Warming up for dinner: Torpor and arousal in hibernating Natterer's bats (Myotis nattereri) studied by radio telemetry

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 182, Issue 4, 2012, Pages 569-578

  Hope, Paul R ^a,b   Jones, Gareth ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b Basingstoke Canal Authority   (United Kingdom)

Author keywords

Body temperature; Energy conservation; Hibernation

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ANIMAL DISEASE; AROUSAL; ARTICLE; BAT; BODY SIZE; BODY TEMPERATURE; CHRONOBIOLOGY; FEEDING BEHAVIOR; FEMALE; FORELIMB; GROWTH, DEVELOPMENT AND AGING; HIBERNATION; MALE; MOTOR ACTIVITY; PHYSIOLOGY; RADIOFREQUENCY RADIATION; REMOTE SENSING; SEASON; SKIN TEMPERATURE; TEMPERATURE; UNITED KINGDOM;

ANIMALS; AROUSAL; BEHAVIOR, ANIMAL; BODY SIZE; BODY TEMPERATURE; CHIROPTERA; CHRONOBIOLOGY PHENOMENA; ENGLAND; FEEDING BEHAVIOR; FEMALE; FORELIMB; HIBERNATION; MALE; MOTOR ACTIVITY; RADIO WAVES; REMOTE SENSING TECHNOLOGY; SEASONS; SKIN TEMPERATURE; TEMPERATURE;

MAMMALIA; MYOTIS NATTERERI; VESPERTILIONIDAE;

EID: 84859839607     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-011-0631-x     Document Type: Article

References (68)

