Significance
Chytridiomycosis has resulted in the serious decline and extinction of >200 species of amphibians worldwide and poses the greatest threat to biodiversity of any known disease. This fungal disease is currently known to be caused by
Batrachochytrium dendrobatidis
, hitherto the only species within the entire phylum of the Chytridiomycota known to parasitize vertebrate hosts. We describe the discovery of a second highly divergent, chytrid pathogen,
Batrachochytrium salamandrivorans
sp. nov., that causes lethal skin infections in salamanders, which has resulted in steep declines in salamander populations in northwestern Europe. Our finding provides another explanation for the phenomenon of amphibian biodiversity loss that is emblematic of the current global biodiversity crisis.
In the Netherlands, the fire salamander (Salamandra salamandra) is at the edge of its geographic range and is restricted to three small populations in the extreme south of the country. Despite the species being listed as ‘Endangered’ on the national Red List, the situation was considered to be stable. However, from 2008 onwards dead individuals were seen on more than one occasion. A sharp decline in numbers has been observed since 2010 (96%; ), but we were unable to attribute this to any known cause of amphibian decline, such as chytridiomycosis, ranavirus or habitat degradation. The present work describes this enigmatic decline, and we discuss these results in the context of possible causes.
The inconsistent distribution of large-scale infection mediated die-offs and the subsequent population declines of several animal species, urges us to understand how, when, and why species are affected by disease. It is often unclear when or under what conditions a pathogen constitutes a threat to a host. Often, variation of environmental conditions plays a role. Globally Batrachochytrium dendrobatidis (Bd) causes amphibian declines; however, host responses are inconsistent and this fungus appears equally capable of reaching a state of endemism and subsequent co-existence with native amphibian assemblages. We sought to identify environmental and temporal factors that facilitate host-pathogen coexistence in northern Europe. To do this, we used molecular diagnostics to examine archived and wild amphibians for infection and general linear mixed models to explore relationships between environmental variables and prevalence of infection in 5 well-sampled amphibian species. We first detected infection in archived animals collected in 1999, and infection was ubiquitous, but rare, throughout the study period (2008-2010). Prevalence of infection exhibited significant annual fluctuations. Despite extremely rare cases of lethal chytridiomycosis in A. obstetricans, Bd prevalence was uncorrelated with this species' population growth. Our results suggest context dependent and species-specific host susceptibility. Thus, we believe recent endemism of Bd coincides with environmentally driven Bd prevalence fluctuations that preclude the build-up of Bd infection beyond the critical threshold for large-scale mortality and host population crashes.
Lack of disease spill-over between adjacent populations has been associated with habitat fragmentation and the absence of population connectivity. We here present a case which describes the absence of the spill-over of the chytrid fungus Batrachochytrium salamandrivorans (Bsal) between two connected subpopulations of fire salamanders (Salamandra salamandra). Based on neutrally evolving microsatellite loci, both subpopulations were shown to form a single genetic cluster, suggesting a shared origin and/or recent gene flow. Alpine newts (Ichthyosaura alpestris) and fire salamanders were found in the landscape matrix between the two sites, which are also connected by a stream and separated by no obvious physical barriers. Performing a laboratory trial using alpine newts, we confirmed that Bsal is unable to disperse autonomously. Vector-mediated dispersal may have been impeded by a combination of sub-optimal connectivity, limited dispersal ability of infected hosts and a lack of suitable dispersers following the rapid, Bsal-driven collapse of susceptible hosts at the source site. Although the exact cause remains unclear, the aggregate evidence suggests that Bsal may be a poorer disperser than previously hypothesized. The lack of Bsal dispersal between neighbouring salamander populations opens perspectives for disease management and stresses the necessity of implementing biosecurity measures preventing human-mediated spread.
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