Hibernation and daily torpor in Australian and New Zealand bats: does the climate zone matter?1
Fritz Geiser
A K , Artiom Bondarenco A , Shannon E. Currie A B , Anna C. Doty A C , Gerhard Körtner A , Bradley S. Law D , Chris R. Pavey A E , Alexander Riek A F , Clare Stawski A G , Christopher Turbill A H , Craig K. R. Willis A I and R. Mark Brigham A J
+ Author Affiliations
- Author Affiliations
A Centre for Behavioural and Physiological Ecology, Zoology CO2, University of New England, Armidale, NSW 2351, Australia.
B Department of Evolutionary Ecology, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke Straße 17, 10315 Berlin, Germany.
C Department of Biology, California State University Bakersfield, Bakersfield, CA 93311, USA.
D NSW Primary Industries, Parramatta, NSW 2124, Australia.
E CSIRO Land and Water, PMB 44, Winnellie, NT 0822, Australia.
F Institute of Animal Welfare and Animal Husbandry, Friedrich-Loeffler-Institut, Dörnbergstraße 25/27, 29223 Celle, Germany.
G Department of Biology, Norwegian University of Science and Technology, Trondheim 7491, Norway.
H Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW 2753, Australia.
I Department of Biology and Centre for Forest Interdisciplinary Research, University of Winnipeg, Winnipeg, MB R3B 2E9, Canada.
J Department of Biology, University of Regina, Regina, SK S4S 0A2, Canada.
K Corresponding author. Email: fgeiser@une.edu.au
Australian Journal of Zoology 67(6) 316-330 https://doi.org/10.1071/ZO20025
Submitted: 3 May 2020 Accepted: 18 August 2020 Published: 14 September 2020
Abstract
We aim to summarise what is known about torpor use and patterns in Australian and New Zealand (ANZ) bats from temperate, tropical/subtropical and arid/semiarid regions and to identify whether and how they differ. ANZ bats comprise ~90 species from 10 families. Members of at least nine of these are known to use torpor, but detailed knowledge is currently restricted to the pteropodids, molossids, mystacinids, and vespertilionids. In temperate areas, several species can hibernate (use a sequence of multiday torpor bouts) in trees or caves mostly during winter and continue to use short bouts of torpor for the rest of the year, including while reproducing. Subtropical vespertilionids also use multiday torpor in winter and brief bouts of torpor in summer, which permit a reduction in foraging, probably in part to avoid predators. Like temperate-zone vespertilionids they show little or no seasonal change in thermal energetics during torpor, and observed changes in torpor patterns in the wild appear largely due to temperature effects. In contrast, subtropical blossom-bats (pteropodids) exhibit more pronounced daily torpor in summer than winter related to nectar availability, and this involves a seasonal change in physiology. Even in tropical areas, vespertilionids express short bouts of torpor lasting ~5 h in winter; summer data are not available. In the arid zone, molossids and vespertilionids use torpor throughout the year, including during desert heat waves. Given the same thermal conditions, torpor bouts in desert bats are longer in summer than in winter, probably to minimise water loss. Thus, torpor in ANZ bats is used by members of all or most families over the entire region, its regional and seasonal expression is often not pronounced or as expected, and it plays a key role in energy and water balance and other crucial biological functions that enhance long-term survival by individuals.
Additional keywords: body temperature, fattening, heterothermy, metabolic rate, passive rewarming, regions, roosts, season.
References
Aldridge, H. D. J. N., and Brigham, R. M. (1988). Load carrying and maneuverability in insectivorous bats: a test of the 5% “rule” of radio telemetry. Journal of Mammalogy 69, 379–382.| Load carrying and maneuverability in insectivorous bats: a test of the 5% “rule” of radio telemetry.Crossref | GoogleScholarGoogle Scholar |
Ancillotto, L., Budinski, I., Nardone, V., Di Salvo, I., Della Corte, M., Bosso, L., Conti, P., and Russo, D. (2018). What is driving the range expansion in a common bat? Hints from thermoregulation and habitat selection. Behavioural Processes 157, 540–546.
| What is driving the range expansion in a common bat? Hints from thermoregulation and habitat selection.Crossref | GoogleScholarGoogle Scholar | 29870799PubMed |
Arlettaz, R., Ruchet, C., Aeschimann, J., Brun, E., Genoud, M., and Vogel, P. (2000). Physiological traits affecting the distribution and wintering strategy of the bat Tadarida teniotis. Ecology 81, 1004–1014.
| Physiological traits affecting the distribution and wintering strategy of the bat Tadarida teniotis.Crossref | GoogleScholarGoogle Scholar |
Barclay, R. M. R., Lausen, C. L., and Hollis, L. (2001). What’s hot and what’s not: defining torpor in free-ranging birds and mammals. Canadian Journal of Zoology 79, 1885–1890.
