Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome

Department of Biology and Centre for Forest Interdisciplinary Research, University of Winnipeg, Winnipeg, MB, Canada R3B 2E9.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 04/2012; 109(18):6999-7003. DOI: 10.1073/pnas.1200374109
Source: PubMed


White-nose syndrome (WNS) is an emerging disease of hibernating bats associated with cutaneous infection by the fungus Geomyces destructans (Gd), and responsible for devastating declines of bat populations in eastern North America. Affected bats appear emaciated and one hypothesis is that they spend too much time out of torpor during hibernation, depleting vital fat reserves required to survive the winter. The fungus has also been found at low levels on bats throughout Europe but without mass mortality. This finding suggests that Gd is either native to both continents but has been rendered more pathogenic in North America by mutation or environmental change, or that it recently arrived in North America as an invader from Europe. Thus, a causal link between Gd and mortality has not been established and the reason for its high pathogenicity in North America is unknown. Here we show that experimental inoculation with either North American or European isolates of Gd causes WNS and mortality in the North American bat, Myotis lucifugus. In contrast to control bats, individuals inoculated with either isolate of Gd developed cutaneous infections diagnostic of WNS, exhibited a progressive increase in the frequency of arousals from torpor during hibernation, and were emaciated after 3-4 mo. Our results demonstrate that altered torpor-arousal cycles underlie mortality from WNS and provide direct evidence that Gd is a novel pathogen to North America from Europe.

