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Environment is associated with chytrid infection and skin microbiome richness on an amphibian rich island (Taiwan)

  • McCallum, M. L. Vertebrate biodiversity losses point to a sixth mass extinction. Biodivers. Conserv. 24, 2497–2519 (2015).

    Google Scholar 

  • Wake, D. B. & Vredenburg, V. T. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc. Natl. Acad. Sci. 105, 11466–11473. https://doi.org/10.1073/pnas.0801921105 (2008).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Blehert, D. S. et al. Bat white-nose syndrome: An emerging fungal pathogen?. Science 323, 227. https://doi.org/10.1126/science.1163874 (2009).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Pautasso, M., Aas, G., Queloz, V. & Holdenrieder, O. European ash (Fraxinus excelsior) dieback—A conservation biology challenge. Biol. Cons. 158, 37–49 (2013).

    Google Scholar 

  • Daszak, P., Cunningham, A. A. & Hyatt, A. D. Infectious disease and amphibian population declines. Divers. Distrib. 9, 141–150 (2003).

    Google Scholar 

  • Fisher, M. C., Gow, N. A. R. & Gurr, S. J. Tackling emerging fungal threats to animal health, food security and ecosystem resilience. Philos. Trans. R. Soc. B Biol. Sci. https://doi.org/10.1098/rstb.2016.0332 (2016).

    Article 

    Google Scholar 

  • Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Lips, K. R., Reeve, J. D. & Witters, L. R. Ecological traits predicting amphibian population declines in Central America. Conserv. Biol. 17, 1078–1088 (2003).

    Google Scholar 

  • Zipkin, E. F., DiRenzo, G. V., Ray, J. M., Rossman, S. & Lips, K. R. Tropical snake diversity collapses after widespread amphibian loss. Science 367, 814–816. https://doi.org/10.1126/science.aay5733 (2020).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Berger, L. et al. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl. Acad. Sci. 95, 9031–9036 (1998).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Martel, A. et al. Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346, 630–631. https://doi.org/10.1126/science.1258268 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yap, T. A., Koo, M. S., Ambrose, R. F., Wake, D. B. & Vredenburg, V. T. Averting a North American biodiversity crisis. Science 349, 481–482 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Weldon, C., du Preez, L. H., Hyatt, A. D., Muller, R. & Speare, R. Origin of the amphibian chytrid fungus. Emerg. Infect. Dis. 10, 2100–2105 (2004).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Talley, B. L., Muletz, C. R., Vredenburg, V. T., Fleischer, R. C. & Lips, K. R. A century of Batrachochytrium dendrobatidis in Illinois amphibians (1888–1989). Biol. Cons. 182, 254–261 (2015).

    Google Scholar 

  • Rodriguez, D., Becker, C., Pupin, N., Haddad, C. & Zamudio, K. Long-term endemism of two highly divergent lineages of the amphibian-killing fungus in the Atlantic Forest of Brazil. Mol. Ecol. 23, 774–787 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Goka, K. et al. Amphibian chytridiomycosis in Japan: Distribution, haplotypes and possible route of entry into Japan. Mol. Ecol. 18, 4757–4774 (2009).

    CAS 
    PubMed 

    Google Scholar 

  • Bataille, A. et al. Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians. Mol. Ecol. 23, 4196–4209. https://doi.org/10.1111/mec.12385 (2013).

    CAS 
    Article 

    Google Scholar 

  • O’Hanlon, S. J. et al. Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360, 621–627. https://doi.org/10.1126/science.aar1965 (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Swei, A. et al. Is chytridiomycosis an emerging infectious disease in Asia?. PLoS ONE 6, e23179 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bai, C. M., Garner, T. W. J. & Li, Y. M. First evidence of Batrachochytrium dendrobatidis in China: Discovery of chytridiomycosis in introduced American bullfrogs and native amphibians in the Yunnan Province, China. EcoHealth 7, 127–134. https://doi.org/10.1007/s10393-010-0307-0 (2010).