| What’s hot and what’s not: defining torpor in free-ranging birds and mammals.Crossref | GoogleScholarGoogle Scholar |
Barnes, B. M. (1989). Freeze avoidance in a mammal: body temperatures below 0°C in an Arctic hibernator. Science 244, 1593–1595.
| Freeze avoidance in a mammal: body temperatures below 0°C in an Arctic hibernator.Crossref | GoogleScholarGoogle Scholar | 2740905PubMed |
Bartels, W., Law, B. S., and Geiser, F. (1998). Daily torpor and energetics in a tropical mammal, the northern blossom-bat Macroglossus minimus (Megachiroptera). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 168, 233–239.
| Daily torpor and energetics in a tropical mammal, the northern blossom-bat Macroglossus minimus (Megachiroptera).Crossref | GoogleScholarGoogle Scholar | 9591364PubMed |
Bartholomew, G. A., Leitner, P., and Nelson, J. E. (1964). Body temperature, oxygen consumption, and heart rate in three species of Australian flying foxes. Physiological Zoology 37, 179–198.
| Body temperature, oxygen consumption, and heart rate in three species of Australian flying foxes.Crossref | GoogleScholarGoogle Scholar |
Baudinette, R. V., Churchill, S. K., Christian, K. A., Nelson, J. E., and Hudson, P. J. (2000). Energy, water balance, and roost environment in three Australian cave-dwelling bats. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 170, 439–446.
| Energy, water balance, and roost environment in three Australian cave-dwelling bats.Crossref | GoogleScholarGoogle Scholar | 11083527PubMed |
Bieber, C., Lebl, K., Stalder, G., Geiser, F., and Ruf, T. (2014). Body mass dependent use of hibernation: why not prolong the active season, if they can? Functional Ecology 28, 167–177.
| Body mass dependent use of hibernation: why not prolong the active season, if they can?Crossref | GoogleScholarGoogle Scholar |
Bondarenco, A. (2014). Torpor and thermal energetics in Australian arid zone bats. Ph.D. Thesis, University of New England, Armidale,
Bondarenco, A., Körtner, G., and Geiser, F. (2013). Some like it cold: summer torpor by freetail bats in the Australian arid zone. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 183, 1113–1122.
| Some like it cold: summer torpor by freetail bats in the Australian arid zone.Crossref | GoogleScholarGoogle Scholar | 23989287PubMed |
Bondarenco, A., Körtner, G., and Geiser, F. (2014). Hot bats: extreme thermal tolerance in a desert heat wave. Naturwissenschaften 101, 679–685.
| Hot bats: extreme thermal tolerance in a desert heat wave.Crossref | GoogleScholarGoogle Scholar | 25005222PubMed |
Bondarenco, A., Körtner, G., and Geiser, F. (2016). How to keep cool in a hot desert: torpor in two species of free-ranging bats in summer. Temperature 3, 476–483.
| How to keep cool in a hot desert: torpor in two species of free-ranging bats in summer.Crossref | GoogleScholarGoogle Scholar |
Brigham, R. M. (1987). The significance of winter activity by the big brown bat (Eptesicus fuscus): the influence of energy reserves. Canadian Journal of Zoology 65, 1240–1242.
| The significance of winter activity by the big brown bat (Eptesicus fuscus): the influence of energy reserves.Crossref | GoogleScholarGoogle Scholar |
Brigham, R. M., and Geiser, F. (1998). Seasonal activity patterns of Nyctophilus bats based on mist-net captures. Australian Mammalogy 20, 349–352.
Bureau of Meteorology (BOM) (2020). Climate Classification Maps. Available at: bom.gov.au/climate/data/ [accessed 1 July 2020]
Chenery, M. (2018). Behaviour and physiology of free-ranging little forest bats (Vepadelus vulturnus) during winter. B.Sc.(Honours) Thesis, University of New England, Armidale.
Churchill, S. (1998). ‘Australian Bats.’ (Reed: Sydney.)
Coburn, D. K., and Geiser, F. (1998). Seasonal changes in energetics and torpor patterns in the subtropical blossom-bat Syconycteris australis (Megachiroptera). Oecologia 113, 467–473.
| Seasonal changes in energetics and torpor patterns in the subtropical blossom-bat Syconycteris australis (Megachiroptera).Crossref | GoogleScholarGoogle Scholar | 28308026PubMed |
Currie, S. E. (2018). No effect of season on the electrocardiogram of long eared bats (Nyctophilus gouldi) during torpor. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 188, 695–705.
| No effect of season on the electrocardiogram of long eared bats (Nyctophilus gouldi) during torpor.Crossref | GoogleScholarGoogle Scholar | 29623413PubMed |
Currie, S. E., Körtner, G., and Geiser, F. (2014). Heart rate as a predictor of metabolic rate in heterothermic bats. The Journal of Experimental Biology 217, 1519–1524.
| Heart rate as a predictor of metabolic rate in heterothermic bats.Crossref | GoogleScholarGoogle Scholar | 24436390PubMed |
Currie, S. E., Körtner, G., and Geiser, F. (2015a). Measuring subcutaneous temperature and differential rates of rewarming from hibernation and daily torpor in two species of bats. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 190, 26–31.
| Measuring subcutaneous temperature and differential rates of rewarming from hibernation and daily torpor in two species of bats.Crossref | GoogleScholarGoogle Scholar |
Currie, S. E., Noy, K., and Geiser, F. (2015b). Passive rewarming from torpor in hibernating bats: minimizing metabolic costs and cardiac demands. The American Journal of Physiology 308, R34–R41.
