Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Ecology and impacts of white-nose syndrome on bats

Abstract

The recent introduction of Pseudogymnoascus destructans (the fungal pathogen that causes white-nose syndrome in bats) from Eurasia to North America has resulted in the collapse of North American bat populations and restructured species communities. The long evolutionary history between P. destructans and bats in Eurasia makes understanding host life history essential to uncovering the ecology of P. destructans. In this Review, we combine information on pathogen and host biology to understand the patterns of P. destructans spread, seasonal transmission ecology, the pathogenesis of white-nose syndrome and the cross-scale impact from individual hosts to ecosystems. Collectively, this research highlights how early pathogen detection and quantification of host impacts has accelerated the understanding of this newly emerging infectious disease.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Global distribution of Pseudogymnoascus destructans.
Fig. 2: Seasonality and within-site transmission of Pseudogymnoascus destructans.
Fig. 3: Effects of Pseudogymnoascus destructans infection on bat hosts.
Fig. 4: Impacts of Pseudogymnoascus destructans on bat populations.
Fig. 5: General mechanisms of host persistence.

Similar content being viewed by others

References

  1. 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 (2012).

    PubMed  Google Scholar 

  2. Frick, W. F. et al. An emerging disease causes regional population collapse of a common North American bat species. Science 329, 679–682 (2010).

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  4. Turner, G. & Reeder, D. Update of white-nose syndrome in bats, September 2009. Bat Res. News 50, 47–53 (2009).

    Google Scholar 

  5. Reichard, J. D. et al. Interannual survival of Myotis lucifugus (Chiroptera: Vespertilionidae) near the epicenter of white-nose syndrome. Northeast. Nat. 21, N56–N59 (2014).

    Google Scholar 

  6. Dzal, Y., McGuire, L. P., Veselka, N. & Fenton, M. B. Going, going, gone: the impact of white-nose syndrome on the summer activity of the little brown bat (Myotis lucifugus). Biol. Lett. 7, 392–394 (2011).

    PubMed  Google Scholar 

  7. Francl, K. E., Ford, W. M., Sparks, D. W. & Brack, V. Capture and reproductive trends in summer bat communities in West Virginia: assessing the impact of white-nose syndrome. J. Fish. Wildl. Manag. 3, 33–42 (2012).

    Google Scholar 

  8. Ford, W. M., Britzke, E. R., Dobony, C. A., Rodrigue, J. L. & Johnson, J. B. Patterns of acoustical activity of bats prior to and following white-nose syndrome occurrence. J. Fish. Wildl. Manag. 2, 125–134 (2011).

    Google Scholar 

  9. Powers, K. E., Reynolds, R. J., Orndorff, W., Ford, W. M. & Hobson, C. S. Post-white-nose syndrome trends in Virginias cave bats, 2008–2013. J. Ecol. Nat. Environ. 7, 113–123 (2015).

    Google Scholar 

  10. Powers, K. E. et al. Monitoring the status of gray bats (Myotis grisescens) in Virginia, 2009–2014, and potential impacts of white-nose syndrome. Southeast. Nat. 15, 127–137 (2016).

    Google Scholar 

  11. Reynolds, R. J., Powers, K. E., Orndorff, W., Ford, W. M. & Hobson, C. S. Changes in rates of capture and demographics of Myotis septentrionalis (northern long-eared bat) in western Virginia before and after onset of white-nose syndrome. Northeast. Nat. 23, 195–204 (2016).

    Google Scholar 

  12. Coleman, J. T. H. & Reichard, J. D. Bat white-nose syndrome in 2014: a brief assessment seven years after the discovery of a virulent fungal pathogen in North America. Outlooks Pest Manag. 25, 374–377 (2014).

    Google Scholar 

  13. Turner, G. G., Reeder, D. M. & Coleman, J. T. H. A five-year assessment of mortality and geographic spread of white-nose syndrome in North American bats and look to the future. Bat Res. News 52, 13–27 (2011).

    Google Scholar 

  14. Nocera, T., Ford, W. M., Silvis, A. & Dobony, C. A. Patterns of acoustical activity of bats prior to and 10 years after WNS on Fort Drum Army Installation, New York. Glob. Ecol. Conserv. 18, e00633 (2019).

    Google Scholar 

  15. Brooks, R. T. Declines in summer bat activity in central New England 4 years following the initial detection of white-nose syndrome. Biodivers. Conserv. 20, 2537–2541 (2011).

    Google Scholar 

  16. Meteyer, C. U. et al. Histopathologic criteria to confirm white-nose syndrome in bats. J. Vet. Diagn. Invest. 21, 411–414 (2009).

    PubMed  Google Scholar 

  17. Blehert, D. S. et al. Bat white-nose syndrome: an emerging fungal pathogen? Science 323, 227–227 (2009).

    CAS  PubMed  Google Scholar 

  18. Chaturvedi, V. et al. Morphological and molecular characterizations of psychrophilic fungus Geomyces destructans from New York bats with white nose syndrome (WNS). PLoS ONE 5, e10783 (2010).

