Journal of Comparative Physiology B

, Volume 188, Issue 4, pp 695–705 | Cite as

No effect of season on the electrocardiogram of long-eared bats (Nyctophilus gouldi) during torpor

  • Shannon E. Currie
Original Paper


Heterothermic animals regularly undergo profound alterations of cardiac function associated with torpor. These animals have specialised tissues capable of withstanding fluctuations in body temperature > 30 °C without adverse effects. In particular, the hearts of heterotherms are able to resist fibrillation and discontinuity of the cardiac conduction system common in homeotherms during hypothermia. To investigate the patterns of cardiac conduction in small insectivorous bats which enter torpor year round, I simultaneously measured ECG and subcutaneous temperature (Tsub) of 21 Nyctophilus gouldi (11 g) during torpor at a range of ambient temperatures (Ta 1–28 °C). During torpor cardiac conduction slowed in a temperature dependent manner, primarily via prolongation along the atrioventricular pathway (PR interval). A close coupling of depolarisation and repolarisation was retained in torpid bats, with no isoelectric ST segment visible until animals reached Tsub <6 °C. There was little change in ventricular repolarisation (JT interval) with decreasing Tsub, or between rest and torpor at mild Ta. Bats retained a more rapid rate of ventricular conduction and repolarisation during torpor relative to other hibernators. Throughout all recordings across seasons (> 2500 h), there was no difference in ECG morphology or heart rate during torpor, and no manifestations of significant conduction blocks or ventricular tachyarrhythmias were observed. My results demonstrate the capacity of bat hearts to withstand extreme fluctuations in rate and temperature throughout the year without detrimental arrhythmogenesis. I suggest that this conduction reserve may be related to flight and the daily extremes in metabolism experienced by these animals, and warrants further investigation of cardiac electrophysiology in other flying hibernators.


Arrhythmia Heart Electrocardiogram Metabolism Thermoregulation 



I would like to thank Fritz Geiser, Jack Tatler and Philip Currie for their helpful comments on the manuscript. This research was supported by a University of New England Postdoctoral Research Fellowship, Sagol School of Neuroscience Postdoctoral Fellowship and a Faculty of Life Sciences Postdoctoral Fellowship from Tel Aviv University.


