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Interspecific variation in evaporative water loss and temperature response, but not metabolic rate, among hibernating bats

  • 1.

    Lyman, C. P. & Chatfield, P. O. Physiology of hibernation in mammals. Physiol. Rev. 35, 403–425 (1955).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 2.

    Geiser, F. Hibernation. Curr. Biol. 23, R188–R193 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 3.

    Humphries, M. M., Thomas, D. W. & Speakman, J. R. Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature 418, 313–316 (2002).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 4.

    Wilkinson, G. S. & Adams, D. M. Recurrent evolution of extreme longevity in bats. Biol. Lett. 15, 20180860 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 5.

    Frick, W. F., Reynolds, D. S. & Kunz, T. H. Influence of climate and reproductive timing on demography of little brown myotis Myotis lucifugus. J. Anim. Ecol. 79, 128–136 (2010).

    PubMed 
    Article 

    Google Scholar 

  • 6.

    Willis, C. K. Trade-offs influencing the physiological ecology of hibernation in temperate-zone bats. Integr. Comp. Biol. 57, 1214–1224 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 7.

    Lane, J. E. In Living in a Seasonal World 51–61 (Springer, 2012).

  • 8.

    Inouye, D. W., Barr, B., Armitage, K. B. & Inouye, B. D. Climate change is affecting altitudinal migrants and hibernating species. Proc. Natl. Acad. Sci. 97, 1630–1633 (2000).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 9.

    Lane, J. E., Kruuk, L. E., Charmantier, A., Murie, J. O. & Dobson, F. S. Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature 489, 554–557 (2012).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 10.

    Feder, M. E. In New Directions in Ecological Physiology (eds M. E. Feder, A. F. Bennett, W. W. Burggren, & R. B Huey) 38–75 (Cambridge University Press, 1987).

  • 11.

    Geiser, F. Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66, 239–274. https://doi.org/10.1146/annurev.physiol.66.032102.115105 (2004).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 12.

    Boyles, J. G. et al. A global heterothermic continuum in mammals. Glob. Ecol. Biogeogr. 22, 1029–1039 (2013).

    Article 

    Google Scholar 

  • 13.

    Ruf, T. & Arnold, W. Effects of polyunsaturated fatty acids on hibernation and torpor: A review and hypothesis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1044-1052. https://doi.org/10.1152/ajpregu.00688.2007 (2008).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 14.

    Ruf, T. & Geiser, F. Daily torpor and hibernation in birds and mammals. Biol. Rev. Camb. Philos. Soc. https://doi.org/10.1111/brv.12137 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 15.

    Heldmaier, G., Ortmann, S. & Elvert, R. Natural hypometabolism during hibernation and daily torpor in mammals. Respir. Physiol. Neurobiol. 141, 317–329 (2004).

    PubMed 
    Article 

    Google Scholar 

  • 16.

    van Breukelen, F. & Martin, S. L. The hibernation continuum: Physiological and molecular aspects of metabolic plasticity in mammals. Physiology 30, 273–281 (2015).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 17.

    Nowack, J., Levesque, D. L., Reher, S. & Dausmann, K. H. Variable climates lead to varying phenotypes: ‘Weird’mammalian torpor and lessons from non-Holarctic species. Front. Ecol. Evol. 8, 60 (2020).

    Article 

    Google Scholar 

  • 18.

    Stawski, C., Willis, C. & Geiser, F. The importance of temporal heterothermy in bats. J. Zool. 292, 86–100 (2014).

    Article 

    Google Scholar 

  • 19.

    Thomas, D. W., Dorais, M. & Bergeron, J.-M. Winter energy budgets and cost of arousals for hibernating little brown bats, Myotis lucifugus. J. Mammal. 71, 475–479 (1990).

    Article 

    Google Scholar 

  • 20.

    Kunz, T. H., Wrazen, J. A. & Burnett, C. D. Changes in body mass and fat reserves in pre-hibernating little brown bats (Myotis lucifugus). Ecoscience 5, 8–17 (1998).

    Article 

    Google Scholar 

  • 21.

    Thomas, D. W. & Cloutier, D. Evaporative water loss by hibernating little brown bats, Myotis lucifugus. Physiol. Zool. 65, 443–456 (1992).

    Article 

    Google Scholar 

  • 22.

    Kornfeld, S. F., Biggar, K. K. & Storey, K. B. Differential expression of mature microRNAs involved in muscle maintenance of hibernating little brown bats, Myotis lucifugus: A model of muscle atrophy resistance. Genom. Proteom. Bioinform. 10, 295–301 (2012).

    CAS 
    Article 

    Google Scholar 

  • 23.

    Eddy, S. F., Morin, P. Jr. & Storey, K. B. Differential expression of selected mitochondrial genes in hibernating little brown bats, Myotis lucifugus. J. Exp. Zool. A Comp. Exp. Biol. 305, 620–630 (2006).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 24.

