Does the fungus causing white-nose syndrome pose a significant risk to Australian bats?
Peter Holz
A G , Jasmin Hufschmid A , Wayne S. J. Boardman B , Phillip Cassey C , Simon Firestone A , Lindy F. Lumsden D , Thomas A. A. Prowse C F , Terry Reardon E and Mark Stevenson A
+ Author Affiliations
- Author Affiliations
A Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, 250 Princes Highway, Werribee, Vic. 3030, Australia.
B School of Animal and Veterinary Science, Williams Building, Roseworthy Campus, The University of Adelaide, Roseworthy, SA 5371, Australia.
C Centre for Applied Conservation Science, and School of Biological Sciences, Benham Building, North Terrace Campus, The University of Adelaide, Adelaide, SA 5005, Australia.
D Arthur Rylah Institute for Environmental Research, Department of Environment, Land, Water and Planning, 123 Brown Street, Heidelberg, Vic. 3084, Australia.
E South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
F Present address: School of Mathematical Sciences, Ingkarni Wardli Building, North Terrace Campus, The University of Adelaide, Adelaide, SA 5005, Australia.
G Corresponding author. Email: holzp@student.unimelb.edu.au
Wildlife Research 46(8) 657-668 https://doi.org/10.1071/WR18194
Submitted: 20 June 2018 Accepted: 27 July 2019 Published: 4 December 2019
Abstract
Context: Pseudogymnoascus destructans is the fungus responsible for white-nose syndrome (WNS), which has killed millions of hibernating bats in North America, but also occurs in bats in Europe and China without causing large-scale population effects. This is likely to be due to differences in species susceptibility and behaviour, and environmental factors, such as temperature and humidity. Pseudogymnoascus destructans is currently believed to be absent from Australia.
Aims: To ascertain the level of risk that white-nose syndrome poses for Australian bats.
Methods: This risk analysis examines the likelihood that P. destructans enters Australia, the likelihood of the fungus coming in contact with native bats on successful entry, and the potential consequences should this occur.
Key results: This risk assessment concluded that it is very likely to almost certain that P. destructans will enter Australia, and it is likely that bats will be exposed to the fungus over the next 10 years. Eight cave-dwelling bat species from southern Australia are the ones most likely to be affected.
Conclusions: The risk was assessed as medium for the critically endangered southern bent-winged bat (Miniopterus orianae bassanii), because any increase in mortality could affect its long-term survival. The risk to other species was deemed to range from low to very low, owing to their wider distribution, which extends beyond the P. destructans risk zone.
Implications: Although Australia’s milder climate may preclude the large mortality events seen in North America, the fungus could still significantly affect Australian bat populations, particularly bent-winged bats. Active surveillance is required to confirm Australia’s continuing WNS-free status, and to detect the presence of P. destructans should it enter the country. Although White-nose Syndrome Response Guidelines have been developed by Wildlife Health Australia to assist response agencies in the event of an incursion of WNS into bats in Australia, these guidelines would be strengthened by further research to characterise Australian cave temperatures and hibernating bat biology, such as length of torpor bouts and movement over winter. Risk-mitigation strategies should focus on education programs that target cavers, show-cave managers and tourists, particularly those who have visited regions where WNS is known to occur.
Additional keywords: Miniopterus orianae bassanii, Pseudogymnoascus destructans, risk assessment, southern bent-winged bat.
References
Ballmann, A. E., Torkelson, M. R., Bohuski, E. A., Russell, R. E., and Blehert, D. S. (2017). Dispersal hazards of Pseudogymnoascus destructans by bats and human activity at hibernacula in summer. Journal of Wildlife Diseases 53, 725–735.| Dispersal hazards of Pseudogymnoascus destructans by bats and human activity at hibernacula in summer.Crossref | GoogleScholarGoogle Scholar | 28640713PubMed |
Bamford, M., Watkins, D., Bancroft, W., Tischler, G., and Wahl, J. (2008). ‘Migratory Shorebirds of the East Asian–Australasian Flyway; Population Estimates and Internationally Important Sites.’ (Wetlands International – Oceania: Canberra, ACT, Australia.)