  1. Andrews MT (2007) Advances in molecular biology of hibernation in mammals. BioEssays 29:431–440 CrossRefPubMedGoogle Scholar
  2. Arnold W, Ruf T, Frey-Roos F, Bruns U (2011) Diet-independent remodeling of cellular membranes precedes seasonally changing body temperature in a hibernator. PLoS One 6:e18641. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ayettey AS, Tagoe CNB, Yates RD (1990) Fine structure of subendocardial (Purkinje) cells of the insect-eating bat (Pipistrellus pipistrellus). J Anat 373:37–42Google Scholar
  4. Barnes BM (1989) Freeze avoidance in a mammal: body temperatures below 0 °C in an Arctic hibernator. Science 244:1593–1595. CrossRefPubMedGoogle Scholar
  5. Bartholomew GA, Hudson JW (1962) Hibernation, estivation, temperature regulation, evaporative water loss, and heart rate of the pigmy possum. Cercartetus nanus. Physiol Zool 35:94–107CrossRefGoogle Scholar
  6. Bartholomew GA, Hudson JW, Howell TR (1962) Body temperature, oxygen consumption, evaporative water loss, and heart rate in the poor-will. Condor 64(2):117–125. CrossRefGoogle Scholar
  7. Brauch KM, Dhruv ND, Hanse EA, Andrews MT (2005) Digital transcriptome analysis indicates adaptive mechanisms in the heart of a hibernating mammal. Physiol Genom 23(2):227–234. CrossRefGoogle Scholar
  8. Burlington RF, Bowers WD Jr, Daum RC, Ashbaugh P (1972) Ultrastructural changes in heart tissue during hibernation. Cryobiology 9:224–228. CrossRefPubMedGoogle Scholar
  9. Burlington RF, Vogel JA, Burton TM, Salkovitz IA (1971) Cardiac output and regional blood flow in hypoxic woodchucks. Am J Physiol 220:1565–1568PubMedGoogle Scholar
  10. Canals M, Atala C, Grossi B, Iriarte-Díaz J (2005) Relative size of hearts and lungs of small bats. Acta Chiropterol 7:65–72CrossRefGoogle Scholar
  11. Canals M, Iriarte-Diaz J, Grossi B (2011) Biomechanical, respiratory and cardiovascular adaptations of bats and the case of the small community of bats in Chile. In: Klika V (ed) Biomechanics in applications. InTech.
  12. Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181. CrossRefPubMedGoogle Scholar
  13. Currie SE, Körtner G, Geiser F (2014) Heart rate as a predictor of metabolic rate in heterothermic bats. J Exp Biol 217:1519–1524CrossRefPubMedGoogle Scholar
  14. Currie SE, Körtner G, Geiser F (2015) Measuring subcutaneous temperature and differential rates of rewarming from hibernation and daily torpor in two species of bats. Comp Biochem Physiol A Physiol 190:26–31CrossRefGoogle Scholar
  15. Currie SE, Stawski C, Geiser F (2017) Cold-hearted bats: uncoupling of heart rate and metabolism during torpor at subzero temperatures. J Exp Biol. PubMedGoogle Scholar
  16. Dawe AR, Morrison PR (1955) Characteristics of the hibernating heart. Am Heart J 49:367–384CrossRefPubMedGoogle Scholar
  17. Duker GD, Olsson S-O, Hect NH, Senturia JB, Johansson BW (1983) Ventricular fibrillation in hibernators and non-hibernators. Cryobiology 20:407–420CrossRefPubMedGoogle Scholar
  18. Duker GD, Sjoquist P-O, Johansson BW (1987) Monophasic action potentials during induced hypothermia in hedgehog and guinea pig hearts. Am J Physiol Heart Circ Physiol 253:H1083–H1088CrossRefGoogle Scholar
  19. Eagles DA, Jacques LB, Taboada J, Wagner CW, Daikun TA (1988) Cardiac arrhythmias during arousal from hibernation in three species of rodents. Am J Physiol Reg Integr Comp Physiol 254:R102–R108CrossRefGoogle Scholar
  20. Eddy SF, Storey KB (2004) Up-regulation of fatty acid-binding proteins during hibernation in the little brown bat Myotis lucifugus. Biochim Biophys Acta 1676:63–70CrossRefPubMedGoogle Scholar
  21. Eddy SF, Storey KB (2007) p38MAPK regulation of transcription factor tagets in muscle and heart of the hibernating bat Myotis lucifugus. Cell Biochem Funct 25:759–765CrossRefPubMedGoogle Scholar
  22. Elvert R, Heldmaier G (2005) Cardiorespiratory and metabolic reactions during entrance into torpor in dormice, Glis glis. J Exp Biol 208:1373–1383CrossRefPubMedGoogle Scholar
  23. Folk GE, Dickson EW, Hunt JM, Nilles EJ, Thrift DL (2008) QT intervals compared in small and large hibernators and humans. Biol Rhythm Res 39:427–438CrossRefGoogle Scholar
  24. Geiser F, Brigham RM (2000) Torpor, thermal biology and energetics in Australian long-eared bats (Nyctophilus). J Comp Physiol B 170:153–162CrossRefPubMedGoogle Scholar
