Skip to main content
SpringerLink
Log in

Hibernation in warm hibernacula by free-ranging Formosan leaf-nosed bats, Hipposideros terasensis, in subtropical Taiwan

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

Abstract

The subtropical Formosan leaf-nosed bats, Hipposideros terasensis (Hipposideridae), show little activity during winter. It has never been determined whether in winter they exhibit hibernation and multi-day periods of low body temperature. The objectives of this study were to understand the winter activity pattern of H. terasensis and to examine whether it enters hibernation during winter. We monitored the skin temperature (T sk) of nine free-ranging H. terasensis by attaching temperature-sensitive transmitters during the winters of 2007–2008 and 2008–2009. The results showed that H. terasensis entered hibernation from late December to early March. H. terasensis, however, differs from temperate hibernating bats in several ways: (1) it is capable of hibernation at roost temperature (T r) and T sk > 20°C; (2) hibernation at high T r and T sk does not lead to a relatively high arousal frequency; and (3) adults do not increase body mass in autumn prior to hibernation. To test the hypothesis that H. terasensis feeds frequently during the hibernation period to compensate for the high energetic demands of hibernating in warm hibernacula, we recorded the number and timing of bats that emerged from and entered into a hibernaculum, which contained more than 1,000 bats. From 30 December 2007 to 29 February 2008, an average of only 8.4 bats (<1%) per night (29 nights) emerged from the hibernaculum. Adult bats lost an average of 13–14% of body mass during an approximately 70-day hibernation period. We suggest that H. terasensis might have remarkably low torpid metabolic rates during hibernation.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

Abbreviations

AF:

Adult female

AM:

Adult male

JM:

Juvenile male

JF:

Juvenile female

BMR:

Basal metabolic rate

TMR:

Torpid metabolic rate

T a :

Air temperature

T b :

Body temperature

T b_min :

Minimum body temperature

T r :

Roost temperature

T sk :

Skin temperature

References

  • 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

    Article  Google Scholar 

  • Arlettaz R, Ruchet C, Aeschimann J, Brun E, Genoud M, Vogel P (2000) Physiological traits affecting the distribution and wintering strategy of the bat Tadarida teniotis. Ecology 81:1004–1014

    Google Scholar 

  • 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 

  • Avery MI (1985) Winter activity of pipistrelle bats. J Anim Ecol 54:721–738

    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 Mammal 77:1102–1106

    Article  Google Scholar 

  • Boyles JG, Dunbar MB, Whitaker JO Jr (2006) Activity following arousal in winter in North American vespertilionid bats. Mammal Rev 36:267–280

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Carey C (1993) Why do hibernators periodically arouse? Overview. In: Carey C, Florant GL, Wunder BA, Horwitz B (eds) Life in the cold: ecological, physiological and molecular mechanisms. Westview, Boulder, pp 24–35

    Google Scholar 

  • Chen SF (1995) Activity patterns and food habits of sympatric Formosan leaf-nosed bat (Hipposideros armiger) and Formosan horseshoe bat (Rhinolophus monoceros) in Yangmingshan area. M.S. thesis, National Taiwan University, Taipei

  • Chen CW (1998) Reproductive ecology of Taiwan Leaf-nosed bat (Hipposideros terasensis) in Chungliau area, Nantou county. M.S. thesis, Tunghai University, Taichung

  • Cheng HC, Lee LL (2002) Postnatal growth, age estimation, and sexual maturity in the Formosan leaf-nosed bat (Hipposideros terasensis). J Mammal 83:785–793

    Article  Google Scholar 

  • Cheng HC, Lee LL (2004) Temporal variations in the size and composition of Formosan leaf-nosed bat (Hipposideros terasensis) colonies in central Taiwan. Zool Stud 43:787–794

    Google Scholar 

  • Clark BS, Clark BK, Leslie DM Jr (2002) Seasonal variation in activity patterns of the endangered Ozark big-eared bat (Corynorhinus townsendii ingens). J Mammal 83:590–598

    Article  Google Scholar 

  • Daan S (1973) Activity during natural hibernation in three species of vespertilionid bats. Neth J Zool 23:1–71

    Article  Google Scholar 

  • Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429:825–826

    Article  CAS  PubMed  Google Scholar 

  • Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2005) Hibernation in the tropics: lessons from a primate. J Comp Physiol B 175:147–155