Currie, S. E., Stawski, C., and Geiser, F. (2018). Cold-hearted bats: uncoupling of heart rate and metabolism during torpor at subzero temperatures. The Journal of Experimental Biology 221, jeb170894.
| Cold-hearted bats: uncoupling of heart rate and metabolism during torpor at subzero temperatures.Crossref | GoogleScholarGoogle Scholar | 29113989PubMed |
Currie, S. E., Boonman, A., Troxell, S., Yovel, Y., and Voigt, C. C. (2020). Echolocation at high intensity imposes metabolic costs on flying bats. Nature Ecology & Evolution , .
| Echolocation at high intensity imposes metabolic costs on flying bats.Crossref | GoogleScholarGoogle Scholar |
Czenze, Z. J., and Dunbar, M. (2020). Body mass affects short-term heterothermy in Neotropical bats. Biotropica , .
| Body mass affects short-term heterothermy in Neotropical bats.Crossref | GoogleScholarGoogle Scholar |
Czenze, Z. J., Jonasson, K. A., and Willis, C. K. R. (2017a). Thrifty females, frisky males: winter energetics of hibernating bats from a cold climate. Physiological and Biochemical Zoology 90, 502–511.
| Thrifty females, frisky males: winter energetics of hibernating bats from a cold climate.Crossref | GoogleScholarGoogle Scholar | 28641050PubMed |
Czenze, Z. J., Brigham, R. M., Hickey, A. J. R., and Parsons, S. (2017b). Cold and alone? Roost choice and season affect torpor patterns in lesser long-eared bats. Oecologia 183, 1–8.
| Cold and alone? Roost choice and season affect torpor patterns in lesser long-eared bats.Crossref | GoogleScholarGoogle Scholar | 27561779PubMed |
Czenze, Z. J., Brigham, R. M., Hickey, A. J. R., and Parsons, S. (2017c). Winter climate affects torpor patterns and roost choice in New Zealand lesser short-tailed bats. Journal of Zoology 303, 236–243.
| Winter climate affects torpor patterns and roost choice in New Zealand lesser short-tailed bats.Crossref | GoogleScholarGoogle Scholar |
Czenze, Z. J., Brigham, R. M., Hickey, A. J. R., and Parsons, S. (2017d). Stressful summers? Torpor expression differs between high- and low-latitude populations of bats. Journal of Mammalogy 98, 1249–1255.
| Stressful summers? Torpor expression differs between high- and low-latitude populations of bats.Crossref | GoogleScholarGoogle Scholar |
Dawson, W. R., and Hudson, J. W. (1970). Birds. In ‘Comparative Physiology of Thermoregulation. Vol. 1’. (Ed. G. C. Whittow.) pp. 223–310. (Academic Press: New York.)
Dixon, K. J., and Rose, R. W. (2003). Thermal energetics of Nyctophilus geoffroyi (Chiroptera: Vespertilionidae) at the southern limit of its distribution. Australian Journal of Zoology 51, 43–50.
| Thermal energetics of Nyctophilus geoffroyi (Chiroptera: Vespertilionidae) at the southern limit of its distribution.Crossref | GoogleScholarGoogle Scholar |
Doty, A. C., Stawski, C., Currie, S. E., and Geiser, F. (2016a). Black or white? Physiological implications of roost colour and choice in a microbat. Journal of Thermal Biology 60, 162–170.
| Black or white? Physiological implications of roost colour and choice in a microbat.Crossref | GoogleScholarGoogle Scholar | 27503729PubMed |
Doty, A. C., Stawski, C., Law, B. S., and Geiser, F. (2016b). Post-wildfire physiological ecology of an Australian microbat. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 186, 937–946.
| Post-wildfire physiological ecology of an Australian microbat.Crossref | GoogleScholarGoogle Scholar | 27245066PubMed |
Dunbar, M. B., and Brigham, R. M. (2010). Thermoregulatory variation among populations of bats along a latitudinal gradient. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 180, 885–893.
| Thermoregulatory variation among populations of bats along a latitudinal gradient.Crossref | GoogleScholarGoogle Scholar | 20213177PubMed |
Dwyer, P. D. (1964). Seasonal changes in activity and weight of Miniopterus schreibersii blepotis (Chiroptera) in northeastern New South Wales. Australian Journal of Zoology 12, 52–69.
| Seasonal changes in activity and weight of Miniopterus schreibersii blepotis (Chiroptera) in northeastern New South Wales.Crossref | GoogleScholarGoogle Scholar |
Geiser, F. (2006). Energetics, thermal biology, and torpor in Australian bats. In ‘Functional and Evolutionary Ecology of Bats’. (Eds A. Zubaid, G. F. McCracken, and T. H. Kunz.) pp. 5–22. (Oxford University Press: New York.)
