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Prevalence and Phenology of White-Nose Syndrome Fungus Pseudogymnoascus Destructans in Bats from Poland

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Prevalence and Phenology of White-Nose Syndrome Fungus Pseudogymnoascus Destructans in Bats from Poland Cent. Eur. J. Biol. • 9(4) • 2014 • 437-443 DOI: 10.2478/s11535-013-0280-z Central European Journal of Biology Prevalence and phenology of white-nose syndrome fungus Pseudogymnoascus destructans in bats from Poland Research Article Konrad Sachanowicz1*, Arkadiusz Stępień2, Mateusz Ciechanowski3 1Museum and Institute of Zoology PAS, 00-679 Warszawa, Poland 241-933 Piekary Śląskie, Poland 3Department of Vertebrate Ecology and Zoology, University of Gdańsk, 80-308 Gdańsk, Poland Received 21 May 2013; Accepted 23 October 2013 Abstract: Pseudogymnoascus destructans (Pd), a parasitic fungus (being responsible for a disease known as white-nose syndrome, WNS) that caused mass mortality of cave-dwelling, hibernating bats in North America, appears to be native of Europe, where it also occurs on wintering bats, but no similar outbreaks of WNS have been recorded. Herein, we provide the first account on prevalence and phenology of P. destructans in Poland. Bats were counted once per month, from October or January to May (2010-2013), in an abandoned ore mine in southern Poland. Presence of P. destructans in two samples was confirmed by sequencing of isolated fungal DNA. Observations of phenotypically identical mycosis on bats hibernating at this site in March 2006 are likely to be the first known records of P. destructans from Poland. All Pd-suspected individuals were Myotis myotis with an exception of one Myotis daubentonii. The first Pd-suspected bats were noted in mid-February, but their number was the highest in March, what overlapped with maximum numbers of hibernating M. myotis. The prevalence in March was 7%-27% of M. myotis individuals. No mass mortality of bats was observed in the mine, with only three dead individuals found in the hibernaculum which hosted up to 130 bats, representing 6-7 species. Keywords: White-nose syndrome • Geomycosis • Chiroptera • Hibernation • Myotis myotis • Mortality © Versita Sp. z o.o. 1. Introduction caused mass mortality of cave-dwelling, vespertilionid bats in North America, being responsible for, so-called, A number of emerging fungal pathogens appear to be white-nose syndrome (WNS) [2,3]. increasing their frequency and abundance worldwide, The syndrome itself, first noticed in 2006, can be leading to severe, often continental or global, crises recognized by white hyphae and conidia growing on in biodiversity and ecosystem functioning [1]. The the muzzle, ears, wing membranes and even invading mechanisms hidden behind such an increase remain hair follicles of infected bats. WNS appeared only largely unknown, although environmental pollution, during hibernation, thus has been restricted to the climate change and intercontinental transport are often temperate zone, and affected only the species wintering blamed. Some of the mentioned fungal pathogens in underground roosts (hibernacula). The fungus was gained international interest, e.g. the chytrid fungus described as new for science in 2009, as Geomyces Batrachochytrium dendrobatidis, responsible for series destructans [5]. Later, phylogenetic analysis of Nearctic of extinctions or declines of more than 500 amphibian Geomyces and its allies placed the new pathogen in a species worldwide, or aquatic oomycete Aphanomyces separate genus Pseudogymnoascus [6]. It appeared astaci that caused a devastating decline in native to be psychrophilous, with no growth above 19.8°C European freshwater crayfish [1]. Recently, another and optimum at 12.5-15.8°C, but with production parasitic fungus, Pseudogymnoascus destructans, of abundant microconidia only below 12°C, a clear * E-mail: [email protected] 437 White-nose syndrome fungus in bats from Poland adaptation for propagation in microclimate typical for Although it became clear that the visual bat hibernacula [7]. Experimental infections of captive manifestation of P. destructans infections on the bats confirmed that P. destructans is responsible for exterior of bats in Europe developed mostly before the WNS pathogenesis [8], most often causing death of end of the hibernation period, i.e. March [18], the only infected individuals in case of North American species. detailed investigation of seasonal dynamics has been Infection causes ulcers, lesions, skin irritation and conducted at a single northwest German locality during severe damage to the invaded tissue [9,10]. Immune two consecutive seasons [20]. No such data is available reconstitution inflammatory syndrome (IRIS) probably for central Europe. The only published record of the triggers or contributes to that damage, as hibernation fungus from Poland concerns a studied sample from is associated with immune suppression, while return a M. myotis individual, collected in March 2010 at an to euthermia results in its rapid reversal [11]. Bats unknown locality in the southwest of the country [20]. In infected with P. destructans probably face severe this paper we provide the first account of the temporal evaporative water loss, thus