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Research Paper

Hibernation temperature-dependent Pseudogymnoascus destructans infection intensity in Palearctic bats

ORCID Icon, ORCID Icon, , , , , , , , , , , , , ORCID Icon, & ORCID Icon show all
Pages 1734-1750 | Received 04 Aug 2018, Accepted 03 Nov 2018, Published online: 03 Dec 2018

References

  • Turbill C, Bieber C, Ruf T. Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc R Soc B. 2011;278:3355–3363. PubMed PMID: 21450735; PubMed Central PMCID: PMC3177628.
  • Blehert DS. Fungal disease and the developing story of bat white-nose syndrome. PLoS Pathog. 2012;8:e1002779.
  • Blehert DS, Hicks AC, Behr M, et al. Bat white-nose syndrome: an emerging fungal pathogen? Science. 2009;323:227.
  • Frick WF, Pollock JF, Hicks AC, et al. An emerging disease causes regional population collapse of a common North American bat species. Science. 2010;329:679–682.
  • Lorch JM, Palmer JM, Lindner DL, et al. First detection of bat white-nose syndrome in Western North America. mSphere. 2016;1(4):e00148–16. PubMed PMID: 27504499; PubMed Central PMCID: PMC4973635.
  • Hayman DTS, Pulliam JT, Marshall JC, et al. Environment, host, and fungal traits predict continental-scale white-nose syndrome in bats. Sci Adv. 2016;2:e1500831.
  • Perry RW. A review of factors affecting cave climates for hibernating bats in temperate North America. Environ Rev. 2013;21:28–39.
  • Gargas A, Trest MT, Christensen M, et al. Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon. 2009;108:147–154.
  • Minnis AM, Lindner DL. Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol. 2013;117:638–649.
  • Lorch JM, Muller LK, Russell RE, 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. 2013;79(4):1293–1301.
  • Bandouchova H, Bartonička T, Berková H, et al. Pseudogymnoascus destructans: evidence of virulent skin invasion for bats under natural conditions, Europe. Transbound Emerg Dis. 2015;62:1–5.
  • Meteyer CU, Buckles EL, Blehert DS, et al. Histopathologic criteria to confirm white-nose syndrome in bats. J Vet Diagn Invest. 2009;21:411–414.
  • Pikula J, Amelon SK, Bandouchova H, et al. White-nose syndrome pathology grading in Nearctic and Palearctic bats. PLoS One. 2017;12(8):e0180435.
  • Bandouchova H, Bartonicka T, Berkova H, et al. Alterations in the health of hibernating bats under pathogen pressure. Sci Rep. 2018;8(1):6067. PubMed PMID: 29666436.
  • Bernard RF, Foster JT, Willcox EV, et al. 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. 2015;51:519–522.
  • Zukal J, Bandouchova H, Bartonička T, et al. White-nose syndrome fungus: A generalist pathogen of hibernating bats. PLoS One. 2014;9:e97224.
  • Zukal J, Bandouchova H, Brichta J, et al. White-nose syndrome without borders: pseudogymnoascus destructans infection confirmed in Asia. Sci Rep. 2016;6:19829.
  • Moore MS, Field KA, Behr MJ, 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 Biochem Syst Environ Physiol. 2018;188:163–176.
  • Bouma HR, Carey HV, Kroese FG. Hibernation: the immune system at rest? J Leukoc Biol. 2010;88(4):619–624. PubMed PMID: 20519639.
  • Meteyer CU, Barber D, Mandl JN. Pathology in euthermic bats with white nose syndrome suggests a natural manifestation of immune reconstitution inflammatory syndrome. Virulence. 2012;3:583–588.
  • Brook CE, Dobson AP. Bats as ‘special’ reservoirs for emerging zoonotic pathogens. Trends Microbiol. 2015;23(3):172–180. PubMed PMID: 25572882.
  • Frick WF, Cheng TL, Langwig KE, et al. Pathogen dynamics during invasion and establishment of white-nose syndrome explain mechanisms of host persistence. Ecology. 2017;98:624–631.
  • Field KA, Johnson JS, Lilley TM, et al. The white-nose syndrome transcriptome: activation of anti-fungal host responses in wing tissue of hibernating little brown myotis. PLoS Pathog. 2015;11(10):e1005168. PubMed PMID: 26426272; PubMed Central PMCID: PMC4591128.
  • Lilley TM, Prokkola JM, Johnson JS, et al. Immune responses in hibernating little brown myotis (Myotis lucifugus) with white-nose syndrome. Proc R Soc B Biol Sci. 2017;284:20162232.
