1932

Abstract

Ancient enzootic associations between wildlife and their infections allow evolution to innovate mechanisms of pathogenicity that are counterbalanced by host responses. However, erosion of barriers to pathogen dispersal by globalization leads to the infection of hosts that have not evolved effective resistance and the emergence of highly virulent infections. Global amphibian declines driven by the rise of chytrid fungi and chytridiomycosis are emblematic of emerging infections. Here, we review how modern biological methods have been used to understand the adaptations and counteradaptations that these fungi and their amphibian hosts have evolved. We explore the interplay of biotic and abiotic factors that modify the virulence of these infections and dissect the complexity of this disease system. We highlight progress that has led to insights into how we might in the future lessen the impact of these emerging infections.

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2021-10-08
2024-10-15
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Literature Cited

  1. 1. 
    Abramyan J, Stajich JE. 2012. Species-specific chitin-binding module 18 expansion in the amphibian pathogen Batrachochytrium dendrobatidis. mBio 3:e00150-12
    [Google Scholar]
  2. 2. 
    Antwis RE, Weldon C. 2017. Amphibian skin defences show variation in ability to inhibit growth of Batrachochytrium dendrobatidis isolates from the Global Panzootic Lineage. Microbiology 163:1835–38
    [Google Scholar]
  3. 3. 
    Bataille A, Cashins SD, Grogan L, Skerratt LF, Hunter D et al. 2015. Susceptibility of amphibians to chytridiomycosis is associated with MHC class II conformation. Proc. R. Soc. B 282:20143127
    [Google Scholar]
  4. 4. 
    Bates KA, Clare FC, O'Hanlon S, Bosch J, Brookes L et al. 2018. Amphibian chytridiomycosis outbreak dynamics are linked with host skin bacterial community structure. Nat. Commun. 9:693
    [Google Scholar]
  5. 5. 
    Bates KA, Shelton JMG, Mercier VL, Hopkins KP, Harrison XA et al. 2019. Captivity and infection by the fungal pathogen Batrachochytrium salamandrivorans perturb the amphibian skin microbiome. Front. Microbiol. 10:1834
    [Google Scholar]
  6. 6. 
    Beard KH, O'Neill EM. 2005. Infection of an invasive frog Eleutherodactylus coqui by the chytrid fungus Batrachochytrium dendrobatidis in Hawaii. Biol. Conserv. 126:591–95
    [Google Scholar]
  7. 7. 
    Berger L, Hyatt AD, Speare R, Longcore JE. 2005. Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Dis. Aquat. Organ. 68:51–63
    [Google Scholar]
  8. 8. 
    Berger L, Speare R, Daszak P, Green DE, Cunningham AA et al. 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. PNAS 95:9031–36
    [Google Scholar]
  9. 9. 
    Bernardo-Cravo AP, Schmeller DS, Chatzinotas A, Vredenburg VT, Loyau A. 2020. Environmental factors and host microbiomes shape host-pathogen dynamics. Trends Parasitol 36:616–33
    [Google Scholar]
  10. 10. 
    Betancourt-Roman CM, O'Neil CC, James TY. 2016. Rethinking the role of invertebrate hosts in the life cycle of the amphibian chytridiomycosis pathogen. Parasitology 143:1723–29
    [Google Scholar]
  11. 11. 
    Beukema W, Pasmans F, Van Praet S, Ferri-Yáñez F, Kelly M et al. 2021. Microclimate limits thermal behaviour favourable to disease control in a nocturnal amphibian. Ecol. Lett. 24:27–37
    [Google Scholar]
  12. 12. 
    Blaustein AR, Jones DK, Urbina J, Cothran RD, Harjoe C et al. 2020. Effects of invasive larval bullfrogs (Rana catesbeiana) on disease transmission, growth and survival in the larvae of native amphibians. Biol. Invasions 22:1771–84
    [Google Scholar]
  13. 13. 