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Available from: Gudrun Wibbelt, Sep 30, 2015
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    • "A particularly virulent fungal pathogen (Pseudogymnoascus destructans; Pd) emerged in hibernating bats in eastern North America in 2006 (Blehert et al. 2009; Minnis and Lindner 2013). Likely an introduced species to North America (Warnecke et al. 2012), Pd has spread rapidly since its discovery. In the laboratory, infection is spread by physical contact between bats (i.e. "
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    ABSTRACT: Viral, bacterial, parasitic and fungal pathogens pose a significant, current threat to global biodiversity. A virulent fungal pathogen (Pseudogymnoascus destructans; Pd) emerged in hibernating bats in eastern North America in 2006. In this paper, we seek to inform epidemiological models of the progression of Pd into populations of the little brown bat (Myotis lucifugus) in central Canada by characterizing the spatial genetic structure of the host ahead of the imminent arrival of Pd. We sampled 242 bats from eight hibernacula spanning 92,623 km 2 and two ecozones. We genotyped all individuals at eight mi-crosatellite loci and sequenced 300 bp of HVII in a subset (n = 72) to test the null hypothesis of contemporary pan-mixia. We found evidence of spatial genetic structure associated with ecozone boundaries, and a predominant north–west to south–east directionality of bat movements among hibernacula, which opposes the current approach of the pathogen. Our large study area (larger than the dispersal distance of individual bats) allowed us to detect the first evidence of contemporary population structure among hibernacula of M. lucifugus. Our results suggest that the potential spread of Pd into north-central Canada may be retarded by the opposing direction of gene flow of the host species, and our findings of directional gene flow can be used to inform management strategies for the spread of Pd into the area. Keywords White nose syndrome Á Little brown bat Á Central North America Á Spatial genetic structure Á Hibernacula Á Ecozones
    Conservation Genetics 04/2015; DOI:10.1007/s10592-015-0719-z · 2.19 Impact Factor
    • "By the summer of 2014, WNS was confirmed in 25 states in the United States and in five provinces in Canada. Rapid expansion of the Pseudogymnoascus destructans (formerly known as Geomyces destructans) fungus, the causative agent of WNS (Lorch et al. 2011, Warnecke et al. 2012), together with reports of mass mortality in infected hibernation sites (hibernacula; Turner et al. 2011, U.S. Fish and Wildlife Service 2012), generated widespread concern that endangerment of already vulnerable bat species will be exacerbated (Blehert et al. 2009, Foley et al. 2011). Spread of white-nose syndrome occurs on at least three spatial scales: (1) within groups of individuals that roost in hibernation sites (individual level), (2) between hibernacula (hibernaculum level), and (3) at large landscape scales, e.g., county-level transmission between counties, a scale for which incidence data are available as the U.S. Fish and Wildlife Service records occurrences of white-nose syndrome in the contiguous United States by county (available online). "
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    ABSTRACT: White-nose syndrome (WNS) is an emerging infectious disease that has resulted in severe declines of its hibernating bat hosts in North America. The ongoing epidemic of white-nose syndrome is a multi-scale phenomenon it causes hibernaculum-level extirpations, while simultaneously spreading over larger spatial scales. We investigate a neglected topic in ecological epidemiology: how local pathogen-driven extirpations impact large-scale pathogen spread. Previous studies have identified risk factors for propagation of WNS over hibernaculum and landscape scales but none of these have tested the hypothesis that separation of spatial scales and disease-induced mortality at the hibernaculum level might slow or halt its spread. To test this hypothesis, we developed a mechanistic multi-scale model parameterized using white-nose syndrome.county and site incidence data that connects hibernaculum-level susceptible-infectious-removed (SIR) epidemiology to the county-scale contagion process. Our key result is that hibernaculum-level extirpations will not inhibit county-scale spread of WNS. We show that over 80% of counties of the contiguous USA are likely to become infected before the current epidemic is over and that geometry of habitat connectivity is such that host refuges are exceedingly rare. The macroscale spatiotemporal infection pattern that emerges from local SIR epidemiological processes falls within a narrow spectrum of possible outcomes, suggesting that recolonization, rescue effects, and multi-host complexities at local scales are not important to forward propagation of WNS at large spatial scales. If effective control measures are not implemented, precipitous declines in bat populations are likely, particularly in cave-dense regions that constitute the main geographic corridors of the USA, a serious concern for bat conservation.
    Ecological Applications 04/2015; 25(3):621-633. DOI:10.1890/14-0417.1 · 4.09 Impact Factor
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    • "Therefore, our analyses of rewarming rates focus on the first three months of the experiment using only iButton-based data. Bats exhibited advanced disease by three months [18] so these data reliably reflect arousal patterns of bats with WNS. We tested whether the timing of arousals from torpor differed from a random distribution using a Rayleigh's test [55]. "
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    ABSTRACT: The emerging wildlife disease white-nose syndrome (WNS) affects both physiology and behaviour of hibernating bats. Infection with the fungal pathogen Pseudogymnoascus destructans (Pd), the first pathogen known to target torpid animals, causes an increase in arousal frequency during hibernation, and therefore premature depletion of energy stores. Infected bats also show a dramatic decrease in clustering behaviour over the winter. To investigate the interaction between disease progression and torpor expression we quantified physiological (i.e., timing of arousal, rewarming rate) and behavioural (i.e., arousal synchronisation, clustering) aspects of rewarming events over four months in little brown bats (Myotis lucifugus) experimentally inoculated with Pd. We tested two competing hypotheses: 1) Bats adjust arousal physiology adaptively to help compensate for an increase in energetically expensive arousals. This hypothesis predicts that infected bats should increase synchronisation of arousals with colony mates to benefit from social thermoregulation and/or that solitary bats will exhibit faster rewarming rates than clustered individuals because rewarming costs fall as rewarming rate increases. 2) As for the increase in arousal frequency, changes in arousal physiology and clustering behaviour are maladaptive consequences of infection. This hypothesis predicts no effect of infection or clustering behaviour on rewarming rate and that disturbance by normothermic bats contributes to the overall increase in arousal frequency. We found that arousals of infected bats became more synchronised than those of controls as hibernation progressed but the pattern was not consistent with social thermoregulation. When a bat rewarmed from torpor, it was often followed in sequence by up to seven other bats in an arousal "cascade". Moreover, rewarming rate did not differ between infected and uninfected bats, was not affected by clustering and did not change over time. Our results support our second hypothesis and suggest that disturbance, not social thermoregulation, explains the increased synchronisation of arousals. Negative pathophysiological effects of WNS on energy conservation may therefore be compounded by maladaptive changes in behaviour of the bats, accelerating fat depletion and starvation. Copyright © 2014. Published by Elsevier Inc.
    Physiology & Behavior 03/2015; 140:71-78. DOI:10.1016/j.physbeh.2014.12.013 · 2.98 Impact Factor
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