Global Patterns of the Fungal Pathogen Batrachochytrium Dendrobatidis Support Conservation Urgency
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ORIGINAL RESEARCH published: 16 July 2021 doi: 10.3389/fvets.2021.685877 Global Patterns of the Fungal Pathogen Batrachochytrium dendrobatidis Support Conservation Urgency Deanna H. Olson 1*, Kathryn L. Ronnenberg 1, Caroline K. Glidden 2, Kelly R. Christiansen 1 and Andrew R. Blaustein 3 1 Pacific Northwest Research Station, United States Department of Agriculture (USDA) Forest Service, Corvallis, OR, United States, 2 Department of Biology, Stanford University, Stanford, CA, United States, 3 Department of Integrative Biology, Oregon State University, Corvallis, OR, United States The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) is a skin pathogen that can cause the emerging infectious disease chytridiomycosis in susceptible species. It has been considered one of the most severe threats to amphibian biodiversity. We aimed to provide an updated compilation of global Bd occurrences by host taxon and geography, and with the larger global Bd dataset we reanalyzed Bd associations with environmental metrics at the world and regional scales. We also compared our Bd data compilation with a recent independent assessment to provide a more comprehensive Edited by: Rachel E. Marschang, count of species and countries with Bd occurrences. Bd has been detected in 1,375 Laboklin GmbH & Co. KG, Germany of 2,525 (55%) species sampled, more than doubling known species infections since Reviewed by: 2013. Bd occurrence is known from 93 of 134 (69%) countries at this writing; this Hudson Alves Pinto, compares to known occurrences in 56 of 82 (68%) countries in 2013. Climate-niche Minas Gerais State University, Brazil Gonçalo Rosa, space is highly associated with Bd detection, with different climate metrics emerging Zoological Society of London, as key predictors of Bd occurrence at regional scales; this warrants further assessment United Kingdom relative to climate-change projections. The accretion of Bd occurrence reports points to *Correspondence: Deanna H. Olson the common aims of worldwide investigators to understand the conservation concerns [email protected] for amphibian biodiversity in the face of potential disease threat. Renewed calls for better mitigation of amphibian disease threats resonate across continents with amphibians, Specialty section: This article was submitted to especially outside Asia. As Bd appears to be able to infect about half of amphibian Zoological Medicine, taxa and sites, there is considerable room for biosecurity actions to forestall its spread a section of the journal using both bottom-up community-run efforts and top-down national-to-international Frontiers in Veterinary Science policies. Conservation safeguards for sensitive species and biodiversity refugia are Received: 26 March 2021 Accepted: 15 June 2021 continuing priorities. Published: 16 July 2021 Keywords: amphibian chytrid, Bd, climate associations, emerging infectious disease, fungal pathogen Citation: Olson DH, Ronnenberg KL, Glidden CK, Christiansen KR and INTRODUCTION Blaustein AR (2021) Global Patterns of the Fungal Pathogen Batrachochytrium dendrobatidis The Earth is undergoing a “biodiversity crisis,” with population losses and species extinctions Support Conservation Urgency. occurring at unprecedented rates (1–6). Contributing factors to biodiversity losses are multifaceted Front. Vet. Sci. 8:685877. and are complicated by species, population- and site-specific differences. Anthropogenic stressors doi: 10.3389/fvets.2021.685877 such as habitat loss and fragmentation, chemical contamination, introduced species, and climate Frontiers in Veterinary Science | www.frontiersin.org 1 July 2021 | Volume 8 | Article 685877 Olson et al. Global Bd Occurrence Patterns change are key factors influencing losses across taxonomic in 2008, hosted by Imperial College, UK. This exportable groups. Furthermore, there is increasing recognition of health database and mapping application provided the first global-scale concerns as species are exposed to emerging infectious diseases visualization of an amphibian panzootic (19, 28). The broad use (EIDs) [e.g., coral disease outbreaks (7, 8); sea star wasting disease of Bd-Maps.net led to the development of an analogous but (9); bat white-nose syndrome (10, 11); avian West Nile virus (12); more comprehensive online database for Ranavirus, the Global >50 United States (US) wildlife disease factsheets (13)]. Ranavirus Reporting System [GRRS (31)]. The GRRS inspired For the especially vulnerable vertebrate class Amphibia, the the development of the more sophisticated amphibian chytrid Global Amphibian Assessment first reported 32.5% of species disease portal for both Bd and Bsal, AmphibianDisease.org, as threatened with extinction (14) and that estimate has since hosted by AmphibiaWeb and the University of California at risen to 40% of species (5, 6), with an increase in concern for Berkeley (41). The Bd-Maps.net dataset is currently in transition disease impacts (2, 15–20). Amphibian diseases span both lethal to AmphibianDisease.org, providing continuity of and a means and sublethal multiple-host species infections by microparasites to archive the Global Bd Mapping project from 2007 to present. such as trematodes (21), bacteria (22), fungi (15, 23, 24), The importance of globally accessible online databases for protists (25, 26), and viruses (16, 24). Information on amphibian discerning pathogen occurrence patterns is multifold. First, gaps disease-causing pathogens has increased substantially in the in knowledge are readily apparent by species and location last two decades, especially relative to field surveillance of and can guide subsequent inventory and monitoring efforts; taxonomic and geographic patterns of pathogen occurrences at there is support that taxonomic and geographic gaps have global scales (27–31) and experimental research that illustrates been filled over time (28, 42, 43). Second, world occurrence species-specific vulnerabilities and interacting factors (24, 32). maps of amphibian pathogens [e.g., Bd (28, 42, 43)] have been Keeping informed about rapid advances in research and widely used for education and outreach across disciplines, raising monitoring of amphibian diseases is challenging. Further awareness of potential emerging threat factors and informing complicating the challenge of tracking host-pathogen patterns conservation efforts. For example, global Bd maps have appeared of disease threats, anthropogenic processes are linked with in textbooks (44), museum and zoo exhibits (e.g., Panama amphibian disease dynamics. For example, human-mediated exhibit by Smithsonian Institution; US National Zoo exhibit, translocation of amphibian EIDs is an increasing concern, Washington, DC; Fungi and Their Diversity exhibit, Hesse especially for chytridiomycosis, the disease caused by the chytrid Museum, Wiesbaden, Germany), and other multimedia venues fungal pathogens Batrachochytrium dendrobatidis (Bd) and [(45, 46); e.g., ArgoFilms 2009 film for the Public Broadcasting B. salamandrivorans (Bsal). These two pathogens are associated System’s Nature TV show, Frogs: The Thin Green Line]. Third, with amphibian infections across continents and disease-caused knowledge of pathogen occurrences can inform biosecurity mortality resulting in population losses (14, 17–20, 33, 34). procedures to forestall human-mediated translocation (47–49). Amphibian chytridiomycosis research has transitioned In addition, global datasets can enable novel metadata analyses from initial pathogen identification associated with amphibian of specific hypotheses; the global Bd database has contributed to a mortality [Bd (35); Bsal (23)] to understanding pathogen variety of analyses of host-pathogen and disease-threat dynamics occurrences and patterns of amphibian losses as knowledge of [e.g., (50–53)]. However, the initial Bd online database had some host-susceptibility, pathogen strain virulence, and transmission constraints. Occurrences of the disease chytridiomycosis were scenarios has unfolded (15, 17, 19, 24, 33, 34). Several geographic not tracked, as Bd occurrence studies often do not report the origins of Bd have been proposed, spanning Asia, Africa, and development of disease signs in sampled animals. Additionally, North and South America (36–40). A recent genetic analysis we now understand that disease emergence varies with Bd strain reported east Asia to be a Bd biodiversity hotspot, where the (34, 54), and as of this writing, the Bd database has not recorded source of Bd was traced to the Korean Peninsula and one lineage Bd lineages with surveillance data, nor have most published showed the signature of an ancestral population tied to global sources isolated or reported the strain(s) surveyed. Furthermore, emergence in the early twentieth century (34). Scheele et al. the initial Bd database was not set up to report zoospore loads (17) estimated that Bd chytridiomycosis has contributed to for samples—these were not being reported in 2007, and even the declines of 6.5% of amphibian species, and categorized Bd today, not all publications report Bd zoospore loads. Owing to as one of the most destructive invasive species. Lambert et al. continuing requests for the world Bd database, renewed calls for (18) concurred that Bd chytridiomycosis irrefutably harmed comprehensive analyses of world-scale data of amphibian disease amphibians but because their re-analysis could not reproduce threat patterns (18), and significantly increasing reports of Bd the specific results of Scheele et al. (17), they called for a research and surveillance