Skip to main content
Log in

Warming up and shipping out: arousal and emergence timing in hibernating little brown bats (Myotis lucifugus)

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Phenology refers to the timing of events in the annual cycle of organisms. For temperate-zone mammals, hibernation is one such event, but little is known about its phenology. Hibernation consists of energy-saving torpor bouts interspersed with energetically expensive arousals to normothermic T b, and hibernators should benefit from mechanisms which reduce arousal costs and help them time arousals to coincide with foraging opportunities. In a previous study, we showed that, in contrast to hibernating bats from warmer climates, little brown bats (Myotis lucifugus) from central Canada abandon a circadian pattern to arousal in the middle of winter when there is no chance of feeding. Here, we used temperature telemetry to test whether they would re-synchronize arousals with normal foraging time (i.e. sunset) during late winter as the chance of foraging or emergence opportunities improves, and whether they would synchronize arousals with conspecifics, possibly to exploit social thermoregulation. We also used passive transponders to test whether energy reserves and/or sex differences in reproductive timing influence phenology and the sensitivity of emergence timing to environmental cues. In contrast to patterns in mid-winter, after 7 April 2013, bats synchronized arousals with sunset and with conspecifics. Females emerged earlier than males, and females in the best condition emerged first while body condition had no influence on male emergence timing. Both male and female bats appeared to time emergence with falling barometric pressure, a cue that predicts favourable foraging conditions for bats but which, unlike outside temperature, would have been readily detectable by bats inside the hibernaculum. Our results highlight hibernation traits associated with extreme winter energy limitation for insect-eating bats in cold climates and illustrate the influence of reproductive timing and environmental conditions on hibernation energetics and phenology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aldridge H, Brigham RM (1988) Load carrying and maneuverability in an insectivorous bat: a test of the 5% “rule” of radio-telemetry. J Mamm 69:379–382

    Article  Google Scholar 

  • Anthony ELP, Stack MH, Kunz TH (1981) Night roosting and the nocturnal time budget of the little brown bat, Myotis lucifugus: effects of reproductive status, prey density, and environmental conditions. Oecologia 51:151–156

    Article  Google Scholar 

  • Arlettaz R, Christe P, Lugon A, Perrin N, Vogel P (2001) Food availability dictates the timing of parturition in insectivorous mouse-eared bats. Oikos 95:105–111

    Article  Google Scholar 

  • Arnold W (1993) Energetics of social hibernation. In: Carey C, Florant GL, Wunder BA, Horowitz B (eds). Life in the cold. Ecological, physiological, and molecular mechanisms. Westview Press, Inc. Boulder, CO, pp 65–80

  • Audet D, Thomas DW (1996) Evaluation of the accuracy of body temperature measurement using external radio transmitters. Can J Zool 74:1778–1781

    Article  Google Scholar 

  • Barclay RMR, Kalcounis MC, Crampton LH, Stefan C, Vonhof MJ, Wilkinson L, Brigham RM (1996) Can external radiotransmitters be used to assess body temperature and torpor in bats? J Mamm 77:1102–1106

    Article  Google Scholar 

  • Bieber C, Lebl K, Stalder G, Geiser F, Ruf T (2014) Body mass dependent use of hibernation: why not prolong the active season, if they can? Funct Ecol 28:167–177

    Article  Google Scholar 

  • Boratyński JS, Willis CKR, Jefimow M, Wojciechowski MS (2014) Huddling enhances survival of hibernating bats by reducing evaporative water loss. Comp Biochem Physiol A 179:125–132

    Article  Google Scholar 

  • Both C, Van Asch M, Bijlsma RG, Van Den Burg AB, Visser ME (2009) Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J Anim Ecol 78:73–83

    Article  PubMed  Google Scholar 

  • Boyles JG, Storm JJ, Brack V Jr (2008) Thermal benefits of clustering during hibernation—a field test of competing hypotheses on Myotis sodalis. Funct Ecol 22:632–6369

    Article  Google Scholar 

  • Czenze ZJ, Park AD, Willis CKR (2013) Staying cold through dinner: cold-climate bats rewarm with conspecifics but not sunset during hibernation. J Comp Physiol B 183:1–8

    Article  Google Scholar 

  • Frick WF, Reynolds DS, Kunz TH (2010) Influence of climate and reproductive timing on demography of little brown myotis (Myotis lucifugus). J Anim Ecol 79:128–136

    Article  PubMed  Google Scholar 

  • Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274

    Article  CAS  PubMed  Google Scholar 

  • Geiser F (2013) Hibernation. Curr Biol 23:R188–R193

    Article  CAS  PubMed  Google Scholar 

  • Geiser F, Brigham RM (2012) The other functions of torpor. In: Ruf T, Arnold W, Bieber C, Millesi E (eds) Living in a seasonal world. Springer, Berlin Heidelberg, pp 109–121

