Abstract
Winter energy stores are finite and factors influencing patterns of activity are important for overwintering energetics and survival. Hibernation patterns (e.g., torpor bout duration and arousal frequency) often depend on microclimate, with more stable hibernacula associated with greater energy savings than less stable hibernacula. We monitored hibernation patterns of individual big brown bats (Eptesicus fuscus; Palisot de Beauvois, 1796) overwintering in rock-crevices that are smaller, drier, and less thermally stable than most known cave hibernacula. While such conditions would be predicted to increase arousal frequency in many hibernators, we did not find support for this. We found that bats were insensitive to changes in hibernacula microclimate (temperature and humidity) while torpid. We also found that the probability of arousal from torpor remained under circadian influence, likely because throughout the winter during arousals, bats commonly exit their hibernacula. We calculated that individuals spend most of their energy on maintaining a torpid body temperature a few degrees above the range of ambient temperatures during steady-state torpor, rather than during arousals as is typical of other small mammalian hibernators. Flight appears to be an important winter activity that may expedite the benefits of euthermic periods and allow for short, physiologically effective arousals. Overall, we found that big brown bats in rock crevices exhibit different hibernation patterns than conspecifics hibernating in buildings and caves.
Summary statement
In a population of prairie-living bats, we show an uncommon hibernation pattern consisting of short, infrequent arousals, and estimate the majority of their energy stores are expended while torpid rather than euthermic.
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Abbreviations
- Ear :
-
energetic cost of arousal
- Ebout :
-
energetic cost of arousal bouts
- Ecool :
-
energetic cost of cooling
- Eeu :
-
energetic cost of euthermy
- Eflight :
-
energetic cost of mid-winter flight
- Etor :
-
energetic cost of torpor bouts
- Ewin :
-
winter energy expenditure
- MR:
-
metabolic rate
- Ta :
-
ambient temperature
- Tb :
-
body temperature
- Th :
-
hibernaculum temperature
- Tset :
-
body-temperature set point
- Tsk−eu :
-
euthermic skin temperature
- Tsk−tor :
-
torpid skin temperature
- Ttor−min :
-
minimum torpid skin temperature
- TMRmin :
-
minimum torpid metabolic rate
- WVPabs :
-
absolute water vapor pressure
References
Alberta Climate Information Service [ACIS] (2015) Current and historical Alberta weather station data viewer. ACIS, Agriculture and Forestry Ministry, Government of Alberta, Edmonton. http://agriculture.alberta.ca/acis/alberta-weather-data-viewer.jsp
Aldridge HDJN, Brigham RM (1988) Load carrying and maneuverability in an insectivorous bat: a test of the 5% rule of radio-telemetry. J Mammal 69:379–382. https://doi.org/10.2307/1381393
Armitage KB, Blumstein DT, Woods BC (2003) Energetics of hibernating yellow-bellied marmots (Marmota flaviventris). Comp Biochem Physiol A 134:101–114. https://doi.org/10.1016/S1095-6433(02)00219-2
Arnold W, Heldmaier G, Ortmann S, Pohl H, Ruf T, Steinlechner S (1991) Ambient temperatures in hibernacula and their energetic consequences for alpine marmots Marmota marmota. J Therm Biol 16:223–226. https://doi.org/10.1016/0306-4565(91)90029-2
Audet D, Thomas DW (1996) Evaluation of the accuracy of body temperature measurement using external radio transmitters. Can J Zool 74(9):1778–1781. https://doi.org/10.1139/z96-196
Baerwald EF, Barclay RM (2011) Patterns of activity and fatality of migratory bats at a wind energy facility in Alberta, Canada. J Wildl Manag 75(5):1103–1114. https://doi.org/10.1002/jwmg.147
