Abstract
Acclimation to lower temperatures decreases energy expenditure in ectotherms but increases oxygen consumption in most endotherms, when dropped below thermoneutrality. Such differences should be met by adjustments in oxygen transport through blood. Changes in hematological variables in correspondence to that in metabolic rates are, however, not fully understood, particularly in non-avian reptiles. We investigated the effect of thermal acclimation on a snake model, the grass snakes (Natrix natrix). After 6 months of acclimation to either 18 °C or 32 °C hematocrit, hemoglobin concentration, erythrocyte number, and size were assessed. All variables revealed significantly lower values under warm compared to cold ambient temperature. Our data suggest that non-avian reptiles, similarly as birds, reduce erythrocyte fraction under energy-demanding temperatures. Due to low deformability of nucleated erythrocytes in sauropsids, such reduced fraction may be important in decreasing blood viscosity to optimize blood flow. Novel findings on flexible erythrocyte size provide an important contribution to this optimization process.
References
Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press
Birchard GF (1997) Optimal hematocrit: theory, regulation and implications. Am Zool 37(1):65–72
Bury S, Cichoń M, Bauchinger U, Sadowska ET (2018) High oxidative stress despite low energy metabolism and vice versa: insights through temperature acclimation in an ectotherm. J Therm Biol 78:36–41. https://doi.org/10.1016/j.jtherbio.2018.08.003
Czarnoleski M, Labecka AM, Starostová Z, Sikorska A, Bonda-Ostaszewska E, Woch K, Kubicka L, Kratochvil L, Kozlowski J (2017) Not all cells are equal: effects of temperature and sex on the size of different cell types in the Madagascar ground gecko Paroedura picta. Biol open:bio-025817. https://doi.org/10.1242/bio.025817
Davis KB, Parker NC (1990) Physiological stress in striped bass: effect of acclimation temperature. Aquaculture 91:349–358. https://doi.org/10.1016/0044-8486(90)90199-w
Deveci D, Stone PCW, Egginton S (2001) Differential effect of cold acclimation on blood composition in rats and hamsters. J Comp Physiol B 171:135–143. https://doi.org/10.1007/s003600000156
Eckstein HP (1993). Untersuchungen zur Ökologie der Ringelnatter: (Natrix natrix Linnaeus 1758); Abschlußbericht Ringelnatter-Projekt-Wuppertal (1986–91). Verlag für Ökologie und Faunistik
Fowler NO, Holmes JC (1975) Blood viscosity and cardiac output in acute experimental anemia. J Appl Physiol 39:453–456. https://doi.org/10.1152/jappl.1975.39.3.453
Goodman RM, Heah TP (2010) Temperature-induced plasticity at cellular and organismal levels in the lizard Anolis carolinensis. Integr Zool 5(3):208–217. https://doi.org/10.1111/j.1749-4877.2010.00206.x
Graham MS, Fletcher GL (1983) Blood and plasma viscosity of winter flounder: influence of temperature, red cell concentration, and shear rate. Can J Zool 61(10):2344–2350. https://doi.org/10.1139/z83-310
Graham MS, Haedrich RL, Fletcher GL (1985) Hematology of three deep-sea fishes: a reflection of low metabolic rates. Comp Biochem Phys A 80:79–84. https://doi.org/10.1016/0300-9629(85)90682-6
Greenwald OE (1971) The effect of body temperature on oxygen consumption and heart rate in the Sonora gopher snake Pituophis catenifer affinis Hallowell. Copeia 98:98. https://doi.org/10.2307/1441603
Gregory TR (2002) A bird’s-eye view of the C-value enigma: genome size, cell size and metabolic rate in the class Aves. Evolution 56:121. https://doi.org/10.1554/0014-3820(2002)056[0121:absevo]2.0.co;2
