Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Chytrid fungi and global amphibian declines

Abstract

Discovering that chytrid fungi cause chytridiomycosis in amphibians represented a paradigm shift in our understanding of how emerging infectious diseases contribute to global patterns of biodiversity loss. In this Review we describe how the use of multidisciplinary biological approaches has been essential to pinpointing the origins of amphibian-parasitizing chytrid fungi, including Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans, as well as to timing their emergence, tracking their cycles of expansion and identifying the core mechanisms that underpin their pathogenicity. We discuss the development of the experimental methods and bioinformatics toolkits that have provided a fuller understanding of batrachochytrid biology and informed policy and control measures.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Fig. 1: Global distribution of Batrachochytrium.
Fig. 2: Global spread of Batrachochytrium dendrobatidis and the amphibian trade.
Fig. 3: Factors influencing the virulence of batrachochytrids.
Fig. 4: Pathogenic potential of batrachochytrids.

References

  1. 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. USA 95, 9031–9036 (1998). First study detailing the discovery of amphibian chytridiomycosis and linking chytrid fungi to amphibian declines.

    CAS  PubMed  Google Scholar 

  2. Longcore, J. E., Pessier, A. P. & Nichols, D. K. Batrachochytrium dendrobatidis gen et sp nov, a chytrid pathogenic to amphibians. Mycologia 91, 219–227 (1999). Naming of Batrachochytrium dendrobatidis and description of its lifecycle.

    Google Scholar 

  3. Fisher, M. C., Garner, T. W. J. & Walker, S. F. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu. Rev. Microbiol. 63, 291–310 (2009).

    CAS  PubMed  Google Scholar 

  4. Scheele, B. et al. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363, 1459–1463 (2019). Analysis of the temporal emergence of chytridiomycosis and the numbers of amphibian species affected.

    CAS  PubMed  Google Scholar 

  5. Martel, A. et al. Batrachochytrium salamandrivorans sp nov causes lethal chytridiomycosis in amphibians. Proc. Natl Acad. Sci. USA 110, 15325–15329 (2013). Discovery of Batrachochytrium salamandrivorans and description of its lifecycle.

    CAS  PubMed  Google Scholar 

  6. Houlahan, J. E., Findlay, C. S., Schmidt, B. R., Meyer, A. H. & Kuzmin, S. L. Quantitative evidence for global amphibian population declines. Nature 404, 752–755 (2000).

    CAS  PubMed  Google Scholar 

  7. Berger, L., Hyatt, A. D., Speare, R. & Longcore, J. E. Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Dis. Aquat. Organ. 68, 51–63 (2005).

    PubMed  Google Scholar 

  8. 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. Organ. 60, 141–148 (2004).

    CAS  PubMed  Google Scholar 

  9. Olson, D. H. & Ronnenberg, K. L. Global Bd Mapping Project: 2014 update. FrogLog 22, 17–21 (2014).

    Google Scholar 

  10. Stegen, G. et al. Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans. Nature 544, 353–356 (2017).

    CAS  PubMed  Google Scholar 

  11. Martel, A. et al. Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346, 630–631 (2014). Discovery of the Southeast Asian origins of B. salamandrivorans and its restricted host range.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 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 (2017).

    PubMed  PubMed Central  Google Scholar 

  13. Lips, K. R. et al. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc. Natl Acad. Sci. USA 103, 3165–3170 (2006).

    CAS  PubMed  Google Scholar 

  14. Carvalho, T., Becker, C. G. & Toledo, L. F. Historical amphibian declines and extinctions in Brazil linked to chytridiomycosis. Proc. Biol. Sci. 284, 20162254 (2017).

    PubMed  PubMed Central  Google Scholar 

  15. Weldon, C., Channing, A., Misinzo, G. & Cunningham, A. A. Disease driven extinction in the wild of the Kihansi spray toad (Nectophrynoides asperginis). Preprint at https://doi.org/10.1101/677971 (2019).

  16. Yong, E. The Worst Disease Ever Recorded. The Atlantic https://www.theatlantic.com/science/archive/2019/03/bd-frogs-apocalypse-disease/585862/ (2019).

  17. Boyle, D. G. et al. Cryo-archiving of Batrachochytrium dendrobatidis and other chytridiomycetes. Dis. Aquat. Organ. 56, 59–64 (2003).

