Abstract
The psychrophilic fungus Pseudogymnoascus destructans (formerly known as Geomyces destructans) is considered the etiological agent of white-nose disease (WND), an emerging disease which affects bats during their hibernation period. This disease is clinically characterized by the growth of a white fungus on muzzle, ears, and wings’ membranes of affected bats. This infection caused the death of several million bats in North America. Conversely, European bats show no evidence of significant mortality occurrences associated with P. destructans colonization. This fungus has been isolated from bats in at least 15 European countries since 2008, but was never before reported in the Iberian Peninsula. This study describes the first case report of P. destructans colonization in bats from Portugal. We isolated P. destructans from three hibernating Myotis blythii (lesser mouse-eared bat) with visual signs of P. destructans colonization, during a routine visit to a mine located in the Trás-os-Montes region, Northern Portugal. M. blythii is one of the rarest bat species in Europe, classified as critically endangered in Portugal. P. destructans was obtained from at least three different parts of the body of each specimen analyzed. The identification of the respective fungal isolates was based on the macroscopic and microscopic characterization of the cultures and confirmed by PCR-based analysis. All nucleotide sequences obtained showed 100 % identity with previous data reported for P. destructans. This new finding improves the current knowledge about the European distribution of P. destructans, which is of great interest for forthcoming studies on the fungus dispersion and impact among bat populations at regional and/or global level.
This is a preview of subscription content, access via your institution.

References
Aşan N, Albayrak I (2011) Taxonomic status of Myotis myotis (Borkhausen, 1797) and Myotis blythii (Tomes, 1857) in Turkey (Mammalia: Chiroptera). Turk J Zool 35:357–365
Barros P (2012) Contribución al conocimiento de la distribución de quirópteros en el norte y centro de Portugal. Barbastella 5:19–31
Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JTH, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB (2009) Bat white-nose syndrome: an emerging fungal pathogen. Science 323:227
Cabral MJ (coord), Almeida J, Almeida PR, Dellinger T, Ferrand de Almeida N, Oliveira ME, Palmeirim JM, Queiroz AL, Rogado L, Santos-Reis M (eds) (2006) Livro Vermelho dos Vertebrados de Portugal. 2ª ed. Instituto da Conservação da Natureza/Assírio & Alvim. Lisboa. 660 pp
Cryan PM, Meteyer CU, Boyles JG, Blehert DS (2013) White-nose syndrome in bats: Illuminating the darkness. BMC Biol 11:47
Dietz C, Helversen OV, Nill D (2009) Bats of Britain, Europe & Northwest Africa. A & C Black Publishers Ltd., London
Foley J, Clifford D, Castle K, Cryan PM, Ostfeld RS (2010) Investigating and managing the rapid emergence of white-nose syndrome, a novel, fatal, infectious disease of hibernating bats. Biol Conserv 25:223–231
Gargas A, Trest MT, Christensen M, Volk TJ, Blehert DS (2009) Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon 108:147–154
Martínková N, Bačkor P, Bartonička T, Blažková P, Červený J, Falteisek L, Gaisler J, Hanzal V, Horáček D, Hubálek Z, Jahelková H, Kolařík M, Korytár L, Kubátová A, Lehotská B, Lehotský R, Lučan RK, Májek O, Matějů J, Rehák Z, Šafář J, Tájek P, Tkadlec E, Uhrin M, Wagner J, Weinfurtová D, Zima J, Zukal J, Horáček I (2010) Increasing incidence of Geomyces destructans fungus in bats from the Czech Republic and Slovakia. PLoS ONE 5:e13853
Meteyer CU, Buckles EL, Blehert DS, Hicks AC, Green DE, Shearn-Bochsler V, Thomas NJ, Gargas A, Behr MJ (2009) Histopathologic criteria to confirm white-nose syndrome in bats. J Vet Diagn Invest 21:411–414
Minnis AM, 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 Biol 117:638–649