    Bletz MC, Kelly M, Sabino-Pinto J, Bales E, Van Praet S et al. 2018. Disruption of skin microbiota contributes to salamander disease. Proc. R. Soc. B 285:20180758
    [Google Scholar]
  14. 14. 
    Bletz MC, Loudon AH, Becker MH, Bell SC, Woodhams DC et al. 2013. Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. Ecol. Lett. 16:807–20
    [Google Scholar]
  15. 15. 
    Blooi M, Laking AE, Martel A, Haesebrouck F, Jocque M et al. 2017. Host niche may determine disease-driven extinction risk. PLOS ONE 12:e0181051
    [Google Scholar]
  16. 16. 
    Bosch J, Martínez-Solano I, García-París M. 2001. Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biol. Conserv. 97:331–37
    [Google Scholar]
  17. 17. 
    Bosch J, Sanchez-Tome E, Fernandez-Loras A, Oliver JA, Fisher MC, Garner TWJ. 2015. Successful elimination of a lethal wildlife infectious disease in nature. Biol. Lett. 11:20150874
    [Google Scholar]
  18. 18. 
    Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD. 2004. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis. Aquat. Org. 60:141–48
    [Google Scholar]
  19. 19. 
    Brannelly LA, Roberts AA, Skerratt LF, Berger L. 2017. Epidermal cell death in frogs with chytridiomycosis. PeerJ 5:e2925
    [Google Scholar]
  20. 20. 
    Briggs CJ, Knapp RA, Vredenburg VT 2010. Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. PNAS 107:9695–700
    [Google Scholar]
  21. 21. 
    Briggs CJ, Vredenburg VT, Knapp RA, Rachowicz LJ. 2005. Investigating the population-level effects of chytridiomycosis: an emerging infectious disease of amphibians. Ecology 86:3149–59
    [Google Scholar]
  22. 22. 
    Brutyn M, D'Herde K, Dhaenens M, Van Rooij P, Verbrugghe E et al. 2012. Batrachochytrium dendrobatidis zoospore secretions rapidly disturb intercellular junctions in frog skin. Fungal Genet. Biol. 49:830–37
    [Google Scholar]
  23. 23. 
    Buck JC, Truong L, Blaustein AR. 2011. Predation by zooplankton on Batrachochytrium dendrobatidis: biological control of the deadly amphibian chytrid fungus?. Biodivers. Conserv. 20:3549–53
    [Google Scholar]
  24. 24. 
    Campbell CR, Voyles J, Cook DI, Dinudom A. 2012. Frog skin epithelium: electrolyte transport and chytridiomycosis. Int. J. Biochem. Cell B 44:431–34
    [Google Scholar]
  25. 25. 
    Cashins SD, Grogan LF, McFadden M, Hunter D, Harlow PS et al. 2013. Prior infection does not improve survival against the amphibian disease chytridiomycosis. PLOS ONE 8:e56747
    [Google Scholar]
  26. 26. 
    Clare FC, Halder JB, Daniel O, Bielby J, Semenov MA et al. 2016. Climate forcing of an emerging pathogenic fungus across a montane multi-host community. Philos. Trans. R. Soc. B 371:20150454
    [Google Scholar]
  27. 27. 
    Cohen JM, Venesky MD, Sauer EL, Civitello DJ, McMahon TA et al. 2017. The thermal mismatch hypothesis explains host susceptibility to an emerging infectious disease. Ecol. Lett. 20:184–93
    [Google Scholar]
  28. 28. 
    Crawford AJ, Lips KR, Bermingham E 2010. Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. PNAS 107:13777–82
    [Google Scholar]
  29. 29. 
    Daly JW. 1998. Thirty years of discovering arthropod alkaloids in amphibian skin. J. Nat. Prod. 61:162–72
    [Google Scholar]
  30. 30. 
    Daly JW, Kaneko T, Wilham J, Garraffo HM, Spande TF et al. 2002. Bioactive alkaloids of frog skin: Combinatorial bioprospecting reveals that pumiliotoxins have an arthropod source. PNAS 99:13996–4001
    [Google Scholar]
  31. 31. 