Geiser, F. (2020). Seasonal expression of avian and mammalian daily torpor and hibernation: not a simple summer–winter affair. Frontiers in Physiology 11, 436.
| Seasonal expression of avian and mammalian daily torpor and hibernation: not a simple summer–winter affair.Crossref | GoogleScholarGoogle Scholar | 32508673PubMed |
Geiser, F., and Baudinette, R. V. (1987). Seasonality of torpor and thermoregulation in three dasyurid marsupials. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 157, 335–344.
| Seasonality of torpor and thermoregulation in three dasyurid marsupials.Crossref | GoogleScholarGoogle Scholar |
Geiser, F., and Brigham, R. M. (2000). Torpor, thermal biology, and energetics in Australian long-eared bats (Nyctophilus). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 170, 153–162.
| Torpor, thermal biology, and energetics in Australian long-eared bats (Nyctophilus).Crossref | GoogleScholarGoogle Scholar | 10791575PubMed |
Geiser, F., Drury, R. L., Körtner, G., Turbill, C., Pavey, C. R., and Brigham, R. M. (2004). Passive rewarming from torpor in mammals and birds: energetic, ecological and evolutionary implications. In ‘Life in the Cold: Evolution, Mechanisms, Adaptation, and Application. Twelfth International Hibernation Symposium. Biological Papers of the University of Alaska #27’. (Eds B. M. Barnes, and H. V. Carey.) pp. 51–62. (Institute of Arctic Biology, University of Alaska: Fairbanks, AK.)
Geiser, F., Stawski, C., Bondarenco, A., and Pavey, C. R. (2011). Torpor and activity in a free-ranging tropical bat: implications for the distribution and conservation of mammals? Naturwissenschaften 98, 447–452.
| Torpor and activity in a free-ranging tropical bat: implications for the distribution and conservation of mammals?Crossref | GoogleScholarGoogle Scholar | 21416134PubMed |
Grimpo, K., Legler, K., Heldmaier, G., and Exner, C. (2013). That’s hot: golden spiny mice display torpor even at high ambient temperatures. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 183, 567–581.
| That’s hot: golden spiny mice display torpor even at high ambient temperatures.Crossref | GoogleScholarGoogle Scholar | 23212435PubMed |
Hall, L. S. (1982). The effect of cave microclimate on winter roosting behaviour in the bat, Miniopterus schreibersii blepotis. Australian Journal of Ecology 7, 129–136.
| The effect of cave microclimate on winter roosting behaviour in the bat, Miniopterus schreibersii blepotis.Crossref | GoogleScholarGoogle Scholar |
Hall, L. S. (1984). And then there were bats. In ‘Vertebrate Zoogeography and Evolution in Australasia’. (Eds M. Archer, and G. Clayton.) pp. 837–852. (Heperian Press: Carlisle.)
Hall, L. S., and Pettigrew, J. (1995). The bat with the stereo nose. Australian Natural History 24, 26–28.
Hall L. S., Richards G. C. (1979). Bats of eastern Australia. Queensland Museum booklet no. 12.
Hand, S. J., Beck, R. M. D., Archer, M., Simmons, A. B., Gunnell, G. F., Scofield, R. P., Tennyson, A. J. D., DePietri, V. L., Salisbury, S. W., and Worthy, T. H. (2018). A new large-bodied omnivorous bat (Nocilionidea: Mystacinidae) reveals lost morphological and ecological diversity since the Miocene in New Zealand. Scientific Reports 8, 235.
| A new large-bodied omnivorous bat (Nocilionidea: Mystacinidae) reveals lost morphological and ecological diversity since the Miocene in New Zealand.Crossref | GoogleScholarGoogle Scholar | 29321543PubMed |
Heldmaier, G., and Steinlechner, S. (1981). Seasonal pattern and energetics of short daily torpor in the Djungarian hamster, Phodopus sungorus. Oecologia 48, 265–270.
| Seasonal pattern and energetics of short daily torpor in the Djungarian hamster, Phodopus sungorus.Crossref | GoogleScholarGoogle Scholar | 28309811PubMed |
Heller, H. C., and Hammel, H. T. (1972). CNS control of body temperature during hibernation. Comparative Biochemistry and Physiology Part A: Physiology 41, 349–359.
| CNS control of body temperature during hibernation.Crossref | GoogleScholarGoogle Scholar |
Henshaw, R. E. (1970). Thermoregulation in bats. In ‘About Bats’. (Eds B. H. Slaugher, and D. W. Walton.) pp. 188–232. (Southern Methodist University Press: Dallas.)
