Skip to main content
SpringerLink
Log in

The influence of reproductive condition and concurrent environmental factors on torpor and foraging patterns in female big brown bats (Eptesicus fuscus)

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

Abstract

Unlike many othe r mammals, bats in temperate regions employ short bouts of torpor throughout the reproductive period to maintain a positive energy balance. In addition to decreasing energy expenditure during the day, they typically alter foraging patterns as well. It is well known that various environmental conditions influence both torpor and foraging patterns, but studies of these factors often have focussed on one element in isolation thus it is not known how the two behaviours are collectively influencing temperate bats. The objective of our study was to assess how reproductive condition and environmental factors concurrently affect energy balance in female big brown bats (Eptesicus fuscus). We equipped pregnant and lactating bats in southwest Saskatchewan, Canada with temperature-sensitive radio-transmitters. While transmitters were active, skin temperature data were collected and foraging patterns were determined using triangulation. Of the various environmental and physiological parameters used to model torpor characteristics, roost type was the most important factor. Bats roosting in trees used deeper and longer torpor bouts than those roosting in buildings. Lactating bats had a tendency to forage for longer durations than pregnant bats, and often made more foraging trips. When taken together, we found that foraging duration and torpor duration were not directly related during pregnancy, but exhibited an inverse relationship during lactation. This provides support for the hypothesis that there are physiological trade-offs for reproductive bats and suggests that how bats compensate is not entirely predictable based on current environmental conditions.

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

T sk :

Skin temperature

T a :

Ambient temperature

T b :

Body temperature

T onset :

Torpor onset temperature

HI:

Heterothermy index

w i :

Akaike weight

AICc :

Bias corrected akaike information criterion

LMM:

Linear mixed model

References

  • Aldridge HDJN, Brigham RM (1991) Factors influencing foraging time in two aerial insectivores: the bird Chordeiles minor and the bat Eptesicus fuscus. Can J Zool 69:62–69

    Article  Google Scholar 

  • Anthony ELP, Kunz TH (1977) Feeding strategies of the little brown bat, Myotis lucifugus, in southern New Hampshire. Ecology 58:775–786

    Article  Google Scholar 

  • Anthony ELP, Stack MH, Kunz TH (1981) Night roosting and the nocturnal time budget of the little brown bat, Myotis lucifugus: effects of reproductive status, prey density, and environmental conditions. Oecologia 51:151–156

    Article  Google Scholar 

  • Arbuthnott D, Brigham RM (2007) The influence of a local temperature inversion on the foraging behaviour of big brown bats, Eptesicus fuscus. Acta Chiropterol 9:193–201

    Article  Google Scholar 

  • Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178

    Article  Google Scholar 

  • Barclay RMR (1989) The effect of reproductive condition on the foraging behavior of female hoary bats, Lasiurus cinereus. Behav Ecol Sociobiol 24:31–37

    Article  Google Scholar 

  • Barclay MR (1991) Population structure of temperate zone insectivorous bats in relation to foraging behaviour and energy demand. J Anim Ecol 60:165–178

    Article  Google Scholar 

  • Barclay RMR (1994) Constraints on reproduction by flying vertebrates: energy and calcium. Am Nat 144:1021–1031

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using S4 classes. vol R package version 0.999999-0

  • Beasley CA, Adams CJ (1994) Relationships between environmental factors and capture time of male pink bollworm (Lepidoptera: Gelechiidae) moths in traps baited with sex pheromone. J Econ Entomol 87:986–992

    Google Scholar 

  • Benton TF, Bryant DM, Cole L, Crick HQP (2002) Linking agricultural practice to insect and bird populations: a historical study over three decades. J Appl Ecol 39:673–687

    Article  Google Scholar 

  • Bouma HR, Carey HV, Kroaes FGM (2010) Hibernation: the immune system at rest? J Leukoc Biol 88:619–624

    Article  CAS  PubMed  Google Scholar 

  • Boyles JG, Smit B, McKechnie AE (2011) A new comparative metric for estimating heterothermy in endotherms. Physiol Biochem Zool 84:115–123

    Article  PubMed  Google Scholar 

  • Brigham RM (1991) Flexibility in foraging and roosting behaviour by the big brown bat (Eptesicus fuscus). Can J Zool 69:117–121

    Article  Google Scholar 

  • Brigham RM, Körtner G, Maddocks TA, Geiser F (2000) Seasonal use of torpor by free-ranging Australian Owlet-Nightjars (Aegotheles cristatus). Physiol Biochem Zool 73:613–620