    Chapter  Google Scholar 

  • Grahn DA, Miller JD, Houng VS, Heller HC (1994) Persistence of circadian rhythmicity in hibernating ground squirrels. Am J Physiol Regul Integr Comp Physiol 266:251–1258

    Google Scholar 

  • Heller HC, Ruby NF (2004) Sleep and circadian rhythms in mammalian torpor. Annu Rev Physiol 66:275–289

    Article  CAS  PubMed  Google Scholar 

  • Hope PR, Jones G (2012) Warming up for dinner: torpor and arousal in hibernating Natterer’s bats (Myotis nattereri) studied by radio telemetry. J Comp Physiol B 182:569–578

    Article  PubMed  Google Scholar 

  • Inouye DW, Barr WA, Armitage KB, Inouye BD (2000) Climate change is affecting altitudinal migrants and hibernating species. PNAS 97:1630–1633

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jonasson KA, Willis CKR (2012) Hibernation energetics of little brown bats. J Exp Biol 215:2141–2149

    Article  PubMed  Google Scholar 

  • Körtner G, Geiser F (2000) The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol Intern 17:103–128

    Article  Google Scholar 

  • Lane JE, Kruuk LE, Charmantier A, Murie JO, Dobson FS (2012) Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature 489:554–557

    Article  CAS  PubMed  Google Scholar 

  • Linacre E, Geerts B (1997) Climate and weather explained 1997. Routledge, London

    Google Scholar 

  • Lovegrove BG, Lobban KD, Levesque DL (2014) Mammal survival at the Cretaceous-Palaeogene boundary: metabolic homeostasis in prolonged tropical hibernation in tenrecs. Proc Roy Soc B. doi:10.1098/rspb.2014.1304

    Google Scholar 

  • Lutgens FK, Tarbuck EJ (2013) The atmosphere an introduction to meterology, 12th edn. Pearson

  • Lyman CP (1982) Who is who among the hibernators. In: Lyman CP, Willis JS, Malan A, Wang LCH (eds) Hibernation and torpor in mammals and birds. Academic Press, New York, pp 2–36

    Google Scholar 

  • Murie JO, Harris MA (1982) Annual variation of spring emergence and breeding in Columbian ground squirrels (Spermophilus columbianus). J Mamm 63:431–439

    Article  Google Scholar 

  • National Climate Data and Information Archive (2013) Environment Canada. http://www.climate.weatheroffice.gc.ca. Accessed 21 Oct 2013

  • Negraeff OE, Brigham RM (1995) The influence of moonlight on the activity of little brown bats (Myotis lucifugus). Z Saugetierkd 60:330–336

    Google Scholar 

  • Norquay KJO, Willis CKR (2014) Hibernation phenology of Myotis lucifugus. J Zool Lon. (In press)

  • Ozgul A, Childs DZ, Oli MK, Armitage KB, Blumstein DT, Olson LE, Tuljapurkar Sand Coulson T (2010) Coupled dynamics of body mass and population growth in response to environmental change. Nature 466:482–485

    Article  CAS  PubMed  Google Scholar 

  • Paige KN (1995) Bats and barometric pressure: conserving limited energy and tracking insects from the roost. Funct Ecol 9:463–467

    Article  Google Scholar 

  • Park KJ, Jones G, Ransome RD (2000) Torpor, arousal and activity of hibernating greater horseshoe bats (Rhinolophus ferrumequinum). Funct Ecol 14:580–588

    Article  Google Scholar 

  • Perry RW (2012) A review of factors affecting cave climates for hibernating bats in temperate North America. Environ Rev 21:28–39

    Article  Google Scholar 

  • Pflitsch A, Wiles M, Horrocks R, Piasecki J, Ringeis J (2010) Dynamicclimatologic processes of barometric cave systems using the example of Jewel Cave and Wind Cave in South Dakota, U.S.A. Acta Carsologica 39:449–462

    Google Scholar 

  • Racey PA, Swift SM (1981) Variations in gestation length in a colony of pipistrelle bats (Pipistrellus pipistrellus) from year to year. J Reprod Fertil 61:123–129

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria ISBN 3-900051-07-0, http://www.R-project.org

  • Reeder DM, Frank CL, Turner GG, Meteyer CU, Kurta A et al (2012) Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS One 7:e38920

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Revel FG, Herwig A, Garidou ML, Dardente H, Menet JS, Masson-Pévet M, Simonneaux V, Saboureau M, Pévet P (2007) The circadian clock stops ticking during deep hibernation in the European hamster. Proc Nat Acad Sci USA 104:13816–13820

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ruby NF, Dark J, Burns DE, Heller HC, Zucker I (2002) The suprachiasmatic nucleus is essential for circadian body temperature rhythms in hibernating ground squirrels. J Neurosci 221:357–364

    Google Scholar 

  • Schorr RA, Lukacs PM, Florant GL (2009) Body mass and winter severity as predictors of overwinter survival in Preble’s meadow jumping mouse. J Mamm 90:17–24

