Skip to main content

Thermoregulatory variation among populations of bats along a latitudinal gradient

Abstract

Most studies of hibernation physiology sample individuals from populations within a single geographic area, yet some species have large ranges meaning populations likely experience area-specific levels of energetic challenges. As well, few studies have assessed within-season variation. Since physiological adjustments often are influenced by environmental factors, and the types of environments vary with geography, we expected variance in hibernation patterns among geographically separated populations. Our specific goal was to measure intraspecific variation in torpid metabolic rate (TMR) and body temperature (T b) as a function of ambient temperature (T a) for a non-migratory and migratory species to determine whether there is a continuum in physiological responses based on latitude. We chose big brown (Eptesicus fuscus) and eastern red bats (Lasiurus borealis) as model species and sampled individuals from populations throughout each species’ winter range. In both species, individuals from southern populations maintained higher TMR at cooler T as and lower TMR at warmer T as than those from northern populations. Big brown bats from southern populations regulated T b during torpor at higher levels and there was no significant difference in T b between populations of eastern red bats. Although metabolic responses were similar across the gradient between species, the effect was more dramatic in big brown bats. Our data demonstrate a continuum in thermoregulatory response, ranging from classic hibernation in northern populations to a pattern more akin to daily torpor in southern populations. Our research highlights the potential usefulness of bats as model organisms to address questions about within-species physiological variation in wild populations.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • American Society of Mammalogists Animal Care and Use Committee (1998) Guidelines for the capture, handling, and care of mammals as approved by the American Society of Mammalogists. J Mammal 79:1416–1431

    Article  Google Scholar 

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

    Google Scholar 

  • Aschoff J (1981) Thermal conductance in mammals and birds: its dependence on body size and circadian phase. Comp Biochem Physiol 69:611–619

    Article  Google Scholar 

  • Audet D, Thomas DWT (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 radiotransmittors be used to assess body temperature and torpor in bats? J Mammal 77:1102–1106

    Article  Google Scholar 

  • Boyles JG, Timpone JC, Robbins LW (2003) Late winter observations of red bats, Lasiurus borealis, and evening bats, Nycticeius humeralis, in Missouri. Bat Res News 44:59–61

    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 

  • Boyles JG, Dunbar MB, Storm JJ, Brack V Jr (2007) Energy availability influences microclimate selection of hibernating bats. J Exp Biol 210:4345–4350

    Article  PubMed  Google Scholar 

  • Bozinovic F, Muñoz JLP, Naya DE, Cruz-Neto AP (2007) Adjusting energy expenditures to energy supply: food availability regulates torpor use and organ size in the Chilean mouse-opossum Thylamys elegans. J Comp Physiol B 177:393–400

    Article  PubMed  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 

  • Coburn DK, Geiser F (1998) Seasonal changes in energetics and torpor patterns in the subtropical blossom-bat Syconycteris australis (Megachiroptera). Oecologia 113:467–473

    Article  Google Scholar 

  • Cryan PM (2003) Seasonal distribution of migratory tree bats (Lasiurus and Lasionycteris) in North America. J Mammal 84:579–593

    Article  Google Scholar 

  • Dunbar MB, Tomasi TE (2006) Arousal patterns, metabolism, and a winter energy budget of eastern red bats (Lasiurus borealis). J Mammal 87:1096–1102

    Article  Google Scholar 

  • Gannon WL, Sikes RS, and the Animal Care, Use Committee of the American Society of Mammalogists (2007) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 88:809–823

    Article  Google Scholar 

  • Garland T Jr, Adolph SC (1991) Physiological differentiation of vertebrate populations. Annu Rev Ecol Syst 22:193–228

    Article  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 158:25–38

    Article  CAS  PubMed  Google Scholar 

  • Geiser F (2007) Yearlong hibernation in a marsupial mammal. Naturwiss 94:941–944

    Article  CAS  PubMed  Google Scholar 

  • Geiser F, Baudinette RV (1987) Seasonality of torpor and thermoregulation in three dasyurid marsupials. J Comp Physiol B 157:335–344