Baudinette, R. V., Churchill, S. K., Christian, K. A., Nelson, J. E., and Hudson, P. J. (2000). Energy, water balance and the roost microenvironment in three Australian cave-dwelling bats (Microchiroptera). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 170, 439–446.
| Energy, water balance and the roost microenvironment in three Australian cave-dwelling bats (Microchiroptera).Crossref | GoogleScholarGoogle Scholar | 11083527PubMed |
Bernard, R. F., and McCracken, G. F. (2017). Winter behavior of bats and the progression of white-nose syndrome in the southeastern United States. Ecology and Evolution 7, 1487–1496.
| Winter behavior of bats and the progression of white-nose syndrome in the southeastern United States.Crossref | GoogleScholarGoogle Scholar | 28261459PubMed |
Bernard, R. F., Foster, J. T., Willcox, E. V., Parise, K. L., and McCracken, G. F. (2015). 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. Journal of Wildlife Diseases 51, 519–522.
| 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.Crossref | GoogleScholarGoogle Scholar | 25647588PubMed |
Blehert, D. S., Hicks, A. C., Behr, M., Meteyer, C. U., Berlowski-Zier, B. M., Buckles, E. L., Coleman, J. T., Darling, S. R., Gargas, A., Niver, R., Okoniewski, J. C., Rudd, R. J., and Stone, W. B. (2009). Bat white-nose syndrome: an emerging fungal pathogen? Science 323, 227.
| Bat white-nose syndrome: an emerging fungal pathogen?Crossref | GoogleScholarGoogle Scholar | 18974316PubMed |
Breed, A. C., Field, H. E., Smith, C. S., Edmonston, J., and Meers, J. (2010). Bats without borders: long-distance movements and implications for disease risk management. EcoHealth 7, 204–212.
| Bats without borders: long-distance movements and implications for disease risk management.Crossref | GoogleScholarGoogle Scholar | 20645122PubMed |
Campbell, S., Coulson, G., and Lumsden, L. F. (2010). Divergent microclimates in artificial and natural roosts of the large-footed myotis (Myotis macropus). Acta Chiropterologica 12, 173–185.
| Divergent microclimates in artificial and natural roosts of the large-footed myotis (Myotis macropus).Crossref | GoogleScholarGoogle Scholar |
Churchill, S. K. (1991). Distribution, abundance and roost selection of the orange horseshoe-bat, Rhinonycteris aurantius, a tropical cave-dweller. Wildlife Research 18, 343–353.
| Distribution, abundance and roost selection of the orange horseshoe-bat, Rhinonycteris aurantius, a tropical cave-dweller.Crossref | GoogleScholarGoogle Scholar |
Cryan, P. M., Meteyer, C. U., Boyles, J. G., and Blehert, D. S. (2010). Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. BMC Biology 8, 135.
| Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology.Crossref | GoogleScholarGoogle Scholar | 21070683PubMed |
Cryan, P. M., Meteyer, C. U., Blehert, D. S., Lorch, J. M., Reeder, D. M., Turner, G. G., Webb, J., Behr, M., Verant, M., Russell, R. E., and Castle, K. T. (2013). Electrolyte depletion in white-nose syndrome bats. Journal of Wildlife Diseases 49, 398–402.
| Electrolyte depletion in white-nose syndrome bats.Crossref | GoogleScholarGoogle Scholar | 23568916PubMed |
DAWR (2016). ‘Biosecurity Import Risk Analysis Guidelines: Managing Biosecurity Risks for Imports into Australia.’ (Department of Agriculture and Water Resources: Canberra, ACT, Australia.)
Deem, S. L., Karesh, W. B., and Weisman, W. (2001). Putting theory into practice: wildlife health in conservation. Conservation Biology 15, 1224–1233.
| Putting theory into practice: wildlife health in conservation.Crossref | GoogleScholarGoogle Scholar |
DSE (2013). ‘Advisory List of Threatened Vertebrate Fauna in Victoria.’ (Victorian Government Department of Sustainability and Environment: Melbourne, Vic., Australia.)
Ehlman, S. M., Cox, J. J., and Crowley, P. H. (2013). Evaporative water loss, spatial distributions, and survival in white-nose-syndrome-affected little brown myotis: a model. Journal of Mammalogy 94, 572–583.
| Evaporative water loss, spatial distributions, and survival in white-nose-syndrome-affected little brown myotis: a model.Crossref | GoogleScholarGoogle Scholar |
Elliott, J., Heesterbeek, S., Lukensmeyer, C., and Slocum, N. (2005). ‘Participatory Methods Toolkit. A Practitioner’s Manual.’ (King Baudouin Foundation: Brussels, Belgium.)