Hetem, R. S., Maloney, S. K., Fuller, A., and Mitchell, D. (2016). Heterothermy in large mammals: inevitable or implemented? Biological Reviews of the Cambridge Philosophical Society 91, 187–205.
| Heterothermy in large mammals: inevitable or implemented?Crossref | GoogleScholarGoogle Scholar | 25522232PubMed |
Hock, R. J. (1951). The metabolic rates and body temperatures of bats. The Biological Bulletin 101, 289–299.
| The metabolic rates and body temperatures of bats.Crossref | GoogleScholarGoogle Scholar |
Hosken, D. J. (1997). Thermal biology and metabolism of the greater long-eared bat, Nyctophilus major (Chiroptera: Vespertilionidae). Australian Journal of Zoology 45, 145–156.
| Thermal biology and metabolism of the greater long-eared bat, Nyctophilus major (Chiroptera: Vespertilionidae).Crossref | GoogleScholarGoogle Scholar |
Hosken, D. J., and Withers, P. C. (1997). Temperature regulation and metabolism of an Australian bat, Chalinolobus gouldii (Chiroptera: Vespertilionidae) when euthermic and torpid. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 167, 71–80.
| Temperature regulation and metabolism of an Australian bat, Chalinolobus gouldii (Chiroptera: Vespertilionidae) when euthermic and torpid.Crossref | GoogleScholarGoogle Scholar | 9051907PubMed |
Hudson, J. W., and Scott, I. M. (1979). Daily torpor in the laboratory mouse Mus musculus var albino. Physiological Zoology 52, 205–218.
| Daily torpor in the laboratory mouse Mus musculus var albino.Crossref | GoogleScholarGoogle Scholar |
Jonasson, K. A., and Willis, C. K. R. (2012). Hibernation energetics of free-ranging little brown bats. The Journal of Experimental Biology 215, 2141–2149.
| Hibernation energetics of free-ranging little brown bats.Crossref | GoogleScholarGoogle Scholar | 22623203PubMed |
Körtner, G., Riek, A., Pavey, C., and Geiser, F. (2016). Activity patterns and torpor in two free-ranging carnivorous marsupials in arid Australia in relation to precipitation, reproduction and ground cover. Journal of Mammalogy 97, 1555–1564.
| Activity patterns and torpor in two free-ranging carnivorous marsupials in arid Australia in relation to precipitation, reproduction and ground cover.Crossref | GoogleScholarGoogle Scholar |
Kulzer, E., Nelson, J. E., McKean, J., and Möhres, F. P. (1970). Untersuchungen über die Temperaturregulation australischer Fledermäuse (Microchiroptera). Zeitschrift fur Vergleichende Physiologie 69, 426–451.
| Untersuchungen über die Temperaturregulation australischer Fledermäuse (Microchiroptera).Crossref | GoogleScholarGoogle Scholar |
Lebl, K., Bieber, C., Adamik, P., Fietz, J., Morris, P., Pilastro, A., and Ruf, T. (2011). Survival rates in a small hibernator, the edible dormouse: a comparison across Europe. Ecography 34, 683–692.
| Survival rates in a small hibernator, the edible dormouse: a comparison across Europe.Crossref | GoogleScholarGoogle Scholar | 23447711PubMed |
Leitner, P., and Nelson, J. E. (1967). Body temperature, oxygen consumption and heart rate in the Australian false vampire bat, Macroderma gigas. Comparative Biochemistry and Physiology 21, 65–74.
| Body temperature, oxygen consumption and heart rate in the Australian false vampire bat, Macroderma gigas.Crossref | GoogleScholarGoogle Scholar | 6033844PubMed |
Levy, O., Dayan, T., and Kronfeld-Schor, N. (2011). Adaptive thermoregulation in golden spiny mice: the influence of season and food availability on body temperature. Physiological and Biochemical Zoology 84, 175–184.
| Adaptive thermoregulation in golden spiny mice: the influence of season and food availability on body temperature.Crossref | GoogleScholarGoogle Scholar | 21460528PubMed |
Liu, J.-N., and Karasov, W. H. (2011). Hibernation in warm hibernacula by free-ranging Formosan leaf-nosed bats, Hipposideros terasensis, in subtropical Taiwan. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 181, 125–135.
| Hibernation in warm hibernacula by free-ranging Formosan leaf-nosed bats, Hipposideros terasensis, in subtropical Taiwan.Crossref | GoogleScholarGoogle Scholar | 20714727PubMed |
Lovegrove, B. G., Körtner, G., and Geiser, F. (1999). The energetic cost of arousal from torpor in the marsupial Sminthopsis macroura: benefits of summer ambient temperature cycles. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 169, 11–18.
| The energetic cost of arousal from torpor in the marsupial Sminthopsis macroura: benefits of summer ambient temperature cycles.Crossref | GoogleScholarGoogle Scholar |
Lyman, C. P. (1970). Thermoregulation and metabolism in bats. In ‘Biology of Bats’. (Ed. W. A. Wimsatt.) pp. 301–330. (Academic Press: New York.)