    Daskin JH, Alford RA, Puschendorf R. 2011. Short-term exposure to warm microhabitats could explain amphibian persistence with Batrachochytrium dendrobatidis. PLOS ONE 6:e26215
    [Google Scholar]
  32. 32. 
    Deknock A, Goethals P, Croubels S, Lens L, Martel A, Pasmans F. 2020. Towards a food web based control strategy to mitigate an amphibian panzootic in agricultural landscapes. Glob. Ecol. Evol. 24:e01314
    [Google Scholar]
  33. 33. 
    Di Rosa I, Simoncelli F, Fagotti A, Pascolini R. 2007. The proximate cause of frog declines?. Nature 447:E45
    [Google Scholar]
  34. 34. 
    Doddington BJ, Bosch J, Oliver JA, Grassly NC, Garcia G et al. 2013. Context-dependent amphibian host population response to an invading pathogen. Ecology 94:1795–804
    [Google Scholar]
  35. 35. 
    Drake DL, Altig R, Grace JB, Walls SC. 2007. Occurrence of oral deformities in larval anurans. Copeia 2007 449–58
    [Google Scholar]
  36. 36. 
    Drees KP, Lorch JM, Puechmaille SJ, Parise KL, Wibbelt G et al. 2017. Phylogenetics of a fungal invasion: origins and widespread dispersal of white-nose syndrome. mBio 8:e01941-17
    [Google Scholar]
  37. 37. 
    Ellison A, Zamudio K, Lips K, Muletz-Wolz C. 2020. Temperature-mediated shifts in salamander transcriptomic responses to the amphibian-killing fungus. Mol. Ecol. 29:325–43
    [Google Scholar]
  38. 38. 
    Ellison AR, DiRenzo GV, McDonald CA, Lips KR, Zamudio KR. 2017. First in vivo Batrachochytrium dendrobatidis transcriptomes reveal mechanisms of host exploitation, host-specific gene expression, and expressed genotype shifts. Genes Genom. Genet. 7:269–78
    [Google Scholar]
  39. 39. 
    Ellison AR, Tunstall T, DiRenzo GV, Hughey MC, Rebollar EA et al. 2015. More than skin deep: functional genomic basis for resistance to amphibian chytridiomycosis. Genome Biol. Evol. 7:286–98
    [Google Scholar]
  40. 40. 
    Eskew EA, Shock BC, LaDouceur EEB, Keel K, Miller MR et al. 2018. Gene expression differs in susceptible and resistant amphibians exposed to Batrachochytrium dendrobatidis. Roy. Soc. Open. Sci. 5:170910
    [Google Scholar]
  41. 41. 
    Farrer RA, Fisher MC. 2017. Describing genomic and epigenomic traits underpinning emerging fungal pathogens. Adv. Genet. 100:73–140
    [Google Scholar]
  42. 42. 
    Farrer RA, Martel A, Verbrugghe E, Abouelleil A, Ducatelle R et al. 2017. Genomic innovations linked to infection strategies across emerging pathogenic chytrid fungi. Nat. Commun. 8:814742
    [Google Scholar]
  43. 43. 
    Farrer RA, Weinert LA, Bielby J, Garner TWJ, Balloux F et al. 2011. Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. PNAS 108:18732–36
    [Google Scholar]
  44. 44. 
    Fisher MC, Bosch J, Yin Z, Stead DA, Walker J et al. 2009. Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Mol. Ecol. 18:415–29
    [Google Scholar]
  45. 45. 
    Fisher MC, Garner TWJ. 2020. Chytrid fungi and global amphibian declines. Nat. Rev. Microbiol. 18:332–43
    [Google Scholar]
  46. 46. 
    Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC et al. 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–94
    [Google Scholar]
  47. 47. 
    Fites JS, Ramsey JP, Holden WM, Collier SP, Sutherland DM et al. 2013. The invasive chytrid fungus of amphibians paralyzes lymphocyte responses. Science 342:366–69
    [Google Scholar]
  48. 48. 