  • Garner TWJ, Rowcliffe JM, Fisher MC. Climate change, chytridiomycosis or condition: an experimental test of amphibian survival. Global Change Biol. 2011;17(2):667–675.
  • Ribas L, Li M-S, Doddington BJ, et al. Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis. PLoS One. 2009;4:e8408.
  • Flieger M, Bandouchova H, Cerny J, et al. Vitamin B2 as a virulence factor in Pseudogymnoascus destructans skin infection. Sci Rep. 2016;6:33200.
  • Weitzman I, Summerbell RC. The dermatophytes. Clin Microbiol Rev. 1995;8:240–259.
  • Reeder SM, Palmer JM, Prokkola JM, et al. Pseudogymnoascus destructans transcriptome changes during white-nose syndrome infections. Virulence. 2017 Jun 14; DOI:10.1080/21505594.2017.1342910. PubMed PMID: 28614673.
  • Webb PI, Speakman JR, Racey PA. How hot is a hibernaculum? A review of the temperatures at which bats hibernate. Can J Zool. 1996;74:761–765.
  • Kokurewicz T. Sex and age related habitat selection and mass dynamics of Daubenton’s bats Myotis daubentonii(Kuhl, 1817) hibernating in natural conditions. Acta Chiropterol. 2004;6(1):121–144.
  • Nagel A, Nagel R. How do bats choose optimal temperatures for hibernation? Comp Biochem Physiol D. 1991;99:323–326.
  • Boyles JG, Boyles E, Dunlap RK, et al. Long-term microclimate measurements add further evidence that there is no “optimal” temperature for bat hibernation. Mamm Biol. 2017;86:9–16.
  • Verant ML, Boyles JG, Waldrep W, et al. Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. PLoS One. 2012;7:e46280.
  • Grieneisen LE, Brownlee-Bouboulis SA, Johnson JS, et al. Sex and hibernaculum temperature predict survivorship in white-nose syndrome affected little brown myotis (Myotis lucifugus). R Soc Open Sci. 2015;2(2):140470.
  • Langwig KE, Frick WF, Bried JT, et al. Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecol Lett. 2012;15:1050–1057.
  • Langwig KE, Frick WF, Hoyt JR, et al. Drivers of variation in species impacts for a multi-host fungal disease of bats. Philos Trans R Soc B. 2016;371:20150456.
  • Bartonicka T, Bandouchova H, Berkova H, et al. Deeply torpid bats can change position without elevation of body temperature. J Therm Bio. 2017 Jan;63:119–123. PubMed PMID: 28010809.
  • Shuey MM, Drees KP, Lindner DL, et al. Highly sensitive quantitative PCR for the detection and differentiation of Pseudogymnoascus destructans and other Pseudogymnoascus species. Appl Environ Microbiol. 2014;80:1726–1731.
  • Turner GG, Meteyer CU, Barton HD, 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. 2014;50:566–573.
  • Zahradníková A Jr., Kovacova V, Martínková N, et al. Historic and geographic surveillance of Pseudogymnoascus destructans possible from collections of bat parasites. Transbound Emerg Dis. 2018;65(2):303–308. PubMed PMID: 29181887.
  • Team RC. R: A language and environment for statistical computing Vienna, Austria: R Foundation for Statistical Computing; 2018. Available from: http://www.R-project.org/
  • Urbanek S jpeg: read and write JPEG images. R package version 0.1-82014. https://CRAN.R-project.org/package=jpeg
  • Rowlingson B, Diggle P splancs: spatial and Space-Time Point Pattern Analysis. R package version 2. 01-40 2017. Available from: https://CRAN.R-project.org/package=splancs
  • Schindelin J, Rueden CT, Hiner MC, et al. The ImageJ ecosystem: an open platform for biomedical image analysis. Mol Reprod Dev. 2015 Jul-Aug;82(7–8):518–529. PubMed PMID: 26153368; PubMed Central PMCID: PMC5428984.
  • Humphries MM, Thomas DW, Speakman JR. Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature. 2002;418:313–316. PubMed PMID: 12124620.
  • Zukal J, Berková H, Banďouchová H, et al. Bats and Caves: activity and Ecology of Bats Wintering in Caves. In: Karabulut S, editor. Cave Investigation. Rijeka: InTech; 2017. p. 51–75.
  • Badino G. Cave temperatures and global climatic change. Int J Speleol. 2004;33:103–114.
  • Hijmans RJ, Cameron SE, Parra JL, et al. Very high resolution interpolated climate surfaces for global land areas. Int J Clim. 2005;25:1965–1978.