    Article  PubMed  Google Scholar 

  • Davis WH, Hitchcock HB (1965) Biology and migration of the bat, Myotis lucifugus, in New England. J Mammal 46:296–313

    Article  Google Scholar 

  • Davis WH, Reite OB (1967) Responses of bats from temperate regions to changes in ambient temperature. Biol Bull 132:320–328

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Dwyer PD (1964) Seasonal changes in activity and weight of Miniopterus schreibersi blepotis (Chiroptera) in north-eastern New South Wales. Aust J Zool 12:52–69

    Article  Google Scholar 

  • Ewing WG, Studier EH, O’Farrell MJ (1970) Autumn fat deposition and gross body composition in three species of Myotis. Comp Biochem Physiol 36:119–129

    Article  CAS  Google Scholar 

  • French AR (1982) Effects of temperature on the duration of arousal episodes during hibernation. J Appl Physiol 52:216–220

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Funakoshi K, Uchida TA (1978) Studies on the physiological and ecological adaptation of temperate insectivorous bats. 2: Hibernation and winter activity in some cave-dwelling bats. Jpn J Ecol 28:237–261

    Google Scholar 

  • Geiser F (1988) Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? J Comp Physiol B 158:25–37

    Article  CAS  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, Brigham RM (2000) Torpor, thermal biology, and energetics in Australian long-eared bats (Nyctophilus). J Comp Physiol B 170:153–162

    Article  CAS  PubMed  Google Scholar 

  • Geiser F, Kenagy GJ (1988) Torpor duration in relation to temperature and metabolism in hibernating ground squirrels. Physiol Zool 61:442–449

    Google Scholar 

  • Hall LS (1982) The effect of cave microclimate on winter roosting behaviour in the bat, Miniopterus schreibersii blepotis. Aust Ecol 7:129–136

    Article  Google Scholar 

  • Henshaw RE, Folk GE Jr (1966) Relation of thermoregulation to seasonally changing microclimate in two species of bats (Myotis lucifugus and M. sodalist). Physiol Zool 39:223–236

    Google Scholar 

  • Ho YY (2000) Roost selection of Formosan leaf-nosed bat (Hipposideros terasensis). M.S. thesis, National Taiwan University, Taipei

  • Ho YY, Lee LL (2003) Roost selection by Formosan leaf-nosed bats (Hipposideros armiger terasensis). Zool Sci 20:1017–1024

    Article  PubMed  Google Scholar 

  • Kunz TH, Wrazen JA, Burnett CD (1998) Changes in body mass and fat reserves in pre-hibernating little brown bats (Myotis lucifugus). Ecoscience 5:8–17

    Google Scholar 

  • Luis AD, Hudson PJ (2006) Hibernation patterns in mammals: a role for bacterial growth? Funct Ecol 20:471–477

    Article  Google Scholar 

  • Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic Press, New York

    Google Scholar 

  • McNab BK (1974) The behavior of temperate cave bats in a subtropical environment. Ecology 55:943–958

    Article  Google Scholar 

  • Menaker M (1964) Frequency of spontaneous arousal from hibernation in bats. Nature 203:540–541

    Article  CAS  PubMed  Google Scholar 

  • Mormann BM, Robbins LW (2007) Winter roosting ecology of eastern red bats in southwest Missouri. J Wildl Manage 71:213–217

    Article  Google Scholar 

  • Nowak RM (1999) Old World leaf-nosed bats. In: Walker’s bats of the world. The Johns Hopkins University Press, Baltimore, pp 110–114

  • 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 

  • Qumsiyeh MB (1985) The bats of Egypt. Special Publications of the Museum, Texas Technical University, No. 23

  • Ransome RD (1968) The distribution of the Greater horseshoe bat, Rhinolophus ferrumequinum, during hibernation, in relation to environmental factors. J Zool 154:77–112

    Article  Google Scholar 

  • Ransome RD (1971) The effect of ambient temperature on the arousal frequency of the hibernating Greater horseshoe bat, Rhinolophus ferrumequinum, in relation to site selection and the hibernation state. J Zool 164:353–371

    Article  Google Scholar 

  • Richards GC (1989) Nocturnal activity of insectivorous bats relative to temperature and prey availability in tropical Queensland. Aust Wildl Res 16:151–158