    Article  CAS  PubMed  Google Scholar 

  • Bronson FH (1985) Mammalian reproduction: an ecological perspective. Biol Reprod 32:1–26

    Article  CAS  PubMed  Google Scholar 

  • Bryant DM (1975) Breeding biology of house martins Delichon urbica in relation to aerial insect abundance. Ibis 117:180–216

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference, 2nd edn. Springer Science + Business Media Inc., New York

    Google Scholar 

  • Christian N, Geiser F (2007) To use or not to use torpor? Activity and body temperature as predictors. Naturwissenschaften 94:483–487

    Article  CAS  PubMed  Google Scholar 

  • Chruszcz BJ, Barclay RMR (2003) Prolonged foraging bouts of a solitary gleaning/hawking bat, Myotis evotis. Can J Zool 81:823–826

    Article  Google Scholar 

  • Clark BS, Leslie DMJ, Carter TS (1993) Foraging activity of adult female Ozark big-eared bats (Plecotus townsendii ingens) in summer. J Mammal 74:422–427

    Article  Google Scholar 

  • Cryan PM, Wolf BO (2003) Sex differences in the thermoregulation and evaporative water loss of a heterothermic bat, Lasiurus cinereus, during its spring migration. J Exp Biol 206:3381–3390

    Article  PubMed  Google Scholar 

  • Dietz M, Kalko EKV (2007) Reproduction affects flight activity in female and male Daubenton’s bats, Myotis daubentonii. Can J Zool 86:653–664

    Article  Google Scholar 

  • Doucette LI, Brigham RM, Pavey CR, Geiser F (2012) Prey availability affects daily torpor by free-ranging Australian owlet-nightjars (Aegotheles cristatus). Oecologia 169:361–372

    Article  PubMed  Google Scholar 

  • Dzal Y, Brigham RM (2013) The tradeoff between torpor use and reproduction in little brown bats (Myotis lucifugus). J Comp Physiol B 183:279–288

    Article  PubMed  Google Scholar 

  • Encarnação JA, Dietz M (2006) Estimation of food intake and ingested energy in Daubenton’s bats (Myotis daubentonii) during pregnancy and spermatogenesis. Eur J Wildl Res 52:221–227

    Article  Google Scholar 

  • Geiser F, Brigham RM (2012) The other functions of torpor. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world. Springer, Berlin, pp 109–121

    Chapter  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 

  • 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 

  • Henderson LE, Broders HG (2008) Movements and resource selection of the northern long-eared myotis (Myotis septentrionalis) in a forest-agriculture landscape. J Mammal 89:952–963

    Article  Google Scholar 

  • Jacobs DS, Kelly EJ, Mason M, Stoffberg S (2007) Thermoregulation in two free-ranging subtropical insectivorous bat species: Scotophilus species (Vespertilionidae). Can J Zool 85:883–890

    Article  Google Scholar 

  • Klüg BJ, Barclay RMR (2013) Thermoregulation during reproduction in the solitary, foliage-roosting hoary bat (Lasiurus cinereus). J Mammal 94:477–487

    Article  Google Scholar 

  • Körtner G, Geiser F (2000) The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol Int 17:103–128

    Article  PubMed  Google Scholar 

  • Kunz TH, Witaker JO Jr, Wadanoli WD (1995) Dietary energetics of the insectivorous Mexican free-tailed bat (Tadarida brasiliensis) during pregnancy and lactation. Oecologia 101:407–415

    Article  Google Scholar 

  • Kusch J, Weber C, Idelberger S, Koob T (2004) Foraging habitat preferences of bats in relation to food supply and spatial vegetation structures in a western European low mountain range forest. Folia Zool 53:113–128

    Google Scholar 

  • 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 

  • Lausen CL, Barclay RMR (2006) Benefits of living in a building: big brown bats (Eptesicus fuscus) in rocks versus buildings. J Mammal 87:362–370

    Article  Google Scholar 

  • Lovegrove BG, Körtner G, Geiser F (1999) The energetic cost of arousal from torpor in the marsupial Sminthopsis macroura: benefits of summer ambient temperature cycles. J Comp Physiol B 169:11–18

    Article  CAS  PubMed  Google Scholar 

  • Lučan R, Radil J (2010) Variability of foraging and roosting activities in adult females of Daubenton’s bat (Myotis daubentonii) in different seasons. Biologia 65:1072–1080

    Article  Google Scholar 

  • McLean JA, Speakman JR (1999) Energy budgets of lactating and non-reproductive brown long-eared bats (Plecotus auritus) suggest females use compensation in lactation. Funct Ecol 13:360–372