  • Kim KJ, Moskowitz H, Koksalan M. Fuzzy versus statistical linear regression. Eur J Oper Res. 1996;92:417–434.
  • Dubois D, Prade H, editors. Fuzzy sets and probability: misunderstandings, bridges and gaps. [Proceedings 1993] Second IEEE International Conference on Fuzzy Systems; 1993; San Francisco, CA.
  • Jiang H, Kwong CK, Park W-Y. Probabilistic fuzzy regression approach for preference modeling. Eng Appl Artif Intell. 2017;64:286–294.
  • Lee H, Tanaka H. Fuzzy approximations with non-symmetric fuzzy parameters in fuzzy regression analysis. J Oper Res. 1999;42:98–112.
  • Škrabánek P, Martínková N fuzzyreg: fuzzy linear regression. R package version 0.2 2018. Available from: https://CRAN.R-project.org/package=fuzzyreg
  • Bates D, Mächler M, Bolker B, et al. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–48.
  • Briere J-F, Pracros P, Le Roux A-Y, et al. A novel rate model of temperature-dependent development for arthropods. Environ Entomol. 1999;28(1):22–29.
  • Roberts DR, Bahn V, Ciuti S, et al. Cross-validation strategies for data with temporal, spatial, hierarchical, or phylogenetic structure. Ecography. 2017;40(8):913–929.
  • Lorch JM, Meteyer CU, Behr MJ, et al. Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature. 2011;480:376–378.
  • Martínková N, Škrabánek P, Pikula J. Modelling invasive pathogen load from non-destructive sampling data. bioRxiv. 2018. doi: 10.1101/474817.
  • Muggeo VMR. segmented: an R package to fit regression models with broken-line relationships. R News. 2008;8(1):20–25.
  • IUCN. The IUCN red list of threatened species. Version 2016-1 2016 [23-10-2017]. Available from: http://www.iucnredlist.org
  • Douglas D, Peucker T. Algorithms for the reduction of the number of points required to represent a digitized line or its caricature. Can. Cartographer. 1973;10(2):112–122.
  • Bivand R, Keitt T, Rowlingson B rgdal: bindings for the geospatial data abstraction library. R package version 1. 1-10 2016. Available from: https://CRAN.R-project.org/package=rgdal
  • Bivand R, Lewin-Koh N maptools: tools for Reading and Handling Spatial Objects. R package version 0.8-39. 2016.
  • Bivand R, Rundel C rgeos: interface to geometry engine - open source (GEOS). R package version 0. 3-19 2016. Available from: https://CRAN.R-project.org/package=rgeos
  • Hijmans RJ raster: geographic data analysis and modeling. R package version 2. 6-7. 2017. Available from: https://CRAN.R-project.org/package=raster
  • Howarth RJ. Sources for a history of the ternary diagram. Br J Hist Sci. 1996;29:337–356.
  • Hayman DTS, Cryan PM, Fricker PD, et al. Long-term video surveillance and automated analyses reveal arousal patterns in groups of hibernating bats. Methods Ecol Evol. 2017;8(12):1813–1821.
  • Maher SP, Kramer AM, Pulliam JT, et al. Spread of white-nose syndrome on a network regulated by geography and climate. Nat Commun. 2012;3:1306.
  • Turner GG, Reeder DM, Coleman JTH. A five-year assessment of mortality and geographic spread of white-nose syndrome in North American bats, with a look at the future. Update of white-nose syndrome in bats. Bat Res News. 2011;52:13–27.
  • Barlow AM, Worledge L, Miller H, et al. First confirmation of Pseudogymnoascus destructans in British bats and hibernacula. Vet Rec. 2015 Jul 18;177(3):73. PubMed PMID: 25968064.
  • Puechmaille SJ, Verdeyroux P, Fuller H, et al. White-nose syndrome fungus (Geomyces destructans) in bat, France. Emerg Infect Dis. 2010;16:290–293.
  • Wibbelt G, Kurth A, Hellmann D, et al. White-nose syndrome fungus (Geomyces destructans) in bats, Europe. Emerg Infect Dis. 2010;16:1237–1243.
  • Medzhitov R, Schneider DS, Soares MP. Disease tolerance as a defense strategy. Science. 2012;335:936–941.
  • Schneider DS, Ayres JS. Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases [Perspective]. Nat Rev Immunol. 2008 11 01;8:889.
  • Reeder DM, Frank CL, Turner GG, et al. Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS One. 2012;7:e38920.
  • Harazim M, Horáček I, Jakešová L, et al. Natural selection in bats with historical exposure to white-nose syndrome. BMC Zool. 2018;3:8.