    CAS  PubMed  Google Scholar 

  18. Fisher, M. C. et al. Development and worldwide use of non-lethal, and minimal population-level impact, protocols for the isolation of amphibian chytrid fungi. Sci. Rep. 8, 7772 (2018).

    PubMed  PubMed Central  Google Scholar 

  19. Aanensen, D. M., Huntley, D. M., Feil, E. J., al-Own, F. & Spratt, B. G. EpiCollect: linking smartphones to web applications for epidemiology, ecology and community data collection. PLoS One 4, e6968 (2009).

    PubMed  PubMed Central  Google Scholar 

  20. Skerratt, L. F. et al. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth 4, 125–134 (2007).

    Google Scholar 

  21. Morehouse, E. A. et al. Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone. Mol. Ecol. 12, 395–403 (2003).

    CAS  PubMed  Google Scholar 

  22. James, T. Y. et al. Rapid expansion of an emerging fungal disease into declining and healthy amphibian populations. PLoS Pathog. 5, e1000458 (2009).

    PubMed  PubMed Central  Google Scholar 

  23. Hudson, M. A. et al. Dynamics and genetics of a disease-driven species decline to near extinction: lessons for conservation. Sci. Rep. 6, 30772 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Joneson, S., Stajich, J. E., Shiu, S. H. & Rosenblum, E. B. Genomic transition to pathogenicity in chytrid fungi. PLoS Pathog. 7, e1002338 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Farrer, R. A. et al. Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc. Natl Acad. Sci. USA 108, 18732–18736 (2011). First use of population genomics to describe patterns of B. dendrobatidis diversity and its timescale of emergence.

    CAS  PubMed  Google Scholar 

  26. Farrer, R. A. et al. Chromosomal copy number variation, selection and uneven rates of recombination reveal cryptic genome diversity linked to pathogenicity. PLoS Genet. 9, e1003703 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Rosenblum, E. B. et al. Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proc. Natl Acad. Sci. USA 110, 9385–9390 (2013).

    CAS  PubMed  Google Scholar 

  28. 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 

  29. 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 

  30. 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. 22, 4196–4209 (2013).

    CAS  PubMed  Google Scholar 

  31. Rodriguez, D., Becker, C. G., Pupin, N. C., Haddad, C. F. B. & Zamudio, K. R. 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 

  32. 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. Conserv. 182, 254–261 (2015).

    Google Scholar 

  33. O’Hanlon, S. J. et al. Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360, 621–627 (2018). Discovery of the East Asian origins of B. dendrobatidis using population genomics.

    PubMed  PubMed Central  Google Scholar 

  34. Tajima, F. Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Olson, D. H. et al. Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS One 8, e56802 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Byrne, A. Q. et al. Cryptic diversity of a widespread global pathogen reveals expanded threats to amphibian conservation. Proc. Natl Acad. Sci. USA 116, 20382–20387 (2019).

    CAS  PubMed  Google Scholar 

  39. Fu, M. J. & Waldman, B. Ancestral chytrid pathogen remains hypervirulent following its long coevolution with amphibian hosts. Proc. Biol. Sci. 286, 20190833 (2019).

    CAS  PubMed  Google Scholar 

  40. Lips, K. R., Diffendorfer, J., Mendelson, J. R. & Sears, M. W. Riding the wave: Reconciling the roles of disease and climate change in amphibian declines. PLoS Biol. 6, 441–454 (2008).

    CAS  Google Scholar 

  41. Murray, K. et al. The distribution and host range of the pandemic disease chytridiomycosis in Australia, spanning surveys from 1956–2007. Ecology 91, 1557–1558 (2010).

    Google Scholar 

  42. Laurance, W. F., McDonald, K. R. & Speare, R. Australian rain forest frogs: support for the epidemic disease hypothesis. Conserv. Biol. 10, 406–413 (1996).

    Google Scholar 

  43. Lips, K. R. Overview of chytrid emergence and impacts on amphibians. Philos. Trans. R. Soc. Lond. B Biol. Sci. 286, 20190833 (2016).

    Google Scholar 

  44. Fisher, M. C. & Garner, T. W. J. The relationship between the introduction of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal Biol. Rev. 21, 2–9 (2007).

