Broad host susceptibility of North American amphibian species to Batrachochytrium salamandrivorans suggests high invasion potential and biodiversity risk

Abstract

Batrachochytrium salamandrivorans (Bsal) is a fungal pathogen of amphibians that is emerging in Europe and could be introduced to North America through international trade or other pathways. To evaluate the risk of Bsal invasion to amphibian biodiversity, we performed dose-response experiments on 35 North American species from 10 families, including larvae from five species. We discovered that Bsal caused infection in 74% and mortality in 35% of species tested. Both salamanders and frogs became infected and developed Bsal chytridiomycosis. Based on our host susceptibility results, environmental suitability conditions for Bsal, and geographic ranges of salamanders in the United States, predicted biodiversity loss is expected to be greatest in the Appalachian Region and along the West Coast. Indices of infection and disease susceptibility suggest that North American amphibian species span a spectrum of vulnerability to Bsal chytridiomycosis and most amphibian communities will include an assemblage of resistant, carrier, and amplification species. Predicted salamander losses could exceed 80 species in the United States and 140 species in North America.

Using FINDeM for rapid, CRISPR-based detection of the emerging salamandrid fungal pathogen,Batrachochytrium salamandrivorans

“…Conservationists have repeatedly called for more "biosecure" amphibian trade for regions that appear Bsal naïve, such as in the Americas where the introduction of Bsal is expected to cause widespread population declines in the world's greatest salamander diversity hotspot (15).…”

“…While Bd is considered the world's most impactful invasive species (8) and threatens all three orders of amphibians globally (7), Bsal has emerged more recently in Europe, where it has posed a threat to the west Palearctic caudate diversity for at least two decades (9,10). Outside its hypothesized native range in Asia (11), Bsal has been observed in four European countries (Belgium, Germany, Spain, the Netherlands) and, as spill-over events to naïve regions have been noticed repeatedly in Europe (12)(13)(14), there is great concern that the pathogen may spread to the Americas and threaten salamander species in the taxon's global biodiversity hotspot (15).…”

Genome variation in the Batrachochytrium pathogens of amphibians

“…Conversely, Bsal causes disease in, primarily, the Urodela order of amphibia (salamanders and newts), is currently only found in Europe and Asia, and causes multifocal superficial erosions and deep ulcerations of the skin of hosts [ 7 ]. Experimentally, Bsal has also been shown to be able to infect some anurans and cause disease in at least 2 frog species [ 8 ]. To date, only 1 lineage of Bsal has been identified.…”

“…Batrachochytrids show striking differences in genome lengths that oppose this trend: The 73.3-Mb genome assembly for the more host-selective Bsal (at least, compared with Bd ) is 3 times longer than that for the generalist Bd (23.7 Mb). The evolutionary cause of this difference in genomic length is currently unclear but could reflect population dynamics or perhaps reflect that Bsal is also more of generalist than currently experimentally ascertained [ 8 ]. In either case, it is unclear whether Bsal has undergone a genome expansion, or if Bd has undergone a contraction.…”

Ecological Barriers for an Amphibian Pathogen: A Narrow Ecological Niche for Batrachochytrium salamandrivorans in an Asian Chytrid Hotspot

“…In contrast, Bsal mainly affects caudates and several anurans [ 9 , 10 ]. It has led to severe declines in native salamanders only in Europe so far, although the pathogen is present in Asia [ 4 , 5 , 6 , 11 ]; however, the impending threat for the highly diverse North American and Neotropical salamanders is significant [ 12 , 13 , 14 , 15 , 16 , 17 , 18 ]. Knowledge of Bsal ecology is critical as it provides proactive information for amphibian conservation, including identifying new susceptible species and analyzing their occurrences with the identification of the relevant ecological drivers.…”