    PubMed  PubMed Central  Google Scholar 

  19. Gargas, A., Trest, M. T., Christensen, M., Volk, T. J. & Bleher, D. S. Geomyces desctructans sp. nov. associated with bat white-nose syndrome. Mycotaxon 108, 147–154 (2009).

    Google Scholar 

  20. Minnis, A. M. & Lindner, D. L. Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol. 117, 638–649 (2013).

    PubMed  Google Scholar 

  21. Drees, K. P. et al. Phylogenetics of a fungal invasion: origins and widespread dispersal of white-nose syndrome. mBio 8, e01941-17 (2017).

    PubMed  PubMed Central  Google Scholar 

  22. Palmer, J. M., Drees, K. P., Foster, J. T. & Lindner, D. L. Extreme sensitivity to ultraviolet light in the fungal pathogen causing white-nose syndrome of bats. Nat. Commun. 9, 35 (2018).

    PubMed  PubMed Central  Google Scholar 

  23. Reynolds, H. T. & Barton, H. A. Comparison of the white-nose syndrome agent Pseudogymnoascus destructans to cave-dwelling relatives suggests reduced saprotrophic enzyme activity. PLoS ONE 9, e86437 (2014).

    PubMed  PubMed Central  Google Scholar 

  24. Wilson, M. B., Held, B. W., Freiborg, A. H., Blanchette, R. A. & Salomon, C. E. Resource capture and competitive ability of non-pathogenic Pseudogymnoascus spp. and P. destructans, the cause of white-nose syndrome in bats. PLoS ONE 12, e0178968 (2017).

    PubMed  PubMed Central  Google Scholar 

  25. O’Donoghue, A. J. et al. Destructin-1 is a collagen-degrading endopeptidase secreted by Pseudogymnoascus destructans, the causative agent of white-nose syndrome. Proc. Natl Acad. Sci. USA 112, 7478–7483 (2015).

    PubMed  PubMed Central  Google Scholar 

  26. Lorch, J. M. et al. Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480, 376–378 (2011).

    CAS  PubMed  Google Scholar 

  27. Warnecke, L. et al. Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc. Natl Acad. Sci. USA 109, 6999–7003 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Hoyt, J. R. et al. Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome. Proc. Natl Acad. Sci. USA 117, 7255–7262 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Fritze, M. & Puechmaille, S. J. Identifying unusual mortality events in bats: a baseline for bat hibernation monitoring and white-nose syndrome research. Mammal. Rev. 48, 224–228 (2018).

    Google Scholar 

  30. Langwig, K. E. et al. Context dependent conservation responses to wildlife disease. Front. Ecol. Environ. 13, 195–202 (2015).

    Google Scholar 

  31. Lorch, J. M. et al. Snake fungal disease: an emerging threat to wild snakes. Philos. Trans. R. Soc. B Biol. Sci. 371, 20150457 (2016).

    Google Scholar 

  32. Hoyt, J. R. et al. Host persistence or extinction from emerging infectious disease: insights from white-nose syndrome in endemic and invading regions. Proc. R. Soc. B Biol. Sci. https://doi.org/10.1098/rspb.2015.2861 (2016).

    Article  Google Scholar 

  33. Leopardi, S., Blake, D. & Puechmaille, S. J. White-Nose Syndrome fungus introduced from Europe to North America. Curr. Biol. 25, R217–R219 (2015).

    CAS  PubMed  Google Scholar 

  34. Rajkumar, S. S. et al. Clonal genotype of Geomyces destructans among bats with white nose syndrome, New York, USA. Emerg. Infect. Dis. 17, 1273–1276 (2011).

    PubMed  PubMed Central  Google Scholar 

  35. Ren, P. et al. Clonal spread of Geomyces destructans among bats, midwestern and southern United States. Emerg. Infect. Dis. 18, 883–885 (2012).

    PubMed  PubMed Central  Google Scholar 

  36. Puechmaille, S. J. et al. White-nose syndrome: is this emerging disease a threat to European bats? Trends Ecol. Evol. 26, 570–576 (2011).

    PubMed  Google Scholar 

  37. Campana, M. G. et al. White-nose syndrome fungus in a 1918 bat specimen from France. Emerg. Infect. Dis. https://doi.org/10.3201/eid2309.170875 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Martínková, N. et al. Increasing incidence of Geomyces destructans fungus in bats from the Czech Republic and Slovakia. PLoS ONE 5, e13853 (2010).

    PubMed  PubMed Central  Google Scholar 

  39. Puechmaille, S. J. et al. Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS ONE 6, e19167 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Zahradníková, A. Jr. et al. Historic and geographic surveillance of Pseudogymnoascus destructans possible from collections of bat parasites. Transbound. Emerg. Dis. 65, 303–308 (2018).

    PubMed  Google Scholar 

  41. Ruedi, M. et al. Molecular phylogenetic reconstructions identify East Asia as the cradle for the evolution of the cosmopolitan genus Myotis (Mammalia, Chiroptera). Mol. Phylogenet. Evol. 69, 437–449 (2013).