Guyton AC, Richardson TQ (1961) Effect of hematocrit on venous return. Circ Res 9:157–164. https://doi.org/10.1161/01.res.9.1.157
Hawkey CM, Bennett PM, Gascoyne SC, Hart MG, Kirkwood JK (1991) Erythrocyte size, number and haemoglobin content in vertebrates. Brit J Haematol 77(3):392–397. https://doi.org/10.1111/j.1365-2141.1991.tb08590.x
Hermaniuk A, Rybacki M, Taylor JR (2016) Low temperature and polyploidy result in larger cell and body size in an ectothermic vertebrate. Physiol Biochem Zool 89(2):118–129. https://doi.org/10.1086/684974
Hicks JW, Wang T (1996) Functional role of cardiac shunts in reptiles. J Exp Zool Part A 275(2–3):204–216. https://doi.org/10.1002/(SICI)1097-010X(19960601/15)275:2/33.0.CO;2-J
Isaza R, Andrews GA, Coke RL, Hunter RP (2004) Assessment of multiple cardiocentesis in ball pythons (Python regius). J Am Assoc Lab Anim 43(6):35–38
Ji P, Murata-Hori M, Lodish HF (2011) Formation of mammalian erythrocytes: chromatin condensation and enucleation. Trends Cell Biol 21:409–415. https://doi.org/10.1016/j.tcb.2011.04.003
Kozlowski J, Konarzewski M, Gawelczyk AT (2003) Cell size as a link between noncoding DNA and metabolic rate scaling. PNAS 100:14080–14085. https://doi.org/10.1073/pnas.2334605100
MacMahon JA, Hamer A (1975) Effects of temperature and photoperiod on oxygenation and other blood parameters of the sidewinder (Crotalus cerastes): adaptive significance. Comp Biochem Phys A 51:59–69. https://doi.org/10.1016/0300-9629(75)90413-2
Martins ML, Xu DH, Shoemaker CA, Klesius PH (2011) Temperature effects on immune response and hematological parameters of channel catfish Ictalurus punctatus vaccinated with live theronts of Ichthyophthirius multifiliis. Fish & Shellfish Immun 31:774–780. https://doi.org/10.1016/j.fsi.2011.07.015
McNab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University Press
Mueller RL, Gregory TR, Gregory SM, Hsieh A, Boore JL (2008) Genome size, cell size, and the evolution of enucleated erythrocytes in attenuate salamanders. Zoology 111(3):218–230. https://doi.org/10.1016/j.zool.2007.07.010
Murrish DE, Vance VJ (1968) Physiological responses to temperature acclimation in the lizard Uta mearnsi. Comp Biochem Physiol 27(1):329–337. https://doi.org/10.1016/0010-406X(68)90775-5
Niedojadlo J, Bury A, Cichoń M, Sadowska ET, Bauchinger U (2018) Lower haematocrit, haemoglobin and red blood cell number in zebra finches acclimated to cold compared to thermoneutral temperature. J Avian Biol 49(3):jav-01596. https://doi.org/10.1111/jav.01596
Nikinmaa M (2012) Vertebrate red blood cells: adaptations of function to respiratory requirements (Vol. 28). Springer Science & Business Media
Nikinmaa M, Tuurala H, Soivio A (1980) Thermoacclimatory changes in blood oxygen binding properties and gill secondary lamellar structure of Salmo gairdneri. J Comp Physiol 140(3):255–260. https://doi.org/10.1007/BF00690411
Palenske NM, Saunders DK (2003) Blood viscosity and hematology of American bullfrogs (Rana catesbeiana) at low temperature. J Therm Biol 28(4):271–277. https://doi.org/10.1016/S0306-4565(03)00002-0
Pough FH (1980) Blood oxygen transport and delivery in reptiles. Am Zool 20:173–185. https://doi.org/10.1093/icb/20.1.173
Rezende EL, Hammond KA, Chappell MA (2009) Cold acclimation in Peromyscus: individual variation and sex effects in maximum and daily metabolism, organ mass and body composition. J Exp Biol 212:2795–2802. https://doi.org/10.1242/jeb.032789