    Brigham, R., Ianuzzo, C., Hamilton, N. & Fenton, M. Histochemical and biochemical plasticity of muscle fibers in the little brown bat (Myotis lucifugus). J. Comp. Physiol. B. 160, 183–186 (1990).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 25.

    McGuire, L. P., Mayberry, H. W. & Willis, C. K. R. White-nose syndrome increases torpid metabolic rate and evaporative water loss in hibernating bats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 313, R680–R686 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 26.

    Jonasson, K. A. & Willis, C. K. Hibernation energetics of free-ranging little brown bats. J. Exp. Biol. 215, 2141–2149 (2012).

    PubMed 
    Article 

    Google Scholar 

  • 27.

    Klüg-Baerwald, B. J. & Brigham, R. M. Hung out to dry? Intraspecific variation in water loss in a hibernating bat. Oecologia 183, 977–985 (2017).

    ADS 
    PubMed 
    Article 

    Google Scholar 

  • 28.

    Dunbar, M. B. & Brigham, R. M. Thermoregulatory variation among populations of bats along a latitudinal gradient. J. Comp. Physiol. B 180, 885–893 (2010).

    PubMed 
    Article 

    Google Scholar 

  • 29.

    Yacoe, M. E. Protein metabolism in the pectoralis muscle and liver of hibernating bats, Eptesicus fuscus. J. Comp. Physiol. 152, 137–144 (1983).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 30.

    Yacoe, M. E. Maintenance of the pectoralis muscle during hibernation in the big brown bat, Eptesicus fuscus. J. Comp. Physiol. 152, 97–104 (1983).

    Article 

    Google Scholar 

  • 31.

    Twente, J. W. & Twente, J. Biological alarm clock arouses hibernating big brown bats, Eptesicus fuscus. Can. J. Zool. 65, 1668–1674 (1987).

    Article 

    Google Scholar 

  • 32.

    Boratyński, J. S., Willis, C. K., Jefimow, M. & Wojciechowski, M. S. Huddling reduces evaporative water loss in torpid Natterer’s bats, Myotis nattereri. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 179, 125–132 (2015).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 33.

    Hope, P. R. & Jones, G. Warming up for dinner: Torpor and arousal in hibernating Natterer’s bats (Myotis nattereri) studied by radio telemetry. J. Comp. Physiol. B. 182, 569–578 (2012).

    PubMed 
    Article 

    Google Scholar 

  • 34.

    Park, K. J., Jones, G. & Ransome, R. D. Torpor, arousal and activity of hibernating greater horseshoe bats (Rhinolophus ferrumequinum). Funct. Ecol. 14, 580–588 (2000).

    Article 

    Google Scholar 

  • 35.

    Ben-Hamo, M., Muñoz-Garcia, A., Williams, J. B., Korine, C. & Pinshow, B. Waking to drink: Rates of evaporative water loss determine arousal frequency in hibernating bats. J. Exp. Biol. 216, 573–577 (2013).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 36.

    Lausen, C. & Barclay, R. Winter bat activity in the Canadian prairies. Can. J. Zool. 84, 1079–1086 (2006).

    Article 

    Google Scholar 

  • 37.

    McGuire, L. P. et al. Similar physiology in hibernating bats across broad geographic ranges. J. Comp. Physiol. B. https://doi.org/10.1007/s00360-021-01400-x (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 38.

    Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, New York, 2009).

    MATH 
    Book 

    Google Scholar 

  • 39.

    Hothorn, T. & Everitt, B. S. A handbook of statistical analyses using R (CRC Press, London, 2014).

    MATH 
    Book 

    Google Scholar 

  • 40.

    United States Fish and Wildlife Service. National white-nose syndrome decontamination protocol-Version 09-13-2018. http://www.whitenosesyndrome.org (2018).

  • 41.

    Canadian Cooperative Wildlife Health Centre. Guidelines for decontamination of equipment and clothing to prevent the spread of white-nose syndrome (the causal fungus: Pseudogymnoascus destructans) in Canada, http://www2.cwhc-rcsf.ca/wns_decontamination.php (2020).

  • 42.

    R: A language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria, 2020).

  • 43.

    McGuire, L. P., Guglielmo, C. G., Mackenzie, S. A. & Taylor, P. D. Migratory stopover in the long-distance migrant silver-haired bat, Lasionycteris noctivagans. J. Anim. Ecol. 81, 377–385 (2012).

    PubMed 
    Article 

    Google Scholar 

  • 44.

    Nagorsen, D. W. & Brigham, R. M. Bats of British Columbia. Vol. 1 (UBC Press, 1993).

  • 45.

    Villa, B. R. & Cockrum, E. L. Migration in the guano bat Tadarida brasiliensis mexicana (Saussure). J. Mammal. 43, 43–64 (1962).