Maloney, S. K., Bronner, G. N., and Buffenstein, R. (1999). Thermoregulation in the Angolan freetailed bat Mops condylurus: a small mammal that uses hot roosts. Physiological and Biochemical Zoology 72, 385–396.
| Thermoregulation in the Angolan freetailed bat Mops condylurus: a small mammal that uses hot roosts.Crossref | GoogleScholarGoogle Scholar | 10438676PubMed |
McKechnie, A. E., and Mzilikazi, N. (2011). Heterothermy in Afrotropical mammals and birds: a review. Integrative and Comparative Biology 51, 349–363.
| Heterothermy in Afrotropical mammals and birds: a review.Crossref | GoogleScholarGoogle Scholar | 21705792PubMed |
McNab, B. K., and O’Donnell, C. (2018). The behavioural energetics of New Zealand’s bats: daily torpor and hibernation, a continuum. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 223, 18–22.
| The behavioural energetics of New Zealand’s bats: daily torpor and hibernation, a continuum.Crossref | GoogleScholarGoogle Scholar |
Morrison, P. (1959). Body temperatures in some Australian mammals. I. Chiroptera. The Biological Bulletin 116, 484–497.
| Body temperatures in some Australian mammals. I. Chiroptera.Crossref | GoogleScholarGoogle Scholar |
National Institute of Water and Atmospheric Research (NIWA) (2020). Education and Training, Climate Data and Activities. Available at: niwa.co.nz/education-and-training/schools/resources/climate/overview/map_north [accessed 1 July 2020]
Nowack, J., Levesque, D. L., Reher, S., and Dausmann, K. H. (2020). Variable climates lead to varying phenotypes: ‘weird’ mammalian torpor and lessons from lower latitudes. Frontiers in Ecology and Evolution 8, 60.
| Variable climates lead to varying phenotypes: ‘weird’ mammalian torpor and lessons from lower latitudes.Crossref | GoogleScholarGoogle Scholar |
O’Connor, R. S., Wolf, B. O., Brigham, R. M., and McKechnie, A. E. (2017). Avian thermoregulation in the heat: efficient evaporative cooling in two southern African nightjars. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 187, 477–491.
| Avian thermoregulation in the heat: efficient evaporative cooling in two southern African nightjars.Crossref | GoogleScholarGoogle Scholar | 27812726PubMed |
O’Donnell, C. F. J. (2008). Mystacina robusta. The IUCN Red List of Threatened Species 2008: e.T14260A4425606.
O’Donnell, C. F. J., Borkin, K. M., Christie, J. E., Lloyd, B., Parsons, S., and Hitchmough, R. A. (2018). Conservation status of New Zealand bats 2017. New Zealand Threat Classification Series 21. Department of Conservation, Wellington.
Phillips, W. R., and Inwards, S. J. (1985). The annual activity and breeding cycles of Gould’s long-eared bat, Nyctophilus gouldi (Microchiroptera: Vespertilionidae). Australian Journal of Zoology 33, 111–128.
| The annual activity and breeding cycles of Gould’s long-eared bat, Nyctophilus gouldi (Microchiroptera: Vespertilionidae).Crossref | GoogleScholarGoogle Scholar |
Pohl, H. (1961). Temperaturregulation und Tagesperiodik des Stoffwechsels bei Winterschläfern. Zeitschrift fur Vergleichende Physiologie 45, 109–153.
| Temperaturregulation und Tagesperiodik des Stoffwechsels bei Winterschläfern.Crossref | GoogleScholarGoogle Scholar |
Ransome, R. D. (1990). ‘The Natural History of Hibernating Bats.’ (Christopher Helm: London.)
Reher, S., Rabarison, H., and Dausmann, K. H. (2020). Roosting outside the comfort zone – torpor at high ambient temperatures in a Malagasy bat. In ‘German Bat Research Meeting, Frauenchiemsee 10–12 January, Abstracts’. (Eds Goerlitz et al.) p. 27. (Max Planck Intitute for Ornithology: Munich.)
Richards, G. C. (1989). Nocturnal activity of insectivorous bats relative to temperature and prey availability in tropical Queensland. Australian Wildlife Research 16, 151–158.
| Nocturnal activity of insectivorous bats relative to temperature and prey availability in tropical Queensland.Crossref | GoogleScholarGoogle Scholar |
Richards, G. C., Hall, L. S., and Parish, S. (2012). ‘A Natural History of Australian Bats: Working The Night Shift.’ (CSIRO Publishing: Melbourne.)
