Landscape Connectivity Limits the Predicted Impact of Fungal Pathogen Invasion

Abstract

Infectious diseases are major drivers of biodiversity loss. The risk of fungal diseases to the survival of threatened animals in nature is determined by a complex interplay between host, pathogen and environment. We here predict the risk of invasion of populations of threatened Mediterranean salamanders of the genus Lyciasalamandra by the pathogenic chytrid fungus Batrachochytrium salamandrivorans by combining field sampling and lab trials. In 494 samples across all seven species of Lyciasalamandra, B. salamandrivorans was found to be absent. Single exposure to a low (1000) number of fungal zoospores resulted in fast buildup of lethal infections in three L. helverseni. Thermal preference of the salamanders was well within the thermal envelope of the pathogen and body temperatures never exceeded the fungus’ thermal critical maximum, limiting the salamanders’ defense opportunities. The relatively low thermal host preference largely invalidates macroclimatic based habitat suitability predictions and, combined with current pathogen absence and high host densities, suggests a high probability of local salamander population declines upon invasion by B. salamandrivorans. However, the unfavorable landscape that shaped intraspecific host genetic diversity, lack of known alternative hosts and rapid host mortality after infection present barriers to further, natural pathogen dispersal between populations and thus species extinction. The risk of anthropogenic spread stresses the importance of biosecurity in amphibian habitats.

Virulence and Pathogenicity of Chytrid Fungi Causing Amphibian Extinctions

“…Host preferences for higher temperatures (116) or increased body temperature during infection due to behaviors such as basking ( 114) may shift the balance in favor of the host. Any prediction of Batrachochytrium virulence should thus take into account the microclimate conditions that influence the thermal ecology of the host (11,65).…”

Batrachochytrium salamandrivorans’ Amphibian Host Species and Invasion Range

“…These species are: Calotriton arnoldi , Euproctus platycephalus , Lyciasalamandra helverseni , S. algira, and P. anguinus . Further, Bsal -related deaths have been reported in all these species except P. anguinus (Sabino-Pinto et al 2015 ; Martel et al 2014 , 2020 ; Li et al 2020 ) . The recognition of a taxonomic susceptibility in plethodontid caudates also highlights the risk that European cave salamanders ( Speleomantes sp . )…”

Batrachochytrium salamandrivorans Threat to the Iberian Urodele Hotspot

“…The likelihood of Bsal invasion is supported by predicted ecological niche overlap of Bsal with at least seven Iberian urodele species [ 24 ]. Since macroclimatic modeling obscures local host ecology and associated microclimatic conditions, Bsal may infect species that occur in cool and humid microhabitats within Mediterranean landscapes outside the pathogen’s predicted macroscale range [ 17 , 66 ]. Thus, we consider that all Iberian urodele populations could be at risk of infection by Bsal (i.e., broadscale climate refugia are unlikely to be present).…”

“…Refugia would require environmental and body temperatures of the entire host community to exceed those of the thermal tolerance of Bsal long enough to kill the fungus entirely [ 17 , 67 ]. In practice, given the current understanding of the Bsal climate niche [ 17 , 66 ], a complete refugium would mean that the entire suitable host community and the infected environment maintain temperatures of 25 °C or more for at least 10 days. While lower temperatures that fail to eradicate the fungus may still have an impact by temporarily tempering virulence and slowing down fungal growth [ 15 , 16 , 67 ], such conditions could extend the infectious period of an infected host, facilitating fungal survival in the host population with the potential of disease flareups once temperatures drop.…”