    Google Scholar 

  45. Walker, S. F. et al. Invasive pathogens threaten species recovery programs. Curr. Biol. 18, R853–R854 (2008). Detection of long-distance transfer and introduction of African BdCAPE to Alytes muletensis on the Balearic island of Mallorca.

    CAS  PubMed  Google Scholar 

  46. Valenzuela-Sanchez, A. et al. Genomic epidemiology of the emerging pathogen Batrachochytrium dendrobatidis from native and invasive amphibian species in Chile. Transbound. Emerg. Dis. 65, 309–314 (2018).

    CAS  PubMed  Google Scholar 

  47. Jenkinson, T. S. et al. Amphibian-killing chytrid in Brazil comprises both locally endemic and globally expanding populations. Mol. Ecol. 25, 2978–2996 (2016).

    CAS  PubMed  Google Scholar 

  48. Schloegel, L. M. et al. Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Mol. Ecol. 21, 5162–5177 (2012).

    PubMed  Google Scholar 

  49. Greenspan, S. E. et al. Hybrids of amphibian chytrid show high virulence in native hosts. Sci. Rep. 8, 9600 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Doherty-Bone, T. et al. Amphibian chytrid fungus in Africa—realigning hypotheses and the research paradigm. Anim. Conserv. https://doi.org/10.1111/acv.12538 (2019).

  51. Soto-Azat, C., Clarke, B. T., Poynton, J. C. & Cunningham, A. A. Widespread historical presence of Batrachochytrium dendrobatidis in African pipid frogs. Divers. Distrib. 16, 126–131 (2010).

    Google Scholar 

  52. Vredenburg, V. T. et al. Prevalence of Batrachochytrium dendrobatidis in Xenopus collected in Africa (1871–2000) and in California (2001–2010). PLoS One https://doi.org/10.1371/journal.pone.0063791 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Seimon, T. A. et al. Assessing the threat of amphibian chytrid fungus in the Albertine Rift: past, present and future. PLoS One https://doi.org/10.1371/journal.pone.0145841 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Hydeman, M. E. et al. Prevalence and genetic diversity of Batrachochytrium dendrobatidis in Central African island and continental amphibian communities. Ecol. Evol. 7, 7729–7738 (2017).

    PubMed  PubMed Central  Google Scholar 

  55. Bletz, M. C. et al. Widespread presence of the pathogenic fungus Batrachochytrium dendrobatidis in wild amphibian communities in Madagascar. Sci. Rep. 5, 8633 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Kolby, J. E. & Skerratt, L. F. Amphibian chytrid fungus in Madagascar neither shows widespread presence nor signs of certain establishment. PLoS One https://doi.org/10.1371/journal.pone.0139172 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Hirschfeld, M. et al. Dramatic declines of montane frogs in a central African biodiversity hotspot. PLoS One 11, e0155129 (2016).

    PubMed  PubMed Central  Google Scholar 

  58. Griffiths, S. M. et al. Genetic variability and ontogeny predict microbiome structure in a disease-challenged montane amphibian. ISME J. 12, 2506–2517 (2018).

    PubMed  PubMed Central  Google Scholar 

  59. Gower, D. J. et al. Batrachochytrium dendrobatidis Infection and lethal chytridiomycosis in caecilian amphibians (Gymnophiona). Ecohealth 10, 173–183 (2013).

    PubMed  Google Scholar 

  60. Morgan, J. A. T. et al. Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. Proc. Natl Acad. Sci. USA 104, 13845–13850 (2007).

    CAS  PubMed  Google Scholar 

  61. van de Vossenberg, B. T. L. H. et al. Comparative genomics of chytrid fungi reveal insights into the obligate biotrophic and pathogenic lifestyle of Synchytrium endobioticum. Sci. Rep. 9, 8672 (2019).

    PubMed  PubMed Central  Google Scholar 

  62. James, T. Y. et al. Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research. Ecol. Evol. 5, 4079–4097 (2015).

    PubMed  PubMed Central  Google Scholar 

  63. de Roode, J. C. et al. Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad. Sci. USA 102, 7624–7628 (2005).

    PubMed  Google Scholar 

  64. Karvonen, A., Rellstab, C., Louhi, K. R. & Jokela, J. Synchronous attack is advantageous: mixed genotype infections lead to higher infection success in trematode parasites. Proc. Biol. Sci. 279, 171–176 (2012).