Eskew, E. A., and Todd, B. D. (2013). Parallels in amphibian and bat declines from pathogenic fungi. Emerging Infectious Diseases 19, 379–385.
| Parallels in amphibian and bat declines from pathogenic fungi.Crossref | GoogleScholarGoogle Scholar | 23622255PubMed |
Flory, A. R., Kumar, S., Stohlgren, T. J., and Cryan, P. M. (2012). Environmental conditions associated with bat white-nose syndrome mortality in north-eastern United States. Journal of Applied Ecology 49, 680–689.
| Environmental conditions associated with bat white-nose syndrome mortality in north-eastern United States.Crossref | GoogleScholarGoogle Scholar |
Forsythe, A., Giglio, V., Asa, J., and Xu, J. (2018). Phenotypic divergence along geographic gradients reveals potential for rapid adaptation of the white-nose syndrome pathogen, Pseudogymnoascus destructans, in North America. Applied and Environmental Microbiology 84, e00863-18.
| Phenotypic divergence along geographic gradients reveals potential for rapid adaptation of the white-nose syndrome pathogen, Pseudogymnoascus destructans, in North America.Crossref | GoogleScholarGoogle Scholar | 29915107PubMed |
Frick, W. F., Puechmaille, S. J., Hoyt, J. R., Nickel, B. A., Langwig, K. E., Foster, J. T., Barlow, K. E., Bartonicka, T., Feller, D., Haarsma, A. J., Herzog, C., Horacek, I., van der Kooij, J., Mulkens, B., Petrov, B., Reynolds, R., Rodrigues, L., Stihler, C. W., Turner, G. G., and Kilpatrick, A. M. (2015). Disease alters macroecological patterns of North American bats. Global Ecology and Biogeography 24, 741–749.
| Disease alters macroecological patterns of North American bats.Crossref | GoogleScholarGoogle Scholar |
Frick, W. F., Puechmaille, S. J., and Willis, C. K. R. (2016). White-nose syndrome in bats. In ‘Bats in the Anthropocene: Conservation of Bats in a Changing World’. (Eds C. C. Voigt and T. Kingston.) pp. 245–262. (Springer: Heidelberg, Germany.)
Frick, W. F., Cheng, T. L., Langwig, K. E., Hoyt, J. R., Janicki, A. F., Parise, K. L., Foster, J. T., and Kilpatrick, A. M. (2017). Pathogen dynamics during invasion and establishment of white-nose syndrome explain mechanisms of host persistence. Ecology 98, 624–631.
| Pathogen dynamics during invasion and establishment of white-nose syndrome explain mechanisms of host persistence.Crossref | GoogleScholarGoogle Scholar | 27992970PubMed |
Gale, P., Brouwer, A., Ramnial, V., Kelly, L., Kosmider, R., Fooks, A. R., and Snary, E. L. (2010). Assessing the impact of climate change on vector-borne viruses in the EU through the elicitation of expert opinion. Epidemiology and Infection 138, 214–225.
| Assessing the impact of climate change on vector-borne viruses in the EU through the elicitation of expert opinion.Crossref | GoogleScholarGoogle Scholar | 19580695PubMed |
Hibbard, C., and Wilkins, R. (2010). ‘Australasian Species Management Program. Regional Census and Plan.’ (Zoo and Aquarium Association: Sydney, NSW, Australia.)
Holz, P., Hufschmid, J., Boardman, W., Cassey, P., Firestone, S., Lumsden, L., Prowse, T., Reardon, T., and Stevenson, M. (2016). ‘Qualitative Risk Assessment: White-nose Syndrome in Bats in Australia.’ (Wildlife Health Australia: Sydney, NSW, Australia.)
Holz, P. H., Lumsden, L. F., Marenda, M. S., Browning, G. F., and Hufschmid, J. (2018). 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.
| Two subspecies of bent-winged bats (Miniopterus orianae bassanii and oceanensis) in southern Australia have diverse fungal skin flora but not Pseudogymnoascus destructans.Crossref | GoogleScholarGoogle Scholar | 30303979PubMed |
Hosken, D. J., and Withers, P. C. (1997). Temperature regulation and metabolism of an Australian bat, Chalinolobus gouldii (Chiroptera:Vespertilionidae) when euthermic and torpid. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 167, 71–80.