    PubMed  Google Scholar 

  42. Hosseini, P. R., Dhondt, A. A. & Dobson, A. P. Spatial spread of an emerging infectious disease: conjunctivitis in house finches. Ecology 87, 3037–3046 (2006).

    PubMed  Google Scholar 

  43. Kilpatrick, A. M. et al. Predicting the global spread of H5N1 avian influenza. Proc. Natl Acad. Sci. USA 103, 19368–19373 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Lorch, J. M. et al. First detection of bat white-nose syndrome in Western North America. mSphere 1, e00148-16 (2016).

    PubMed  PubMed Central  Google Scholar 

  45. 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  Google Scholar 

  46. Lilley, T. M., Anttila, J. & Ruokolainen, L. Landscape structure and ecology influence the spread of a bat fungal disease. Funct. Ecol. 32, 2483–2496 (2018).

    Google Scholar 

  47. Maher, S. P. et al. Spread of white-nose syndrome on a network regulated by geography and climate. Nat. Commun. 3, 1306 (2012).

    PubMed  Google Scholar 

  48. Davis, W. H. & Hitchcock, H. B. Biology and migration of the bat, Myotis lucifugus, in New England. J. Mammal. 46, 296–313 (1965).

    Google Scholar 

  49. Norquay, K. J. O., Martinez-Nunez, F., Dubois, J. E., Monson, K. M. & Willis, C. K. R. Long-distance movements of little brown bats (Myotis lucifugus). J. Mammal. 94, 506–515 (2013).

    Google Scholar 

  50. Langwig, K. E. et al. Tradeoffs between mobility and infectiousness in the spatial spread of an emerging pathogen. Preprint at bioRxiv https://doi.org/10.1101/2020.05.07.082651 (2020).

    Article  Google Scholar 

  51. Wilder, A. P., Kunz, T. H. & Sorenson, M. D. Population genetic structure of a common host predicts the spread of white-nose syndrome, an emerging infectious disease in bats. Mol. Ecol. 24, 5495–5506 (2015).

    PubMed  Google Scholar 

  52. Thapa, V. et al. Using a novel partitivirus in Pseudogymnoascus destructans to understand the epidemiology of white-nose syndrome. PLoS Pathog. 12, e1006076 (2016).

    PubMed  PubMed Central  Google Scholar 

  53. Kovacova, V. et al. White-nose syndrome detected in bats over an extensive area of Russia. BMC Vet. Res. 14, 192 (2018).

    PubMed  PubMed Central  Google Scholar 

  54. Holz, P. H., Lumsden, L. F., Marenda, M. S., Browning, G. F. & Hufschmid, J. Two subspecies of bent-winged bats (Miniopterus orianae bassanii and oceanensis) in southern Australia have diverse fungal skin flora but not Pseudogymnoascus destructans. PLoS ONE 13, e0204282 (2018).

    PubMed  PubMed Central  Google Scholar 

  55. Lilley, T. M. et al. Population connectivity predicts vulnerability to white-nose syndrome in the Chilean myotis (Myotis chiloensis) — a genomics approach. G3 10, 2117–2126 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Holz, P. et al. Does the fungus causing white-nose syndrome pose a significant risk to Australian bats? Wildl. Res. 46, 657–668 (2019).

    Google Scholar 

  57. Hoyt, J. R. et al. Long-term persistence of Pseudogymnoascus destructans, the causative agent of white-nose syndrome, in the absence of bats. EcoHealth 12, 330–333 (2015).

    PubMed  Google Scholar 

  58. Lorch, J. M. et al. Distribution and environmental persistence of the causative agent of white-nose syndrome, Geomyces destructans, in bat hibernacula of the eastern United States. Appl. Environ. Microbiol. 79, 1293–1301 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Campbell, L. J., Walsh, D. P., Blehert, D. S. & Lorch, J. M. Long-term survival of Pseudogymnoascus destructans at elevated temperatures. J. Wildl. Dis. 56, 278–287 (2020).

    PubMed  Google Scholar 

  60. Verant, M. L., Boyles, J. G., Waldrep, W. Jr. Wibbelt, G. & Blehert, D. S. Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. PLoS ONE 7, e46280 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Langwig, K. E. et al. Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proc. R. Soc. B Biol. Sci. 282, 20142335 (2015).

    Google Scholar 

  62. O’shea, T. J. et al. Bat flight and zoonotic viruses. Emerg. Infect. Dis. 20, 741 (2014).

    PubMed  PubMed Central  Google Scholar 

  63. Perry, R. W. A review of factors affecting cave climates for hibernating bats in temperate North America. Environ. Rev. 21, 28–39 (2013).

    Google Scholar 

  64. 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 (1996).

    Google Scholar 

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

    Article  Google Scholar 

  66. Langwig, K. E. et al. Invasion dynamics of white-nose syndrome fungus, midwestern United States, 2012–2014. Emerg. Infect. Dis. 21, 1023–1026 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Frick, W. F. et al. Pathogen dynamics during invasion and establishment of white-nose syndrome explain mechanisms of host persistence. Ecology 98, 624–631 (2017).

