Home Environment Bats in the Anthropocene: Conservation of Bats in a Changing World
Status of P. Destructans/WNS in Europe
In contrast to the severe impacts WNS has on North American bat species,
P. destructans is commonly found on bats in Europe but is not associated with mass mortality (Wibbelt et al. 2010; Puechmaille et al. 2011a). Europe is a putative source of the pathogen and the pathogen likely arrived in North America by some means of human trade or travel. Ongoing studies on global distribution of P. destructans (S.J. Puechmaille and J.R. Hoyt, unpublished data), including surveys in temperate Asia, may reveal important insights about the global distribution of the pathogen.
Pseudogymnoascus destructans was first reported in Europe by Puechmaille et al. (2010) who sampled a hibernating Myotis myotis from southwestern France showing the typical powdery white fungal growth on its nose. Since then, the fungus has been morphologically and genetically confirmed in 14 countries in Europe (France, Portugal, Belgium, The United Kingdom, The Netherlands, Germany, Switzerland, Austria, Slovakia, Poland, Hungary, Ukraine and Estonia) and convincing photographic evidence further supports its presence in an additional four countries (Luxembourg, Denmark, Romania and Turkey [the European part]) (Martínková et al. 2010; Puechmaille et al. 2010, 2011a; Kubátová et al. 2011; Simonovicová et al. 2011; Mestdagh et al. 2012; Wibbelt et al. 2010, 2013; Burger et al. 2013; Paiva-Cardoso et al. 2014; Sachanowicz et al. 2014). At the continental scale, most European reports are from northeastern France through Belgium, the Netherlands, Germany and the Czech Republic, but it remains unclear whether this pattern of higher prevalence of the fungus is real or reflects sampling bias (Puechmaille et al. 2011a). Studies conducted in Italy, Slovenia and Sweden, where P. destructans was not detected (Voyron et al. 2010; Nilsson 2012; Mulec et al. 2013), support the hypothesis that P. destructans occurrence and/or prevalence varies between different geographic regions in Europe (Puechmaille et al. 2011a).
Puechmaille et al. (2011a) demonstrated that the prevalence of visible signs of
P. destructans on bat wings and nose drastically varied through the hibernation period with the first cases appearing around mid-January. The number of cases increased to reach a peak in March and declined as bats emerged from hibernation. This pattern further complicates comparisons of prevalence of visual signs of fungal growth on bats between sites, regions or years unless surveys are carried out at the same time. Work done in the Czech Republic and Slovakia detected differences in prevalence of bats suspected to carry P. destructans (based on visual observations) between sub-mountain humid to mesic regions (higher prevalence) and mountainous and limestone regions (lower prevalence) (Martínková et al. 2010), supporting the idea that P. destructans is not equally abundant across Europe. Nevertheless, the differences in sampling strategy (spatio-temporal), sampling intensity (number of sites, number of samples), nature of the samples collected (e.g. swab from the bat vs. environment vs. guano) and analysis techniques
(e.g. culture, PCR detection) between different European studies make quantification of these fineand large-scale patterns challenging (Puechmaille et al. 2011a).
All confirmed cases of P. destructans infection come from fungal material collected on bats with the exception of a case from Estonia where the fungus has been isolated and cultured from the walls of the hibernation site, representing the first published isolation of viable spores from the environment in Europe or North America (Puechmaille et al. 2011a). In terms of species, available data suggest that M. myotis is the most commonly infected species (ca. 66 % of cases) with
P. destructans in Europe (Martínková et al. 2010; Puechmaille et al. 2011a). The fungus is known to also infect another nine species of European Myotis (ranked by decreasing order of prevalence): M. dasycneme, M. mystacinus, M. blythii,
M. daubentonii, M. brandtii, M. emarginatus, M. nattereri, M. bechsteinii and
M. escalerai/sp. A. The list of species with P. destructans infection is likely to increase as sampling intensity increases as illustrated by the recent Zukal et al. (2014) study which reported infection of a few individuals from three more species of the family Vespertilionidae, Eptesicus nilssonii, Plecotus auritus and Barbastella Barbastellus, as well as on a single individual of Rhinolophus hipposideros, of the family Rhinolophidae.