    Article 
    PubMed 

    Google Scholar 

  • Yang, H. et al. First detection of the amphibian chytrid fungus Batrachochytrium dendrobatidis in free-ranging populations of amphibians on mainland Asia: Survey in South Korea. Dis. Aquat. Org. 86, 9–13 (2009).

    Google Scholar 

  • Fong, J. J. et al. Early 1900s detection of Batrachochytrium dendrobatidis in Korean amphibians. PLoS ONE 10, e0115656 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Kusrini, M., Skerratt, L., Garland, S., Berger, L. & Endarwin, W. Chytridiomycosis in frogs of Mount Gede Pangrango, Indonesia. Diseases Aquat. Organ. 82, 187–194 (2008).

    CAS 

    Google Scholar 

  • Laking, A. E., Ngo, H. N., Pasmans, F., Martel, A. & Nguyen, T. T. Batrachochytrium salamandrivorans is the predominant chytrid fungus in Vietnamese salamanders. Sci. Rep. 7, 44443. https://doi.org/10.1038/srep44443 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhu, W. et al. A survey for Batrachochytrium salamandrivorans in Chinese amphibians. Curr. Zool. 60, 729–735 (2014).

    Google Scholar 

  • Beukema, W. et al. Environmental context and differences between native and invasive observed niches of Batrachochytrium salamandrivorans affect invasion risk assessments in the Western Palaearctic. Divers. Distrib. 24, 1788–1801. https://doi.org/10.1111/ddi.12795 (2018).

    Article 

    Google Scholar 

  • Auliya, M. et al. The global amphibian trade flows through Europe: The need for enforcing and improving legislation. Biodivers. Conserv. https://doi.org/10.1007/s10531-016-1193-8 (2016).

    Article 

    Google Scholar 

  • Scheffers, B. R., Edwards, D. P., Diesmos, A., Williams, S. E. & Evans, T. A. Microhabitats reduce animal’s exposure to climate extremes. Glob. Change Biol. 20, 495–503 (2014).

    Google Scholar 

  • Schmeller, D. S. et al. People, pollution and pathogens—Global change impacts in mountain freshwater ecosystems. Sci. Total Environ. 622–623, 756–763. https://doi.org/10.1016/j.scitotenv.2017.12.006 (2018).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Bernardo-Cravo, A., Schmeller, D. S., Chatzinotas, A., Vredenburg, V. T. & Loyau, A. Environmental factors and host microbiomes shape host-pathogen dynamics. Trends Parasitol. 36, 29–36 (2020).

    Google Scholar 

  • Harris, R. N. et al. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J. 3, 818–824. https://doi.org/10.1038/ismej.2009.27 (2009).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Harris, R. N., James, T. Y., Lauer, A., Simon, M. A. & Patel, A. Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth 3, 53–56. https://doi.org/10.1007/s10393-10005-10009-10391 (2006).

    Article 

    Google Scholar 

  • Piovia-Scott, J. et al. Greater species richness of bacterial skin symbionts better suppresses the amphibian fungal pathogen Batrachochytrium dendrobatidis. Microb. Ecol. 74, 217–226 (2017).

    PubMed 

    Google Scholar 

  • Ellison, S., Knapp, R. A., Sparagon, W., Swei, A. & Vredenburg, V. T. Reduced skin bacterial diversity correlates with increased pathogen infection intensity in an endangered amphibian host. Mol. Ecol. 28, 127–140 (2019).

    PubMed 

    Google Scholar 

  • Jani, A. J. & Briggs, C. J. The pathogen Batrachochytrium dendrobatidis disturbs the frog skin microbiome during a natural epidemic and experimental infection. Proc. Natl. Acad. Sci. USA 111, E5049-5058. https://doi.org/10.1073/pnas.1412752111 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kueneman, J. G. et al. The amphibian skin-associated microbiome across species, space and life history stages. Mol. Ecol. 23, 1238–1250 (2014).