    PubMed  Google Scholar 

  68. Zukal, J. et al. White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. Sci. Rep. 6, 19829 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 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  Google Scholar 

  70. Wilcox, A. et al. Behaviour of hibernating little brown bats experimentally inoculated with the pathogen that causes white-nose syndrome. Anim. Behav. 88, 157–164 (2014).

    Google Scholar 

  71. Meteyer, C. U., Barber, D. & Mandl, J. N. Pathology in euthermic bats with white nose syndrome suggests a natural manifestation of immune reconstitution inflammatory syndrome. Virulence 3, 583–588 (2012).

    PubMed  PubMed Central  Google Scholar 

  72. Meteyer, C. U. et al. Recovery of little brown bats (Myotis lucifugus) from natural infection with Geomyces destructans, white-nose syndrome. J. Wildl. Dis. 47, 618–626 (2011).

    PubMed  Google Scholar 

  73. Fuller, N. W. et al. Disease recovery in bats affected by white-nose syndrome. J. Exp. Biol. 223, jeb211912 (2020).

    PubMed  Google Scholar 

  74. Field, K. A. et al. The white-nose syndrome transcriptome: activation of anti-fungal host responses in wing tissue of hibernating bats. PLOS Pathog. 11, e1005168 (2015).

    PubMed  PubMed Central  Google Scholar 

  75. Shelburne, S. A. et al. Immune reconstitution inflammatory syndrome: emergence of a unique syndrome during highly active antiretroviral therapy. Medicine 81, 213–227 (2002).

    PubMed  Google Scholar 

  76. Pikula, J. et al. White-nose syndrome pathology grading in Nearctic and Palearctic bats. PLoS ONE 12, e0180435 (2017).

    PubMed  PubMed Central  Google Scholar 

  77. Hoyt, J. R. et al. Widespread occurrence of Pseudogymnoascus destructans in northeast China. Emerg. Infect. Dis. 22, 140–142 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Ballmann, A. E., Torkelson, M. R., Bohuski, E. A., Russell, R. E. & Blehert, D. S. Dispersal hazards of Pseudogymnoascus destructans by bats and human activity at hibernacula in summer. J. Wildl. Dis. 53, 725–735 (2017).

    PubMed  Google Scholar 

  79. Dobony, C. A. et al. Little brown myotis persist despite exposure to white-nose syndrome. J. Fish Wildl. Manag. 2, 190–195 (2011).

    Google Scholar 

  80. Thomas, D. W., Fenton, M. B. & Barclay, R. M. R. Social behavior of the little brown bat, Myotis lucifugus. I. Mating behavior. Behav. Ecol. Sociobiol. 6, 129–136 (1979).

    Google Scholar 

  81. Parsons, K. N., Jones, G., Davidson-Watts, I. & Greenaway, F. Swarming of bats at underground sites in Britain — implications for conservation. Biol. Conserv. 111, 63–70 (2003).

    Google Scholar 

  82. Jiang, T. et al. Autumn flight activity of the greater horseshoe bat at hibernacula. Anim. Biol. 66, 119–131 (2016).

    Google Scholar 

  83. van Schaik, J. et al. Bats swarm where they hibernate: compositional similarity between autumn swarming and winter hibernation assemblages at five underground sites. PLoS ONE 10, 1 (2015).

    Google Scholar 

  84. Fenton, M. B. Summer activity of Myotis lucifugus (Chiroptera: Vespertilionidae) at hibernacula in Ontario and Quebec. Can. J. Zool. 47, 597–602 (1969).

    Google Scholar 

  85. 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).

    Google Scholar 

  86. Hoyt, J. R. et al. Cryptic connections illuminate pathogen transmission within community networks. Nature 563, 710–713 (2018).

    CAS  PubMed  Google Scholar 

  87. 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 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  89. Lučan, R. K. et al. Ectoparasites may serve as vectors for the white-nose syndrome fungus. Parasit. Vectors 9, 16 (2016).

    PubMed  PubMed Central  Google Scholar 

  90. Hudson, H. J. Fungal Biology (CUP Archive, 1992).

  91. Ainsworth, G. Fungal parasites of vertebrates. in Fungal Population: An Advanced Treatise Vol. 211 (Elsevier, 2013).

  92. Zhao, Z., Liu, H., Wang, C. & Xu, J. R. Erratum to: comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 15, 6 (2014).

    PubMed  PubMed Central  Google Scholar 

  93. Zukal, J. et al. White-nose syndrome fungus: a generalist pathogen of hibernating bats. PLoS ONE 9, e97224 (2014).

    PubMed  PubMed Central  Google Scholar 

  94. Bernard, R. F., Foster, J. T., Willcox, E. V., Parise, K. L. & McCracken, G. F. Molecular detection of the causative agent of white-nose syndrome on Rafinesque’s big-eared bats (Corynorhinus rafinesquii) and two species of migratory bats in the southeastern USA. J. Wildl. Dis. 51, 519–522 (2015).