    Fu MJ, Waldman B. 2019. Ancestral chytrid pathogen remains hypervirulent following its long coevolution with amphibian hosts. Proc. R. Soc. B 286:20190833
    [Google Scholar]
  49. 49. 
    Garmyn A, Van Rooij P, Pasmans F, Hellebuyck T, Van den Broeck W et al. 2012. Waterfowl: potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis. PLOS ONE 7:e35038
    [Google Scholar]
  50. 50. 
    Garner TW, Schmidt BR, Martel A, Pasmans F, Muths E et al. 2016. Mitigating amphibian chytridiomycoses in nature. Philos. Trans. R. Soc. B 371:20160207
    [Google Scholar]
  51. 51. 
    Garner TWJ, Perkins MW, Govindarajulu P, Seglie D, Walker S et al. 2006. The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biol. Lett. 2:455–59
    [Google Scholar]
  52. 52. 
    Garner TWJ, Rowcliffe JM, Fisher MC. 2011. Climate change, chytridiomycosis or condition: an experimental test of amphibian survival. Glob. Change Biol. 17:667–75
    [Google Scholar]
  53. 53. 
    Garner TWJ, Walker S, Bosch J, Leech S, Rowcliffe JM et al. 2009. Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118:783–91
    [Google Scholar]
  54. 54. 
    Greener MS, Verbrugghe E, Moira K, Blooi M, Beukema W et al. 2020. Presence of low virulence chytrid fungi could protect European amphibians from more deadly strains. Nat. Commun. 11:5393
    [Google Scholar]
  55. 55. 
    Grogan LF, Robert J, Berger L, Skerratt LF, Scheele BC et al. 2018. Review of the amphibian immune response to chytridiomycosis, and future directions. Front. Immunol. 9:2536
    [Google Scholar]
  56. 56. 
    Hamilton PT, Richardson JML, Anholt BR. 2012. Daphnia in tadpole mesocosms: trophic links and interactions with Batrachochytrium dendrobatidis. Freshw. Biol. 57:676–83
    [Google Scholar]
  57. 57. 
    Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR et al. 2009. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J 3:818–24
    [Google Scholar]
  58. 58. 
    Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL. 2000. Quantitative evidence for global amphibian population declines. Nature 404:752–55
    [Google Scholar]
  59. 59. 
    Jani AJ, Knapp RA, Briggs CJ. 2017. Epidemic and endemic pathogen dynamics correspond to distinct host population microbiomes at a landscape scale. Proc. R. Soc. B 284:20170944
    [Google Scholar]
  60. 60. 
    Johnson M, Speare R. 2003. Survival of Batrachochytrium dendrobatidis in water: quarantine and control implications. Emerg. Infect. Dis. 9:922–25
    [Google Scholar]
  61. 61. 
    Knapp RA, Fellers GM, Kleeman PM, Miller DAW, Vredenburg VT et al. 2016. Large-scale recovery of an endangered amphibian despite ongoing exposure to multiple stressors. PNAS 113:11889–94
    [Google Scholar]
  62. 62. 
    Kosch TA, Bataille A, Didinger C, Eimes JA, Rodriguez-Brenes S et al. 2016. Major histocompatibility complex selection dynamics in pathogen-infected túngara frog (Physalaemus pustulosus) populations. Biol. Lett. 12:20160345
    [Google Scholar]
  63. 63. 
    Lam BA, Walton DB, Harris RN. 2011. Motile zoospores of Batrachochytrium dendrobatidis move away from antifungal metabolites produced by amphibian skin bacteria. EcoHealth 8:36–45
    [Google Scholar]
  64. 64. 
    Lauer A, Simon MA, Banning JL, Andre E, Duncan K, Harris RN 2007. Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia 2007 630–40
    [Google Scholar]
  65. 65. 
    Li Z, Martel A, Bogaerts S, Gocmen B, Pafilis P et al. 2020. Landscape connectivity limits the predicted impact of fungal pathogen invasion. J. Fungi. 6:205
    [Google Scholar]
  66. 66. 
