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      Seasonal Pattern of Batrachochytrium dendrobatidis Infection and Mortality in Lithobates areolatus: Affirmation of Vredenburg's “10,000 Zoospore Rule”

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          Abstract

          To fully comprehend chytridiomycosis, the amphibian disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), it is essential to understand how Bd affects amphibians throughout their remarkable range of life histories. Crawfish Frogs ( Lithobates areolatus) are a typical North American pond-breeding species that forms explosive spring breeding aggregations in seasonal and semipermanent wetlands. But unlike most species, when not breeding Crawfish Frogs usually live singly—in nearly total isolation from conspecifics—and obligately in burrows dug by crayfish. Crayfish burrows penetrate the water table, and therefore offer Crawfish Frogs a second, permanent aquatic habitat when not breeding. Over the course of two years we sampled for the presence of Bd in Crawfish Frog adults. Sampling was conducted seasonally, as animals moved from post-winter emergence through breeding migrations, then back into upland burrow habitats. During our study, 53% of Crawfish Frog breeding adults tested positive for Bd in at least one sample; 27% entered breeding wetlands Bd positive; 46% exited wetlands Bd positive. Five emigrating Crawfish Frogs (12%) developed chytridiomycosis and died. In contrast, all 25 adult frogs sampled while occupying upland crayfish burrows during the summer tested Bd negative. One percent of postmetamorphic juveniles sampled were Bd positive. Zoospore equivalents/swab ranged from 0.8 to 24,436; five out of eight frogs with zoospore equivalents near or >10,000 are known to have died. In summary, Bd infection rates in Crawfish Frog populations ratchet up from near zero during the summer to over 25% following overwintering; rates then nearly double again during and just after breeding—when mortality occurs—before the infection wanes during the summer. Bd-negative postmetamorphic juveniles may not be exposed again to this pathogen until they take up residence in crayfish burrows, or until their first breeding, some years later.

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          Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America.

          Epidermal changes caused by a chytridiomycete fungus (Chytridiomycota; Chytridiales) were found in sick and dead adult anurans collected from montane rain forests in Queensland (Australia) and Panama during mass mortality events associated with significant population declines. We also have found this new disease associated with morbidity and mortality in wild and captive anurans from additional locations in Australia and Central America. This is the first report of parasitism of a vertebrate by a member of the phylum Chytridiomycota. Experimental data support the conclusion that cutaneous chytridiomycosis is a fatal disease of anurans, and we hypothesize that it is the proximate cause of these recent amphibian declines.
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            Colloquium paper: are we in the midst of the sixth mass extinction? A view from the world of amphibians.

            Many scientists argue that we are either entering or in the midst of the sixth great mass extinction. Intense human pressure, both direct and indirect, is having profound effects on natural environments. The amphibians--frogs, salamanders, and caecilians--may be the only major group currently at risk globally. A detailed worldwide assessment and subsequent updates show that one-third or more of the 6,300 species are threatened with extinction. This trend is likely to accelerate because most amphibians occur in the tropics and have small geographic ranges that make them susceptible to extinction. The increasing pressure from habitat destruction and climate change is likely to have major impacts on narrowly adapted and distributed species. We show that salamanders on tropical mountains are particularly at risk. A new and significant threat to amphibians is a virulent, emerging infectious disease, chytridiomycosis, which appears to be globally distributed, and its effects may be exacerbated by global warming. This disease, which is caused by a fungal pathogen and implicated in serious declines and extinctions of >200 species of amphibians, poses the greatest threat to biodiversity of any known disease. Our data for frogs in the Sierra Nevada of California show that the fungus is having a devastating impact on native species, already weakened by the effects of pollution and introduced predators. A general message from amphibians is that we may have little time to stave off a potential mass extinction.
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              Spread of Chytridiomycosis Has Caused the Rapid Global Decline and Extinction of Frogs

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                10 March 2011
                : 6
                : 3
                : e16708
                Affiliations
                [1 ]Department of Biology, Indiana State University, Terre Haute, Indiana, United States of America
                [2 ]Wildlife Disease Laboratories, San Diego Zoo Institute for Conservation Research, San Diego, California, United States of America
                [3 ]Terre Haute Center for Medical Education, Indiana University School of Medicine, Terre Haute, Indiana, United States of America
                University of Minnesota, United States of America
                Author notes

                Conceived and designed the experiments: MJL VK JH AP. Performed the experiments: MJL VK JH AP. Analyzed the data: MJL VK JH AP. Contributed reagents/materials/analysis tools: MJL AP. Wrote the paper: MJL VK JH AP.

                Article
                PONE-D-10-05494
                10.1371/journal.pone.0016708
                3053364
                21423745
                d8a7c0e1-f202-4248-b3a5-8af95aaa5dbf
                Kinney 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
                : 24 November 2010
                : 12 January 2011
                Page count
                Pages: 10
                Categories
                Research Article
                Biology
                Ecology
                Community Ecology
                Ecological Risk
                Ecological Environments
                Aquatic Environments
                Freshwater Environments
                Terrestrial Environments
                Ecological Metrics
                Population Size
                Biodiversity
                Conservation Science
                Ecophysiology
                Freshwater Ecology
                Global Change Ecology
                Species Extinction
                Immunology
                Immunity
                Inflammation
                Immune Response
                Microbiology
                Mycology
                Fungi
                Applied Microbiology
                Emerging Infectious Diseases
                Host-Pathogen Interaction

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                Uncategorized

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