    PubMed  Google Scholar 

  95. Turner, G. G. et al. Nonlethal screening of bat-wing skin with the use of ultraviolet fluorescence to detect lesions indicative of white-nose syndrome. J. Wildl. Dis. 50, 566–573 (2014).

    PubMed  Google Scholar 

  96. USFWS. White-nose syndrome occurrence map - by year. https://www.whitenosesyndrome.org/where-is-wns (2020).

  97. Wibbelt, G. et al. Skin lesions in European hibernating bats associated with Geomyces destructans, the etiologic agent of white-nose syndrome. PLoS ONE 8, e74105 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Bandouchova, H. et al. Alterations in the health of hibernating bats under pathogen pressure. Sci. Rep. 8, 6067 (2018).

    PubMed  PubMed Central  Google Scholar 

  99. Warnecke, L. et al. Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality. Biol. Lett. https://doi.org/10.1098/rsbl.2013.0177 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  100. Herreid, C. F. 2nd, Bretz, W. L. & Schmidt-Nielsen, K. Cutaneous gas exchange in bats. Am. J. Physiol. 215, 506–508 (1968).

    PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  102. Cryan, P. M., Uphoff Meteyer, C., Boyles, J. G. & Blehert, D. S. Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. BMC Biol. 8, 135 (2010).

    PubMed  PubMed Central  Google Scholar 

  103. Mayberry, H. W., McGuire, L. P. & Willis, C. K. Body temperatures of hibernating little brown bats reveal pronounced behavioural activity during deep torpor and suggest a fever response during white-nose syndrome. J. Comp. Physiol. B 188, 333–343 (2018).

    CAS  PubMed  Google Scholar 

  104. McGuire, L. P., Mayberry, H. W. & Willis, C. K. 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  Google Scholar 

  105. 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. https://doi.org/10.7589/2012-10-242 (2013).

    Article  PubMed  Google Scholar 

  106. Lilley, T. M. et al. White-nose syndrome survivors do not exhibit frequent arousals associated with Pseudogymnoascus destructans infection. Front. Zool. 13, 12 (2016).

    PubMed  PubMed Central  Google Scholar 

  107. Carey, C. S. & Boyles, J. G. Interruption to cutaneous gas exchange is not a likely mechanism of WNS-associated death in bats. J. Exp. Biol. 218, 1986–1989 (2015).

    PubMed  Google Scholar 

  108. Lilley, T. M. et al. Immune responses in hibernating little brown myotis (Myotis lucifugus) with white-nose syndrome. Proc. R. Soc. B Biol. Sci. 284, 20162232 (2017).

    Google Scholar 

  109. Field, K. et al. Anti-fungal immune responses to Pseudogymnoasces destructans in bats affected by white-nose syndrome. J. Immunol. 192 (Suppl. 1), 207.13 (2014).

    Google Scholar 

  110. Reeder, S. M. et al. Pseudogymnoascus destructans transcriptome changes during white-nose syndrome infections. Virulence 8, 1695–1707 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Harazim, M. et al. Natural selection in bats with historical exposure to white-nose syndrome. BMC Zool. 3, 8 (2018).

    Google Scholar 

  112. Davy, C. M. et al. Transcriptional host–pathogen responses of Pseudogymnoascus destructans and three species of bats with white-nose syndrome. Virulence 11, 781–794 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Moore, M. S. et al. Energy conserving thermoregulatory patterns and lower disease severity in a bat resistant to the impacts of white-nose syndrome. J. Comp. Physiol. B 188, 163–176 (2018).

    PubMed  Google Scholar 

  114. Field, K. A. et al. Effect of torpor on host transcriptomic responses to a fungal pathogen in hibernating bats. Mol. Ecol. 27, 3727–3743 (2018).

    CAS  Google Scholar 

  115. Johnson, J. S. et al. Antibodies to Pseudogymnoascus destructans are not sufficient for protection against white-nose syndrome. Ecol. Evol. 5, 2203–2014 (2015).

    PubMed  PubMed Central  Google Scholar 

  116. 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 (2019).

    PubMed  PubMed Central  Google Scholar 

  117. Thogmartin, W. E., King, R. A., McKann, P. C., Szymanski, J. A. & Pruitt, L. Population-level impact of white-nose syndrome on the endangered Indiana bat. J. Mammal. 93, 1086–1098 (2012).

    Google Scholar 

  118. Verant, M. L., Meteyer, C. U., Stading, B. & Blehert, D. S. Experimental infection of Tadarida brasiliensis with Pseudogymnoascus destructans, the fungus that causes white-nose syndrome. mSphere 3, e00250-18 (2018).

    PubMed  PubMed Central  Google Scholar 

  119. Rodhouse, T. J. et al. Evidence of region-wide bat population decline from long-term monitoring and Bayesian occupancy models with empirically informed priors. Ecol. Evol. 9, 11078–11088 (2019).

    PubMed  PubMed Central  Google Scholar 

  120. Marroquin, C. M., Lavine, J. O. & Windstam, S. T. Effect of humidity on development of Pseudogymnoascus destructans, the causal agent of bat white-nose syndrome. Northeast. Nat. 24, 54–64 (2017).