    Liew N, Moya MJM, Wierzbicki CJ, Hollinshead M, Dillon MJ et al. 2017. Chytrid fungus infection in zebrafish demonstrates that the pathogen can parasitize non-amphibian vertebrate hosts. Nat. Commun. 8:15048
    [Google Scholar]
  67. 67. 
    Liu P, Stajich JE. 2015. Characterization of the Carbohydrate Binding Module 18 gene family in the amphibian pathogen Batrachochytrium dendrobatidis. Fungal Genet. Biol. 77:31–39
    [Google Scholar]
  68. 68. 
    Longcore JE, Pessier AP, Nichols DK. 1999. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–27
    [Google Scholar]
  69. 69. 
    Longo AV, Fleischer RC, Lips KR. 2019. Double trouble: Co-infections of chytrid fungi will severely impact widely distributed newts. Biol. Invasions 21:2233–45
    [Google Scholar]
  70. 70. 
    Longo AV, Zamudio KR. 2017. Environmental fluctuations and host skin bacteria shift survival advantage between frogs and their fungal pathogen. ISME J 11:349–61
    [Google Scholar]
  71. 71. 
    Longo AV, Zamudio KR. 2017. Temperature variation, bacterial diversity and fungal infection dynamics in the amphibian skin. Mol. Ecol. 26:4787–97
    [Google Scholar]
  72. 72. 
    Lorch JM, Knowles S, Lankton JS, Michell K, Edwards JL et al. 2016. Snake fungal disease: an emerging threat to wild snakes. Philos. Trans. R. Soc. B 371:20150457
    [Google Scholar]
  73. 73. 
    Maniero GD, Carey C. 1997. Changes in selected aspects of immune function in the leopard frog, Rana pipiens, associated with exposure to cold. J. Comp. Physiol. B 167:256–63
    [Google Scholar]
  74. 74. 
    Marcum RD, St-Hilaire S, Murphy PJ, Rodnick KJ. 2010. Effects of Batrachochytrium dendrobatidis infection on ion concentrations in the boreal toad Anaxyrus (Bufo) boreas boreas. Dis. Aquat. Organ. 91:17–21
    [Google Scholar]
  75. 75. 
    Martel A, Blooi M, Adriaensen C, Van Rooij P, Beukema W et al. 2014. Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346:630–31
    [Google Scholar]
  76. 76. 
    Martel A, Spitzen-van der Sluijs A, Blooi M, Bert W, Ducatelle R et al. 2013. Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. PNAS 110:15325–29
    [Google Scholar]
  77. 77. 
    McDonald CA, Ellison AR, Toledo LF, James TY, Zamudio KR. 2020. Gene expression varies within and between enzootic and epizootic lineages of Batrachochytrium dendrobatidis (Bd) in the Americas. Fungal Biol 124:34–43
    [Google Scholar]
  78. 78. 
    McKnight DT, Carr LJ, Bower DS, Schwarzkopf L, Alford RA, Zenger KR. 2020. Infection dynamics, dispersal, and adaptation: understanding the lack of recovery in a remnant frog population following a disease outbreak. Heredity 125:110–23
    [Google Scholar]
  79. 79. 
    McMahon TA, Brannelly LA, Chatfield MWH, Johnson PTJ, Joseph MB et al. 2013. Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in the absence of infection. PNAS 110:210–15
    [Google Scholar]
  80. 80. 
    McMahon TA, Rohr JR. 2015. Transition of chytrid fungus infection from mouthparts to hind limbs during amphibian metamorphosis. EcoHealth 12:188–93
    [Google Scholar]
  81. 81. 
    McMahon TA, Sears BF, Venesky MD, Bessler SM, Brown JM et al. 2014. Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature 511:224–27
    [Google Scholar]
  82. 82. 
    Medina D, Garner TWJ, Carrascal LM, Bosch J. 2015. Delayed metamorphosis of amphibian larvae facilitates Batrachochytrium dendrobatidis transmission and persistence. Dis. Aquat. Organ. 117:85–92
    [Google Scholar]
  83. 83. 
