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Winter torpor expression varies in four bat species with differential susceptibility to white-nose syndrome

  • Wang, L.C.H. Ecological, physiological, and biochemical aspects of torpor in mammals and birds in Advances in comparative and environmental physiology (ed. Wang, L.C.H.) 361–401 (Springer, 1989).

  • Humphries, M.M., Speakman, J.R., & Thomas, D.W. Temperature, hibernation energetics, and the cave and continental distributions of little brown myotis in Functional and Evolutionary Ecology of Bats (ed. Zubaid, A., McCracken, G.F., & Kunz, T.H.) 23–37 (Oxford Press, 2005).

  • Hudson, J.W. Torpidity in mammals in Comparative physiology of thermoregulation. (ed. Whittow, G.C., Hudson, J.W., & Deavers, D.R.) 97–165 (Academic Press, 1973).

  • Geiser, F. & Ruf, T. Hibernation versus daily torpor in mammals and birds: Physiological variables and classification of torpor patterns. Phys. Zool. 68, 935–966 (1995).

    Article 

    Google Scholar 

  • Davis, W. H. & Hitchcock, H. B. Biology and migration of the bat, Myotis lucifugus, New England. J. Mamm. 46, 296–313. https://doi.org/10.2307/1377850 (1965).

    Article 

    Google Scholar 

  • Speakman, J. R. & Rowland, A. Preparing for inactivity: How insectivorous bats deposit a fat store for hibernation. Proc. Nutr. Soc. 58, 123–131. https://doi.org/10.1079/PNS19990017 (1999).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Boyles, J. G., Johnson, J. S., Blomberg, A. & Lilley, T. M. Optimal hibernation theory. Mammal Rev. 50, 91–100. https://doi.org/10.1111/mam.12181 (2020).

    Article 

    Google Scholar 

  • Britzke, E. R., Sewell, P., Hohmann, M. G., Smith, R. & Scott, R. Use of temperature-sensitive transmitters to monitor the temperature profiles of hibernating bats affected with white-nose syndrome. Northeast. Nat. 17, 239–246. https://doi.org/10.1656/045.017.0207 (2010).

    Article 

    Google Scholar 

  • Halsall, A. L., Boyles, J. G. & Whitaker, J. O. Jr. Body temperature patterns of big browns during winter in a building hibernaculum. J. Mamm. 93, 497–503. https://doi.org/10.1644/11-MAMM-A-262.1 (2012).

    Article 

    Google Scholar 

  • Johnson, J. S., Lacki, M. J., Thomas, S. C. & Grider, J. F. Frequent arousals from winter torpor in Rafinesque’s big-eared bat (Corynorhinus rafinesquii). PLoS ONE 7, e49754. https://doi.org/10.1371/journal.pone.0049754 (2012).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jonasson, K. A. & Willis, C. K. R. Hibernation energetics of free-ranging little brown bats. J. Exp. Bio. 215, 2141–2149. https://doi.org/10.1242/jeb.066514 (2012).

    Article 

    Google Scholar 

  • Day, K. M. & Tomasi, T. E. Winter energetics of female Indiana bats Myotis sodalis. Physiol. Biochem. Zool. 87, 56–64. https://doi.org/10.1086/671563 (2014).

    Article 
    PubMed 

    Google Scholar 

  • Meierhofer, M. B. et al. Winter habitats of bats in Texas. PLoS ONE 14, e0220839. https://doi.org/10.1371/journal.pone.0220839 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Boyles, J. G. Benefits of knowing the costs of disturbance to hibernating bats. Wildl. Soc. Bull. 41, 388–392. https://doi.org/10.1002/wsb.755 (2017).

    Article 

    Google Scholar 

  • Frick, W. F. et al. Pathogen dynamics during invasion and establishment of white-nose syndrome explain mechanisms of host persistence. Ecology 98, 624–631. https://doi.org/10.1002/ecy.1706 (2017).