    PubMed 

    Google Scholar 

  • Kueneman, J. G. Ecology of the Amphibian Skin-Associated Microbiome and Its Role in Pathogen Defense (University of Colorado at Boulder, 2015).

    Google Scholar 

  • Kueneman, J. G. et al. Community richness of amphibian skin bacteria correlates with bioclimate at the global scale. Nat. Ecol. Evolut. 3, 381–389. https://doi.org/10.1038/s41559-019-0798-1 (2019).

    Article 

    Google Scholar 

  • Jiménez, R. R. & Sommer, S. The amphibian microbiome: Natural range of variation, pathogenic dysbiosis, and role in conservation. Biodivers. Conserv. 26, 763–786. https://doi.org/10.1007/s10531-016-1272-x (2017).

    Article 

    Google Scholar 

  • Walke, J. B. et al. Amphibian skin may select for rare environmental microbes. ISME J 8, 2207–2217. https://doi.org/10.1038/ismej.2014.77 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • McKenzie, V. J., Bowers, R. M., Fierer, N., Knight, R. & Lauber, C. L. Co-habiting amphibian species harbor unique skin bacterial communities in wild populations. ISME J 6, 588–596. https://doi.org/10.1038/ismej.2011.129 (2012).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Bates, K. A. et al. Amphibian chytridiomycosis outbreak dynamics are linked with host skin bacterial community structure. Nat. Commun. 9, 693. https://doi.org/10.1038/s41467-018-02967-w (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ellison, S. et al. The influence of habitat and phylogeny on the skin microbiome of amphibians in Guatemala and Mexico. Microb. Ecol. 78, 257–267 (2019).

    PubMed 

    Google Scholar 

  • Fisher, M. C., Pasmans, F. & Martel, A. Virulence and pathogenicity of chytrid fungi causing amphibian extinctions. Annu. Rev. Microbiol. https://doi.org/10.1146/annurev-micro-052621-124212 (2021).

    Article 
    PubMed 

    Google Scholar 

  • Haver, M. et al. The role of abiotic variables in an emerging global amphibian fungal disease in mountains. Sci. Total Environ. 815, 152735 (2021).

    PubMed 

    Google Scholar 

  • Turner, A., Wassens, S., Heard, G. & Peters, A. Temperature as a driver of the pathogenicity and virulence of amphibian chytrid fungus Batrachochytrium dendrobatidis: A systematic review. J. Wildl. Dis. 57, 477–494 (2021).

    PubMed 

    Google Scholar 

  • Woodhams, D., Alford, R., Briggs, C., Johnson, M. & Rollins-Smith, L. Life history trade-offs influence disease in changing climates: Strategies of an amphibian pathogen. Ecology 89, 1627–1639 (2008).

    PubMed 

    Google Scholar 

  • Sonn, J. M., Berman, S. & Richards-Zawacki, C. L. The influence of temperature on chytridiomycosis in vivo. EcoHealth 14, 762–770. https://doi.org/10.1007/s10393-017-1269-2 (2017).

    Article 
    PubMed 

    Google Scholar 

  • Schmidt, B., Küpfer, E., Geiger, C., Wolf, S. & Schär, S. Elevated temperature clears chytrid fungus infections from tadpoles of the midwife toad, Alytes obstetricans. Amphibia-Reptilia 32, 276–280 (2011).

    Google Scholar 

  • Bielby, J., Cooper, N., Cunningham, A. A., Garner, T. W. J. & Purvis, A. Predicting susceptibility to future declines in the world’s frogs. Conserv. Lett. 1, 82–90 (2008).

    Google Scholar 

  • Gray, M. J., Miller, D. L. & Hoverman, J. T. Ecology and pathology of amphibian ranaviruses. Dis. Aquat. Org. 87, 243–266 (2009).