Bagg AM, Gunn WWH, Miller DS, Nichols JT, Smith W, Wolfarth FP (1950) Barometric pressure-patterns and spring bird migration. Wilson Bull 62(1):5–19
Bailey HP (1979) Semi-arid climates: their definition and distribution. In Agriculture in semi-arid environments (eds. Hall, A. E., Cannell, G. H., and Lawton, H. W., pp. 73–97. Berlin
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 Mammal 77:1102–1106. https://doi.org/10.2307/1382791
Baumber J, South FE, Ferren L, Zatzman ML (1971) A possible basis for periodic arousals during hibernation: Accumulation of ketone bodies. Life Sci 10(8):463–467. https://doi.org/10.1016/0024-3205(71)90308-0
Ben-Hamo M, Muñoz-Garcia A, Williams JB, Korine C, Pinshow B (2013) Waking to drink: rates of evaporative water loss determine arousal frequency in hibernating bats. J Exp Biol 216(4):573–577. https://doi.org/10.1242/jeb.078790
Bernard RF, Willcox EV, Jackson RT, Brown VA, McCracken GF (2021) Feasting, not fasting: winter diets of cave hibernating bats in the United States. Front Zool 18:1–3
Bieber C, Ruf T (2009) Summer dormancy in edible dormice (Glis glis) without energetic constraints. Naturwissenschaften 96:165–171. https://doi.org/10.1007/s00114-008-0471-z
Blejwas KM, Pendleton GW, Kohan ML, Beard LO (2021) The Milieu Souterrain Superficiel as hibernation habitat for bats: implications for white-nose syndrome. J Mammal 102(4):1110–1127. https://doi.org/10.1093/jmammal/gyab050
Boratyński JS, Willis CKR, Jefimow M, Wojciechowski MS (2015) Huddling reduces evaporative water loss in torpid Natterer’s bats, Myotis nattereri. Comp Biochem Physiol A 179:125–132. https://doi.org/10.1016/j.cbpa.2014.09.035
Boyles JG, Brack V (2009) Modeling survival rates of hibernating mammals with individual-based models of energy expenditure. J Mammal 90(1):9–16. https://doi.org/10.1644/08-MAMM-A-205.1
Boyles JG, McKechnie AE (2010) Energy conservation in hibernating endotherms: why suboptimal temperatures are optimal. Ecol Modell 221(12):1644–1647. https://doi.org/10.1016/j.ecolmodel.2010.03.018
Boyles JG, Dunbar MB, Whitaker JO (2006) Activity following arousal in winter in north American vespertilionid bats. Mammal Rev 36(4):267–280. https://doi.org/10.1111/j.1365-2907.2006.00095.x
Boyles JG, Storm JJ, Brack V (2008) Thermal benefits of clustering during hibernation: a field test of competing hypotheses on Myotis sodalis. Funct Ecol 22(4):632–636
Brack V Jr, Twente JW (1985) The duration of the period of hibernation of three species of vespertilionid bats. I. Field studies. Can J Zool 63(12):2952–2954. https://doi.org/10.1139/z85-442
Brice T, Hall T (2016) Vapor pressure. National Weather Service. URL http://www.srh.noaa.gov/epz/?n=wxcalc_vaporpressure
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 183:859–866
Czenze ZJ, Jonasson KA, Willis CK (2017) Thrifty females, frisky males: winter energetics of hibernating bats from a cold climate. Physiol Biochem Zool 90(4):502–511. https://doi.org/10.1086/692623
Daan S, Barnes BM, Strijkstra AM (1991) Warming up for sleep?—ground squirrels sleep during arousals from hibernation. Neurosci Lett 128(2):265–268. https://doi.org/10.1016/0304-3940(91)90276-Y
Dunbar MB, Brigham RM (2010) Thermoregulatory variation among populations of bats along a latitudinal gradient. J Comp Physiol B 180:885–893
Dunbar MB, Tomasi TE (2006) Arousal patterns, metaboilc rate, and an energy budget of eastern red bats (Lasiurus borealis) in winter. J Mammal 87(6):1096–1102. https://doi.org/10.1644/05-MAMM-A-254R3.1