Ruiz G, Rosenmann M, Veloso A (1989) Altitudinal distribution and blood values in the toad, Bufo spinulosus Wiegmann. Comp Biochem Physiol A 94(4):643–646. https://doi.org/10.1016/0300-9629(89)90609-9
Rutskina IM, Litvinov NA, Roshchevskaya IM, Roshchevskii MP (2009) Temperature adaptation of the heart in the grass snake (Natrix natrix L.), common European viper (Vipera berus L.), and steppe viper (Vipera renardi Christoph)(Reptilia: Squamata: Serpentes). Russ J Ecol 40(5):314–319. https://doi.org/10.1134/S1067413609050026
Snyder GK, Sears RD (2006) Red blood cell size and the Fåhraeus–Lindqvist effect. Can J Zool 84(3):419–424. https://doi.org/10.1139/z06-011
Snyder GK, Sheafor BA (1999) Red blood cells: centerpiece in the evolution of the vertebrate circulatory system. Am Zool 39(2):189–198. https://doi.org/10.1093/icb/39.2.189
Starostová Z, Kubička L, Konarzewski M, Kozłowski J, Kratochvíl L (2009) Cell size but not genome size affects scaling of metabolic rate in eyelid geckos. Am Nat 174:E100–E105. https://doi.org/10.1086/603610
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 8(5):e64715. https://doi.org/10.1371/journal.pone.0064715
Stier A, Bize P, Schull Q, Zoll J, Singh F, Geny B, Gros F, Royer C, Masseim S, Criscuolo F (2013) Avian erythrocytes have functional mitochondria, opening novel perspectives for birds as animal models in the study of ageing. Front Zool 10(1):33. https://doi.org/10.1186/1742-9994-10-33
Stinner JN (1987) Cardiovascular and metabolic responses to temperature in Coluber constrictor. Am J Physiol-Reg I 253:R222–R227. https://doi.org/10.1152/ajpregu.1987.253.2.r222
Wack RF, Hansen E, Small M, Poppenga R, Bunn D, Johnson CK (2012) Hematology and plasma biochemistry values for the giant garter snake (Thamnophis gigas) and valley garter snake (Thamnophis sirtalis fitchi) in the central valley of California. J Wildl Dis 48(2):307–313. https://doi.org/10.7589/0090-3558-48.2.307
Wang T, Warburton S, Abe A, Taylor T (2001) Vagal control of heart rate and cardiac shunts in reptiles: relation to metabolic state. Exp Physiol 86(6):777–784. https://doi.org/10.1113/eph8602296
Windberger U, Baskurt OK (2007) Comparative hemorheology. In: Baskurt et al. (Eds.) Handbook of hemorheology and hemodynamics, IOS press
Yamaguchi K, Jürgens KD, Bartels H, Piiper J (1987) Oxygen transfer properties and dimensions of red blood cells in high-altitude camelids, dromedary camel and goat. J Comp Physiol B 157(1):1–9. https://doi.org/10.1007/BF00702722
Acknowledgements
We thank four anonymous reviewers for their valuable comments on the manuscript.
Funding
This study was supported by grants from the National Science Centre, Poland, to SB (grant no. UMO-2016/21/N/NZ8/00959), UB (grant no. UMO-2013/11/B/N28/00907), and DS of Jagiellonian University (DS/WIBNOZ/INOS/757).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Snake collection and experimental procedures were performed according to the permits from II Local Ethical Committee (permit no. 132/2016 from 26.05.2015) and Regional Directory of Nature Conservation (permit no. OP-I.6401.21.2015.PKw from 2.07.2015) in Cracow.
Additional information
Communicated by: Lars Koerner
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(XLSX 11 kb)
Rights and permissions
About this article
Cite this article
Bury, S., Bury, A., Sadowska, E.T. et al. More than just the numbers—contrasting response of snake erythrocytes to thermal acclimation. Sci Nat 106, 24 (2019). https://doi.org/10.1007/s00114-019-1617-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-019-1617-x