    Medina EM, Robinson KA, Bellingham-Johnstun K, Ianiri G, Laplante C et al. 2020. Genetic transformation of Spizellomyces punctatus, a resource for studying chytrid biology and evolutionary cell biology. eLife 9:e52741
    [Google Scholar]
  84. 84. 
    Meyer W, Seegers U, Schnapper A, Neuhaus H, Himstedt W, Toepfer-Petersen E. 2007. Possible antimicrobial defense by free sugars on the epidermal surface of aquatic vertebrates. Aquat Biol 1:167–75
    [Google Scholar]
  85. 85. 
    Moss AS, Carty N, Francisco MJS. 2010. Identification and partial characterization of an elastolytic protease in the amphibian pathogen Batrachochytrium dendrobatidis. Dis. Aquat. Organ. 92:149–58
    [Google Scholar]
  86. 86. 
    Moss AS, Reddy NS, Dortaj IM, Francisco MJS. 2008. Chemotaxis of the amphibian pathogen Batrachochytrium dendrobatidis and its response to a variety of attractants. Mycologia 100:1–5
    [Google Scholar]
  87. 87. 
    Moyes DL, Richardson JP, Naglik JR. 2015. Candida albicans-epithelial interactions and pathogenicity mechanisms: scratching the surface. Virulence 6:338–46
    [Google Scholar]
  88. 88. 
    Nguyen TT, Nguyen TV, Ziegler T, Pasmans F, Martel A. 2017. Trade in wild anurans vectors the urodelan pathogen Batrachochytrium salamandrivorans into Europe. Amphibia-Reptilia 38:554–56
    [Google Scholar]
  89. 89. 
    Oficialdegui FJ, Sanchez MI, Monsalve-Carcano C, Boyero L, Bosch J. 2019. The invasive red swamp crayfish (Procambarus clarkii) increases infection of the amphibian chytrid fungus (Batrachochytrium dendrobatidis). Biol. Invasions 21:3221–31
    [Google Scholar]
  90. 90. 
    O'Hanlon SJ, Rieux A, Farrer RA, Rosa GM, Waldman B et al. 2018. Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360:621–27
    [Google Scholar]
  91. 91. 
    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:e56802
    [Google Scholar]
  92. 92. 
    Padgett-Flohr GE, Goble ME 2007. Evaluation of tadpole mouthpart depigmentation as a diagnostic test for infection by Batrachochytrium dendrobatidis for four California anurans. J. Wildlife Dis. 43:690–99
    [Google Scholar]
  93. 93. 
    Parris MJ, Beaudoin JG. 2004. Chytridiomycosis impacts predator-prey interactions in larval amphibian communities. Oecologia 140:626–32
    [Google Scholar]
  94. 94. 
    Pask JD, Cary TL, Rollins-Smith LA. 2013. Skin peptides protect juvenile leopard frogs (Rana pipiens) against chytridiomycosis. J. Exp. Biol. 216:2908–16
    [Google Scholar]
  95. 95. 
    Pessier AP, Nichols DK, Longcore JE, Fuller MS. 1999. Cutaneous chytridiomycosis in poison dart frogs (Dendrobates spp.) and White's tree frogs (Litoria caerulea). J. Vet. Diagn. Investig. 11:194–99
    [Google Scholar]
  96. 96. 
    Piotrowski JS, Annis SL, Longcore JE. 2004. Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15
    [Google Scholar]
  97. 97. 
    Poorten TJ, Rosenblum EB. 2016. Comparative study of host response to chytridiomycosis in a susceptible and a resistant toad species. Mol. Ecol. 25:5663–79
    [Google Scholar]
  98. 98. 
    Prostak SM, Robinson KA, Titus MA, Fritz-Laylin LK. 2021. The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom. Curr. Biol. 31:61192–205.e6
    [Google Scholar]
  99. 99. 
    Puschendorf R, Hoskin CJ, Cashins SD, McDonald K, Skerratt LF et al. 2011. Environmental refuge from disease-driven amphibian extinction. Conserv. Biol. 25:956–64
    [Google Scholar]
  100. 100. 