| Temperature regulation and metabolism of an Australian bat, Chalinolobus gouldii (Chiroptera:Vespertilionidae) when euthermic and torpid.Crossref | GoogleScholarGoogle Scholar | 9051907PubMed |
Hoyt, J. R., Langwig, K. E., Okoniewski, J., Frick, W. F., Stone, W. B., and Kilpatrick, A. M. (2015). Long-term persistence of Pseudogymnoascus destructans, the causative agent of white-nose syndrome, in the absence of bats. EcoHealth 12, 330–333.
| Long-term persistence of Pseudogymnoascus destructans, the causative agent of white-nose syndrome, in the absence of bats.Crossref | GoogleScholarGoogle Scholar | 25260801PubMed |
Hoyt, J. R., Langwig, K. E., Sun, K., Lu, G., Parise, K. L., Jiang, T., Frick, W. F., Foster, J. T., Feng, J., and Kilpatrick, A. M. (2016a). Host persistence or extinction from emerging infectious disease: insights from white-nose syndrome in endemic and invading regions. Proceedings. Biological Sciences 283, 20152861.
| Host persistence or extinction from emerging infectious disease: insights from white-nose syndrome in endemic and invading regions.Crossref | GoogleScholarGoogle Scholar | 26962138PubMed |
Hoyt, J. R., Sun, K., Parise, K. L., Lu, G., Langwig, K. E., Jiang, T., Yang, S., Frick, W. F., Kilpatrick, A. M., Foster, J. T., and Feng, J. (2016b). Widespread bat white-nose syndrome fungus, northeastern China. Emerging Infectious Diseases 22, 140–142.
| Widespread bat white-nose syndrome fungus, northeastern China.Crossref | GoogleScholarGoogle Scholar | 26673906PubMed |
Hoyt, J. R., Langwig, K. E., White, J. P., Kaarakka, H. M., Redell, J. A., Kurta, A., DePue, J. E., Scullon, W. H., Parise, K. L., Foster, J. T., Frick, W. F., and Kilpatrick, A. M. (2018). Cryptic connections illuminate pathogen transmission within community networks. Nature 563, 710–713.
| Cryptic connections illuminate pathogen transmission within community networks.Crossref | GoogleScholarGoogle Scholar | 30455422PubMed |
Jakob-Hoff, R., MacDiarmid, S., Lees, C., Miller, P., Travis, D., and Kock, R. (2014). ‘Manual of Procedures for Wildlife Disease Risk Analysis.’ (World Organisation for Animal Health: Paris, France.)
Kunz, T. H., Braun de Torrez, E., Bauer, D., Lobova, T., and Fleming, T. H. (2011). Ecosystem services provided by bats. Annals of the New York Academy of Sciences 1223, 1–38.
| Ecosystem services provided by bats.Crossref | GoogleScholarGoogle Scholar | 21449963PubMed |
Langwig, K. E., Frick, W. F., Bried, J. T., Hicks, A. C., Kunz, T. H., and Kilpatrick, A. M. (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.
| Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome.Crossref | GoogleScholarGoogle Scholar | 22747672PubMed |
Langwig, K. E., Frick, W. F., Reynolds, R., Parise, K. L., Drees, K. P., Hoyt, J. R., Cheng, T. L., Kunz, T. H., Foster, J. T., and Kilpatrick, A. M. (2015). Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proceedings. Biological Sciences 282, 20142335.
| Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome.Crossref | GoogleScholarGoogle Scholar | 25473016PubMed |
Lorch, J. M., Meteyer, C. U., Behr, M. J., Boyles, J. G., Cryan, P. M., Hicks, A. C., Ballmann, A. E., Coleman, J. T., Redell, D. N., Reeder, D. M., and Blehert, D. S. (2011). Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480, 376–378.
| Experimental infection of bats with Geomyces destructans causes white-nose syndrome.Crossref | GoogleScholarGoogle Scholar | 22031324PubMed |
Lorch, J. M., Muller, L. K., Russell, R. E., O’Connor, M., Lindner, D. L., and Blehert, D. S. (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.
| Distribution and environmental persistence of the causative agent of white-nose syndrome, Geomyces destructans, in bat hibernacula of the eastern United States.Crossref | GoogleScholarGoogle Scholar | 23241985PubMed |
Lorch, J. M., Palmer, J. M., Lindner, D. L., Ballmann, A. E., George, K. G., Griffin, K., Knowles, S., Huckabee, J. R., Haman, K. H., Anderson, C. D., Becker, P. A., Buchanan, J. B., Foster, J. T., and Blehert, D. S. (2016). First detection of bat white-nose syndrome in western North America. MSphere 1, .