Riek, A., and Geiser, F. (2013). Allometry of thermal variables in mammals: consequences of body size and phylogeny. Biological Reviews of the Cambridge Philosophical Society 88, 564–572.
| Allometry of thermal variables in mammals: consequences of body size and phylogeny.Crossref | GoogleScholarGoogle Scholar | 23301808PubMed |
Riek, A., Körtner, G., and Geiser, F. (2010). Thermobiology, energetics and activity patterns of the eastern tube-nosed bat (Nyctimene robinsoni) in the Australian tropics: effect of temperature and lunar cycle. The Journal of Experimental Biology 213, 2557–2564.
| Thermobiology, energetics and activity patterns of the eastern tube-nosed bat (Nyctimene robinsoni) in the Australian tropics: effect of temperature and lunar cycle.Crossref | GoogleScholarGoogle Scholar | 20639416PubMed |
Ruf, T., and Geiser, F. (2015). Daily torpor and hibernation in birds and mammals. Biological Reviews of the Cambridge Philosophical Society 90, 891–926.
| Daily torpor and hibernation in birds and mammals.Crossref | GoogleScholarGoogle Scholar | 25123049PubMed |
Schleucher, E. (2004). Torpor in birds: taxonomy, energetics, and ecology. Physiological and Biochemical Zoology 77, 942–949.
| Torpor in birds: taxonomy, energetics, and ecology.Crossref | GoogleScholarGoogle Scholar | 15674768PubMed |
Sheriff, M. J., Williams, C. T., Kenagy, G. J., Buck, C. L., and Barnes, B. M. (2012). Thermoregulatory changes anticipate hibernation onset by 45 days: data from free-living arctic ground squirrels. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 182, 841–847.
| Thermoregulatory changes anticipate hibernation onset by 45 days: data from free-living arctic ground squirrels.Crossref | GoogleScholarGoogle Scholar | 22526260PubMed |
Song, X., Körtner, G., and Geiser, F. (1997). Thermal relations of metabolic rate reduction in a hibernating marsupial. The American Journal of Physiology 273, R2097–R2104.
| 9435666PubMed |
Speakman, J. R., and Racey, P. A. (1991). No cost of echolocation for bats in flight. Nature 350, 421–423.
| No cost of echolocation for bats in flight.Crossref | GoogleScholarGoogle Scholar | 2011191PubMed |
Speakman, J. R., and Thomas, D. W. (2003). Physiological ecology and energetics of bats. In ‘Bat Ecology’ (Eds T. H. Kunz, and M. B. Fenton.) pp. 430–490. (University of Chicago Press: Chicago.)
Speakman, J. R., Webb, P. I., and Racey, P. A. (1991). Effects of disturbance on the energy expenditure of hibernating bats. Journal of Applied Ecology 28, 1087–1104.
| Effects of disturbance on the energy expenditure of hibernating bats.Crossref | GoogleScholarGoogle Scholar |
Stawski, C. (2010). Torpor during the reproductive season in a free-ranging subtropical bat, Nyctophilus bifax. Journal of Thermal Biology 35, 245–249.
| Torpor during the reproductive season in a free-ranging subtropical bat, Nyctophilus bifax.Crossref | GoogleScholarGoogle Scholar |
Stawski, C., and Currie, S. E. (2016). Effect of roost choice on winter torpor patterns of a free-ranging insectivorous bat. Australian Journal of Zoology 64, 132–134.
| Effect of roost choice on winter torpor patterns of a free-ranging insectivorous bat.Crossref | GoogleScholarGoogle Scholar |
Stawski, C., and Geiser, F. (2010a). Seasonality of torpor patterns and physiological variables of a free-ranging subtropical bat. The Journal of Experimental Biology 213, 393–399.
| Seasonality of torpor patterns and physiological variables of a free-ranging subtropical bat.Crossref | GoogleScholarGoogle Scholar | 20086123PubMed |
Stawski, C., and Geiser, F. (2010b). Fat and fed: frequent use of summer torpor in a subtropical bat. Naturwissenschaften 97, 29–35.
| Fat and fed: frequent use of summer torpor in a subtropical bat.Crossref | GoogleScholarGoogle Scholar | 19756460PubMed |
Stawski, C., and Geiser, F. (2011). Do season and distribution affect thermal energetics of a hibernating bat endemic to the tropics and subtropics? The American Journal of Physiology 301, R542–R547.
Stawski, C., and Geiser, F. (2012). Will temperature effects or phenotypic plasticity determine the thermal response of a heterothermic tropical bat to climate change? PLoS One 7, e40278.
| Will temperature effects or phenotypic plasticity determine the thermal response of a heterothermic tropical bat to climate change?Crossref | GoogleScholarGoogle Scholar | 22802959PubMed |
Stawski, C., Turbill, C., and Geiser, F. (2009). Hibernation by a free-ranging subtropical bat (Nyctophilus bifax). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 179, 433–441.
| Hibernation by a free-ranging subtropical bat (Nyctophilus bifax).Crossref | GoogleScholarGoogle Scholar | 19112568PubMed |
Stawski, C., Willis, C. K. R., and Geiser, F. (2014). The importance of temporal heterothermy in bats. Journal of Zoology 292, 86–100.
| The importance of temporal heterothermy in bats.Crossref | GoogleScholarGoogle Scholar |
Thomas, D. W. (1995). The physiological ecology of hibernation in vespertilionid bats. Symposia of the Zoological Society of London 67, 233–244.