    Article 

    Google Scholar 

  • 46.

    Kunkel, E. L. Ecology and energetics of partial migration and facultative hibernation of Mexican free-tailed bats MS thesis, Texas Tech University (2020).

  • 47.

    Sandel, J. K. et al. Use and selection of winter hibernacula by the eastern pipistrelle (Pipistrellus subflavus) in Texas. J. Mammal. 82, 173–178 (2001).

    Article 

    Google Scholar 

  • 48.

    Jones, C. & Pagels, J. Notes on a population of Pipistrellus subflavus in southern Louisiana. J. Mammal. 49, 134–139 (1968).

    Article 

    Google Scholar 

  • 49.

    McClure, M. M. et al. A hybrid corelative-mechanistic approach for modeling and mapping winter distributions of North American bat species. J. Biogeogr. 48, 2429–2444 (2021).

    Article 

    Google Scholar 

  • 50.

    McClure, M. M. et al. Linking surface and subterranean climate: Implications for the study of hibernating bats and other cave dwellers. Ecosphere 11, E03274 (2020).

    Article 

    Google Scholar 

  • 51.

    Perry, R. W. A review of factors affecting cave climates for hibernating bats in temperate North America. Environ. Rev. 21, 28–39. https://doi.org/10.1139/er-2012-0042 (2013).

    Article 

    Google Scholar 

  • 52.

    Hranac, C. R. et al. What is winter? Modelling spatial variation in bat host traits and hibernation and their implications for overwintering energetics. Ecol. Evol. 11, 11604–11614 (2021).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 53.

    McGuire, L., Muise, K. A., Shrivastav, A. & Willis, C. K. R. No evidence of hyperphagia during prehibernation in a northern population of little brown bats (Myotis lucifugus). Can. J. Zool. 94, 821–827 (2016).

    CAS 
    Article 

    Google Scholar 

  • 54.

    Czenze, Z. J., Jonasson, K. A. & Willis, C. K. Thrifty females, frisky males: Winter energetics of hibernating bats from a cold climate. Physiol. Biochem. Zool. 90, 502–511 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 55.

    Kurta, A. The misuse of relative humidity in ecological studies of hibernating bats. Acta Chiropt. 16, 249–254 (2014).

    Article 

    Google Scholar 

  • 56.

    Weller, T. J. et al. A review of bat hibernacula across the western United States: Implications for white-nose syndrome surveillance and management. PLoS One 13, e0205647 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 57.

    Gearhart, C., Adams, A. M., Pinshow, B. & Korine, C. Evaporative water loss in Kuhl’s pipistrelles declines along an environmental gradient, from mesic to hyperarid. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 240, 110587 (2020).

    CAS 
    Article 

    Google Scholar 

  • 58.

    Thomas, D. W. & Geiser, F. Periodic arousals in hibernating mammals: Is evaporative water loss involved?. Funct. Ecol. 11, 585–591 (1997).

    Article 

    Google Scholar 

  • 59.

    Haase, C. G. et al. Incorporating evaporative water loss into bioenergetic models of hibernation to test for relative influence of host and pathogen traits on white-nose syndrome. PLoS One 14, e0222311 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 60.

    Willis, C. K. Conservation physiology and conservation pathogens: White-nose syndrome and integrative biology for host–pathogen systems. Integr. Comp. Biol. 55, 631–641 (2015).

    PubMed 
    Article 

    Google Scholar 

  • 61.

    Frick, W. F. et al. Disease alters macroecological patterns of North American bats. Glob. Ecol. Biogeogr. 24, 741–749 (2015).

    Article 

    Google Scholar 

  • 62.

    Willis, C. K., Menzies, A. K., Boyles, J. G. & Wojciechowski, M. S. Evaporative water loss is a plausible explanation for mortality of bats from white-nose syndrome. Integr. Comp. Biol. 51, 364–373. https://doi.org/10.1093/icb/icr076 (2011).

    Article 
    PubMed 

    Google Scholar 

  • 63.

    Wilder, A. P., Frick, W. F., Langwig, K. E. & Kunz, T. H. Risk factors associated with mortality from white-nose syndrome among hibernating bat colonies. Biol. Lett. 7, 950–953 (2011).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 64.

    Langwig, K. E. et al. Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecol. Lett. 15, 1050–1057. https://doi.org/10.1111/j.1461-0248.2012.01829.x (2012).

    Article 
    PubMed 

    Google Scholar 

  • 65.

    Voigt, C. C. & Kingston, T. Bats in the Anthropocene: Conservation of Bats in a Changing World (Springer, New York, 2016).

    Book 

    Google Scholar 

  • 66.

    Kahle, D. & Wickham, H. ggmap: Spatial visualization with ggplot2. R J. 5, 144–161 (2013).

    Article 

    Google Scholar 


  • Source: Ecology - nature.com

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