    PubMed  Google Scholar 

  65. Ghosh, P. The Ecology of Chytrid Lineages in Southern Africa. PhD thesis, Imperial College London (2019).

  66. Farrer, R. A. et al. Genomic innovations linked to infection strategies across emerging pathogenic chytrid fungi. Nat. Commun. 8, 14742 (2017). Comparative and functional genomic description of batrachochytrid virulence.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Farrer, R. A. & Fisher, M. C. Describing genomic and epigenomic traits underpinning emerging fungal pathogens. Adv. Genet. 100, 73–140 (2017).

    PubMed  Google Scholar 

  68. Abramyan, J. & Stajich, J. E. Species-specific chitin-binding module 18 expansion in the amphibian pathogen Batrachochytrium dendrobatidis. mBio. 3, e00150-12 (2012).

    PubMed  PubMed Central  Google Scholar 

  69. Van Rooij, P. et al. Development of in vitro models for a better understanding of the early pathogenesis of Batrachochytrium dendrobatidis infections in amphibians. Altern. Lab. Anim. 38, 519–528 (2010). First description of a skin explant model of chytridiomycosis.

    PubMed  Google Scholar 

  70. Liew, N. et al. Chytrid fungus infection in zebrafish demonstrates that the pathogen can parasitize non-amphibian vertebrate hosts. Nat. Commun. 8, 15048 (2017). First description of a non-amphibian vertebrate model of chytridiomycosis.

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Voyles, J. Phenotypic profiling of Batrachochytrium dendrobatidis, a lethal fungal pathogen of amphibians. Fungal Ecol. 4, 196–200 (2011).

    Google Scholar 

  72. Fisher, M. C. et al. Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Mol. Ecol. 18, 415–429 (2009).

    CAS  PubMed  Google Scholar 

  73. Langhammer, P. F. et al. A fungal pathogen of amphibians, Batrachochytrium dendrobatidis, attenuates in pathogenicity with in vitro passages. PLoS One https://doi.org/10.1371/journal.pone.0077630 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Voyles, J. et al. Experimental evolution alters the rate and temporal pattern of population growth in Batrachochytrium dendrobatidis, a lethal fungal pathogen of amphibians. Ecol. Evol. 4, 3633–3641 (2014).

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  76. Refsnider, J. M., Poorten, T. J., Langhammer, P. F., Burrowes, P. A. & Rosenblum, E. B. Genomic correlates of virulence attenuation in the deadly amphibian chytrid fungus, Batrachochytrium dendrobatidis. G3 5, 2291–2298 (2015).

    CAS  PubMed  Google Scholar 

  77. Kriger, K. M. & Hero, J. M. Altitudinal distribution of chytrid (Batrachochytrium dendrobatidis) infection in subtropical Australian frogs. Austral Ecol. 33, 1022–1032 (2008).

    Google Scholar 

  78. Kriger, K. M., Pereoglou, F. & Hero, J. M. Latitudinal variation in the prevalence and intensity of chytrid (Batrachochytrium dendrobatidis) infection in Eastern Australia. Conserv. Biol. 21, 1280–1290 (2007).

    PubMed  Google Scholar 

  79. Kriger, K. M. & Hero, J. M. Large-scale seasonal variation in the prevalence and severity of chytridiomycosis. J. Zool. 271, 352–359 (2007).

    Google Scholar 

  80. Clare, F. C. et al. Climate forcing of an emerging pathogenic fungus across a montane multi-host community. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 20150454 (2016).

    PubMed  PubMed Central  Google Scholar 

  81. Garner, T. W. J., Rowcliffe, J. M. & Fisher, M. C. Climate change, chytridiomycosis or condition: an experimental test of amphibian survival. Glob. Change Biol. 17, 667–675 (2011).

    Google Scholar 

  82. Raffel, T. R., Halstead, N. T., McMahon, T. A., Davis, A. K. & Rohr, J. R. Temperature variability and moisture synergistically interact to exacerbate an epizootic disease. Proc. Biol. Sci. 282, 20142039 (2015).

    PubMed  PubMed Central  Google Scholar 

  83. Ortiz-Santaliestra, M. E., Fisher, M. C., Fernandez-Beaskoetxea, S., Fernandez-Beneitez, M. J. & Bosch, J. Ambient ultraviolet B radiation and prevalence of infection by Batrachochytrium dendrobatidis in two amphibian species. Conserv. Biol. 25, 975–982 (2011).