Palmeirim JM, Rodrigues L, Rainho A, Ramos MJ (1999) Chiroptera. In: Mamíferos Terrestres de Portugal Continental, Açores e Madeira. Instituto da Conservação da Natureza & Centro de Biologia Ambiental (eds), Lisboa, 199 pp, pp 41–95
Puechmaille SJ, Verdeyroux P, Fuller H, Ar Gouilh MM, Bekaert M, Teeling EC (2010) White-nose syndrome fungus (Geomyces destructans) in bat, France. Emerg Infect Dis 16:290–293
Puechmaille SJ, Wibbelt G, Korn V, Fuller H, Forget F, Mühldorfer K, Kurth A, Bogdanowicz W, Borel C, Bosch T, Cherezy T, Drebet M, Görföl T, Haarsma AJ, Herhaus F, Hallart G, Hammer M, Jungmann C, Le Bris Y, Lutsar L, Masing M, Mulkens B, Passior K, Starrach M, Wojtaszewski A, Zöphel U, Teeling EC (2011) Pan-european distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS ONE 6:e19167
Reeder DM, Frank CL, Turner GG, Meteyer CU, Kurta A, Britzke ER, Vodzak ME, Darling SR, Stihler CW, Hicks AC, Roymon J, Grieneisen LE, Brownlee SA, Muller LK, Blehert DS (2012) Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS ONE 7:e38920
Rodrigues L, Zahn A, Rainho A, Palmeirim JM (2003) Contrasting the roosting behaviour and phenology of an insectivorous bat (Myotis myotis) in its southern and northern distribution ranges. Mammalia 67:321–335
Simmons NB (2005) Order Chiroptera. In: Wilson DE, Reeder DM (eds) Mammal species of the world. A taxonomic and geographic reference, 3rd edn. The Johns Hopkins University Press, Baltimore, pp 500–518
Šimonovičová A, Pangallo D, Chovanová K, Lehotská B (2011) Geomyces destructans associated with bat disease WNS detected in Slovakia. Biologia 66:562–564
Stadelmann B, Lin LK, Kunz TH, Ruedi M (2007) Molecular phylogeny of new world Myotis (Chiroptera, Vespertilionidae) inferred from mitochondrial and nuclear DNA genes. Mol Phylogenet Evol 43:32–48
U.S. Fish and Wildlife Service (2014) Press Release: U.S. Fish and Wildlife Service Awards $1.4 Million in Grants for Work on Deadly Bat Disease: $2 Million Available in Second Round. http://www.fws.gov/news/ShowNews.cfm?ID=98B74A03-93CF-4557-4EFFE9EC01166810. Accessed 15 May 2014
Verant ML, Boyles JG, Waldrep W Jr, Wibbelt G, Blehert DS (2012) Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. PLoS ONE 7:e46280
Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misra V, Cryan PM, Wibbelt G, Blehert DS, Willis CKR (2012) Inoculation of a North American bat with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Natl Acad Sci U S A 109:6999–7003
Wibbelt G, Kurth A, Hellmann D, Weishaar M, Barlow A, Veith M, Prüger J, Görföl T, Grosche L, Bontadina F, Zöphel U, Seidl HP, Seidl HP, Blehert DS (2010) White-nose syndrome fungus (Geomyces destructans) in bats, Europe. Emerg Infect Dis 16:1237–1242
Wibbelt G, Puechmaille SJ, Ohlendorf B, Mühldorfer K, Bosch T, Görföl T, Passior K, Kurth A, Lacremans D, Forget F (2013) Skin lesions in European hibernating bats associated with Geomyces destructans, the etiologic agent of white-nose syndrome. PLoS ONE 8:e74105
Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214
Acknowledgments
This study was supported by funding from several ecological monitoring projects of the Laboratory of Applied Ecology (University of Trás-os-Montes and Alto Douro) and by Portuguese Foundation for Science and Technology (FCT) through the project PEst-OE/AGR/UI4033/2014 and the PhD Grant SFRH/BD/77872/2011.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. Gortázar
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 15 kb)
Rights and permissions
About this article
Cite this article
Paiva-Cardoso, M.d.N., Morinha, F., Barros, P. et al. First isolation of Pseudogymnoascus destructans in bats from Portugal. Eur J Wildl Res 60, 645–649 (2014). https://doi.org/10.1007/s10344-014-0831-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10344-014-0831-2
Keywords
- Pseudogymnoascus destructans
- White-nose disease
- WND
- Bat
- Myotis blythii
- Portugal