    Google Scholar 

  121. Grieneisen, L. E., Brownlee-Bouboulis, S. A., Johnson, J. S. & Reeder, D. M. Sex and hibernaculum temperature predict survivorship in white-nose syndrome affected little brown myotis (Myotis lucifugus). R. Soc. Open Sci. 2, 140470 (2015).

    PubMed  PubMed Central  Google Scholar 

  122. Johnson, J. S. et al. Host, pathogen, and environmental characteristics predict white-nose syndrome mortality in captive little brown myotis (Myotis lucifugus). PLoS ONE https://doi.org/10.1371/journal.pone.0112502 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  123. Hayman, D. T., Pulliam, J. R., Marshall, J. C., Cryan, P. M. & Webb, C. T. Environment, host, and fungal traits predict continental-scale white-nose syndrome in bats. Sci. Adv. 2, e1500831 (2016).

    PubMed  PubMed Central  Google Scholar 

  124. Verant, M. L. et al. Determinants of Pseudogymnoascus destructans within bat hibernacula: Implications for surveillance and management of white-nose syndrome. J. Appl. Ecol. 55, 820–829 (2018).

    PubMed  PubMed Central  Google Scholar 

  125. McGuire, L. P. et al. White-nose syndrome disease severity and a comparison of diagnostic methods. EcoHealth 13, 60–71 (2016).

    PubMed  Google Scholar 

  126. Willis, C. K. R., 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 (2011).

    PubMed  Google Scholar 

  127. 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  Google Scholar 

  128. Pannkuk, E. L., Gilmore, D. F., Savary, B. J. & Risch, T. S. Triacylglyceride (TAG) profiles of integumentary lipids isolated from three bat species determined by matrix-assisted laser desorption-ionization time-of-flight mass spectrometry (MALDI-TOF MS). Can. J. Zool. 90, 1117–1127 (2012).

    CAS  Google Scholar 

  129. Pannkuk, E. L. et al. Glycerophospholipid profiles of bats with white-nose syndrome. Physiol. Biochem. Zool. 88, 425–432 (2015).

    PubMed  PubMed Central  Google Scholar 

  130. Avena, C. V. et al. Deconstructing the bat skin microbiome: influences of the host and the environment. Front. Microbiol. 7, 1753 (2016).

    PubMed  PubMed Central  Google Scholar 

  131. Lemieux-Labonté, V., Simard, A., Willis, C. K. & Lapointe, F.-J. Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome. Microbiome 5, 115 (2017).

    PubMed  PubMed Central  Google Scholar 

  132. Ange-Stark, M. A. et al. White-nose syndrome restructures bat skin microbiomes. Preprint at bioRxiv https://doi.org/10.1101/614842 (2019).

    Article  Google Scholar 

  133. Hoyt, J. R. et al. Bacteria isolated from bats inhibit the growth of Pseudogymnoascus destructans, the causative agent of white-nose syndrome. PLoS ONE 10, e0121329 (2015).

    PubMed  PubMed Central  Google Scholar 

  134. Moore, M. S. et al. Hibernating little brown myotis (Myotis lucifugus) show variable immunological responses to white-nose syndrome. PLoS ONE 8, e58976 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  135. Rocke, T. E. et al. Virally-vectored vaccine candidates against white-nose syndrome induce anti-fungal immune response in little brown bats (Myotis lucifugus). Sci. Rep. 9, 6788 (2019).

    PubMed  PubMed Central  Google Scholar 

  136. Donaldson, M. E. et al. Profiling the immunome of little brown myotis provides a yardstick for measuring the genetic response to white-nose syndrome. Evolut. Appl. 10, 1076–1090 (2017).

    CAS  Google Scholar 

  137. Davy, C. M. et al. White-nose syndrome is associated with increased replication of a naturally persisting coronaviruses in bats. Sci. Rep. 8, 15508 (2018).

    PubMed  PubMed Central  Google Scholar 

  138. Martínková, N. et al. Hibernation temperature-dependent Pseudogymnoascus destructans infection intensity in Palearctic bats. Virulence 9, 1734–1750 (2018).

    Google Scholar 

  139. Langwig, K. E. et al. Resistance in persisting bat populations after white-nose syndrome invasion. Philos. Trans. R. Soc. B: Biol. Sci. 372, 20160044 (2017).

    Google Scholar 

  140. Maslo, B., Valent, M., Gumbs, J. F. & Frick, W. F. Conservation implications of ameliorating survival of little brown bats with white-nose syndrome. Ecol. Appl. 25, 1832–1840 (2015).

    PubMed  Google Scholar 

  141. Maslo, B. et al. High annual survival in infected wildlife populations may veil a persistent extinction risk from disease. Ecosphere 8, e02001 (2017).

    Google Scholar 

  142. Dowling, Z. R. & O’Dell, D. I. Bat use of an island off the coast of Massachusetts. Northeast. Nat. 25, 362–382 (2018).