1. Audet D, Thomas DW (1996) Evaluation of the accuracy of body temperature measurement using external radio transmitters. Can J Zool 74: 1778-1781.
2. Avery MI (1985) Winter activity of pipistrelle bats. J Anim Ecol 54: 721-738.
3. Avery MI (1986) The winter activity of noctule bats (Nyctalus noctula). J Zool 209: 296-299.
4. Baumer J, South FE, Fellen L, Zatzman ML (1971) A possible basis for periodic arousals during hibernation: accumulation of ketone bodies. Life Sci 10: 463-471.
5. Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JTH, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323: 227.
6. Boyles JG, Brack V (2009) Modeling survival rates of hibernating mammals with individual-based models of energy expenditure. J Mammal 90: 9-16.
7. Boyles JG, Dunbar MB, Whitaker JO Jr (2006) Activity following arousal in winter in North American vespertilionid bats. Mammal Rev 36: 267-280.
8. Brigham RM (1987) The significance of winter activity by the big brown bat Eptesicus fuscus: the influence of energy reserves. Can J Zool 65: 1240-1242.
9. Burton RS, Reichman OJ (1999) Does immune challenge affect torpor duration? Funct Ecol 13: 232-237.
10. Cryan PM, Meteyer CU, Boyles JG, Blehert DS (2010) Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of pathology. BMC Biol 8: 135.
11. Csorba G, Ujhelyi P, Thomas N (2003) Horseshoe bats of the world (Chiroptera: Rhinolophidae). Alana books, Shropshire.
12. Daan S (1973) Activity during natural hibernation in three species of vespertilionid bats. Neth J Zool 23: 1-71.
13. Daan S, Barnes BM, Strijkstra AM (1991) Warming up for sleep? Ground squirrels sleep during arousal from hibernation. Neurosci Lett 128: 265-268.
14. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429: 825-826.
15. Dietz C, von Helversen O, Nill D (2009) Bats of Britain, Europe and northwest Africa. A and C Black, London.
16. Dunbar MB, Tomasi TE (2006) Arousal patterns, metabolic rate, and an energy budget of eastern red bats (Lasiurus borealis) in winter. J Mammal 87: 1096-1102.
17. Entwistle AC, Racey PA, Speakman JR (1998) The reproductive cycle and determination of sexual maturity in male brown long-eared bats, Plecotus auritus (Chiroptera: Vespertilionidae). J Zool 244: 1-63.
18. Fowler PA, Racey PA (1990) Daily and seasonal cycles of body temperature and aspects of heterothermy in the hedgehog Erinaceus europaeus. J Comp Physiol B 160: 299-307.
19. French AR (1976) Periodicity of recurrent hypothermia during hibernation in the pocket mouse, Perognathus longimembris. J Comp Physiol A 115: 87-100.
20. French AR (1985) Allometries of the durations of torpor and euthermic intervals during mammalian hibernation: a test of the theory of metabolic control of the timing and changes in body temperature. J Comp Physiol B 156: 13-19.
21. Frick WF, Pollock JF, Hicks AC, Langwig KE, Reynolds DS, Turner GG, Butchkoski CM, Kunz TH (2010) An emerging disease causes regional population collapse of a common North American bat species. Science 329: 679-682.
22. Galster WA, Morrison P (1972) Cyclic changes in carbohydrate concentrations during hibernation in the arctic ground squirrel. Am J Physiol 218: 1228-1232.
23. Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68: 935-966.
24. Gregor F, Bauerova Z (1987) The role of Diptera in the diet of Natterer's bat, Myotis nattereri. Folia Zool 36: 13-19.
25. Guilday JE (1948) Little brown bats copulating in winter. J Mammal 29: 416-417.
26. Guthrie MJ (1933) Notes on the seasonal movements and habits of some cave bats. J Mammal 14: 1-19.
27. Hays GC, Speakman JR, Webb PI (1991) Why do brown long-eared bats (Plecotus auritus) fly in winter? Physiol Zool 65: 554-567.
28. Heller HC, Ruby NF (2004) Sleep and circadian rhythms in mammalian torpor. Annu Rev Physiol 66: 275-289.
29. Humphries MM, Kramer DL, Thomas DW (2003) The role of energy availability in mammalian hibernation: an experimental test in free-ranging eastern chipmunks. Physiol Biochem Zool 76: 180-186.
30. Jonasson KA, Willis CKR (2011) Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome. PLoS One 6: e21061.
31. Jones G, Rydell J (1994) Foraging strategy and predation risk as factors influencing emergence time in echolocating bats. Phil Trans R Soc Lond B 346: 445-455.
32. Karpovich SA, Tøien Ø, Buck CL, Barnes BM (2009) Energetics of arousal episodes in hibernating arctic ground squirrels. J Comp Physiol B 179: 691-700.
33. Kokurewicz T (2004) Sex and age related habitat selection and mass dynamics of Daubenton's bats Myotis daubentonii (Kuhl, 1817) hibernating in natural conditions. Acta Chiropt 6: 121-144.
34. Lausen CL, Barclay RMR (2006) Winter bat activity in the Canadian prairies. Can J Zool 84: 1079-1086.
35. Liu J-N, Karasov WH (2011) Hibernation in warm hibernacula by free-ranging Formosan leaf-nosed bats, Hipposideros terasensis, in subtropical Taiwan. J Comp Physiol B 181: 125-135.
36. Lyman CP, Chatfield PO (1955) Physiology of hibernation in mammals. Physiol Rev 35: 403-425.