| First detection of bat white-nose syndrome in western North America.Crossref | GoogleScholarGoogle Scholar | 27504499PubMed |
Maloney, S. K., Bronner, G. N., and Buffenstein, R. (1999). Thermoregulation in the Angolan free-tailed bat Mops condylurus: a small mammal that uses hot roosts. Physiological and Biochemical Zoology 72, 385–396.
| Thermoregulation in the Angolan free-tailed bat Mops condylurus: a small mammal that uses hot roosts.Crossref | GoogleScholarGoogle Scholar | 10438676PubMed |
Moutou, F., Dufour, B., and Ivanov, Y. (2001). A qualitative assessment of the risk of introducing foot and mouth disease into Russia and Europe from Georgia, Armenia and Azerbaijan. Revue Scientifique et Technique (International Office of Epizootics) 20, 723–730.
| A qualitative assessment of the risk of introducing foot and mouth disease into Russia and Europe from Georgia, Armenia and Azerbaijan.Crossref | GoogleScholarGoogle Scholar |
Murray, N., MacDiarmid, S. C., Wooldridge, M., Gummow, B., Morley, R. S., Weber, S. E., Giovannini, A., and Wilson, D. (2010). ‘Handbook on Import Risk Analysis for Animals and Animal Products.’ (World Organisation for Animal Health: Paris, France.)
Puechmaille, S. J., Frick, W. F., Kunz, T. H., Racey, P. A., Voigt, C. C., Wibbelt, G., and Teeling, E. C. (2011a). White-nose syndrome: is this emerging disease a threat to European bats? Trends in Ecology & Evolution 26, 570–576.
| White-nose syndrome: is this emerging disease a threat to European bats?Crossref | GoogleScholarGoogle Scholar |
Puechmaille, S. J., Fuller, H., and Teeling, E. C. (2011b). Effect of sample preservation methods on the viability of Geomyces destructans, the fungus associated with white-nose syndrome in bats. Acta Chiropterologica 13, 217–221.
Puechmaille, S. J., Wibbelt, G., Korn, V., Fuller, H., Forget, F., Muhldorfer, K., Kurth, A., Bogdanowicz, W., Borel, C., Bosch, T., Cherezy, T., Drebet, M., Gorfol, T., Haarsma, A. J., Herhaus, F., Hallart, G., Hammer, M., Jungmann, C., Le Bris, Y., Lutsar, L., Masing, M., Mulkens, B., Passior, K., Starrach, M., Wojtaszewski, A., Zophel, U., and Teeling, E. C. (2011c). Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS One 6, e19167.
| Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality.Crossref | GoogleScholarGoogle Scholar | 21556356PubMed |
Shelley, V., Kaiser, S., Shelley, E., Williams, T., Kramer, M., Haman, K., Keel, K., and Barton, H. A. (2013). Evaluation of strategies for the decontamination of equipment for Geomyces destructans, the causative agent of white-nose syndrome (WNS). Journal of Caves and Karst Studies 75, 1–10.
| Evaluation of strategies for the decontamination of equipment for Geomyces destructans, the causative agent of white-nose syndrome (WNS).Crossref | GoogleScholarGoogle Scholar |
Smith, K. F., Sax, D. F., and Lafferty, K. D. (2006). Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20, 1349–1357.
| Evidence for the role of infectious disease in species extinction and endangerment.Crossref | GoogleScholarGoogle Scholar | 17002752PubMed |
Snary, E. L., Ramnial, V., Breed, A. C., Stephenson, B., Field, H. E., and Fooks, A. R. (2012). Qualitative release assessment to estimate the likelihood of henipavirus entering the United Kingdom. PLoS One 7, e27918.
| Qualitative release assessment to estimate the likelihood of henipavirus entering the United Kingdom.Crossref | GoogleScholarGoogle Scholar | 22328916PubMed |
Speakman, J. R., and Thomas, D. W. (2003). Physiological ecology and energetics of bats. In ‘Bat Ecology’. (Eds T. H. Kunz and M. B. Fenton.) pp. 430–492. (The University of Chicago Press: Chicago, IL, USA.)