Environment Canada (2023) Environment and Climate Change Canada Historical Climate Data. https://climate.weather.gc.ca/index_e.html. Accessed 16 May 2023
French AR (1977) Circannual rhythmicity and entrainment of surface activity in the hibernator, Perognathus longimembris. J Mammal 58(1):37–43. https://doi.org/10.2307/1379725
French AR (1985) Allometries of the durations of torpid and euthermic intervals during mammalian hibernation: a test of the theory of metabolic control of the timing of changes in body temperature. J Comp Physiol B 156:13–19
Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274. https://doi.org/10.1146/annurev.physiol.66.032102.115105
Geiser F (2021) Ecological physiology of daily torpor and hibernation. Springer, Cham, Switzerland
Geiser F, Broome LS (1993) The effect of temperature on the pattern of torpor in a marsupial hibernator. J Comp Physiol B 163:133–137
Geiser F, Kenagy GJ (1988) Torpor duration in relation to temperature and metabolism in hibernating ground squirrels. Physiol Zool 61(5):442–449. https://doi.org/10.1086/physzool.61.5.30161266
Halsall AL, Boyles JG, Whitaker JO (2012) Body temperature patterns of big brown bats during winter in a building hibernaculum. J Mammal 93(2):497–503. https://doi.org/10.1644/11-MAMM-A-262.1
Hayman DT, Cryan PM, Fricker PD, Dannemiller NG (2017) Long-term video surveillance and automated analyses reveal arousal patterns in groups of hibernating bats. Methods Ecol Evol 8(12):1813–1821. https://doi.org/10.1111/2041-210X.12823
Heldmaier G, Ortmann S, Körtner G (1993) Energy requirement of hibernating alpine marmots. In: Carey C, Florant GL, Wunder MB, Horwitz BA (eds) Life in the cold — ecological, physiological, and molecular mechanisms. Boulder, Colorado, pp 175–183
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
Hope PR, Jones G (2013) An entrained circadian cycle of peak activity in a population of hibernating bats. J Mammal 94(2):497–505. https://doi.org/10.1644/12-MAMM-A-095.1
Humphries MM, Thomas DW, Speakman JR (2002) Climate-mediated energetic constraints on the distribution of hibernating mammals. Lett Nat 418:313–316
Humphries MM, Thomas DW, Kramer DL (2003) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76(2):165–179. https://doi.org/10.1086/367950
Humphries MM, Speakman JR, Thomas DW (2006) Temperature, hibernation energetics, and the cave and continental distributions of little brown myotis. In: Zubaid A, McCracken GF, Kunz TH (eds) Functional and evolutionary ecology of bats. Oxford University Press, New York, pp 23–37
Jonasson KA, Willis CKR (2012) Hibernation energetics of free-ranging little brown bats. J Exp Biol 215(12):2141–2149. https://doi.org/10.1242/jeb.066514
Klüg-Baerwald BJ, Brigham RM (2017) Hung out to dry? Intraspecific variation in water loss in a hibernating bat. Oecologia 183:977–985. https://doi.org/10.1007/s00442-017-3837-0
Klüg-Baerwald BJ, Gower LE, Lausen C, Brigham RM (2016) Environmental correlates and energetics of winter flight by bats in Southern Alberta, Canada. Can J Zool 94(12):829–836. https://doi.org/10.1139/cjz-2016-0055
Klüg-Baerwald BJ, Lausen CL, Brigham RM (2017) Home is where you hang your bat: winter roost selection by prairie-living big brown bats (Eptesicus fuscus). J Mammal 98(3):752–760. https://doi.org/10.1093/jmammal/gyx039
Klüg-Baerwald BJ, Lausen CL, Wissel B, Brigham RM (2021) Meet you at the local watering hole? Evidence of dehydration in and use of an artificial water resource by hibernating bats in the prairies. Act Chiropterol 23(2):405–411. https://doi.org/10.3161/15081109ACC2021.23.2.010
Körtner G, Song X, Geiser F (1998) Rhythmicity of torpor in a marsupial hibernator, the mountain pygmy-possum (Burramysparvus), under natural and laboratory conditions. J Comp Physiol B 168:631–638