  25. Geiser F, Augee ML, Raison JK (1984) Thermal response of liver mitochondrial membranes of the heterothermic bat (Miniopterus schreibersii) in summer and winter. J Therm Biol 9:183–188CrossRefGoogle Scholar
  26. Geiser F, Baudinette RV, McMurchie EJ (1989) The effect of temperature on the isolated perfused hearts of heterothermic marsupials. Comp Biochem Physiol A Physiol 93A:331–335CrossRefGoogle Scholar
  27. Geiser F, Currie SE, O’Shea KA, Hiebert SM (2014) Torpor and hypothermia: reversed hysteresis of metabolic rate and body temperature. Am J Physiol Reg Integr Comp Physiol 307:R1324–R1329. CrossRefGoogle Scholar
  28. Giroud S, Frare C, Strijkstra A, Boerema A, Arnold W, Ruf T (2013) Membrane phospholipid fatty acid composition regulates cardiac SERCA activity in a hibernator, the Syrian hamster (Mesocricetus auratus). PLoS One 8:e63111. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hudson JW (1965) Temperature regulation and torpidity in the pygmy mouse, Baiomys taylori. Physiol Zool 38:243–254CrossRefGoogle Scholar
  30. Hudson JW, Eller RR (1974) 42K efflux, EKG, and tension in isolated perfused hearts of white-footed mice. Comp Biochem Physiol A Physiol 49:743–755CrossRefGoogle Scholar
  31. Johansson BW (1996) The hibernator heart—nature’s model of resistance to ventricular fibrillation. Cardiovasc Res 31:826–832PubMedGoogle Scholar
  32. Kossmann CE, Fawcett DW (1961) The sarcoplasmic reticulum of skeletal and cardiac muscle. Circulation 24:336–348CrossRefGoogle Scholar
  33. Kulzer E (1967) Die Herztätigkeit bei lethargischen und winterschlafenden Fledermäusen. Z Vergl Physiol 56:63–94CrossRefGoogle Scholar
  34. Lasiewski RC, Lasiewski RJ (1967) Physiological responses of the blue-throated and Rivoli’s hummingbirds. Auk 84:34–48. CrossRefGoogle Scholar
  35. Levin E, Yom-Tov Y, Hefetz A, Kronfeld-Schor N (2013) Changes in diet, body mass and fatty acid composition during pre-hibernation in a subtropical bat in relation to NPY and AgRP expression. J Comp Physiol B 183:157–166. CrossRefPubMedGoogle Scholar
  36. Lyman CP, Blinks DC (1959) The effect of temperature on the isolated hearts of closely related hibernators and non-hibernators. J Cell Comp Physiol 54:53–63. CrossRefPubMedGoogle Scholar
  37. Lyman CP, O’Brien RC (1960) Circulatory changes in the thirteen-lined ground squirrel during the hibernation cycle. Bull Mus Comp Zool 124:353–372Google Scholar
  38. Lyman CP, Willis JS, Malan A, Wang LCH (eds) (1982) Hibernation and torpor in mammals and birds. Academic, New YorkGoogle Scholar
  39. Mertens A, Steidl O, Steinlechner S, Meyer M (2008) Cardiac dynamics during daily torpor in the Djungarian hamster (Phodopus sungorus). Am J Physiol Reg Integr Comp Physiol 294:R639–R650CrossRefGoogle Scholar
  40. Michael CR, Menaker M (1963) The effect of temperature on the isolated heart of the bat Myotis lucifugus. J Cell Comp Physiol 62:355–358CrossRefPubMedGoogle Scholar
  41. Mihova D, Hechavarrίa JC (2016) The electrocardiogram signal of Seba’s short-tailed bat Carollia perspicillata. J Comp Physiol (A). Google Scholar
  42. Morhardt JE (1970) Heart rates, breathing rates, and the effects of atropine and acetylcholine on white-footed mice (Peromyscus sp.) during daily torpor. Comp Biochem Physiol 33:441–457CrossRefPubMedGoogle Scholar
  43. Nardone RM (1955) Electrocardiogram of the Artic ground squirrel during hibernation and hypothermia. Am J Physiol 182:364–368PubMedGoogle Scholar
  44. Neuweiler G (2000) The biology of bats. Oxford University Press, OxfordGoogle Scholar
  45. Noujaim SF, Lucca E, Munoz V, Persaud D, Berenfeld O, Meijler FL, Jalife J (2004) From mouse to whale: a universal scaling relation for the PR interval of the electrocardiogram of mammals. Circulation 110:2802–2808CrossRefPubMedGoogle Scholar
  46. Phillips WR, Inwards SJ (1985) The annual activity and breeding cycles of Gould’s long-eared bat, Nyctophilus gouldi (Microchioptera: Vespertilionidae). Aust J Zool 33:111–126CrossRefGoogle Scholar
  47. Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2014) _nlme: Linear and nonlinear mixed effect models. R package version 3.1-117. Accessed 9 Mar 2014
  48. Rousset F, Ferdy J-B (2014) Testing environmental and genetic effects in the presence of spatial autocorrelation. Ecography 37:781–790CrossRefGoogle Scholar