    Article 
    PubMed 

    Google Scholar 

  • Cheng, T. L. et al. The scope and severity of white-nose syndrome on hibernating bats in North America. Conserv. Biol. 35, 1586–1597. https://doi.org/10.1111/cobi.13739 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cryan, P. M., Meteyer, C. U., Boyles, J. G. & Blehert, D. S. Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. BMC Biol. 8, 1–8 (2010).

    Article 

    Google Scholar 

  • Cryan, P. M. et al. Electrolyte depletion in white-nose syndrome bats. J. Wild. Dis. 49, 398–402 (2013).

    CAS 
    Article 

    Google Scholar 

  • Frick, W. F. et al. Disease alters macroecological patterns of North American bats. Glob. Ecol. Biogeogr. 24, 741–749. https://doi.org/10.1111/geb.12290 (2015).

    Article 

    Google Scholar 

  • Bernard, R.F., Willcox, E.V., Parise, K.L., Foster, J.T., & McCracken, G.F. White-nose syndrome fungus, Pseudogymnoascus destructans, on bats captured emerging from caves during winter in the southeastern United States. BMC Zool. https://doi.org/10.1186/s40850-017-0021-2 (2017).

  • Davy, C. M. et al. The other white-nose syndrome transcriptome: Tolerant and susceptible hosts respond differently to the pathogen Pseudogymnoascus destructans. Ecol. Evol. 7, 7161–7170. https://doi.org/10.1002/ece3.3234 (2015).

    Article 

    Google Scholar 

  • Lilley, T. M. et al. Resistance is futile: RNA-sequencing reveals differing responses to bat fungal pathogen in Nearctic Myotis lucifugus and Palearctic Myotis myotis. Oecologia 191, 295–309. https://doi.org/10.1007/s00442-019-04499-6 (2019).

    ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bernard, R. F. & McCracken, G. F. Winter behavior of bats and the progression of white-nose syndrome in the southeastern United States. Ecol. Evol. 7, 1487–1496. https://doi.org/10.1002/ece3.2772 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Moosman, P.R., Warner, D.P., Hendren, R.H., & Hosler, M.J. Potential for monitoring eastern small-footed bats on talus slopes. Northeast. Nat. https://www.jstor.org/stable/26453719 (2015).

  • Bernard, R. F. et al. Identifying research needs to inform white-nose syndrome management decisions. Cons. Sci. Prac. 2(e220), 2020. https://doi.org/10.1111/csp2.220 (2020).

    Article 

    Google Scholar 

  • Reynolds, D. S., Shoemaker, K., Oettingen, S. V. & Najjar, S. High rates of winter activity and arousals in two New England bat species: implications for a reduced white-nose syndrome impact?. Northeast. Nat. 24, B188–B208. https://doi.org/10.1656/045.024.s720 (2017).

    Article 

    Google Scholar 

  • Bernard, R. F., Willcox, E. V., Jackson, R. T., Brown, V. A. & McCracken, G. F. Feasting, not fasting: Winter diets of cave hibernating bats in the United States. Front. Zool. 18, 1–13. https://doi.org/10.1186/s12983-021-00434-9 (2021).

    Article 

    Google Scholar 

  • Prendergast, B. J., Freeman, D. A., Zucker, I. & Nelson, R. J. Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. Am. J. Phys. 282, 1054–1062. https://doi.org/10.1152/ajpregu.00562.2001 (2002).

    Article 

    Google Scholar 

  • Dobony, C. A. et al. Little brown myotis persist despite exposure to white-nose syndrome. J. Fish Wild. 2, 190–195. https://doi.org/10.3996/022011-JFWM-014 (2011).

    Article 

    Google Scholar 

  • Rowley, J. J. & Alford, R. A. Hot bodies protect amphibians against chytrid infection in nature. Sci. Rep. 3, 1–4. https://doi.org/10.1038/srep01515 (2013).