    Google Scholar 

  143. Cheng, T. L. et al. Higher fat stores contribute to persistence of little brown bat populations with white-nose syndrome. J. Anim. Ecol. 88, 591–600 (2019).

    PubMed  Google Scholar 

  144. Bohn, S. et al. Evidence of ‘sickness behaviour’ in bats with white-nose syndrome. Behaviour 153, 981–1003 (2016).

    Google Scholar 

  145. Raberg, L., Sim, D. & Read, A. F. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318, 812–814 (2007).

    CAS  PubMed  Google Scholar 

  146. Auteri, G. G. & Knowles, L. L. Decimated little brown bats show potential for adaptive change. Sci. Rep. 10, 3023 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  147. Gignoux-Wolfsohn, S. A. et al. Genomic signatures of evolutionary rescue in bats surviving white-nose syndrome. Preprint at bioRxiv https://doi.org/10.1101/470294 (2019).

    Article  Google Scholar 

  148. Lilley, T. M. et al. Genome-wide changes in genetic diversity in a population of Myotis lucifugus affected by white-nose syndrome. G3 10, 2007–2020 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  149. Shuey, M. M., Drees, K. P., Lindner, D. L., Keim, P. & Foster, J. T. Highly sensitive quantitative PCR for the detection and differentiation of Pseudogymnoascus destructans and other Pseudogymnoascus species. Appl. Environ. Microbiol. 80, 1726–1731 (2014).

    PubMed  PubMed Central  Google Scholar 

  150. Muller, L. K. et al. Bat white-nose syndrome: a real-time TaqMan polymerase chain reaction test targeting the intergenic spacer region of Geomyces destructans. Mycologia 105, 253–259 (2013).

    CAS  PubMed  Google Scholar 

  151. 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 (2017).

    PubMed  PubMed Central  Google Scholar 

  152. Russell, R. E., Thogmartin, W. E., Erickson, R. A., Szymanski, J. & Tinsley, K. Estimating the short-term recovery potential of little brown bats in the eastern United States in the face of white-nose syndrome. Ecol. Model. 314, 111–117 (2015).

    Google Scholar 

  153. Fletcher, Q. E., Webber, Q. M. & Willis, C. K. Modelling the potential efficacy of treatments for white-nose syndrome in bats. J. Appl. Ecol. 57, 1283–1291 (2020).

    Google Scholar 

  154. Cheng, T. L. et al. Efficacy of a probiotic bacterium to treat bats affected by the disease white-nose syndrome. J. Appl. Ecol. 54, 701–708 (2017).

    Google Scholar 

  155. Hoyt, J. R. et al. Field trial of a probiotic bacteria to protect bats from white-nose syndrome. Sci. Rep. 9, 9158 (2019).

    PubMed  PubMed Central  Google Scholar 

  156. Cornelison, C., Gabriel, K., Barlament, C. & Crow, S. Jr. Inhibition of Pseudogymnoascus destructans growth from conidia and mycelial extension by bacterially produced volatile organic compounds. Mycopathologia 177, 1–10 (2014).

    CAS  PubMed  Google Scholar 

  157. Chaturvedi, S. et al. Antifungal testing and high-throughput screening of compound library against Geomyces destructans, the etiologic agent of geomycosis (WNS) in bats. PLoS ONE 6, e17032 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  158. Court, M. H. et al. Pharmacokinetics of terbinafine in little brown myotis (Myotis lucifugus) infected with Pseudogymnoascus destructans. Am. J. Vet. Res. 78, 90–99 (2017).

    CAS  PubMed  Google Scholar 

  159. Kilpatrick, A. M. et al. Impact of censusing and research on wildlife populations. Conserv. Sci. Pract. 2, e264 (2020).

    Google Scholar 

  160. 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  Google Scholar 

  161. Garzoli, L. et al. First isolation of Pseudogymnoascus destructans, the fungal causative agent of white-nose disease, in bats from Italy. Mycopathologia 184, 637–644 (2019).

    CAS  PubMed  Google Scholar 

  162. Pavlinić, I., Đaković, M. & Lojkić, I. Pseudogymnoascus destructans in Croatia confirmed. Eur. J. Wildl. Res. 61, 325–328 (2015).

    Google Scholar 

  163. das Neves Paiva-Cardoso, M. et al. First isolation of Pseudogymnoascus destructans in bats from Portugal. Eur. J. Wildl. Res. 60, 645–649 (2014).

    Google Scholar 

  164. Barlow, A. et al. First confirmation of Pseudogymnoascus destructans in British bats and hibernacula. Vet. Rec. 177, 73–73 (2015).

    CAS  PubMed  Google Scholar 

  165. Simonovicova, A., Pangallo, D., Chovanova, K. & Lehotska, B. Geomyces destructans associated with bat disease WNS detected in Slovakia. Biologia 66, 562–564 (2011).

    Google Scholar 

  166. Sachanowicz, K., Stępień, A. & Ciechanowski, M. Prevalence and phenology of white-nose syndrome fungus Pseudogymnoascus destructans in bats from Poland. Cent. Eur. J. Biol. 9, 437–443 (2014).