Thomas, D. W., Dorais, M., and Bergeron, J.-M. (1990). Winter energy budgets and cost of arousals for hibernating little brown bats, Myotis lucifugus. Journal of Mammalogy 71, 475–479.
| Winter energy budgets and cost of arousals for hibernating little brown bats, Myotis lucifugus.Crossref | GoogleScholarGoogle Scholar |
Turbill, C. (2008). Winter activity of Australian tree-roosting bats: influence of temperature and climatic patterns. Journal of Zoology 276, 285–290.
| Winter activity of Australian tree-roosting bats: influence of temperature and climatic patterns.Crossref | GoogleScholarGoogle Scholar |
Turbill, C., and Geiser, F. (2008). Hibernation by tree-roosting bats. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 178, 597–605.
| Hibernation by tree-roosting bats.Crossref | GoogleScholarGoogle Scholar | 18210129PubMed |
Van Dyck, S., Gynther, I., and Baker, A. (2013) ‘Field Companion to the Mammals of Australia.’ (New Holland Publishers: Sydney, NSW, Australia.)
van Harten, E., Lawrence, R., Lumsden, L., Meyers, N., Reardon, T., and Weyland, J. (2018). ‘Winter Activity Patterns of the Critically Endangered Southern Bent-wing Bat in Temperate Australia.’ (Australasian Bat Society: Richmond, NSW, Australia.)
Verant, M. L., Boyles, J. G., Waldrep, W., Wibbelt, G., and Blehert, D. S. (2012). Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. PLoS One 7, e46280.
| Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome.Crossref | GoogleScholarGoogle Scholar | 23029462PubMed |
Verant, M. L., Meteyer, C. U., Speakman, J. R., Cryan, P. M., Lorch, J. M., and Blehert, D. S. (2014). White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. BMC Physiology 14, 10.
| White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host.Crossref | GoogleScholarGoogle Scholar | 25487871PubMed |
Warnecke, L., Turner, J. M., Bollinger, T. K., Misra, V., Cryan, P. M., Blehert, D. S., Wibbelt, G., and Willis, C. K. (2013). Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality. Biology Letters 9, 20130177.
| Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality.Crossref | GoogleScholarGoogle Scholar | 23720520PubMed |
White, N. (2017). Management of the risk of white nose syndrome. Information for field excursion participants In ‘17th International Congress of Speleology’, 23–29 July. (Eds K. Moore, and S. White.) (Australian Speleological Federation: Sydney, NSW, Australia.)
Wildlife Health Australia (2017). ‘White-nose Syndrome Response Guidelines.’ Available at https://wildlifehealthaustralia.com.au/Portals/0/Documents/ProgramProjects/WNS_response_guidelines_1.1_Jul_2019.pdf [verified October 2019].
Willis, C. K., Menzies, A. K., Boyles, J. G., and Wojciechowski, M. S. (2011). Evaporative water loss is a plausible explanation for mortality of bats from white-nose syndrome. Integrative and Comparative Biology 51, 364–373.
| Evaporative water loss is a plausible explanation for mortality of bats from white-nose syndrome.Crossref | GoogleScholarGoogle Scholar | 21742778PubMed |
Woolhouse, M. E., and Gowtage-Sequeria, S. (2005). Host range and emerging and reemerging pathogens. Emerging Infectious Diseases 11, 1842–1847.
| Host range and emerging and reemerging pathogens.Crossref | GoogleScholarGoogle Scholar | 16485468PubMed |
Zukal, J., Bandouchova, H., Bartonicka, T., Berkova, H., Brack, V., Brichta, J., Dolinay, M., Jaron, K. S., Kovacova, V., Kovarik, M., Martinkova, N., Ondracek, K., Rehak, Z., Turner, G. G., and Pikula, J. (2014). White-nose syndrome fungus: a generalist pathogen of hibernating bats. PLoS One 9, e97224.
| White-nose syndrome fungus: a generalist pathogen of hibernating bats.Crossref | GoogleScholarGoogle Scholar | 25295526PubMed |
Zukal, J., Bandouchova, H., Brichta, J., Cmokova, A., Jaron, K. S., Kolarik, M., Kovacova, V., Kubatova, A., Novakova, A., Orlov, O., Pikula, J., Presetnik, P., Suba, J., Zahradnikova, A., and Martinkova, N. (2016). White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. Scientific Reports 6, 19829.
| White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America.Crossref | GoogleScholarGoogle Scholar | 26821755PubMed |
