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Abstract

The rapid worldwide emergence of the amphibian pathogen Batrachochytrium dendrobatidis (Bd) is having a profound negative impact on biodiversity. However, global research efforts are fragmented and an overarching synthesis of global infection data is lacking. Here, we provide results from a community tool for the compilation of worldwide Bd presence and report on the analyses of data collated over a four-year period. Using this online database, we analysed: 1) spatial and taxonomic patterns of infection, including amphibian families that appear over- and under-infected; 2) relationships between Bd occurrence and declining amphibian species, including associations among Bd occurrence, species richness, and enigmatic population declines; and 3) patterns of environmental correlates with Bd, including climate metrics for all species combined and three families (Hylidae, Bufonidae, Ranidae) separately, at both a global scale and regional (U.S.A.) scale. These associations provide new insights for downscaled hypothesis testing. The pathogen has been detected in 52 of 82 countries in which sampling was reported, and it has been detected in 516 of 1240 (42%) amphibian species. We show that detected Bd infections are related to amphibian biodiversity and locations experiencing rapid enigmatic declines, supporting the hypothesis that greater complexity of amphibian communities increases the likelihood of emergence of infection and transmission of Bd. Using a global model including all sampled species, the odds of Bd detection decreased with increasing temperature range at a site. Further consideration of temperature range, rather than maximum or minimum temperatures, may provide new insights into Bd-host ecology. Whereas caution is necessary when interpreting such a broad global dataset, the use of our pathogen database is helping to inform studies of the epidemiology of Bd, as well as enabling regional, national, and international prioritization of conservation efforts. We provide recommendations for adaptive management to enhance the database utility and relevance.

Citation: Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, et al. (2013) Mapping the Global Emergence of Batrachochytrium dendrobatidis, the Amphibian Chytrid Fungus. PLoS ONE 8(2): e56802. doi:10.1371/journal.pone.0056802

Editor: Jason E. Stajich, University of California Riverside, United States of America

Received: September 12, 2012; Accepted: January 16, 2013; Published: February 27, 2013

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Funding: Funds were provided by the UK Natural Environmental Research Council (E006701/1), The ERAnet BIODIVERSA project RACE, The Wellcome Trust (WT08972), and the US Forest Service, Pacific Northwest Research Station. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

¶ Membership of The Bd Mapping Group is provided in the Acknowledgments.

Introduction

The specter of multiple-host infectious diseases leading to the rapid devastation of entire communities is alarming but, so far, rare. However, a handful of highly virulent multi-host pathogens are known, and these have had profound impacts across populations and species (e.g., the rinderpest Morbillivirus; West Nile Virus; bat Geomyces destructans). Rapid aggregation, synthesis, and analysis of disease data are needed to advance both science and management of such diseases. While technological advances have aided our ability to respond to emerging disease, such as by the use of proactive modeling [1], our ability to rapidly detect, assess, and report globally-emerging pathogens has lagged for wild animal diseases that are not zoonotic or are not transmitted to livestock or companion animals. For these diseases, infection and mortality are often cryptic and research studies may take years to be completed before being published.

Herein we report on a community surveillance effort addressing the emergence of the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd). Approximately one-third of global amphibian species have imperiled status, and the emergence of Bd is known to be a proximate driver of amphibian species declines and extinctions [2]–[8]. Bd has an unusually wide host-range: it has been detected infecting hundreds of species. Cascading effects owing to declines of multiple host species as a result of chytridiomycosis could potentially undermine ecosystem stability and function [9], [10], although some studies have not supported key functional roles of amphibians in local ecosystems [11]. Hence, although caution is necessary because amphibians' ecological roles will vary with location, as a worst case scenario, the potential of Bd to act synergistically with other anthropogenic drivers may catastrophically disturb biological communities and substantially contribute to the ongoing 6^th mass extinction event [8].

Although infectious diseases are a normal component of wildlife ecology, only recently are diseases being widely recognized as critical conservation concerns, notably for amphibians [12]. Bd was described as a species in the late 1990s [13], and our basic biological knowledge of this novel pathogen is still accruing. After over a dozen years of research, many aspects of its ecology, epidemiology, and pathogenicity remain uncertain. For example, vectors and pathways of transmission of Bd across spatial scales are little understood, as are the factors affecting species-specific susceptibility to the clinical disease, chytridiomycosis [14], [15], although reservoir amphibian hosts have been identified, including some involved in commercial trade of amphibians [16]–[20]. Bd genotype affects Bd virulence, and population genomics studies have shown that the worldwide emergence of chytridiomycosis has occurred as a consequence of 20^th-century emergence of an aggressive lineage [16]. Concern has heightened about Bd transmission in various arms of the commercial trade in amphibians which annually involves millions of individuals [15], [21]. Transmission pathways may include migratory waterbirds [22], and some regional studies have reported an association of Bd occurrence with amphibian species' proximity to human development, suggesting uncharacterised pathways of introduction and transmission [23]. Bd has been detected in water samples [24], supporting transmission via fomites. Due to the recent recognition of Bd as an emerging infectious disease and an invasive species, Bd was listed as a notifiable disease by the World Organization of Animal Health (OIE) in 2009, resulting in international recommendations to forestall further spread via anthropogenic activities [25]. The need for effective surveillance, including rapid data accrual and interpretation in order to identify emerging patterns and processes, is integral to the progression of both Bd science and management objectives. In particular, our incomplete understanding of the global distribution of Bd is key information that is required to assess the importance of various mechanisms that may have contributed to the rapid emergence of chytridiomycosis [26] or continue to contribute to the ongoing spread of Bd.

We report on the outputs of a multi-phase project for compiling worldwide Bd data and maintaining an updated system for global-scale assessment of the pathogen, the Global Bd Mapping Project [27]. A web-based system (www.Bd-maps.net) for collation of Bd incidence and associated metadata was produced [28], with the aims of providing new insights into both Bd occurrence patterns and the development of hypotheses for the study of Bd ecology and epidemiology, and to inform species- and land-management planning efforts. Using data gleaned from the published literature or submitted as primary data to Bd-maps.net by members of the Bd Mapping Group over a four year period, we report: 1) spatial and taxonomic patterns of infection, including amphibian families that appear over- and under-infected; 2) rela