    Google Scholar 

  167. Hayes, M. A. The geomyces fungi: ecology and distribution. Bioscience 62, 819–823 (2012).

    Google Scholar 

  168. Kendrick, B. The Fifth Kingdom (Hackett Publishing, 2017).

  169. Palmer, J. M. et al. Molecular characterization of a heterothallic mating system in Pseudogymnoascus destructans, the fungus causing white-nose syndrome of bats. G3 4, 1755–1763 (2014).

    PubMed  PubMed Central  Google Scholar 

  170. Tennessee Wildlife Resources Agency. Tennessee Winter Bat Population and White-nose Syndrome Monitoring Reports (Tennessee Wildlife Resources Agency, 2020).

  171. Colatskie, S. Missouri Bat Hibernacula Survey Results of 2011–2017, Following White-Nose Syndrome Arrival (Missouri Department of Conservation, 2017).

  172. Graeter, G. Annual Program Report 2008–2009. 110–115 (Wildlife Diversity Program, Division of Wildlife Management, NC Wildlife Resources Commission, 2009).

  173. Graeter, G. Annual Program Report 2009–2010. 127–137 (Wildlife Diversity Program, Division of Wildlife Management, NC Wildlife Resources Commission, 2010).

  174. Kindel, J. Final Report: White-nose Syndrome Grants to States, F15AC00694 (South Carolina Department of Natural Resources, 2016).

  175. Kindel, J. Final Report: White-nose Syndrome Grants to States SC-E-F16AP00833 (South Carolina Department of Natural Resources, 2017).

  176. Morris, T. & Ferrall, E. 2019 White-nose Syndrome Season Summary (Wildlife Resources Division, Georgia Department of Natural Resources, 2020).

  177. Cressler, C. E., McLeod, D. V., Rozins, C., Van Den Hoogen, J. & Day, T. The adaptive evolution of virulence: a review of theoretical predictions and empirical tests. Parasitology 143, 915–930 (2016).

    PubMed  Google Scholar 

  178. Lacki, M. J., Hayes, J. P., Kurta, A. & Tuttle, M. D. Bats in Forests: Conservation and Management (JHU Press, 2007).

  179. Miller, K. E. Trophic, habitat, distubance and conservation linkages between bat and aquatic communities in two Connecticut rivers. Doctoral dissertation, Wesleyan University. https://doi.org/10.14418/wes01.3.20 (2013).

  180. Morningstar, D. E., Robinson, C. V., Shokralla, S. & Hajibabaei, M. Interspecific competition in bats and diet shifts in response to white-nose syndrome. Ecosphere 10, e02916 (2019).

    Google Scholar 

  181. Jachowski, D. S. et al. Disease and community structure: white-nose syndrome alters spatial and temporal niche partitioning in sympatric bat species. Divers. Distrib. 20, 1002–1015 (2014).

    Google Scholar 

  182. Kunz, T. H., de Torrez, E. B., Bauer, D., Lobova, T. & Fleming, T. H. in Year in Ecology and Conservation Biology Vol. 1223 Annals of the New York Academy of Sciences (eds Ostfeld, R. S. & Schlesinger, W. H.) 1–38 (Blackwell Science Publishing, 2011).

  183. Maine, J. J. & Boyles, J. G. Bats initiate vital agroecological interactions in corn. Proc. Natl Acad. Sci. https://doi.org/10.1073/pnas.1505413112 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  184. Frank, E. G. The Effects of Bat Population Losses on Infant Mortality through Pesticide Use in the US. (PhD thesis, Columbia University, 2016).

  185. Wray, A. K. et al. Incidence and taxonomic richness of mosquitoes in the diets of little brown and big brown bats. J. Mammal. 99, 668–674 (2018).

    Google Scholar 

  186. Reiskind, M. H. & Wund, M. A. Experimental assessment of the impacts of northern long-eared bats on ovipositing Culex (Diptera: Culicidae) mosquitoes. J. Med. Entomol. 46, 1037–1044 (2009).

    PubMed  Google Scholar 

  187. Clare, E. L. et al. The diet of Myotis lucifugus across Canada: assessing foraging quality and diet variability. Mol. Ecol. 23, 3618–3632 (2014).

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank S. Yamada for assistance with data curation, N. Fuller, N. Laggan, A. Grimaudo and J. Reichard for helpful comments on the manuscript, and the US National Science Foundation for funding (DEB-1911853).

Author information

Authors and Affiliations

Authors

Contributions

J.R.H. and K.E.L. drafted the original figures. All authors contributed to writing the original draft and to the editing of the revised work.

Corresponding author

Correspondence to Joseph R. Hoyt.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Microbiology thanks M. Fisher, N. Martinkova and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hoyt, J.R., Kilpatrick, A.M. & Langwig, K.E. Ecology and impacts of white-nose syndrome on bats. Nat Rev Microbiol 19, 196–210 (2021). https://doi.org/10.1038/s41579-020-00493-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41579-020-00493-5

This article is cited by

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology