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      Introduced bullfrog facilitates pathogen invasion in the western United States

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          Abstract

          Batrachochytrium dendrobatidis ( Bd), a causal agent of the amphibian fungal skin disease chytridiomycosis, has been implicated in the decline and extinction of over 200 species worldwide since the 1970s. Despite almost two decades of research, the history of Bd and its global spread is not well understood. However, the spread of the Global Panzootic Lineage of Bd ( Bd-GPL), the lineage associated with amphibian die-offs, has been linked with the American bullfrog ( Rana [ Aqurana] catesbeiana) and global trade. Interestingly, R. catesbeiana is native to the eastern U.S., where no Bd-related declines have been observed despite Bd’s presence since the late 1800s. In contrast Bd has been found to have emerged in California and Mexico in the 1960s and 1970s, after which epizootics ( i. e., epidemics in wildlife) ensued. We hypothesize that Bd-GPL spread from the eastern U.S. with the introduction of R. catesbeiana into the western US, resulting in epizootics and declines of native host species. Using museum records, we investigated the historical relationship between R. catesbeiana and Bd invasion in the western US and found that R. catesbeiana arrived in the same year or prior to Bd in most western watersheds that had data for both species, suggesting that Bd-GPL may have originated in the eastern US and R. catesbeiana may have facilitated Bd invasion in the western US. To predict areas with greatest suitability for Bd, we created a suitability model by integrating habitat suitability and host availability. When we incorporated invasion history with high Bd suitability, we found that watersheds with non-native R. catesbeiana in the mountain ranges of the West Coast have the highest disease risk. These findings shed light on the invasion history and disease dynamics of Bd in North America. Targeted historical surveys using archived specimens in natural history collections and present-day field surveys along with more localized, community-level studies, monitoring, and surveillance are needed to further test this hypothesis and grow our understanding of the disease ecology and host-pathogen dynamics of Bd.

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          Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community.

          Pathogens rarely cause extinctions of host species, and there are few examples of a pathogen changing species richness and diversity of an ecological community by causing local extinctions across a wide range of species. We report the link between the rapid appearance of a pathogenic chytrid fungus Batrachochytrium dendrobatidis in an amphibian community at El Copé, Panama, and subsequent mass mortality and loss of amphibian biodiversity across eight families of frogs and salamanders. We describe an outbreak of chytridiomycosis in Panama and argue that this infectious disease has played an important role in amphibian population declines. The high virulence and large number of potential hosts of this emerging infectious disease threaten global amphibian diversity.
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            Spread of Chytridiomycosis Has Caused the Rapid Global Decline and Extinction of Frogs

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              Spatial filtering to reduce sampling bias can improve the performance of ecological niche models

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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: ResourcesRole: SoftwareRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                16 April 2018
                2018
                : 13
                : 4
                : e0188384
                Affiliations
                [1 ] Institute of the Environment and Sustainability, University of California, Los Angeles, California, United States of America
                [2 ] Museum of Vertebrate Zoology, University of California, Berkeley, California, United States of America
                [3 ] Department of Biology, San Francisco State University, San Francisco, California, United States of America
                [4 ] Department of Environmental Health Sciences, University of California, Los Angeles, California, United States of America
                Imperial College Faculty of Medicine, UNITED KINGDOM
                Author notes

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

                Author information
                http://orcid.org/0000-0002-1704-2720
                Article
                PONE-D-17-04085
                10.1371/journal.pone.0188384
                5901863
                29659568
                5e29fcf0-d590-4642-8b28-572920e611bc
                © 2018 Yap et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 31 January 2017
                : 6 November 2017
                Page count
                Figures: 2, Tables: 0, Pages: 13
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 1258133
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 1633948
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 1441652
                Award Recipient :
                This work was supported by National Science Foundation 1258133, 1633948 (V.T.V.), and 1441652 (M.S.K.).
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amphibians
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Fungal Pathogens
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Fungal Pathogens
                Biology and Life Sciences
                Mycology
                Fungal Pathogens
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Evolutionary Emergence
                Ecology and Environmental Sciences
                Species Colonization
                Invasive Species
                Biology and Life Sciences
                Zoology
                Animal Diseases
                Epizootics
                People and places
                Geographical locations
                North America
                People and places
                Geographical locations
                North America
                United States
                Custom metadata
                Data are available from the amphibian disease portal ( amphibiandisease.org) at https://n2t.net/ark:/21547/AxB2. All other relevant data are within the paper and its Supporting Information files.

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