    Article  Google Scholar 

  • Geiser F, Ferguson C (2001) Intraspecific differences in behaviour and physiology: effects of captive breeding on patterns of torpor in feathertail gliders. J Comp Physiol B 171:569–576

    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 

  • 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

    Google Scholar 

  • Geiser F, Holloway JC, Körtner G, Maddocks TA, Turbill C, Brigham RM (2000) Do patterns of torpor differ between free-ranging and captive mammals and birds? In: Heldmaier G, Klingenspor M (eds) Life in the cold. Springer, Germany, pp 95–102

    Google Scholar 

  • Humphries MM, Thomas DW, Speakman JR (2002) Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature 418:313–316

    Article  CAS  PubMed  Google Scholar 

  • Humphries MM, Thomas DW, Kramer DL (2003a) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76:165–179

    Article  PubMed  Google Scholar 

  • Humphries MM, Thomas DW, Kramer DL (2003b) The role of energy availability in mammalian hibernation: an experimental test in free-ranging eastern chipmunks. Physiol Biochem Zool 76:180–186

    Article  PubMed  Google Scholar 

  • Humphries MM, Umbanhowar J, McCann KS (2004) Bioenergetic prediction of climate change impacts on Northern mammals. Integr Comp Biol 44:152–162

    Article  Google Scholar 

  • King WJ, Festa-Bianchet M, Hatfield SE (1991) Determinants of reproductive success in female Columbian ground squirrels. Oecologia 86:528–534

    Article  Google Scholar 

  • Kurta A, Baker RH (1990) Eptesicus fuscus. Mammalian Species 356:1–10

    Article  Google Scholar 

  • Liknes ET, Scott SM, Swanson DL (2002) Seasonal acclimatization in the American goldfinch revisited: to what extent do metabolic rates vary seasonally? Condor 104:548–557

    Article  Google Scholar 

  • Lyman CP (1948) The oxygen consumption and temperature regulation of hibernating hamsters. J Exp Biol 109:55–78

    CAS  Google Scholar 

  • Mager KJ, Nelson TA (2001) Roost-site selection by eastern red bats (Lasiurus borealis). Am Midl Nat 145:120–126

    Article  Google Scholar 

  • Milam-Dunbar MB (2005) Ecophysiology of hibernating eastern red bats (Lasiurus borealis). Dissertation, Missouri State University

  • Mills RS, Barrett GW, Farrell MP (1975) Populations dynamics of the big brown bat (Eptesicus fuscus) in southwestern Ohio. J Mammal 56:591–604

    Article  Google Scholar 

  • Moorman CE, Russel KR, Menzel MA, Lohr SM (1999) Bats roosting in deciduous leaf litter. Bat Res News 40:74–75

    Google Scholar 

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

    Article  Google Scholar 

  • Mueller P, Diamond J (2007) Metabolic rate and environmental productivity: well-provisioned animals evolved to run and idle fast. Proc Natl Acad Sci USA 98:12550–12554

    Article  Google Scholar 

  • Neuweiler G (2000) Reproduction and development. In: The biology of bats. Oxford University Press, Oxford, pp 236–261

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    Article  CAS  PubMed  Google Scholar 

  • Pörtner HO, Bennett AF, Bozinovic F, Clarke A, Lardies MA, Lucassen M, Pelster B, Schiemer F, Stillman JH (2006) Trade-offs in thermal adaptation: the need for a molecular to ecological integration. Physiol Biochem Zool 79:296–313

    Article  Google Scholar 

  • Racey PA, Entwistle AC (2000) Life-history and reproductive strategies of bats. In: Crichton EG, Krutzsch PH (eds) Reproductive biology of bats. Academic Press, London, pp 363–414

    Chapter  Google Scholar 

  • Rainey WE, Pierson ED, Colberg M, Barclay JH (1992) Bats in hollow redwoods: seasonal use and role in nutrient transfer into old growth communities. Bat Res News 33:71

