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Synopsis Emerging infectious diseases have been of particular interest as a major threat to global biodiversity. In amphibians, two fungal sister taxa, Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal), along with the viral pathogen ranavirus, have affected global populations. Factors such as host traits, abiotic and biotic environmental conditions, and pathogen prevalence contribute to species-specific disease susceptibility. The eastern United States is home to the Appalachian Mountain system, known as a “hotspot” for salamander biodiversity. Bd and ranavirus are present throughout the Appalachians, and a Bsal emergence could be imminent. Throughout the Appalachians are the spotted salamanders, Ambystoma maculatum, a mostly terrestrial salamander that participates in mass breeding migration to ponds and vernal pools in the late spring. Previous experimental studies have shown that spotted salamanders appear to be resistant to Bd and Bsal infection, but the mechanisms behind Bd defense remain unknown. Spotted salamanders emerging from their overwintering habitats were hypothesized to have potent anti-Bd function expressed in their mucus and in their skin microbiomes, as a countermeasure to annual Bd re-emergence. We used non-invasive sampling at two pools during the spotted salamander annual breeding event to (I) determine pathogen prevalence, (II) quantify the antifungal potential of salamander skin mucus, and (III) characterize the diversity and composition of the salamander skin microbiome and contrast it to that of the corresponding environmental microbiome. We did not detect any Bd, Bsal, or ranavirus in the salamanders. The salamander mucus did not inhibit Bd growth in vitro, and anti-Bd bacteria were at low relative abundance in the microbiome. The salamander microbiome sourced a proportion of bacteria from the environment and appeared to select rare taxa from their respective pools; however, their functional relevance in pathogen defense is unclear. Our results suggest that the spotted salamander mucosal secretions and skin microbiome are not the mechanisms of defense against Bd. Rather, elements not captured by the mucosome (e.g., immune cell gene expression) may confer resistance. This study contributes to the understanding of salamander intraspecies variation in disease susceptibility.
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Fungal infection, decline and persistence in the only obligate troglodytic Neotropical salamander
The fungal pathogen Batrachochytrium dendrobatidis ( Bd ) is implicated in global mass die-offs and declines in amphibians. In Mesoamerica, the Bd epidemic wave hypothesis is supported by detection of Bd in historic museum specimens collected over the last century, yet the timing and impact of the early stages of the wave remain poorly understood. Chiropterotriton magnipes , the only obligate troglodytic Neotropical salamander, was abundant in its small range in the decade following its description in 1965, but subsequently disappeared from known localities and was not seen for 34 years. Its decline is roughly coincident with that of other populations of Neotropical salamanders associated with the invasion and spread of Bd . To determine the presence and infection intensity of Bd on C. magnipes and sympatric amphibian species (which are also Bd hosts), we used a noninvasive sampling technique and qPCR assay to detect Bd on museum specimens of C. magnipes collected from 1952 to 2012, and from extant populations of C. magnipes and sympatric species of amphibians. We also tested for the presence of the recently discovered Batrachochytrium salamandivorans ( Bsal ), another fungal chytridiomycete pathogen of salamanders, using a similar technique specific for Bsal . We did not detect Bd in populations of C. magnipes before 1969, while Bd was detected at low to moderate prevalence just prior to and during declines. This pattern is consistent with Bd -caused epizootics followed by host declines and extirpations described in other hosts. We did not detect Bsal in any extant population of C. magnipes . We obtained one of the earliest positive records of the fungus to date in Latin America, providing additional historical evidence consistent with the Bd epidemic wave hypothesis. Genotyping results show that at least one population is currently infected with the Global Panzootic Lineage of Bd , but our genotyping of the historical positive samples was unsuccessful. The lack of large samples from some years and the difficulty in genotyping historical Bd samples illustrate some of the difficulties inherent in assigning causality to historical amphibian declines. These data also provide an important historical baseline for actions to preserve the few known remaining populations of C. magnipes .
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- Award ID(s):
- 1633948
- PAR ID:
- 10317578
- Date Published:
- Journal Name:
- PeerJ
- Volume:
- 8
- ISSN:
- 2167-8359
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.7717/peerj.9763