Kurta A (2014) The misuse of relative humidity in ecological studies of hibernating bats. Acta Chiropterol 16(1):249–254. https://doi.org/10.3161/150811014X683444
Kurta A, Baker RH (1990) Eptesicus fuscus. Mammalian Species 356:1–10
Lausen CL, Barclay RMR (2006) Winter bat activity in the Canadian prairies. Can J Zool 84(8):1079–1086. https://doi.org/10.1139/z06-093
Lee K, So H, Gwag T, Ju H, Lee JW, Yamashita M, Choi I (2010) Molecular mechanism underlying muscle mass retention in hibernating bats: role of periodic arousal. J Cell Physiol 222(2):313–319. https://doi.org/10.1002/jcp.21952
Lemen CA, Freeman PW, White JA (2016) Acoustic evidence of bats using rock crevices in winter: a call for more research on winter roosts in North America. Trans Neb Acad Sci Affil Soc 36:9–13
McGuire LP, Johnson EM, Frick WF, Boyles JG (2021) Temperature alone is insufficient to understand hibernation energetics. J Exp Biol. https://doi.org/10.1242/jeb.239772
Michaelsen TC, Olsen O, Grimstad KJ (2013) Roosts used by bats in late autumn and winter at northern latitudes in Norway. Folia Zool 62(4):297–303. https://doi.org/10.25225/fozo.v62.i4.a7.2013
Moosman PR, Andersen PR, Frasier MG (2017) Use of rock-crevices in winter by big brown bats and eastern small-footed bats in the Appalachian Ridge and Valley of Virginia. Banisteria 48:9–13
Neubaum DJ, Neubaum MA, Ellison LE, O’Shea TJ (2005) Survival and condition of big brown bats (Eptesicus fuscus) after radiotagging. J Mammal 86(1):95–98. https://doi.org/10.1644/1545-1542(2005)086%3C0095:SACOBB%3E2.0.CO;2
Neubaum DJ, O’Shea TJ, Wilson KR (2006) Autumn migration and selection of rock crevices as hibernacula by big brown bats in Colorado. J Mammal 87(3):470–479. https://doi.org/10.1644/05-MAMM-A-252R1.1
Paige KN (1995) Bats and barometric pressure: conserving limited energy and tracking insects from the roost. Funct Ecol 9(3):463–467. https://doi.org/10.2307/2390010
Park KJ, Jones G, Ransome RD (2000) Torpor, arousal and activity of hibernating greater horseshoe bats (Rhinolophus ferrumequinum). Funct Ecol 14(5):580–588
Perry RW (2013) A review of factors affecting cave climates for hibernating bats in temperate North America. Environ Rev 21(1):28–39. https://doi.org/10.1139/er-2012-0042
R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
Ruf T, Bieber C (2023) Why hibernate? Predator avoidance in the edible dormouse. Mamm Res 68:1–11. https://doi.org/10.1007/s13364-022-00652-4
Ruf T, Geiser F (2015) Daily torpor and hibernation in birds and mammals. Biol Rev 90(3):891–926. https://doi.org/10.1111/brv.12137
Rysgaard GN (1942) A study of the cave bats of Minnesota with especial reference to the large brown bat, Eptesicus fuscus fuscus (Beauvois). Am Midl Nat 28(1):245–267. https://doi.org/10.2307/2420702
Sikes RS (2016) 2016 guidelines of the American Society of mammalogists for the use of wild mammals in research and education. J Mammal 97(3):663–688. https://doi.org/10.1093/jmammal/gyw078
Swanson G, Evans C (1936) The hibernation of certain bats in southern Minnesota. J Mammal 17(1):39–43. https://doi.org/10.2307/1374548
Thomas DW (1993) Lack of evidence for a biological alarm clock in bats (Myotis spp.) hibernating under natural conditions. Can J Zool 71(1):1–3. https://doi.org/10.1139/z93-001
Thomas DW (1995) The physiological ecology of hibernation in vespertilionid bats. Symp Zool Soc Lond 67:233–244
Thomas DW, Cloutier D (1992) Evaporative water loss by hibernating little brown bats, Myotis lucifugus. Physiol Zool 65(2):443–456. https://doi.org/10.1086/physzool.65.2.30158262