    Article  Google Scholar 

  • Munn AJ, Kern P, McAllan BM (2010) Coping with chaos: unpredictable food supplies intensify torpor use in an arid-zone marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). Naturwissenschaften 97:601–605

    Article  CAS  PubMed  Google Scholar 

  • Norberg UM, Rayner JMV (1987) Ecological morphology and flight in bats (Mammalia: Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philos Trans R Soc B 316:335–427

    Article  Google Scholar 

  • O’Donnell CFJ (2002) Influence of sex and reproductive status on nocturnal activity of long-tailed bats (Chalinolobus tuberculatus). J Mammal 83:794–803

    Article  Google Scholar 

  • Oelkrug R, Heldmaier G, Meyer CW (2011) Torpor patterns, arousal rates, and temporal organization of torpor entry in wildtype and UCP1-ablated mice. J Comp Physiol B 181:137–145

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Racey PA (1973) Environmental factors affecting the length of gestation in heterothermic bats. J Reprod Fertil S19:175–189

    Google Scholar 

  • Racey PA (1988) Reproductive assessment in bats. In: Kunz TH (ed) Ecology and behavioral methods for the study of bats. Smithsonian Institution Press, Washington, DC, pp 31–43

    Google Scholar 

  • Racey PA, Speakman JR (1987) The energy costs of pregnancy and lactation in heterothermic bats. Symp Zool Soc Lond 57:107–125

    Google Scholar 

  • Racey PA, Swift SM (1981) Variations in gestation length in a colony of pipistrelle bats (Pipistrellus pipistrellus) from year to year. J Reprod Fertil 61:123–129

    Article  CAS  PubMed  Google Scholar 

  • Sano A (2000) Postnatal growth and development of thermoregulative ability in the Japanese greater horseshoe bat, Rhinolophus ferrumequinum nippon, related to maternal care. Mammal Study 25:1–15

    Article  Google Scholar 

  • Scholander PF (1955) Evolution of climatic adaptation in homeotherms. Evolution 9:15–26

    Article  Google Scholar 

  • Speakman JR (2008) The physiological costs of reproduction in small mammals. Philos Trans R Soc B 363:375–398

    Article  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, New York, pp 367–393

    Google Scholar 

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

    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 

  • Wang LCH (1989) Ecological, physiological, and biochemical aspects of torpor in mammals and birds. In: Wang LCH (ed) Animal adaptations to cold, vol 4., Advances in comparative and environmental physiologySpringer, New York, pp 361–401

    Chapter  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 

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

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson LC, Barclay RMR (1997) Differences in the foraging behaviour of male and female big brown bats (Eptesicus fuscus) during the reproductive period. Ecoscience 4:279–285

    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, 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 

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

    Article  CAS  PubMed  Google Scholar 

  • Wojciechowski MS, Jefimow M, Tegowska E (2007) Environmental conditions, rather than season, determine torpor use and temperature selection in large mouse-eared bats (Myotis myotis). Comp Biochem Physiol A Mol Integ Physiol 147:828–840

    Article  Google Scholar 

  • Zahn A (1999) Reproductive success, colony size and roost temperature in attic-dwelling bat Myotis myotis. J Zool 247:275–280

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful for the thoughtful comments and suggestions from 3 anonymous reviewers, B. Klüg, P. Preston, C. Gaudet, and L. Heisler. N. and R. MacDougald and M. and D. Hoffer provided access to bat colonies. We thank P. Preston, S. Jaques, E. Boutillier and T. Allen for assistance in the field. Natural Sciences and Engineering Research Council Discovery Grants (RMB), University of Regina Faculty of Graduate Studies and Research and Fish and Wildlife Development Fund, Cypress Hills Interprovincial Park (JLPR) provided support for this study.

Author information

Authors and Affiliations

  1. Biology Department, University of Regina, 3737 Wascana Parkway, Regina, SK, S4S 0A2, Canada

    Jody L. P. Rintoul & R. Mark Brigham

Authors
  1. Jody L. P. Rintoul
    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 Jody L. P. Rintoul.

Additional information

Communicated by H.V. Carey.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rintoul, J.L.P., Brigham, R.M. The influence of reproductive condition and concurrent environmental factors on torpor and foraging patterns in female big brown bats (Eptesicus fuscus). J Comp Physiol B 184, 777–787 (2014). https://doi.org/10.1007/s00360-014-0837-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-014-0837-9

Keywords

Search

Navigation