    PubMed  Google Scholar 

  84. Walker, S. F. et al. Factors driving pathogenicity vs. prevalence of amphibian panzootic chytridiomycosis in Iberia. Ecol. Lett. 13, 372–382 (2010).

    PubMed  Google Scholar 

  85. Rohr, J. R. et al. Early-life exposure to a herbicide has enduring effects on pathogen-induced mortality. Proc. Biol. Sci. 280, 20131502 (2014).

    Google Scholar 

  86. Briggs, C. J., Knapp, R. A. & Vredenburg, V. T. Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proc. Natl Acad. Sci. USA 107, 9695–9700 (2010). Development of a mathematical epidemiological framework for analysing host/pathogen dynamics.

    CAS  PubMed  Google Scholar 

  87. Garner, T. W. J. et al. Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118, 783–791 (2009).

    Google Scholar 

  88. Ribas, L. et al. Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis. PLoS One 4, e8408 (2009).

    PubMed  PubMed Central  Google Scholar 

  89. Daversa, D. R., Manica, A., Bosch, J., Jolles, J. W. & Garner, T. W. J. Routine habitat switching alters the likelihood and persistence of infection with a pathogenic parasite. Funct. Ecol. 32, 1262–1270 (2018).

    Google Scholar 

  90. Clulow, S. et al. Elevated salinity blocks pathogen transmission and improves host survival from the global amphibian chytrid pandemic: implications for translocations. J. Appl. Ecol. 55, 830–840 (2018).

    CAS  Google Scholar 

  91. Vredenburg, V. T., Knapp, R. A., Tunstall, T. S. & Briggs, C. J. Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc. Natl Acad. Sci. USA 107, 9689–9694 (2010). Epidemiology of the spread of B. dendrobatidis in the North American Sierra Nevada and mountain yellow-legged frogs.

    CAS  PubMed  Google Scholar 

  92. 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 (2016).

    PubMed  PubMed Central  Google Scholar 

  93. Schmeller, D. S. et al. Microscopic aquatic predators strongly affect infection dynamics of a globally emerged pathogen. Curr. Biol. 24, 176–180 (2014). Determination that aquatic fauna can predate and limit B. dendrobatidis infectious stages.

    CAS  PubMed  Google Scholar 

  94. Rohr, J. R., Raffel, T. R., Romansic, J. M., McCallum, H. & Hudson, P. J. Evaluating the links between climate, disease spread, and amphibian declines. Proc. Natl Acad. Sci. USA 105, 17436–17441 (2008).

    CAS  PubMed  Google Scholar 

  95. Pounds, A. J. et al. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439, 161–167 (2006).

    CAS  PubMed  Google Scholar 

  96. Rohr, J. R. & Raffel, T. R. Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proc. Natl Acad. Sci. USA 107, 8269–8274 (2010).

    CAS  PubMed  Google Scholar 

  97. Rachowicz, L. J. & Briggs, C. J. Quantifying the disease transmission function: effects of density on Batrachochytrium dendrobatidis transmission in the mountain yellow-legged frog Rana muscosa. J. Anim. Ecol. 76, 711–721 (2007).

    PubMed  Google Scholar 

  98. Balaz, V. et al. Assessing risk and guidance on monitoring of Batrachochytrium dendrobatidis in Europe through identification of taxonomic selectivity of infection. Conserv. Biol. 28, 213–223 (2014).

    PubMed  Google Scholar 

  99. Bosch, J., Fernandez-Beaskoetxea, S., Garner, T. W. J. & Carrascal, L. M. Long-term monitoring of an amphibian community after a climate change- and infectious disease-driven species extirpation. Glob. Change Biol. 24, 2622–2632 (2018).

    Google Scholar 

  100. Grogan, L. F. et al. Review of the amphibian immune response to chytridiomycosis, and future directions. Front. Immunol. 9, 2536 (2018).

    PubMed  PubMed Central  Google Scholar 

  101. Fites, J. S. et al. The invasive chytrid fungus of amphibians paralyzes lymphocyte responses. Science 342, 366–369 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. McMahon, T. A. et al. Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in the absence of infection. Proc. Natl Acad. Sci. USA 110, 210–215 (2013).