    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 site. J Zool 164:353–371

    Article  Google Scholar 

  • Reite OB, Davis WH (1966) Thermoregulation in bats exposed to low ambient temperatures. Proc Soc Exp Biol Med 121:1212–1215

    CAS  PubMed  Google Scholar 

  • Rodrigue JL, Schuler TM, Menzel MA (2001) Observations of bat activity during prescribed burning in West Virginia. Bat Res News 42:48–49

    Google Scholar 

  • Saugey DA, Vaughn RL, Crump BG, Heidt GA (1998) Notes on the natural history of Lasiurus borealis in Arkansas. J Arkansas Acad Sci 52:92–98

    Google Scholar 

  • Schleucher E, Withers PC (2001) Re-evaluation of the allometry of wet thermal conductance for birds. Comp Biochem Physiol 129:821–827

    CAS  Google Scholar 

  • Schmidt-Nielsen K (1990) Temperature regulation. In: Animal physiology, 4th edn. Cambridge University Press, New York, pp 240–295

  • Scholander PF, Hock R, Irving LV (1950) Adaptation to cold in artic and tropical mammals and birds in relation to body temperature, insulation and basal metabolic rate. Biol Bull 99:259–271

    Article  CAS  PubMed  Google Scholar 

  • Shump KA, Shump AU (1982) Lasiurus borealis. Mammalian Species 183:1–6

    Google Scholar 

  • Soriano PJ, Ruiz A, Arends A (2002) Physiological responses to ambient temperature manipulation by three species of bats from Andean Cloud forests. J Mammal 83:445–457

    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 

  • Twente JW (1955) Some aspects of habitat selection and other behavior of cavern dwelling bats. Ecology 36:706–732

    Article  Google Scholar 

  • Vernberg FJ (1962) Comparative physiology: latitudinal effects on physiological properties of animal populations. Ann Rev Physiol 24:517–544

    Article  CAS  Google Scholar 

  • Vernberg FJ, Tashian RE (1959) Studies on the physiological variation between tropical and temperature zone fiddler crabs of the genus Uca I. Thermal death limits. Ecology 40:589–593

    Article  Google Scholar 

  • Wang LCH (1978) Energetic and field aspects of mammalian torpor: the Richardson’s ground squirrel. In: Wimsatt WA (ed) Strategies in cold. Academic Press, New York, pp 109–145

    Google Scholar 

  • Whitaker JO Jr, Gummer SL (2000) Population structure and dynamics of big brown bats (Eptesicus fuscus) hibernating in buildings. Am Midl Nat 143:389–396

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Willis CKR, Lane JE, Liknes ET, Swanson DL, Brigham RM (2005) Thermal energetics of female big brown bats (Eptesicus fuscus). Can J Zool 83:871–879

    Article  Google Scholar 

  • Withers PC (2001) Design, calibration and calculation for flow-through respirometry systems. Aust J Zool 49:445–461

    Article  Google Scholar 

Download references

Acknowledgments

Financial support was provided by the University of Regina Faculty of Graduate Studies and NSERC (20021-2555-300). We thank J. Boyles, J. Gruver, B. Scullon, T. Tomasi, S. Gardner, S. Samoray, J. Martin (and family), S. Allydog, T. Maddox, D. Aubrey, S. Lund, P. Neary, R. Treble, H. Broders and H. Weger for their comments on earlier drafts, help with analysis and assistance in the field and/or lab. Indiana State University, Missouri State University Bull Shoals Field Station, and the Solon Dixon Forestry Education Center (and staff) provided housing and/or lab space during field work. We also thank the two anonymous reviewers whose comments helped to strengthen our manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Miranda B. Dunbar.

Additional information

Communicated by I. D. Hume.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dunbar, M.B., Brigham, R.M. Thermoregulatory variation among populations of bats along a latitudinal gradient. J Comp Physiol B 180, 885–893 (2010). https://doi.org/10.1007/s00360-010-0457-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-010-0457-y

Keywords

  • Energy
  • Geographic region
  • Hibernation
  • Population
  • Temperature
  • Torpor