37. Mann ME, Zhang Z, Hughes MK, Bradley RS, Miller SK, Rutherford S, Ni F (2008) Proxy-based reconstructions of hemispheric and global surface temperature variations over the past two millennia. Proc Natl Acad Sci USA 105: 13252-13257.
38. Park KJ, Jones G, Ransome RD (1999) Winter activity of a population of greater horseshoe bats Rhinolophus ferrumequinum. J Zool 248: 419-427.
39. Park KJ, Jones G, Ransome RD (2000) Torpor, arousal and activity of hibernating greater horseshoe bats (Rhinolophus ferrumequinum). Funct Ecol 14: 580-588.
40. Pengelley ET, Fisher KC (1961) Rhythmical arousal from hibernation in the golden-mantled ground squirrel, Citellus lateralis tescorum. Can J Zool 39: 105-120.
41. Puechmaille SJ, Frick WF, Kunz TH, Racey PA, Voigt CC, Wibbelt G, Teeling EC (2011) White-nose syndrome: is this emerging disease a threat to European bats? Trends Ecol Evol 26: 570-576.
42. Racey PA, Swift SM (1985) Feeding ecology of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) during pregnancy and lactation. I. Foraging behaviour. J Anim Ecol 54: 205-215.
43. Ransome RD (1968) Distribution of greater horseshoe bats Rhinolophus ferrumequinum during hibernation in relation to environmental factors. J Zool 154: 77-112.
44. Ransome RD (1971) Effect of ambient temperature on arousal frequency of hibernating greater horseshoe bat, Rhinolophus ferrumequinum, in relation to site and hibernation state. J Zool 164: 353-371.
45. Ransome RD (1995) Earlier breeding shortens life in female greater horseshoe bats. Phil Trans R Soc Lond B 350: 153-161.
46. Ransome RD (2002) Winter feeding studies on greater horseshoe bats. English Nature Research Reports 449. English Nature, Peterborough, pp 1-47.
47. Revel FG, Herwig A, Garidou M-L, Dardente H, Menet JS, Masson-Pévet M, Simonneaux V, Saboureau M, Pévet P (2007) The circadian clock stops ticking during sleep deprivation during deep hibernation in the European hamster. Proc Natl Acad Sci USA 104: 13816-13820.
48. Russo D, Jones G, Migliozzi A (2002) Habitat selection by the Mediterranean horseshoe bat, Rhinolophus euryale (Chiroptera: Rhinolophidae) in a rural area of southern Italy and implications for conservation. Biol Conserv 107: 71-81.
49. Rydell J, Entwistle A, Racey PA (1996) Timing of foraging flights of three species of bat in relation to insect activity and predation risk. Oikos 76: 243-252.
50. Shiel CB, McAney CM, Fairley JS (1991) Analysis of the diet of Natterer's bat Myotis nattereri and the common long-eared bat Plecotus auritus in the west of Ireland. J Zool 223: 299-305.
51. Speakman JR, Racey PA (1986) The influence of body condition on sexual development of male brown long-eared bats (Plecotus auritus) in the wild. J Zool 210: 515-525.
52. Speakman JR, Racey PA (1989) Hibernal ecology of the pipistrelle bat: energy-expenditure, water requirements and mass-loss, implications for survival and the function of winter emergence flights. J Anim Ecol 58: 797-813.
53. Stawski C, Turbill C, Geiser F (2009) Hibernation by a free-ranging subtropical bat (Nyctophilus bifax). J Comp Physiol B 179: 433-441.
54. Swift SM, Racey PA (2002) Gleaning as a foraging strategy in Natterer's bat Myotis nattereri. Behav Ecol Sociobiol 52: 408-416.
55. Taylor LR (1963) Analysis of the effects of temperature on insects in flight. J Anim Ecol 32: 99-117.
56. Thomas DW (1993) Lack of evidence for a biological alarm clock in bats (Myotis spp.) hibernating under natural conditions. Can J Zool 71: 1-3.
57. Thomas DW (1995) The physiological ecology of hibernation in vespertilionid bats. Symp Zool Soc Lond 67: 233-244.
58. Thomas DW, Geiser F (1997) Periodic arousals in hibernating mammals: is evaporative water loss involved? Funct Ecol 11: 585-591.
59. Thomas DW, Dorais M, Bergeron J (1990) Winter energy budgets and cost of arousals for hibernating little brown bats Myotis lucifugus. J Mammal 71: 475-479.
60. Tinkle DW, Patterson IG (1965) A study of hibernating populations of Myotis velifer in northwestern Texas. J Mammal 46: 612-633.
61. Turbill C (2006) Thermoregulatory behaviour of tree-roosting chocolate wattled bats (Chalinolobus morio) during summer and winter. J Mammal 87: 318-323.
62. Turbill C, Geiser F (2008) Hibernation by tree roosting bats. J Comp Physiol B 178: 597-605.
63. Twente JW, Twente J (1987) Biological alarm clock arouses hibernating big brown bats, Eptesicus fuscus. Can J Zool 65: 1668-1674.
64. Vaughan N (1997) The diets of British bats (Chiroptera). Mammal Rev 27: 77-94.
65. Vaughan N, Jones G, Harris S (1997) Identification of British bat species by multivariate analysis of echolocation call parameters. Bioacoustics 7: 189-207.
66. Vine PAL (1994) London's lost route to Basingstoke the story of the Basingstoke canal. David & Charles, Newton Abbot.
67. Willis CKR, Brigham RM (2003) Defining torpor in free-ranging bats: experimental evaluation of external temperature-sensitive radio transmitters and the concept of active temperature. J Comp Physiol B 173: 379-389.
68. Willis CKR, Menzies AK, Boyles JG, Wojciechowski MS (2011) Evaporative water loss is a plausible explanation for mortality of bats from white-nose syndrome. Integr Comp Biol 51: 676-690. doi: 10. 1093/icb/icr076.