Energy conserving thermoregulatory patterns and lower disease severity in a bat resistant to the impacts of white-nose syndrome
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The devastating bat fungal disease, white-nose syndrome (WNS), does not appear to affect all species equally. To experimentally determine susceptibility differences between species, we exposed hibernating naïve little brown myotis (Myotis lucifugus) and big brown bats (Eptesicus fuscus) to the fungus that causes WNS, Pseudogymnoascus destructans (Pd). After hibernating under identical conditions, Pd lesions were significantly more prevalent and more severe in little brown myotis. This species difference in pathology correlates with susceptibility to WNS in the wild and suggests that survival is related to different host physiological responses. We observed another fungal infection, associated with neutrophilic inflammation, that was equally present in all bats. This suggests that both species are capable of generating a response to cold tolerant fungi and that Pd may have evolved mechanisms for evading host responses that are effective in at least some bat species. These host–pathogen interactions are likely mediated not just by host physiological responses, but also by host behavior. Pd-exposed big brown bats, the less affected species, spent more time in torpor than did control animals, while little brown myotis did not exhibit this change. This differential thermoregulatory response to Pd infection by big brown bat hosts may allow for a more effective (or less pathological) immune response to tissue invasion.
KeywordsWhite-nose syndrome Pseudogymnoascus destructans Myotis lucifugus Eptesicus fuscus Fungal pathogen Species differences
This study was supported by the United States Fish and Wildlife Service (F11AP00073 to DMR) and the National Science Foundation (DEB-1115895 to WFF and JTF). MSM was partially supported by the National Institute of General Medicine Sciences of the National Institutes of Health (K12GM102778). We thank Cindy Rhone and Gretchen Long for animal care assistance and Kevin Keel for providing P. destructans isolate used for inoculations.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of Bucknell University (see “Materials and methods” for further description).
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57:289–300Google Scholar
- Chaturvedi V, Springer DJ, Behr MJ, Ramani R, Li X, Peck MK, Ren P, Bopp DJ, Wood B, Samsonoff WA, Butchkoski CM (2010) Morphological and molecular characterizations of psychrophilic fungus Geomyces destructans from New York bats with white nose syndrome (WNS). PLoS One 5:e10783CrossRefPubMedPubMedCentralGoogle Scholar
- Johnson JS, Reeder DM, McMichael JW 3rd, Meierhofer MB, Stern DW, Lumadue SS, Sigler LE, Winters HD, Vodzak ME, Kurta A et al (2014) Host, pathogen, and environmental characteristics predict white-nose syndrome mortality in captive little brown myotis (Myotis lucifugus). PLoS One 9:e112502CrossRefPubMedPubMedCentralGoogle Scholar
- Johnson JS, Reeder DM, Lilley TM, Czirják GÁ, Voigt CC, McMichael JW 3rd, Meierhofer MB, Seery CW, Lumadue SS, Altmann AJ et al (2015) Antibodies to Pseudogymnoascus destructans are not sufficient for protection against white-nose syndrome. Ecol Evol 5:2203–2214CrossRefPubMedPubMedCentralGoogle Scholar
- Turner GG, Reeder DM, Coleman JTH (2011) A five-year assessment of mortality and geographic spread of white-nose syndrome in North American bats and a look to the future. Bat Res News 52:13–27Google Scholar
- Turner GG, Meteyer CU, Barton H, Gumbs JF, Reeder DM, Overton B, Bandouchova H, Bartonicka T, Martinkova N, Pikula J et al (2014) Nonlethal screening of bat-wing skin with the use of ultraviolet fluorescence to detect lesions indicative of white-nose syndrome. J Wildlife Dis 50:566–573CrossRefGoogle Scholar
- USFWS (2012) News Release: North American bat death toll exceeds 5.5 million from white-nose syndrome. http://www.fws.gov/whitenosesyndrome/pdf/WNS_Mortality_2012_NR_FINAL.pdf. Accessed 4 May 2012
- Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misra V, Cryan PM, Wibbelt G, Blehert DS, Willis CKR (2012) Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Nat Acad Sci USA 109:6999–7003CrossRefPubMedPubMedCentralGoogle Scholar