Advertisement

The Science of Nature

, 106:24 | Cite as

More than just the numbers—contrasting response of snake erythrocytes to thermal acclimation

  • Stanisław BuryEmail author
  • Agata Bury
  • Edyta T. Sadowska
  • Mariusz Cichoń
  • Ulf Bauchinger
Short Communication
  • 73 Downloads

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.

Keywords

Temperature acclimation Reptile Ectotherm Cell size Nucleated erythrocytes 

Notes

Acknowledgements

We thank four anonymous reviewers for their valuable comments on the manuscript.

Funding information

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).

Compliance with ethical standards

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.

Supplementary material

114_2019_1617_MOESM1_ESM.xlsx (11 kb)
ESM 1 (XLSX 11 kb)

References

  1. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University PressGoogle Scholar
  2. Birchard GF (1997) Optimal hematocrit: theory, regulation and implications. Am Zool 37(1):65–72CrossRefGoogle Scholar
  3. 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 CrossRefPubMedGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefPubMedGoogle Scholar
  7. Eckstein HP (1993). Untersuchungen zur Ökologie der Ringelnatter: (Natrix natrix Linnaeus 1758); Abschlußbericht Ringelnatter-Projekt-Wuppertal (1986–91). Verlag für Ökologie und FaunistikGoogle Scholar
  8. 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 CrossRefPubMedGoogle Scholar
  9. 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 CrossRefPubMedGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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;2CrossRefGoogle Scholar
  14. 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 CrossRefPubMedGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 CrossRefPubMedGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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):35–38Google Scholar
  19. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 CrossRefPubMedGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. McNab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University PressGoogle Scholar
  24. 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 CrossRefPubMedGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. Nikinmaa M (2012) Vertebrate red blood cells: adaptations of function to respiratory requirements (Vol. 28). Springer Science & Business MediaGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 CrossRefGoogle Scholar
  30. Pough FH (1980) Blood oxygen transport and delivery in reptiles. Am Zool 20:173–185.  https://doi.org/10.1093/icb/20.1.173 CrossRefGoogle Scholar
  31. 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 CrossRefPubMedGoogle Scholar
  32. 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 CrossRefPubMedGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. 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 CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefPubMedGoogle Scholar
  37. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. 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 CrossRefPubMedGoogle Scholar
  41. 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 CrossRefPubMedGoogle Scholar
  42. Windberger U, Baskurt OK (2007) Comparative hemorheology. In: Baskurt et al. (Eds.) Handbook of hemorheology and hemodynamics, IOS pressGoogle Scholar
  43. 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 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Environmental SciencesJagiellonian UniversityCracowPoland

Personalised recommendations