Owing to the protection of bats across Europe and the absence of mass mortality, only three studies with limited to moderate numbers of samples have investigated the pathology of P. destructans during the hibernation period (Pikula et al. 2012; Wibbelt et al. 2013; Bandouchova et al. 2015). In Europe, P. destructans invasion of the wing membrane is generally restricted to the epidermis and adnexae without deep invasion into the underlying connective tissue but with occasional formation of neutrophilic pustules, contrasting with the common and extensive invasion of dermal connective tissue in bats from North America (Pikula et al. 2012; Wibbelt et al. 2013; Zukal et al. 2014; Bandouchova et al. 2015). Based on investigation of two euthanized individuals, P. destructans invasion in the skin of the muzzle seems to be more pronounced than invasion of the wing membrane (Pikula et al. 2012; Wibbelt et al. 2013). As damage to the skin of the muzzle may not be as physiologically important for homeostasis as damage to the wing membranes (Cryan et al. 2010; Reeder et al. 2012; Warnecke et al. 2013), we suggest that it may be important to differentiate the pathology of P. destructans on the wing and on the muzzle. If dehydration and fluid loss play an important role in WNS pathophysiology, quantifying wing damage consistently (e.g. following Reeder et al. 2012 or an alternative scoring system) alongside physiological measures of disease severity will be critical for a better understanding of the disease, its progression and species-specific attributes, compared to the commonly reported dichotomous presence/absence of the disease.
The term WNS was originally used to describe the symptoms associated with bats in the field before the disease was fully characterized as a cutaneous infection of skin tissues by the pathogenic fungus, P. destructans (Blehert et al. 2009; Meteyer et al. 2009). As such, the name 'WNS' has changed from referring to a set of symptoms, including visible fungal growth on skin surfaces, depletion of fat reserves, altered torpor patterns and aberrant winter behaviour (Blehert et al. 2009) to referring to the presence of disease as defined by the presence of cutaneous infection characterized by cupping erosions (Meteyer et al. 2009). This has led to confusion and some debate about whether the term WNS should be used to describe infections occurring in Europe, which are pathologically similar to those in North America but which do not include mass mortality or aberrant winter behaviour (Puechmaille et al. 2011a). Despite its original definition as a syndrome (Veilleux 2008; Reeder and Turner 2008; Turner and Reeder 2009), the term WNS is now routinely used to refer the cutaneous infection caused by P. destructans, which have been documented in Europe (Pikula et al. 2012; Wibbelt et al. 2013; Zukal et al. 2014). Some have advocated a name change to clarify a difference between a 'syndrome' and a 'disease' caused by fungal infection (Chaturvedi and Chaturvedi 2011). Inconsistency in the literature could lead to confusion but recent use of the term white-nose disease (WND; Paiva-Cardoso et al. 2014) could clarify the situation by providing terminology reminiscent enough of WNS to avoid confusion but technically consistent with the definition of a disease.
Recent work comparing colony sizes of hibernating vespertilionid bats in North America before and after the emergence of WNS, to current colony sizes in Europe, reveals an intriguing pattern. Before WNS emerged in North America, colony sizes of hibernating bats were, on average, about 10-fold larger than those of similar species in Europe (Frick et al. 2015). However, after the emergence of WNS, colony sizes in eastern North America are no longer statistically different from those in Europe (Frick et al. 2015), raising the following question: Were hibernating bat colonies in Europe once much larger prior to the emergence of WNS there? If WNS is indeed acting as a hidden force on bat populations in Europe, then small winter colony sizes in eastern North America may become the norm for species in North America that manage to persist. However, Frick et al. (2015) also show that 69 % of winter colonies of M. septentrionalis were entirely eliminated within 7 years of WNS detection, suggesting that this species is rapidly disappearing from the landscape. The predicted extinction of M. septentrionalis from WNS begs the question whether past extinctions of bat species may have also occurred in Europe.
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