Skip to main content
SpringerLink
Log in

The tradeoff between torpor use and reproduction in little brown bats (Myotis lucifugus)

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

Abstract

In mammals, reproduction, especially for females is energetically demanding. Therefore, during the reproductive period females could potentially adjust patterns of thermoregulation and foraging in concert to minimise the energetic constraints associated with pregnancy and lactation. We assessed the influence of pregnancy, lactation, and post-lactation on torpor use and foraging behaviour by female little brown bats, Myotis lucifugus. We measured thermoregulation by recording skin temperature and foraging by tracking bats which carried temperature-sensitive radio-tags. We found that individuals, regardless of reproductive condition, used torpor, but the patterns of torpor use varied significantly between reproductive (pregnant and lactating) females and post-lactating females. As we predicted, reproductive females entered torpor for shorter bouts than post-lactating females. Although all females used torpor frequently, pregnant females spent less time in torpor, and maintained higher skin temperatures than either lactating or post-lactating females. This result suggests that delayed offspring development which has been associated with torpor use during pregnancy, may pose a higher risk to an individual’s reproductive success than reduced milk production during lactation. Conversely, foraging behaviour of radio-tagged bats did not vary with reproductive condition, suggesting that even short, shallow bouts of torpor produce substantial energy savings, likely obviating the need to spend more time foraging. Our data clearly show that torpor use and reproduction are not mutually exclusive and that torpor use (no matter how short or shallow) is an important means of balancing the costs of reproduction for M. lucifugus.

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

Similar content being viewed by others

Abbreviations

MR:

Metabolic rate

T b :

Body temperature

T a :

Ambient temperature

T sk :

Skin temperature

T roost :

Roost temperature

LMM:

Linear mixed model

ANOVA:

Analysis of variance

AIC:

Akaike information criterion

AICC :

Bias-corrected Akaike information criterion

References

  • Audet D, Fenton MB (1988) Heterothermy and the use of torpor by the bat Eptesicus fuscus (Chiroptera:Vespertilionidae): a field study. Physiol Zool 61:197–204

    Google Scholar 

  • Audet D, Thomas DW (1996) Evaluation of the accuracy of body temperature measurement using external 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 Mammal 77:1102–1106

    Article  Google Scholar 

  • Bozinovic F, Gricelda R, Cortes A, Rosenmann M (2005) Energetics, thermoregulation and torpor in the Chilean mouse-opossum Thylamys elegans (Didelphidae). Rev Chil Hist Nat 78:199–206

    Google Scholar 

  • Calder WA, Booser J (1973) Hypothermia of broad-tailed Hummingbirds during incubation in nature with ecological correlations. Science 180:751–753

    Article  PubMed  CAS  Google Scholar 

  • Chruszcz BJ, Barclay RMR (2002) Thermoregulatory ecology of a solitary bat, Myotis evotis, roosting in rock crevices. Funct Ecol 16:18–26

    Article  Google Scholar 

  • Csada RD, Brigham RM (1994) Reproduction constrains the use of daily torpor by free-ranging common poorwills (Phalaenoptilus nuttallii) (Aves: Caprimulgidae). J Zool 235:209–216

    Article  Google Scholar 

  • Farmer CG (2003) Reproduction: the adaptive significance of endothermy. Am Nat 162:826–840

    Article  PubMed  CAS  Google Scholar 

  • Fenton MB, Barclay RMR (1980) Myotis lucifugus. Mamm Spp 142:1–8

    Article  Google Scholar 

  • Fietz J, Pflug M, Schlund W, Tataruch F (2005) Influences of the feeding ecology on body mass and possible implications for reproduction in the edible dormouse (Glis glis). J Comp Physiol B 175:45–55

    Article  PubMed  Google Scholar 

  • Fowler PA (1988) Thermoregulation in the female hedgehog, Erinaceus europaeus, during the breeding season. J Reprod Fertil 82(1):285–292

    Google Scholar 

  • Geiser F (1994) Hibernation and daily torpor in marsupials: a review. Aust J Zool 42:1–16

    Article  Google Scholar 

  • Geiser F (1996) Torpor in reproductive endotherms. In: Geiser F, Hulbert AJ, Nicol S (eds) Adaptations to the cold: tenth international hibernation symposium. Armidale UNE Press, Armidale, pp 81–86

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

    Article  PubMed  CAS  Google Scholar 

  • Geiser F, Brigham RM (2012) The other functions of torpor. In: Ruf T, Bieber C, Arnold W, Millesi E (ed) Living in a seasonal world: thermoregulatory and metabolic adaptations. Springer, Heidelberg. doi:10.1007/978-3-642-28678-0_10

  • Geiser F, Masters P (1994) Torpor in relation to reproduction in the mulgara, Dasycercus cristicauda (Dasyuridae: Marsupialia). J Therm Biol 19:33–40