    CAS 
    Article 

    Google Scholar 

  • Verant, M. L. et al. White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. BMC Physiol. 14, 10 (2014).

    Article 

    Google Scholar 

  • Verant, M. L. et al. Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. PLoS ONE 7, e46280. https://doi.org/10.1371/journal.pone.0046280 (2012).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Brownlee-Bouboulis, S. A. & Reeder, D. M. White-nose syndrome-affected little brown Myotis (Myotis lucifugus) increase grooming and other active behaviors during arousals from hibernation. J. Wildl. Dis. 49, 850–859. https://doi.org/10.7589/2012-10-242 (2013).

    Article 
    PubMed 

    Google Scholar 

  • Campbell, J. Tennessee winter bat population and white-nose syndrome monitoring report for 2018–2019. TWRA Wildlife Technical Report 16-4. http://www.tnbwg.org/2019%20Annual%20Monitoring%20Report.pdf (2019).

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

    Article 

    Google Scholar 

  • Langwig, K.E., et al. Drivers of variation in species impacts for a multi-host fungal disease of bats. Philos. Trans. R. Soc. B Biol. Sci. 371, 20150456. https://doi.org/10.1098/rstb.2015.0456 (2016).

  • Aldridge, H.D.J.N., & Brigham, R.M. Load carrying and maneuverability in an insectivorous bat: A test of the 5% ‘rule’ of radio-telemetry. J. Mamm. 69, 379–382. https://doi.org/10.2307/1381393 (1988)

  • Sikes, R. S. et al. Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J. Mamm. 97, 663–688. https://doi.org/10.1093/jmammal/gyw078 (2016).

    Article 

    Google Scholar 

  • Barclay, R. M. R. et al. Can external radiotransmitters be used to assess body temperature and torpor in bats?. J. Mammal. 77, 1102–1106. https://doi.org/10.2307/1382791 (1996).

    Article 

    Google Scholar 

  • Turbill, C., & Geiser, F. Hibernation by tree-roosting bats. J. Comp. Physiol. B. 178, 597–605. https://doi.org/10.1007/s00360-007-0249-1 (2008)

  • 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).

  • Reeder, D. M. et al. Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS ONE 7, e38920. https://doi.org/10.1371/journal.pone.0038920 (2012).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sirajuddin, P. Vulnerability of tri-colored bats (Perimyotis subflavus) to white-nose syndrome in the southeastern United States. M.S thesis at https://www.proquest.com/dissertations-theses/vulnerability-tri-colored-bats-i-perimyotis/docview/2185672601/se-2?accountid=8361 (2018).

  • R Development Core Team 3.6.1. A Language and Environment for Statistical Computing. http://www.r-project.org (2019).

  • Bates, D., Maechler, M., Bolker, B., & Walker, S. lme4: Linear mixed-effects models using ‘Eigen’ and S4. R Packag. version 1.1-13. ftp://cran.r-project.org/pub/R/web/packages/lme4/lme4.pdf. (2017)

  • Czenze, Z. J. & Willis, C. K. R. Warming up and shipping out: Arousal and emergence timing in hibernating little brown bats (Myotis lucifugus). J. Comp. Physiol. B-Biochem. Syst. Environ. Physiol. 185, 575–586. https://doi.org/10.1007/s00360-015-0900-1 (2015).

    Article 

    Google Scholar 

  • Conover, W.J. Practical Nonparametric Statistics. (Wiley, 1999).

