. Vol.12. P.191–222.
  • Kostelecka-Myrcha A. 1973. Regularities of variations of the hematological values characterizing the respiratory function of blood in mammals // Acta Theriologica. Vol.18. P.1–6.
  • Kostelecka-Myrcha A. 2002. The ratio of amount of haemoglobin to total surface area of erythrocytes in mammals // Acta Theriologica. Vol.47. P.209–220.
  • Lantová P., Zub K., Koskela E., Šíchová K. & Borowski Z. 2011. Is there a linkage between metabolism and personality in small mammals? The root vole (Microtus oeconomus) example // Physiology & Behavior. Vol.104. No.3. P.378–383.
  • Lechner A.J. 1976. Respiratory adaptations in burrowing pocket gophers from sea level and high altitude // Journal of Applied Physiology. Vol.41. P.168–173.
  • Lewis J.H. 1992. Comparative hematology: studies on guinea pigs (Cavia porcellus) // Comparative Biochemistry and physiology. Part A: Comparative Physiology. Vol.102. No.3. P.507–512.
  • Long C.A. 2007. Evolution of function and form in camelid erythrocytes // Proceedings of the 2007 WSEAS Int. Conference on Cellular & Molecular Biology – Biophysics & Bioengineering. Athens, Greece, August 26–28, 2007. P.18–24. MacArthur R.A. 1984. Seasonal changes in hematological and respiratory properties of muskrat (Ondatra zibethicus) blood // Canadian Journal of Zoology. Vol.62. No.4. P.537–545.
  • McNab B.K. 2008. An analysis of the factors that influence the level and scaling of mammalian BMR // Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. Vol.151. P.5–28.
  • Moore J.W. 1966. Hemogram of the Chinese hamster // American Journal of Veterinary Research. Vol.27. P.608–610.
  • Musacchia X.J., Wilber C.G. & Gorski T.W. 1955. Hematological studies on mammals from Alaska // Journal of Mammalogy. Vol.36. No.3. P.362–368.
  • Ostojic H., Cifuentes V. & Monge C. 2002. Hemoglobin affinity in Andean rodents // Biological Research. Vol.35. No.1. P.27–30.
  • Panteleyev P.A. 2001. [Water Vole: Mode of the Species]. Moscow: Nauka. 527 p. [In Russian].
  • Patenaude R.P. & Genest F.B. 1977. The hematology and chromosomes of the Canadian beaver (Castor canadensis) // Journal of Zoo Animal Medicine. Vol.8. P.6–9.
  • Promislow D.E.L. 1991. The evolution of mammalian blood parameters: Patterns and their interpretation // Physiological Zoology. Vol.64. P.393–431.
  • Puchalski W. & Heldmaier G. 1986. Seasonal changes of heart weight and erythrocytes in the Djungarian hamster (Phodopus sungorus) // Comparative Biochemistry and Physiology. Part A: Comparative Physiology. Vol.84. No.2. P.259–263.
  • Ramírez-Muñoz M.P., Zúñiga G., Torres-Bugarín O., Portilla E., García-Martínez D., Ramos A., Cantú J.M. & Sánchez-Corona J. 1999. Evaluation of the micronucleus test in peripheral blood erythrocytes by use of the splenectomized model // Comparative Medicine. Vol.49. P.418–420.
  • Reiderson T.H. 2010. Hematology of marine mammals // Weiss D.G. & Wardrop K.J. (eds.). Schalm’s Veterinary Hematology. Ames: Wiley–Blackwell. P.950–957.
  • Ruiz G., Rosenmann M. & Cortes A. 2004. Thermal acclimation and seasonal variations of erythrocyte size in the Andean mouse Phyllotis xanthopygus rupestris // Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. Vol.139. P.405–409.
  • Sabanova R.K. 2010. [The dependency to variability haemotological factors from ambience inhabitance timber mouse on North Caucasus] // Izvestiya Vysshikh Uchebnykh Zavedenii. Severo-Kavkazskii Region. Estestvennye Nauki. Vol.156. No.2. P.104–106 [In Russian].
  • Schmidt-Nielsen K. & Knut S.N. 1984. Scaling: why is animal size so important? Cambridge: Cambridge University Press. 347 p.
  • Segal A.N. 1978. [Thermoregulation in coypu (Myocastor coypus) in summer] // Zoologicheskii Zhurnal. Vol.57. P.1878–1883 [in Russian].
  • Siegel A. & Walton R.M. 2020. Hematology and biochemistry of small mammals // Carpenter J.W. (ed.). Ferrets, Rabbits, and Rodents. Elsevier Science. P.569–582.
  • Sokolov V.E., Lavrov N.P., Agadzhanyan A.K., Shiryaev V.V., Malygin V.M. & Yacenko V.N. 1993. [Muskrat. Morphology, Systematics, Ecology]. Moscow: Nauka. 542 p. [in Russian].
  • Starostová Z., Konarzewski M., Kozłowski J. & Kratochvíl L. 2013. Ontogeny of metabolic rate and red blood cell size in eyelid geckos: species follow different paths // PLoS ONE. Vol.8. No.5. e64715.
  • Tarakhtii E.A. & Davydova Yu.A. 2007. Seasonal variation in hematological indices in bank vole (Clethrionomys glareolus) in different reproductive states // Biology Bulletin. Vol.34. P.9–19.
  • Thomas A. & Ono K. 2015. Diving related changes in the blood oxygen stores of rehabilitating harbor seal pups (Phoca vitulina) // PloS ONE. Vol.10. No.6. e0128930.
  • Turgeon M.L. 2004. Clinical Hematology: Theory and Procedure. Philadelphia: Lippincott Williams & Wilkinson. 570 p.
  • Unruh K.D. 2018. Evaluating how behavioral, environmental and physiological factors have influenced the evolution of mammalian erythrocyte size. PhD Dissertation. Long Beach: California State University. 81 p.
  • Urison N.T. & Buffenstein R. 1994. Kidney concentrating ability of a subterranean xeric rodent, the naked mole–rat (Heterocephalus glaber) // Journal of Comparative Physiology B. Vol.63. No.8. P.676–681.
  • Wauters L.A., Vermeulen M., Van Dongen S., Bertolino S., Molinari A., Tosi G. & Matthysen E. 2007. Effects of spatio-temporal variation in food supply on red squirrel Sciurus vulgaris body size and body mass and its consequences for some fitness components // Ecography. Vol.30. P.51–65.
  • Wei D.B. & Wei L. 2001. The mensuration results of the number of red cell and the content of hemoglobin and myoglobin in plateau zokor // Journal of Qinghai University. Vol.19. P.1–2.
  • Withers P.C. 1978. Models of diffusion-mediated gas exchange in animal burrows // The American Naturalist. Vol.12. P.1101–1112.
  • Wołk E. 1970. Erythrocytes, haemoglobin and haematocrit in the postnatal development of the root vole // Acta Theriologica. Vol.15. No.19. P.283–293.
  • Wołk E. 1985. Hematology of a hibernating rodent — the northern birch mouse // Acta Theriologica. Vol.30. No.22. P.337–348.
  • Wołk E. 1990. Physiological and ecological aspects of mammalian haematology in natural conditions // Centrum Doskonalenia Nauczycieli, Toruñ: P.1–150.
  • Wyckoff S.M. & Frase B.A. 1990. Hematological adaptation to hypoxia in Peromyscus and Microtus at high and low altitude // Transactions of Illinois State Academy of Sciences. Vol.83. P.197–205.