Abstract
Wildlife diseases have been implicated in the declines and extinctions of several species. The ability of a pathogen to persist outside its host, existing as an “environmental reservoir”, can exacerbate the impact of a disease and increase the likelihood of host extinction. Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome in bats, has been found in cave soil during the summer when hibernating bats had likely been absent for several months. However, whether the pathogen can persist over multiple years in the absence of bats is unknown, and long-term persistence of the pathogen can influence whether hibernacula where bats have been locally extirpated due to disease can be subsequently recolonized. Here, we show that P. destructans is capable of long-term persistence in the laboratory in the absence of bats. We cultured P. destructans from dried agar plates that had been kept at 5°C and low humidity conditions (30–40% RH) for more than 5 years. This suggests that P. destructans can persist in the absence of bats for long periods which may prevent the recolonization of hibernation, sites where bat populations were extirpated. This increases the extinction risk of bats affected by this disease.
References
Daszak P, Cunningham AA, and Hyatt AD (2000). Emerging infectious diseases of wildlife - threats to biodiversity and human health. Science 287:443.
de Castro F, and Bolker B (2005). Mechanisms of disease-induced extinction. Ecology Letters 8:117-126.
Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, et al. (2012). Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186-194.
Frick WF, Pollock JF, Hicks AC, Langwig KE, Reynolds DS, Turner GG, et al. (2010). An emerging disease causes regional population collapse of a common north american bat species. Science 329:679-682.
Gargas A, Trest MT, Christensen M, Volk TJ, and Bleher DS (2009). Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon 108:147-154.
Langwig KE, Frick WF, Bried JT, Hicks AC, Kunz TH, and Marm Kilpatrick A (2012). Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecology Letters 15:1050-1057.
Lorch JM, Meteyer CU, Behr MJ, Boyles JG, Cryan PM, Hicks AC, et al. (2011). Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480:376-378.
Lorch JM, Muller LK, Russell RE, O’Connor M, Lindner DL, and Blehert DS (2013). Distribution and Environmental Persistence of the Causative Agent of White-Nose Syndrome, Geomyces destructans, in Bat Hibernacula of the Eastern United States. Applied and Environmental Microbiology 79:1293-1301.
McCallum H (2012). Disease and the dynamics of extinction. Philosophical Transactions of the Royal Society B: Biological Sciences 367:2828-2839.
Minnis AM, and Lindner DL (2013). Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biology 117:638-649.
Mitchell KM, Churcher TS, Garner TWJ, and Fisher MC (2008). Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction. Proceedings of the Royal Society B: Biological Sciences 275:329-334.
Raudabaugh DB, Miller AN (2013) Nutritional capability of and substrate suitability for pseudogymnoascus destructans, the causal agent of bat white-nose syndrome. PLoS ONE 8:e78300.
Reeder DM, Frank CL, Turner GG, Meteyer CU, Kurta A, Britzke ER, et al. (2012). Frequent Arousal from Hibernation Linked to Severity of Infection and Mortality in Bats with White-Nose Syndrome. Plos One 7.
Reynolds HT, Barton HA (2014) Comparison of the white-nose syndrome agent pseudogymnoascus destructans to cave-dwelling relatives suggests reduced saprotrophic enzyme activity. PLoS ONE 9:e86437.
Shelley V, Kaiser S, Shelley E, Williams T, Kramer M, Haman K, et al. (2013) Evaluation of strategies for the decontamination of equipment for Geomyces destructans, the causative agent of white-nose syndrome (WNS). Journal of Cave and Karst Studies 75:1–10.
Turner GG, Reeder DM, and Coleman JTH (2011). A five-year assessment of mortality and geographic spread of white-nose syndrome in North American bats and look to the future. Bat Reseach News 52:13-27.
Verant ML, Boyles JG, Waldrep W, Wibbelt G, and Blehert DS (2012). Temperature-Dependent Growth of Geomyces destructans, the Fungus That Causes Bat White-Nose Syndrome. Plos One 7.
Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misra V, Cryan PM, et al. (2012). Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proceedings of the National Academy of Sciences of the United States of America 109:6999-7003.
Webb PI, Speakman JR, and Racey PA (1996). How hot is a hibernaculum? A review of the temperatures at which bats hibernate. Canadian Journal of Zoology-Revue Canadienne De Zoologie 74:761-765.
Wilcox A, Warnecke L, Turner JM, McGuire LP, Jameson JW, Misra V, et al. (2014). Behaviour of hibernating little brown bats experimentally inoculated with the pathogen that causes white-nose syndrome. Animal Behaviour 88:157-164.
Wilder AP, Frick WF, Langwig KE, and Kunz TH (2011). Risk factors associated with mortality from white-nose syndrome among hibernating bat colonies. Biology Letters 7:950-953.
Acknowledgments
This work was supported by the National Science Foundation (DGE-0741448 to KEL and DEB-1115895 to WFF and AMK), Bat Conservation International, US Fish and Wildlife Service, and New York State Department of Environmental Conservation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hoyt, J.R., Langwig, K.E., Okoniewski, J. 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). https://doi.org/10.1007/s10393-014-0981-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-014-0981-4