    Google Scholar 

  • Murray, K., Skerratt, L., Speare, R. & McCallum, H. Impact and dynamics of disease in species threatened by the amphibian chytrid fungus, Batrachochytrium dendrobatidis. Conserv. Biol. 23, 1242–1252 (2009).

    PubMed 

    Google Scholar 

  • Schmeller, D. S. et al. Microscopic aquatic predators strongly affect infection dynamics of a globally emerged pathogen. Curr. Biol. 24, 176–180. https://doi.org/10.1016/j.cub.2013.11.032 (2014).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Metzger, M. J. et al. Environmental stratifications as the basis for national, European and global ecological monitoring. Ecol. Ind. 33, 26–35. https://doi.org/10.1016/j.ecolind.2012.11.009 (2013).

    Article 

    Google Scholar 

  • Metzger, M. J. et al. A high-resolution bioclimate map of the world: A unifying framework for global biodiversity research and monitoring. Glob. Ecol. Biogeogr. 22, 630–638. https://doi.org/10.1111/geb.12022 (2013).

    Article 

    Google Scholar 

  • Clare, F., Daniel, O., Garner, T. & Fisher, M. Assessing the ability of swab data to determine the true burden of infection for the amphibian pathogen Batrachochytrium dendrobatidis. EcoHealth 13, 360–367. https://doi.org/10.1007/s10393-016-1114-z (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cheng, T. L., Rovito, S. M., Wake, D. B. & Vredenburg, V. T. Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proc. Natl. Acad. Sci. 108, 9502–9507 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Vredenburg, V. T. et al. Pathogen invasion history elucidates contemporary host pathogen dynamics. PLoS ONE 14, e0219981. https://doi.org/10.1371/journal.pone.0219981 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hyatt, A. D. et al. Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Dis. Aquat. Org. 73, 175–192 (2007).

    CAS 

    Google Scholar 

  • Blooi, M. et al. Duplex real-time PCR for rapid simultaneous detection of Batrachochytrium dendrobatidis and B. salamandrivorans in amphibian samples. J. Clin. Microbiol. 51, 4173–4177 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Boyle, D. G., Boyle, D. B., Olsen, V., Morgan, J. A. T. & Hyatt, A. D. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis. Aquat. Org. 60, 141–148 (2004).

    CAS 

    Google Scholar 

  • Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10–12 (2011).

    Google Scholar 

  • Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pruesse, E., Peplies, J. & Glöckner, F. O. SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823–1829 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2012).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Bokulich, N. A. & Mills, D. A. Improved selection of internal transcribed spacer-specific primers enables quantitative, ultra-high-throughput profiling of fungal communities. Appl. Environ. Microbiol. https://doi.org/10.1128/aem.03870-12 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • McMurdie, P. J. & Holmes, S. Waste not, want not: Why rarefying microbiome data is inadmissible. PLoS Comput. Biol. 10, e1003531 (2014).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Abatzoglou, J. T., Dobrowski, S. Z., Parks, S. A. & Hegewisch, K. C. TerraClimate, a high-resolution global dataset of monthly climate and climatic water balance from 1958–2015. Sci. Data 5, 170191. https://doi.org/10.1038/sdata.2017.191 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wells, N., Goddard, S. & Hayes, M. J. A self-calibrating Palmer Drought Severity Index. J. Clim. 17, 2335–2351 (2004).

    Google Scholar 

  • Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60. https://doi.org/10.1186/gb-2011-12-6-r60 (2011).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fisher, M. C. et al. RACE: Risk assessment of chytridiomycosis to European Amphibian Biodiversity. Froglog 101, 45–47 (2012).

    Google Scholar 

  • Carcass detection and consumption by facultative scavengers in forest ecosystem highlights the value of their ecosystem services

    Spatial distribution characteristics and evaluation of soil pollution in coal mine areas in Loess Plateau of northern Shaanxi