    Article  Google Scholar 

  • Richter AR, Humphrey SR, Cope JB, Brack V Jr (1993) Modified cave entrances: Thermal effect on body mass and resulting decline of endangered Indiana bats (Myotis sodalis). Conserv Biol 7:407–415

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Speakman JR, Racey PA (1991) No cost of echolocation for bats in flight. Nature 350:421–423

    Article  CAS  PubMed  Google Scholar 

  • Speakman JR, Thomas DW (2003) Physiological ecology and energetics of bats. In: Kunz TH, Fenton MB (eds) Bat ecology. University of Chicago Press, Chicago, pp 430–490

    Google Scholar 

  • Stawski C, Turbill C, Geiser F (2009) Hibernation by a free-ranging subtropical bat (Nyctophilus bifax). J Comp Physiol B 179:433–441

    Article  PubMed  Google Scholar 

  • Strijkstra AM, Daan S (1997) Sleep during arousal episodes as a function of prior torpor duration in hibernating European ground squirrels. J Sleep Res 6:36–43

    Article  CAS  PubMed  Google Scholar 

  • Thomas DW, Geiser F (1997) Periodic arousals in hibernating mammals: is evaporative water loss involved? Funct Ecol 11:585–591

    Article  Google Scholar 

  • Thomas DW, Fenton MB, Barclay RMR (1979) Social behavior of the little brown bat, Myotis lucifugus. 1. Mating behavior. Behav Ecol 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 Mammal 71:475–479

    Article  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 

  • Turbill C, Geiser F (2008) Hibernation by tree-roosting bats. J Comp Physiol B 178:597–605

    Article  PubMed  Google Scholar 

  • Turbill C, Körtner G, Geiser F (2008) Timing of the daily temperature cycle affects the critical arousal temperature and energy expenditure of lesser long-eared bats. J Exp Biol 211:3871–3878

    Article  PubMed  Google Scholar 

  • Twente JW, Twente J (1987) Biological alarm clock arouses hibernating big brown bats, Eptesicus fuscus. Can J Zool 222:237–245

    Google Scholar 

  • Twente JW, Twente J, Moy RM (1977) Regulation of arousal from hibernation by temperature in three species of Citellus. J Appl Physiol 42:191–195

    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 

  • Wang LCH, Wolowyk M (1988) Torpor in mammals and birds. Can J Zool 66:133–137

    Article  CAS  Google Scholar 

  • Webb PI, Speakman JR, Racey PA (1993) The implication of small reductions in body temperature for radiant and convective heat loss in resting endothermic brown long-eared bats (Plecotus auritus). J Therm Biol 18:131–135

    Article  Google Scholar 

  • Webb PI, Speakman JR, Racey PA (1996) How hot is a hibernaculum? A review of the temperatures at which bats hibernate. Can J Zool 74:761–765

    Article  Google Scholar 

  • Yoshiyuki M (1991) Taxonomic status of Hipposideros terasensis Kishida, 1924, from Taiwan (Mammalia, Chiroptera, Hipposideridae). J Mammal Soc Jpn 16:27–35

    Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall International, New Jersey

    Google Scholar 

Download references

Acknowledgments

We thank Chia-Shien Liu, Kuang-Lung Huang, Chiun-hsiang Chang, Yu-Ta Chuang for help with fieldwork, Fang-Te Chan for anesthetization of animals, and Ting-Li Lin for statistical advice. We also thank Jeff Lorch, Dr. Hannah Carey, and two anonymous reviewers for their constructive comments on an early draft of the manuscript. The research was supported by Taiwan Endemic Species Research Institute.

Author information

Authors and Affiliations

  1. Department of Forest and Wildlife Ecology, University of Wisconsin-Madison, Madison, WI, 53706, USA

    Jian-Nan Liu & William H. Karasov

  2. Endemic Species Research Institute, Jiji, 552, Nantou County, Taiwan

    Jian-Nan Liu

Authors
  1. Jian-Nan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. William H. Karasov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jian-Nan Liu.

Additional information

Communicated by H. V. Carey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, JN., Karasov, W.H. Hibernation in warm hibernacula by free-ranging Formosan leaf-nosed bats, Hipposideros terasensis, in subtropical Taiwan. J Comp Physiol B 181, 125–135 (2011). https://doi.org/10.1007/s00360-010-0509-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-010-0509-3

Keywords

Search

Navigation