  49. Ruf T, Arnold W (2008) Effects of polyunsaturated fatty acids on hibernation and torpor: a review and hypothesis. Am J Physiol Regul Integr Comp Physiol 294:R1044–R1052. CrossRefGoogle Scholar
  50. Ruf T, Geiser F (2015) Daily torpor and hibernation in birds and mammals. Biol Rev 90:891–926. CrossRefPubMedGoogle Scholar
  51. Sarajas HSS (1954) Observations on the electrocardiographic alterations in the hibernating hedgehog. Acta Physiol Scand 32:28–38CrossRefPubMedGoogle Scholar
  52. Schaub R, Prinzinger R (1999) Long-term telemetry of heart rates and energy metabolic rate during the diurnal cycle in normothermic and torpid African blue-naped mousebirds (Urocolius macrourus). Comp Biochem Physiol A Physiol 124:439–445CrossRefGoogle Scholar
  53. Smith DE, Katzung B (1966) Mechanical performace of myocardium from hibernating and non-hibernating mammals. Am Heart J 71:515–521CrossRefPubMedGoogle Scholar
  54. South FE, Jacobs HK (1973) Contraction kinetics of ventricular muscle from hibernating and nonhibernating mammals. Am J Physiol 225:444–449PubMedGoogle Scholar
  55. Stawski C, Willis CKR, Geiser F (2014) The importance of temporal heterothermy in bats. J Zool 292:86–100. CrossRefGoogle Scholar
  56. Steffen JM, Riedesel ML (1982) Pulmonary ventilation and cardiac activity in hibernating and arousing golden-mantled ground squirrels (Spermophilus lateralis). Cryobiology 19:83–91. CrossRefPubMedGoogle Scholar
  57. Studier EH, Howell DJ (1969) Heart rates of female big brown bats in flight. J Mamm 50:842–845CrossRefGoogle Scholar
  58. Swoap SJ (2008) The pharmacology and molecular mechanisms underlying temperature regulation and torpor. Biochem Pharmacol 76:817–824. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Swoap SJ, Gutilla MJ (2009) Cardiovascular changes during daily torpor in the laboratory mouse. Am J Physiol Reg Integr Comp Physiol 297:R769–R774CrossRefGoogle Scholar
  60. Swoap SJ, Körtner G, Geiser F (2017) Heart rate dynamics in a marsupial hibernator. J Exp Biol 220:2939–2946. CrossRefPubMedGoogle Scholar
  61. Thomas SP (1975) Metabolism during flight in two species of bats, Phyllostomus hastatus and Pteropus gouldii. J Exp Biol 63:273–293PubMedGoogle Scholar
  62. Tøien Ø, Blake J, Edgar DM, Grahn DA, Heller HC, Barnes BM (2011) Hibernation in black bears: independence of metabolic suppression for body temperature. Science 331:906–909CrossRefPubMedGoogle Scholar
  63. Turbill C (2006) Roosting and thermoregulatory behaviour of male Gould’s long-eared bats, Nyctophilus gouldi: energetic benefits of thermally unstable tree roosts. Aust J Zool 54(1):57–60. CrossRefGoogle Scholar
  64. Twente JW, Twente J (1978) Autonomic regulation of hibernation by Citellus and Eptesicus. In: Wang LCH, Hudson JW (eds) Strategies in cold: natural torpidity and thermogenesis. Academic, New York, pp 327–373CrossRefGoogle Scholar
  65. van Veen TAB, van der Heyden MAG, van Rijen HVM (2008) The secrets of hibernators’ cardiac conduction reserve. Heart Rhythm 5:1597–1598CrossRefPubMedGoogle Scholar
  66. Wacker CB, Rojas AD, Geiser F (2012) The use of small subcutaneous transponders for quantifying thermal biology and torpor in small mammals. J Therm Biol 37:250–254CrossRefGoogle Scholar
  67. Wang LC-H, Hudson JW (1970) Some physiological aspects of temperature regulation in the normothermic and torpid hispid pocket mouse, Peromyscus hispidus. Comp Biochem Physiol 32:275–293CrossRefPubMedGoogle Scholar
  68. Yatani A, Kim S-J, Kudej RK, Wang Q, Depre C, Irie K, Kranias EG, Vatner SF, Vatner DE (2004) Insights into cardioprotection obtained from study of cellular Ca2+ handling in myocardium of true hibernating mammals. Am J Physiol Heart Circ Physiol 286:H2219–H2228. CrossRefGoogle Scholar
  69. Zimmer MB, Harris MB, Milsom WK (2000) Control of cardiac and ventillation frequencies during hibernation in ground squirrels. In: Heldmaier G, Klingenspor M (eds) Life in the cold: eleventh international hibernation symposium. Springer, BerlinGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centre for Behavioural and Physiological Ecology, ZoologyUniversity of New EnglandArmidaleAustralia
  2. 2.Department of Zoology, Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael

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