    CAS  PubMed  Google Scholar 

  103. Savage, A. E. & Zamudio, K. R. Adaptive tolerance to a pathogenic fungus drives major histocompatibility complex evolution in natural amphibian populations. Proc. Biol. Sci. 283, 20153115 (2016).

    PubMed  PubMed Central  Google Scholar 

  104. Pasmans, F. et al. Fungicidal skin secretions mediate resistance to chytridiomycosis in the European plethodontid genus Speleomantes. PLoS One 8, e63639 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Voyles, J. et al. Shifts in disease dynamics in a tropical amphibian assemblage are not due to pathogen attenuation. Science 359, 1517–1519 (2018).

    CAS  PubMed  Google Scholar 

  106. Bates, K. A. et al. Amphibian chytridiomycosis outbreak dynamics are linked with host skin bacterial community structure. Nat. Commun. 9, 693 (2018).

    PubMed  PubMed Central  Google Scholar 

  107. Kueneman, J. G. et al. Community richness of amphibian skin bacteria correlates with bioclimate at the global scale. Nat. Ecol. Evol. 3, 381–389 (2019).

    PubMed  Google Scholar 

  108. 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 

  109. Kearns, P. J. et al. Fight fungi with fungi: antifungal properties of the amphibian mycobiome. Front. Microbiol. 8, 2494 (2017).

    PubMed  PubMed Central  Google Scholar 

  110. Jenkinson, T. S. et al. Globally invasive genotypes of the amphibian chytrid outcompete an enzootic lineage in coinfections. Proc. Biol. Sci. 285, 20181894 (2018).

    PubMed  PubMed Central  Google Scholar 

  111. Rosa, G. M. et al. Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages. Sci. Rep. 7, 43260 (2017).

    PubMed  PubMed Central  Google Scholar 

  112. Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012). Description of the emerging threat that fungi pose to biota.

    CAS  PubMed  Google Scholar 

  113. American Society for Microbiology. One Health: Fungal Pathogens of Humans, Animals and Plants. Colloq. Rep. (American Society for Microbiology, 2019).

  114. Langwig, K. E. et al. Context-dependent conservation responses to emerging wildlife diseases. Front. Ecol. Env. 13, 195–202 (2015).

    Google Scholar 

  115. Garner, T. W. et al. Mitigating amphibian chytridiomycoses in nature. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 20160207 (2016).

    PubMed  PubMed Central  Google Scholar 

  116. European Food Safety Authority. Risk of survival establishment, spread of Batrachochytrium salamandrivorans (Bsal) in the EU. EFSA J. 16, 5259 (2018).

    Google Scholar 

  117. U.S. Fish & Wildlife Service. Listing Salamanders as Injurious Due to Risk of Salamander Chytrid Fungus (January 12, 2016). fws.gov https://www.fws.gov/injuriouswildlife/salamanders.html (2016).

  118. Canada Border Services Agency. Environment and Climate Change Canada (ECCC)’s Import Restrictions on Salamanders: Customs Notice 17-17. cbsa-asfc.gc.ca https://www.cbsa-asfc.gc.ca/publications/cn-ad/cn17-17-eng.html (2018).

  119. Bosch, J. et al. Successful elimination of a lethal wildlife infectious disease in nature. Biol. Letters 11, 20150874 (2015). First successful mitigation of an invasive chytrid in nature.

    Google Scholar 

  120. Rebollar, E. A. et al. Using ‘omics’ and integrated multi-omics approaches to guide probiotic selection to mitigate chytridiomycosis and other emerging infectious diseases. Front. Microbiol. 7, 68 (2016).

    PubMed  PubMed Central  Google Scholar 

  121. Vredenburg, V. T., Briggs, C. J. & Harris, R. in Fungal Diseases: An Emerging Threat to Human, Animal, and Plant Health. Workshop Summary (eds Olsen, L., Choffnes, E. R., Relman, D. A. & Pray, L.) 342–355 (National Academies Press, 2011).

  122. Daszak, P., Cunningham, A. A. & Hyatt, A. D. Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287, 443–449 (2000).

    CAS  PubMed  Google Scholar 

  123. Blehert, D. S. et al. Bat white-nose syndrome: an emerging fungal pathogen? Science 323, 227–227 (2009).

    CAS  PubMed  Google Scholar 

  124. Worobey, M. et al. Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. Nature 455, 661–664 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  125. Cui, Y. J. et al. Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proc. Natl Acad. Sci. USA 110, 577–582 (2013).