    Article  Google Scholar 

  • Sheriff MJ, Kenagy GJ, Richter M, Lee T, Tøien Ø, Kohl F, Buck CL, Barnes BM (2011) Phenological variation in annual timing of hibernation and breeding in nearby populations of Arctic ground squirrels. Proc R Soc Biol Sci Ser B 278:2369–2375

    Article  Google Scholar 

  • Speakman JR, Webb PI, Racey PA (1991) Effects of disturbance on the energy expenditure of hibernating bats. J Appl Ecol 28:1087–1104

    Article  Google Scholar 

  • Stawski C, Geiser F (2010) Fat and fed: frequent use of summer torpor in a subtropical bat. Naturwissenschaften 97:29–35

    Article  CAS  PubMed  Google Scholar 

  • Storey KB, Storey JM (2004) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev 79:207–233

    Article  PubMed  Google Scholar 

  • Thomas DW (1995) Hibernating bats are sensitive to nontactile human disturbance. J Mamm 76:940–946

    Article  Google Scholar 

  • Thomas DW, Fenton BM, Barclay RMR (1979) Social behavior of the little brown bat, Myotis lucifugus: I. Mating behavior. Behav Ecol and Sociobiol 6:129–136

    Article  Google Scholar 

  • Thomas DW, Dorais M, Bergeron JM (1990) Winter energy budgets and cost of arousals for hibernating little brown bats, Myotis lucifugus. J Mamm 71:475–479

    Article  Google Scholar 

  • Tøien Ø, Blake J, Edgar DM, Grahn DA, Heller HC, Barnes BM (2011) Hibernation in black bears: independence of metabolic suppression from body temperature. Science 331:906–909

    Article  PubMed  Google Scholar 

  • Turbill C (2008) Winter activity of Australian tree-roosting bats: influence of temperature and climatic patterns. J Zool 276:285–290

    Article  Google Scholar 

  • Turner JM, Warnecke L, Wilcox A, Baloun D, Bollinger TK, Misra V, Willis CKR (2015) Conspecific disturbance contributes to altered hibernation patterns in bats with white-nose syndrome. Physiol Behav 140:71–78

    Article  CAS  PubMed  Google Scholar 

  • Twente JW, Twente J, Brack V Jr (1985) The duration of the period of hibernation of three species of vespertilionid bats. II. Laboratory studies. Can J Zool 63:2955–2961

    Article  Google Scholar 

  • Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc B 272:2561–2569

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang LCH (1989) Ecological, physiological, and biochemical aspects of torpor in mammals and birds. In: Wang LCH (ed) Advances in comparative and environmental physiology. Springer Verlag, Berlin, pp 361–401

  • Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misra V, Cryan PM, Wibbelt G, Blehert DS, Willis CKR (2012) Inoculation of a North American bat with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Nat Acad Sci USA 109:6999–7003

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wilkinson GS, South JM (2002) Life history, ecology and longevity in bats. Aging Cell 1:124–131

    Article  CAS  PubMed  Google Scholar 

  • Williams CT, Barnes BM, Buck CL (2012a) Body temperature rhythms persist under the midnight sun but are absent during hibernation in free-living arctic ground squirrels. Biol Lett 8:31–34

    Article  PubMed Central  PubMed  Google Scholar 

  • Williams CT, Barnes BM, Richter M, Buck CL (2012b) Hibernation and circadian rhythms of body temperature in free-living arctic ground squirrels. Physiol Biochem Zool 85:397–404

    Article  PubMed  Google Scholar 

  • Willis CKR, Brigham RM (2003) Defining torpor in free-ranging bats: experimental evaluation of external temperature-sensitive radiotransmitters and the concept of active temperature. J Comp Physiol B 173:379–389

    Article  CAS  PubMed  Google Scholar 

  • Zervanos SM, Salsbury CM, Brown JK (2009) Maintenance of biological rhythms during hibernation in eastern woodchucks (Marmota monax). J Comp Physiol B 179:411–418

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Q. Webber, D. Baloun, A. Menzies, M.A. Collis and H. Mayberry for essential help with fieldwork and L. McGuire for statistical advice. We also thank M. Wiegand, K. Campbell and three anonymous reviewers for excellent comments on an earlier version of this manuscript. Funding was provided by Grants to CKRW from the Natural Sciences and Engineering Research Council (NSERC), the Canada Foundation for Innovation, Manitoba Research and Innovation Fund, Manitoba Hydro Forest Enhancement Program and the University of Winnipeg Chancellor’s Research Chair.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zenon J. Czenze.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Czenze, Z.J., Willis, C.K.R. Warming up and shipping out: arousal and emergence timing in hibernating little brown bats (Myotis lucifugus). J Comp Physiol B 185, 575–586 (2015). https://doi.org/10.1007/s00360-015-0900-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-015-0900-1

Keywords

Navigation