Batrachochytrium salamandrivorans elicits acute stress response in spotted salamanders but not infection or mortality

Abstract

The emerging fungal pathogen Batrachochytrium salamandrivorans (Bsal) is a major threat to amphibian species worldwide with potential to infect many species if it invades salamander biodiversity hotspots in the Americas. Bsal can cause the disease chytridiomycosis, and it is important to assess the risk of Bsal-induced chytridiomycosis to species in North America. We evaluated the susceptibility to Bsal of the common and widespread spotted salamander, Ambystoma maculatum, across life-history stages and monitored the effect of Bsal exposure on growth rate and response of the stress hormone, corticosterone. We conclude that spotted salamanders appear resistant to Bsal because they showed no indication of disease or infection, and experienced minor effects on growth upon exposure. While we focused on a single population for this study, results were consistent across conditions of exposure including high or repeated doses of Bsal, life-stage at exposure, environmental conditions including two temperatures and two substrates, and promoting pathogen infectivity by conditioning Bsal cultures with thyroid hormone. Exposure to high levels of Bsal elicited an acute but not chronic increase in corticosterone in spotted salamanders, and reduced growth. We hypothesize that the early acute increase in corticosterone facilitated mounting an immune response to the pathogen, perhaps through immunoredistribution to the skin, but further study is needed to determine immune responses to Bsal. These results will contribute to development of appropriate Bsal management plans to conserve species at risk of emerging disease.

Skin defenses of North American salamanders against a deadly salamander fungus

“…As we predicted, skin peptides from spotted salamanders ( Ambystoma maculatum ) inhibited the growth of Bsal , consistent with the observation that A. maculatum is Bsal resistant (Martel et al ., 2014; Barnhart et al ., 2019). Similar results were found for Bd .…”

“…Hence, the skin peptide repertoire reflects differences in skin microbiota which, in turn, are influenced by factors like captivity or geographic location of individuals that were sampled in the field (Kueneman et al ., 2014; Loudon et al ., 2014; Krynak et al ., 2016). Despite this limitation, assessing in vitro responses has been a useful tool in previous studies of the anuran‐ Bd system, and we feel that our results provide important insight towards better understanding the disease‐dynamics of chytrid pathogens, particularly Bsal (Woodhams et al ., 2006a; Woodhams et al ., 2006b; Grogan et al ., 2018; Barnhart et al ., 2019).…”

“…Until now, most of our understanding of the interspecific differences in host response to Bsal has come from a limited number of laboratory studies where individual amphibians were experimentally exposed to controlled doses of Bsal zoospores (infective life stage; range: 5 × 10 3 to 5 × 10 6 zoospores), and monitored for changes in infection load (the number of pathogenic organisms on a host; measured via genomic equivalents or GE), clinical signs of disease (e.g. ulcerative skin lesions, lethargy, skin sloughing, loss of righting reflex) and mortality (Blooi et al ., 2013; Martel et al ., 2013; Martel et al ., 2014; Blooi et al ., 2016; Barnhart et al ., 2019; Carter et al ., 2019). Based on these initial studies, host responses to Bsal ranged from resistant (no infection or clinical signs of disease) to lethal (infection resulting in mortality) (Martel et al ., 2014).…”

“…When available, we used information on experimentally observed host responses to chytrid pathogens to guide our predictions. Thus, for A. maculatum , which appear to be Bsal‐ resistant, we predicted that skin peptides would inhibit the growth of Bsal (Martel et al ., 2014; Barnhart et al ., 2019). Because individuals of many species of Plethodon salamanders are often resistant to all but very high doses of Bd , we predicted that P. shermani skin peptides would inhibit the growth of Bd (Chinnadurai et al ., 2009; Vazquez et al ., 2009; Fonner et al ., 2017).…”

Immunological Aspects of Chytridiomycosis

“…However, co-infections with Bd and Bsal are possible and may contribute to increasing mortality [ 19 , 20 ]. This review concentrates primarily on Bd, as much more is known about its immunology and pathology (although, see [ 6 , 19 , 20 , 21 , 22 , 23 ]).…”