Tidemann, C. R. (1993). Reproduction in the bats Vespadelus vulturnus, V. regulus and V. darlingtoni (Microchiroptera: Vespertilionidae) in coastal south-eastern Australia. Australian Journal of Zoology 41, 21–35.
| Reproduction in the bats Vespadelus vulturnus, V. regulus and V. darlingtoni (Microchiroptera: Vespertilionidae) in coastal south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Turbill, C. (2006a). Thermoregulatory behaviour of tree-roosting chocolate wattled bats (Chalinolobus morio) during summer and winter. Journal of Mammalogy 87, 318–323.
| Thermoregulatory behaviour of tree-roosting chocolate wattled bats (Chalinolobus morio) during summer and winter.Crossref | GoogleScholarGoogle Scholar |
Turbill, C. (2006b). Roosting and thermoregulatory behaviour of male Gould’s long-eared bats, Nyctophilus gouldi: energetic benefits of thermally unstable roosts. Australian Journal of Zoology 54, 57–60.
| Roosting and thermoregulatory behaviour of male Gould’s long-eared bats, Nyctophilus gouldi: energetic benefits of thermally unstable roosts.Crossref | GoogleScholarGoogle Scholar |
Turbill, C. (2009). Temperature effects on metabolic rate and torpor in southern forest bats (Vespadelus regulus). Australian Journal of Zoology 57, 125–127.
| Temperature effects on metabolic rate and torpor in southern forest bats (Vespadelus regulus).Crossref | GoogleScholarGoogle Scholar |
Turbill, C., and Geiser, F. (2006). Thermal biology of pregnant and lactating female and male long-eared bats, Nyctophilus geoffroyi and N. gouldi. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 176, 165–172.
| Thermal biology of pregnant and lactating female and male long-eared bats, Nyctophilus geoffroyi and N. gouldi.Crossref | GoogleScholarGoogle Scholar | 16331479PubMed |
Turbill, C., and Geiser, F. (2008). Hibernation by tree-roosting bats. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 178, 597–605.
| Hibernation by tree-roosting bats.Crossref | GoogleScholarGoogle Scholar | 18210129PubMed |
Turbill, C., Law, B. S., and Geiser, F. (2003a). Summer torpor in a free-ranging bat from sub-tropical Australia. Journal of Thermal Biology 28, 223–226.
| Summer torpor in a free-ranging bat from sub-tropical Australia.Crossref | GoogleScholarGoogle Scholar |
Turbill, C., Körtner, G., and Geiser, F. (2003b). Natural use of torpor by a small, tree-roosting bat during summer. Physiological and Biochemical Zoology 76, 868–876.
| Natural use of torpor by a small, tree-roosting bat during summer.Crossref | GoogleScholarGoogle Scholar | 14988802PubMed |
Turbill, C., Körtner, G., and Geiser, F. (2008). Timing of the daily temperature cycle affects the critical arousal temperature and energy expenditure of the lesser long-eared bat. The Journal of Experimental Biology 211, 3871–3878.
| Timing of the daily temperature cycle affects the critical arousal temperature and energy expenditure of the lesser long-eared bat.Crossref | GoogleScholarGoogle Scholar | 19043059PubMed |
Van Etten, E. J. B. (2009). Inter-annual rainfall variability of arid Australia: greater than elsewhere? The Australian Geographer 40, 109–120.
| Inter-annual rainfall variability of arid Australia: greater than elsewhere?Crossref | GoogleScholarGoogle Scholar |
Warnecke, L., Turner, J. M., and Geiser, F. (2008). Torpor and basking in a small arid zone marsupial. Naturwissenschaften 95, 73–78.
| Torpor and basking in a small arid zone marsupial.Crossref | GoogleScholarGoogle Scholar | 17684718PubMed |
Willis, C. K. R., and Brigham, R. M. (2003). Defining torpor in free-ranging bats: experimental evaluation of external temperature-sensitive radiotransmitters and the concept of active temperature. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 173, 379–389.
| Defining torpor in free-ranging bats: experimental evaluation of external temperature-sensitive radiotransmitters and the concept of active temperature.Crossref | GoogleScholarGoogle Scholar |
Willis, C. K. R., Turbill, C., and Geiser, F. (2005). Torpor and thermal energetics in a tiny Australian vespertilionid, the little forest bat (Vespadelus vulturnus). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 175, 479–486.
| Torpor and thermal energetics in a tiny Australian vespertilionid, the little forest bat (Vespadelus vulturnus).Crossref | GoogleScholarGoogle Scholar |
Withers, P. C., Cooper, C. E., Maloney, S. K., Bozinovic, F., and Cruz-Neto, A. P. (2016). ‘Ecological and Environmental Physiology of Mammals.’ (Oxford University Press: Oxford.)