Thomas DW, Geiser F (1997) Periodic arousals in hibernating mammals: is evaporative water loss involved? Funct Ecol 11(5):585–591. https://doi.org/10.1046/j.1365-2435.1997.00129.x
Thomas AJ, Jacobs DS (2013) Factors influencing the emergence times of sympatric insectivorous bat species. Acta Chiropterol 15(1):121–132. https://doi.org/10.3161/150811013X667920
Thomas DW, Fenton MB, Barclay RMR (1979) Social behavior of the little brown bat, Myotis lucifugus: I. mating behaviour. Behav Ecol Sociobiol 6(2):129–136
Thomas DW, Dorais M, Bergeron JM (1990) Winter energy budgets and cost of arousals for hibernating little brown bats, Myotis lucifugus. J Mammal 71(3):475–479. https://doi.org/10.2307/1381967
Turbill C (2008) Winter activity of Australian tree-roosting bats: influence of temperature and climatic patterns. J Zool 276(3):285–290. https://doi.org/10.1111/j.1469-7998.2008.00487.x
US Climate Data (2023) Climate Terre Haute – Indiana. https://www.usclimatedata.com/climate/terre-haute/indiana/united-states/usin0660. Accessed 16 May 2023
Wang LCH, Wolowyk MW (1988) Torpor in mammals and birds. Can J Zool 66(1):133–137. https://doi.org/10.1139/z88-017
Webb PI, Speakman JR, Racey PA (1996) How hot is a hibernaculum? A review of the temperatures at which bats hibernate. Can J Zool 74(4):761–765. https://doi.org/10.1139/z96-087
Whitaker JO Jr, Gummer SL (1992) Hibernation of the big brown bat, Eptesicus fuscus, in buildings. J Mammal 73(2):312–316. https://doi.org/10.2307/1382062
Whitaker JO Jr, Rissler LJ (1992) Winter activity of bats at a mine entrance in Vermillion County, Indiana. Am Midl Nat 1:52–59. https://www.jstor.org/stable/2426321
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
Willis CKR, Turbill C, Geiser F (2005) Torpor and thermal energetics in a tiny Australian vespertilionid, the little forest bat (Vespadelus vulturnus). J Comp Physiol B 175:479–486
Yacoe ME (1983) Maintenance of the pectoralis muscle during hibernation in the big brown bat, Eptesicus fuscus. J Comp Physiol 152(1):97–104
Acknowledgements
We thank V. Rukas, K. Scott, L. Gower, A. Moltzahn, and N. Besler for field assistance; E. Baerwald, J. Boyles and F. Geiser for manuscript review; the staff at Dinosaur Provincial Park for field logistics and in-kind support; Wildlife Conservation Society Canada for sponsorship and administrative assistance; and the Natural Sciences and Engineering Research Council of Canada (Canadian Graduate Scholarship to B.J.K.), University of Regina, and Alberta Conservation Association (ACA Research Grant to C.L.L. and B.J.K.) for funding. We would also like to thank the three anonymous reviewers who’s thoughtful and constructive comments greatly improved the quality of the manuscript.
Funding
This work was supported by the Natural Sciences and Engineering Research Council of Canada [Canadian Graduate Scholarship to B.J.K., Discovery Grant to R.M.B.], the University of Regina [Research Grant to B.J.K.], and Alberta Conservation Association [ACA Research Grant to B.J.K and C.L.L.].
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B.J.K conceived the work; collected, analyzed, and interpreted the data; and drafted the original article. C.L.L. and R.M.B conceived the work and revised the article; S.M.B. interpreted results and revised the original manuscript. All authors approved the final version of article to be published.
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Klüg-Baerwald, B.J., Lausen, C.L., Burns, S.M. et al. Physiological and behavioural adaptations by big brown bats hibernating in dry rock crevices. J Comp Physiol B (2024). https://doi.org/10.1007/s00360-024-01546-4
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DOI: https://doi.org/10.1007/s00360-024-01546-4