    Article  Google Scholar 

  • Geiser F, Pavey CR (2007) Basking and torpor in a rock-dwelling desert marsupial: survival strategies in a resource-poor environment. J Comp Physiol B 177:885–892

    Article  PubMed  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, Seymour RS (1989) Torpor in a pregnant echidna, Tachyglossus aculeatus. Austr Mamm 12:81–82

    Google Scholar 

  • Geiser F, McAllan BM, Brigham RM (2005) Daily torpor in a pregnant dunnart (Sminthopsis macroura Dasyuridae: Marsupialia). Mamm Biol 70:117–121

    Google Scholar 

  • Geiser F, Christian N, Cooper CE, Körtner G, McAllan BM, Pavey CR, Turner JM, Warnecke L, Willis CKR, Brigham RM (2008) Torpor in marsupials: recent advances. In: Lovegrove BG, McKechnie AE (eds) Hypometabolism in animals: torpor, hibernation and cryobiology. Thirteenth international hibernation symposium. University of KwaZulu-Natal, Pietermaritzburg, pp 297–306

  • Grinevitch L, Holroyd SL, Barclay RMR (1995) Sex differences in the use of daily torpor and foraging time by big brown bats (Eptesicus fuscus) during the reproductive season. J Zool 235:301–309

    Article  Google Scholar 

  • Hamilton IM, Barclay RMR (1994) Patterns of daily torpor and day-roost selection by male and female big brown bats (Eptesicus fuscus). Can J Zool 72:744–749

    Article  Google Scholar 

  • Holloway JC, Geiser F (1995) Influence of torpor on daily energy expenditure of the dasyurid marsupial Sminthopsis crassicaudata. Comp Biochem Physiol 112A:59–66

    Article  CAS  Google Scholar 

  • Hoying KM, Kunz TH (1998) Variation in size at birth and post-natal growth in the insectivorous bat Pipistrellus subflavus (Chiroptera: Vespertilionidae). J Zool 245:15–27

    Article  Google Scholar 

  • Kenagy GJ (1989) Daily and seasonal uses of energy stores in torpor and hibernation. In: Malan A, Canguilhem B (eds) Living in the cold: 2nd International Symposium. John Libbey Eurotext Ltd, Montrouge, pp 17–24

    Google Scholar 

  • Körtner G, Pavey CR, Geiser F (2008) Thermal biology, torpor, and activity in free living mulgaras in arid zone Australia during the winter reproductive season. Physiol Biochem Zool 81(4):442–451

    Article  PubMed  Google Scholar 

  • Krishna A, Dominic CJ (1982) Differential rates of fetal growth in two successive pregnancies in the emballonurid bat, Taphozous longimanus Hardwicke. Biol Reprod 27:351–353

    Article  PubMed  CAS  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 

  • Kurta A, Kunz TH (1987) Size of bats at birth and maternal investment during pregnancy. Symp Zool Soc Lond 57:79–106

    Google Scholar 

  • Kurta A, Bell GP, Nagy KA, Kunz TH (1989) Energetics of pregnancy and lactation in free-ranging little brown bats (Myotis lucifugus). Physiol Zool 62:804–818

    Google Scholar 

  • Landau BR, Dawe AR (1960) Observations on a colony of captive ground squirrels throughout the year. In: Lyman CP, Dawe AR (eds) Mammalian hibernation. Bulletin of the Museum of Comparative Zoology, Harvard University, Cambridge, pp 173–189

  • Lausen CL, Barclay RMR (2003) Thermoregulation and roost selection by reproductive female big brown bats (Eptesicus fuscus) roosting in rock crevices. J Zool 260:235–244

    Article  Google Scholar 

  • Lehmer EM, Bossenbroeck JM, Van Horne B (2003) The influence of environment, sex and innate timing mechanisms on body temperature patterns of free-ranging black-tailed prairie dogs (Cynomys ludovicianus). Physiol Biochem Zool 76:72–83

    Google Scholar 

  • Lewis SE (1993) Effect of climatic variation on reproduction by pallid bats (Antrozous pallidus). Can J Zool 67:2468–2472

    Google Scholar 

  • McKechnie AE, Ashdown RAM, Christian MB, Brigham RM (2007) Torpor in an African caprimulgid, the Freckled Nightjar (Caprimulgus tristigma). J Avian Biol 38:261–266

    Google Scholar 

  • McNab B (2006) The energetics of reproduction in endotherms and its implication for their conservation. Integr Comp Biol 46(6):1159–1168

    Article  PubMed  Google Scholar 

  • Morrow G, Nicol SC (2009) Cool Sex? Hibernation and reproduction overlap in the echidna. PLoS ONE 4(6):e6070. doi:10.1371/journal.pone.0006070

  • Morton SR (1978) Torpor and nest-sharing in free-living Sminthopsis crassicaudata (Marsupialia) and Mus musculus (Rodentia). J Mammal 59:569–575

