Post-epizootic salamander persistence in a disease-free refugium suggests poor dispersal ability of Batrachochytrium salamandrivorans

Abstract

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.

Using environmental DNA for detection of Batrachochytrium salamandrivorans in natural water

“…The current scattered distribution of Bsal in Europe (Dalbeck et al, 2018; Spitzen‐van der Sluijs et al, 2016), the poor detectability of sick and deceased individuals (unpubl. data) and the variable prevalence in wild salamander and newt populations (Dalbeck et al, 2018; Spitzen‐van der Sluijs et al, 2016; 2018; Yuan et al, 2018), is factors that make active surveillance for Bsal cost‐ineffective, while Bsal has the potential to further expand (Beukema et al, 2018) either via anthropogenic or natural pathways (e.g., Fitzpatrick, Pasmans, Martel, & Cunningham, 2018; Stegen et al, 2017). Active surveillance for Bsal is performed by collecting skin swabs from the amphibian host (Hyatt et al, 2007), and then analyzing these swabs for the presence of Bsal DNA using quantitative PCR (qPCR) techniques (Blooi et al, 2015a; 2015b).…”

Landscape Connectivity Limits the Predicted Impact of Fungal Pathogen Invasion

“…Although a limited number of contact zones between some of these lineages do exist, the generally inhospitable landscape that shaped this genetic diversity can be expected to result in poor connectivity and marked landscape resistance against the Lyciasalamandra host dispersal. Assuming that salamanders of the genus Lyciasalamandra are the only significant hosts present, this may heavily impact the epidemiology of the infection, since dispersal of B. salamandrivorans has been associated predominantly with dispersal of infected hosts [15]. Ironically, rapid mortality post infection further limits pathogen spread through infected hosts.…”

“…The extent of the impact would, however, also be determined by pathogen transmission success between salamander populations and by host thermal ecology. B. salamandrivorans has been shown to spread slowly [15], and natural (non-anthropogenic) spread is associated with the presence of pathogen carriers [2,16,17]. Salamander body temperatures that exceed the lethal temperatures of 25 • C for B. salamandrivorans could suppress or even eliminate infection [18,19].…”

Conservation decisions under pressure: Lessons from an exercise in rapid response to wildlife disease

“…Even 1–2 extra days might allow a more informed decision, although longer delays are obviously riskier (Scudamore & Harris, ). How long is too long depends on the local policy context and on the characteristics of the disease: for example, Bsal might disperse slowly (Spitzen‐van der Sluijs et al, ), allowing managers more time—possibly weeks—than in the case of pathogens spread by more mobile hosts (e.g., Pseudogymnoascus destructans causing white‐nose syndrome in bats; Foley, Clifford, Castle, Cryan, & Ostfeld, ). Again, such characteristics may be unknown in the case of novel emerging pathogens and diseases, forcing decision‐makers to rely on expert elicitation and making uncertainty inevitable.…”