  • Crawley, M.J. The R Book: Second Edition. (Wiley, 2013)

  • Lenth, R., Singmann, H., Love, J., Buerkner, P., & Herve, M. Package ‘emmeans’. R Packag. version 1.7.0. https://cran.r-project.org/web/packages/emmeans/emmeans.pdf (2021)

  • Best, T.L. & Jennings, J.B. Myotis leibii. Mammalian Species 547, 1–6. https://doi.org/10.2307/3504255 (1997)

  • Frank, C.L., Herzog, C.,. Laske, J.P., & Cardino V. The role of skin temperature in the resistance of Myotis leibii to white-nose syndrome presented at the 49th Symposium of the North American Society for Bat Research, Kalamazoo, Michigan https://www.nasbr.org/resources/docs/meetings/year/2019/NASBR-2019-Abstracts-Draft-191001.pdf (2019)

  • Johnson, J.S., Scafini, M.R., Sewall, B.J., & Turner, G.G. Hibernating bat species in Pennsylvania use colder winter habitats following the arrival of white-nose syndrome in Conservation and Ecology of Pennsylvania’s Bats (ed. Butchkoski, C.M., Reeder, D.M., Turner, G.G., & Whidden, H.P) 181–199 (The Pennsylvania Academy of Science, 2016)

  • Haase, C.G., et al. Body mass and hibernation microclimate may predict bat susceptibility to white‐nose syndrome. Eco. Evo. 11, 506–515 https://doi.org/10.1002/ece3.7070 (2021)

  • Veilleux, J.P. A Noteworthy Hibernation Record of Myotis leibii (Eastern Small-footed Bat) in Massachusetts. Northeast. Nat. 14, 501–502 https://doi.org/10.1656/1092-6194(2007)14[501:ANHROM]2.0.CO;2 (2007)

  • Boyles, J. G., Dunbar, M. B. & Whitaker, J. O. Activity following arousal in winter in North American vespertilionid bats. Mamm. Rev. 36, 267–280. https://doi.org/10.1111/j.1365-2907.2006.00095.x (2006).

    Article 

    Google Scholar 

  • Webb, P. I., Speakman, J. R. & Racey, P. A. How hot is a hibernaculum? A review of the temperatures at which bats hibernate. Can. J. Zool. 74, 761–765. https://doi.org/10.1139/z96-087 (1996).

    Article 

    Google Scholar 

  • Jackson, R.T., Willcox, E.V., Zobel, J.M., & Bernard, R.F. Hibernation behavior of four bat species with differing susceptibility to white-nose syndrome. In review (2021).

  • Fujita, M. S. & Kunz, T. H. Pipstrellus subflavus. Mamm. Spec. 228, 1–6. https://doi.org/10.2307/3504021 (1984).

    Article 

    Google Scholar 

  • Bohn, S. J. et al. Evidence of ‘sickness behaviour’ in bats with white-nose syndrome. Behaviour 152, 981–1003. https://doi.org/10.1163/1568539X-00003384 (2016).

    Article 

    Google Scholar 

  • Tuttle, M. D. Status, causes of decline, and management of endangered gray bats. J. Wild. Manag. 43, 1–17. https://doi.org/10.2307/3800631 (1979).

    Article 

    Google Scholar 

  • Harvey, M.J., Altenbach, J.S., & Best, T.L. Bats of the Eastern United States. (JHU Press, 2011).

  • Klüg-Baerwald, B. J., Lausen, C. L., Willis, C. K. & Brigham, R. M. Home is where you hang your bat: Winter roost selection by prairie-living big brown bats. J. Mamm. 98, 752–760. https://doi.org/10.1093/jmammal/gyx039 (2017).

    Article 

    Google Scholar 

  • Sandel, J. K. et al. Use and selection of winter hibernacula by the eastern pipistrelle (Pipistrellus subflavus) in Texas. J. Mamm. 82, 173–178. https://doi.org/10.1644/1545-1542(2001)082%3c0173:UASOWH%3e2.0.CO;2 (2001).

    Article 

    Google Scholar 

  • Hayes, J. P., Ober, H. K., Sherwin, R. E. Survey and monitoring of bats in Ecological and behavioral methods for the study of bats (ed. Kunz, T. H., Parsons, S.). 120–129 (JHU Press, 2009).


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