    Article  Google Scholar 

  • Nicol SC, Andersen NA (2006) Body temperature as an indicator of egg-laying in the echidna, Tachyglossus aculeatus. J Therm Biol 31:483–490

    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 

  • Quinn GP, Keough MJ (2002) Graphical exploration of data. In: Quinn GP, Keough MJ (eds) Experimental design and data analysis for biologists. Universtiy Press, Cambridge, pp 58–71

    Chapter  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org

  • Racey PA (1973) Environmental factors affecting the length of gestation in heterothermic bats. J Reprod Fertil Suppl 19:175–189

    PubMed  CAS  Google Scholar 

  • Racey PA, Swift SM (1985) Feeding ecology of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) during pregnancy and lactation. J Anim Ecol 54:205–215

    Article  Google Scholar 

  • Randrianambinina B, Rakotondravony D, Radespiel U, Zimmermann E (2003) Seasonal changes in general activity, body mass and reproduction of two small nocturnal primates: a comparison of the golden brown mouse lemur (Microcebus ravelobensis) in Northwestern Madagascar and the brown mouse lemur (Microcebus rufus) in Eastern Madagascar. Primates 44:321–331

    Article  PubMed  Google Scholar 

  • Speakman JR, Racey PA (1987) The energetics of pregnancy and lactation in the brown long-eared bat, Plecotus auritus. In: Fenton MB, Racey PA, Rayner JMV (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge, pp 367–393

    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 

  • Stephenson PJ, Racey PA (1993) Reproductive energetics of the Tenrecidae (Mammalia: Insectivora). I. The large-eared tenrec, Geogale aurita. Physiol Zool 665:643–663

    Google Scholar 

  • Studier EH (1981) Energetic advantages of slight drops in temperature in little brown bats, Myotis lucifugus. Comp Biochem Physiol A 70:537–540

    Article  Google Scholar 

  • Studier EH, O`Farrell MJ (1972) Biology of Myotis thysanodes and M. lucifugus (Chiroptera: Vespertilionidae)—I. Thermoregulation. Comp Biochem Physiol A 41:567–595

    Article  PubMed  CAS  Google Scholar 

  • Turbill C, Geiser F (2006) Thermal physiology of pregnant and lactating female and male long-eared bats, Nyctophilus geoffroyi and N. gouldi. J Comp Physiol B 176:165–172

    Article  PubMed  Google Scholar 

  • Turkenheimer FE, Hinz R, Cunningham VJ (2003) On the undecidability among kinetic models: from model selection to model averaging. J Cereb Blood Flow Metab 23(4):490–498

    Article  Google Scholar 

  • Weather Underground Inc. (2010) Weather History & Data Archive. http://www.wunderground.com/history/

  • Wilde CJ, Knight CR, Racey PA (1999) Influence of torpor on milk protein composition and secretion in lactating bats. J Exp Zool 284:35–41

    Article  PubMed  CAS  Google Scholar 

  • Willis CKR (2007) An energy-based, body temperature threshold between torpor and normothermia for small mammals. Physiol Biochem Zool 80:643–651

    Article  PubMed  Google Scholar 

  • Willis CKR, Brigham RM, Geiser F (2006) Deep, prolonged torpor by pregnant, free-ranging bats. Naturwissenschaften 93:80–83

    Article  PubMed  CAS  Google Scholar 

  • Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Limitations of linear regression applied on ecological data. In: Gail M, Krickeberg K, Samet JM, Tsiatis A, Wong W (eds) Mixed effects models and extensions in ecology with R, 1st edn. Springer Science and Business Media, New York, pp 11–33

    Chapter  Google Scholar 

Download references

Acknowledgments

We are thankful for the comments and insight provided by the anonymous reviewers, as well as B. Fenton, J. Kilgour, S. Lund, D. Riskin, C. Somers, K. Spadafore and N. Veselka. We thank C. and D. Bailey, P. Douglass and S. McPheeters for access to bat colonies and D. Dahrouj, L. Hooton, T. McClenahan and N. Veselka for their help in the field. This study was financially supported by General Electric, Natural Sciences and Engineering Research Council Discovery and Research Tools and Instruments Grants and the University of Regina Faculty of Graduate Studies and Research.

Author information

Author notes

  1. Yvonne A. Dzal

    Present address: Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

Authors and Affiliations

  1. Department of Biology, University of Regina, Regina, SK, S4S 0A2, Canada

    Yvonne A. Dzal & R. Mark Brigham

Authors
  1. Yvonne A. Dzal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Mark Brigham
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yvonne A. Dzal.

Additional information

Communicated by H. V. Carey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dzal, Y.A., Brigham, R.M. The tradeoff between torpor use and reproduction in little brown bats (Myotis lucifugus). J Comp Physiol B 183, 279–288 (2013). https://doi.org/10.1007/s00360-012-0705-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-012-0705-4

Keywords

Search

Navigation