increased frequency of occurrence of P. destructans infection in vespertilionid arousal from hibernation, with the animals often flying bats hibernating in an underground roost in south out of their roost, rapidly depleting their subcutaneous Poland. fat reserves and consequently dying of starvation [12,13]. WNS spreads rapidly during the first years after its appearance, leading to population collapse, even in 2. Experimental Procedures the common and widespread species Myotis lucifugus, that lost 30-99% of individuals spending winter in large We monitored a number of bats in corridors of a bat hibernacula in the eastern part of USA [14]. Also disused ore mine in the Blachówka dolomite quarry rare and endangered species, like Myotis sodalis, suffer (50°24.292´´N, 18°51.239´´E) in Bytom-Sucha Góra from the disease [15], and strong decrease in activity of (Śląsk Upland, south Poland). The mine is the most Myotis spp. during summer was recorded in the areas important part of Tarnowskie Góry-Bytom Undergrounds surrounding underground roosts affected by WNS [16]. designated in 2004 as Special Protected Area (Nature The pathogen being a causative agent of WNS, 2000) for bats and their habitats. The mine maintains P. destructans, has been recorded on bats hibernating the largest winter bat aggregation (up to 130 individuals, underground in several European countries (Austria, representing 6-7 species, recorded in the winter season Belgium, Czech Republic, Denmark, Estonia, France, 2012/2013) in the Silesian Upland (K. Sachanowicz, The Netherlands, Poland, Romania, Slovakia, A. Stępień, unpubl. data). In the mine, the average Switzerland, Turkey, Ukraine) [17-20]. Records of annual temperature reached 5.8°C measured ca 80 m P. destructans confirmed by fungal culture and genetic from its entrance. In the winter months, from January to analyses, were obtained from at least eight bat species: March, mean monthly temperature ranged from 0.5 to Myotis myotis, M. blythii oxygnathus, M. bechsteinii, 4.0°C, while during the period from April to November M. nattereri, M. mystacinus, M. brandtii, M. dasycneme – from 5.0 to 8.0°C; humidity was close to 100% [23]. and M. daubentonii [18,20] and WNS itself was confirmed During three winter seasons, 2010-2013, two in Europe by histopathological evidence [21]. However, authors (A. Stępień, K. Sachanowicz) counted bats it did not lead to mass mortality in any European country on a fixed transect ca 2500 m length, starting from the [20]. Most of bats with visible fungal growth probably grilled entrance of the mine. In the 2010-2012 seasons recovered after the end of hibernation and the most we counted bats once per a month, from October to affected species, M. myotis, reveals constant population May, while in 2013 – from January to May, including growth during the last 20 years with no signs of decline an additional count in March. All visible bats hanging [18]. The WNS-suspected bats have been recorded on on walls, ceiling and hidden in crevices of low (ca 1 to photographs since 1995 [18], ten years before the first 4 m high) walls of corridors were counted and identified American case, leading to the suspicion that the fungus based on external features, without handling. Thus, is native for Europe, transferred to America by humans, several individuals representing sibling species, either presumably by cave explorers. Further experiments M. brandtii or M. mystacinus, were left unidentified to with inoculation of American bats with European and species. American isolates of P. destructans provided direct After observing individuals of M. myotis with evidence that the fungus is most likely a recent invader white fungal growth (suspected P. destructans – later in America, while its high pathogenicity is associated described as ‘Pd-suspected’ [20]) in February 2011, we with lack of resistance to that pathogen in Myotis bats of collected samples of the fungus for genetic analysis North America [22]. in March 2011. Using cotton swabs we collected the 438 K. Sachanowicz et al. fungus from the muzzles of two hibernating M. myotis March 2011. The sequences obtained were submitted and placed them into 1.5 ml plastic tubes. The fungal to the European Nucleotide Archive with accession material was inoculated onto Sabouraud dextrose agar numbers HF911370-HF911371. plates and incubated in the dark at two temperatures (ca. In three consecutive seasons of bat monitoring, we 7°C and 15°C). After 14 days, the outgrowing colonies recorded the first individuals of Pd-suspected M. myotis of the fungus were isolated. The isolates were identified (Figure 2) in February, with the earliest observation based on their phenotypic characteristics, i.e. shape on 16th February 2013. The numbers or Pd-suspected and size of conidia and conidiophores. Fungal DNA bats were highest in March, when we observed also was also isolated from samples to confirm the species maximum numbers of hibernating M. myotis. In the identity. For details of DNA isolation, gene amplification, consecutive years, the prevalence in March was 13%, PCR reactions, products purification, sequencing and 27% and from 11 to 7% of individuals, respectively. We analysis protocols, see [18].
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