    CAS  PubMed  Google Scholar 

  126. Roe, C. C. et al. Dating the Cryptococcus gattii dispersal to the North American Pacific Northwest. mSphere 3, e00499-17 (2018).

    PubMed  PubMed Central  Google Scholar 

  127. Biek, R., Pybus, O. G., Lloyd-Smith, J. O. & Didelot, X. Measurably evolving pathogens in the genomic era. Trends Ecol. Evol. 30, 306–313 (2015).

    PubMed  PubMed Central  Google Scholar 

  128. Rambaut, A. Estimating the rate of molecular evolution: incorporating non-contemporaneous sequences into maximum likelihood phylogenies. Bioinformatics 16, 395–399 (2000).

    CAS  PubMed  Google Scholar 

  129. Rieux, A. & Balloux, F. Inferences from tip-calibrated phylogenies: a review and a practical guide. Mol. Ecol. 25, 1911–1924 (2016).

    PubMed  PubMed Central  Google Scholar 

  130. Croucher, N. J. et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 43, e15 (2015).

    PubMed  Google Scholar 

  131. Greenberg, D. A. & Palen, W. J. A deadly amphibian disease goes global. Science 363, 1386–1388 (2019).

    CAS  PubMed  Google Scholar 

  132. Herrel, A. & van der Meijden, A. An analysis of the live reptile and amphibian trade in the USA compared to the global trade in endangered species. Herpetol. J. 24, 103–110 (2014).

    Google Scholar 

Download references

Acknowledgements

We acknowledge funding from the Natural Environment Research Council (NERC) (NE/E006701/1, NE/E006841/1, NE/G002193/1, NE/K014455/1, NE/K012 509/1, NE/M000591/1, NE/N009800/1, NE/N009967/1, NE/S000844/1, NE/S000992/1), The Morris Animal Foundation (D12ZO-002 and D16ZO-022) and the Leverhulme Trust (RPG-2014-273). We thank S. O’Hanlon and P. Ghosh, who assisted with drafting the figures. M.C.F. is a Fellow in the CIFAR ‘Fungal Kingdom’ Program.

Author information

Authors and Affiliations

Authors

Contributions

Both authors wrote the article.

Corresponding author

Correspondence to Matthew C. Fisher.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Microbiology thanks T. James and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Related links

Amphibian Disease Portal: https://amphibiandisease.org

AmphibiaWeb: https://amphibiaweb.org

CITES: http://www.cites.org

EpiCollect: https://five.epicollect.net/project/bd-global-isolation-protocol

North American Bsal Task Force: http://www.salamanderfungus.org/about-bsal/

TRAFFIC: https://www.traffic.org/

Glossary

Panzootic

Global outbreak of an infectious disease in animals.

Multilocus sequence typing

Matching the DNA sequences of fragments of multiple housekeeping genes in order to assay genetic diversity.

Epizootics

Local outbreaks of an infectious disease in animals.

Bayesian-based haplotype clustering

Population assignment using large numbers of resequenced genomes.

Mutation–drift equilibrium

State of balance in which the rate at which variation is lost through genetic drift is equal to the rate at which new variation is created by mutation.

Tajima’s D statistic

Population genetic test statistic distinguishing between DNA sequences that evolve neutrally (at mutation–drift equilibria) and those that evolve in response to a nonrandom process, such as demographic change or natural selection.

Phased

Subjected to a process of assigning alleles to the paternal and maternal chromosomes.

Crossovers

Segregation of alleles between homologous chromosomes through DNA breaks and reconnections.

Meiosis

Sexual recombination resulting in crossovers.

Mating-type alleles

Genes that regulate compatibility leading to meiosis in fungi, also called mating-type ‘idiomorphs’.

Chromosomal copy number variation

State in which the number of copies of a haplotype varies between one individual and another, also known as ‘aneuploidy’.

Amphibian arks

Ex situ breeding of threatened species in biocontainment facilities.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fisher, M.C., Garner, T.W.J. Chytrid fungi and global amphibian declines. Nat Rev Microbiol 18, 332–343 (2020). https://doi.org/10.1038/s41579-020-0335-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41579-020-0335-x

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing