Date Published: December 10, 2015
Publisher: Public Library of Science
Author(s): Matthew J. Gray, James P. Lewis, Priya Nanjappa, Blake Klocke, Frank Pasmans, An Martel, Craig Stephen, Gabriela Parra Olea, Scott A. Smith, Allison Sacerdote-Velat, Michelle R. Christman, Jennifer M. Williams, Deanna H. Olson, Deborah A. Hogan.
Batrachochytrium salamandrivorans (Bsal) is an emerging fungal pathogen that has caused recent die-offs of native salamanders in Europe and is known to be lethal to at least some North American species in laboratory trials . Bsal appears to have originated in Asia, and may have been introduced by humans into wild populations in Europe through commercial trade of amphibians . Since the first outbreaks of Bsal in the Netherlands, it has been the etiologic agent of mortality events in Belgium (wild) and Germany (captivity), and was recently found in imported salamanders in the United Kingdom [1–4]. Substantial concern has been raised about the associated risk of Bsal to native salamanders in North America . Herein, we review what policy actions are occurring in North America and elsewhere, and call for creation of a North American Bsal Strategic Plan.
Bsal parasitizes the epidermal cells of salamanders (order Urodela), causing skin ulcerations with significant degradation of the epidermis, which is sometimes visible macroscopically (Fig 1) and very obvious histologically (Fig 2). Loss of epidermal integrity with subsequent impairment of vital skin functions (e.g., electrolyte homeostasis, fluid balance, gas exchange, barrier against opportunistic pathogens) leads to death in susceptible species within two to three weeks after exposure [1,2]. Death is generally preceded by a brief episode of abnormal body posture and behavior. Species susceptibility correlates with the ability of Bsal to invade the epidermis, and is species- and developmental-stage–dependent . Whereas some species succumb quickly to chytridiomycosis after Bsal infection, others have been shown to tolerate and eventually clear infection, suggesting the development of acquired immunity . Although experimental exposure to Bsal zoospores leads to mortality in a wide range of salamander species, mortality events in wild salamander populations have been reported only in a single species (fire salamander, Salamandra salamandra). Mortality events in other species may have gone unnoticed due to the secretive nature of salamanders.
North America is a global hotspot for salamander biodiversity, accounting for about 50% of species worldwide . In particular, Mexico and the Appalachian Mountains are collectively home to more than 100 species of lungless salamanders (family Plethodontidae). Both of these areas, along with the Pacific Northwest, are known for their regionally endemic and relictual salamander species. In North American forests, the biomass of salamanders can exceed the biomass of all other vertebrate species [12,13]. Salamanders are centrally nested in aquatic and terrestrial food webs, as predators of various insects (including hosts of human pathogens ) and prey for higher-order predators such as reptiles, birds, and mammals (e.g., ). Indeed, salamanders are vital components of ecosystems, significantly affecting various ecological processes, energy flow, and trophic-level interactions, which ultimately contributes to environmental quality.
Introduced pathogens have significant impact on native wildlife. The related amphibian fungal pathogen, Bd, has had dire effects on its hosts worldwide . The pathogen that causes white-nose syndrome, Pseudogymnoascus destructans, recently introduced from Europe to North America, has decimated many bat populations . The chestnut blight fungus, Cryphonectria parasitica, introduced to North America from Asia in the early 1900s, caused the functional extinction of the American chestnut tree (Castanea dentata), forever changing eastern North American forest ecosystems. As with many invasive species, what we have learned from the emergence of these fungal pathogens in North America is that preventing introduction is the best way to protect populations, and if introduction occurs, rapid response is essential .
Due to the potential threat of Bsal to North American salamanders, creation of a North American Strategic Plan for Bsal is warranted. Several good examples exist of strategic plans for wildlife diseases, such as for white-nose syndrome  and Bd . At a minimum, components should include:
All evidence suggests that we are at a critical time of action to protect global amphibian biodiversity by swift policy actions to prevent the translocation of Bsal (Box 1). Bsal’s potential effects are broad taxonomically, geographically, ecologically, and across a variety of ecosystem services. Hence, response to the threat of Bsal calls for a cooperative effort across nongovernmental organizations, government agencies, academic institutions, zoos, the pet industry, and concerned citizens to avoid the potential catastrophic effects of Bsal on salamanders outside of the pathogen’s endemic regions. Communication, collaboration, and expedited action are key to ensure that Bsal does not become established in North America and decimate wild salamander populations. The template developed for North America may inform similar strategic policy planning for Bsal elsewhere.