    Raffel TR, Rohr JR, Kiesecker JM, Hudson PJ. 2006. Negative effects of changing temperature on amphibian immunity under field conditions. Funct. Ecol. 20:819–28
    [Google Scholar]
  101. 101. 
    Ramsey JP, Reinert LK, Harper LK, Woodhams DC, Rollins-Smith LA. 2010. Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis. Infect. Immun. 78:3981–92
    [Google Scholar]
  102. 102. 
    Reeder NMM, Pessier AP, Vredenburg VT. 2012. A reservoir species for the emerging amphibian pathogen Batrachochytrium dendrobatidis thrives in a landscape decimated by disease. PLOS ONE 7:e33567
    [Google Scholar]
  103. 103. 
    Retallick RWR, McCallum H, Speare R. 2004. Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLOS Biol 2:1965–71
    [Google Scholar]
  104. 104. 
    Ribas L, Li MS, Doddington BJ, Robert J, Seidel JA et al. 2009. Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis. PLOS ONE 4:e8408
    [Google Scholar]
  105. 105. 
    Ribeiro LP, Carvalho T, Becker CG, Jenkinson TS, Leite DD et al. 2019. Bullfrog farms release virulent zoospores of the frog-killing fungus into the natural environment. Sci. Rep 9:13422
    [Google Scholar]
  106. 106. 
    Richards-Zawacki CL. 2010. Thermoregulatory behaviour affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs. Proc. R. Soc. B 277:519–28
    [Google Scholar]
  107. 107. 
    Rodriguez KM, Voyles J. 2020. The amphibian complement system and chytridiomycosis. J. Exp. Zool. A 333:706–19
    [Google Scholar]
  108. 108. 
    Rollins-Smith LA. 2017. Amphibian immunity-stress, disease, and climate change. Dev. Comp. Immunol. 66:111–19
    [Google Scholar]
  109. 109. 
    Rollins-Smith LA, Ramsey JP, Reinert LK, Woodhams DC. 2011. Amphibian immune defenses against chytridiomycosis: impacts of changing environments. Integr. Comp. Biol. 51:552–62
    [Google Scholar]
  110. 110. 
    Rosenblum EB, Poorten TJ, Joneson S, Settles M. 2012. Substrate-specific gene expression in Batrachochytrium dendrobatidis, the chytrid pathogen of amphibians. PLOS ONE 7:e49924
    [Google Scholar]
  111. 111. 
    Rosenblum EB, Poorten TJ, Settles M, Murdoch GK. 2012. Only skin deep: shared genetic response to the deadly chytrid fungus in susceptible frog species. Mol. Ecol. 21:3110–20
    [Google Scholar]
  112. 112. 
    Rosenblum EB, Stajich JE, Maddox N, Eisen MB 2008. Global gene-expression profiles for life stages of the deadly amphibian pathogen Batrachochytrium dendrobatidis. PNAS 105:17034–39
    [Google Scholar]
  113. 113. 
    Rowley JJ, Skerratt LF, Alford RA, Campbell R. 2007. Retreat sites of rain forest stream frogs are not a reservoir for Batrachochytrium dendrobatidis in northern Queensland, Australia. Dis. Aquat. Organ 74:7–12
    [Google Scholar]
  114. 114. 
    Rowley JJL, Alford RA. 2013. Hot bodies protect amphibians against chytrid infection in nature. Sci. Rep. 3:1515
    [Google Scholar]
  115. 115. 
    Russell ID, Larson JG, von May R, Holmes IA, James TY, Rabosky ARD. 2019. Widespread chytrid infection across frogs in the Peruvian Amazon suggests critical role for low elevation in pathogen spread and persistence. PLOS ONE 14:e0222718
    [Google Scholar]
  116. 116. 
    Sauer EL, Cohen JM, Lajeunesse MJ, McMahon TA, Civitello DJ et al. 2020. A meta-analysis reveals temperature, dose, life stage, and taxonomy influence host susceptibility to a fungal parasite. Ecology 101:e02979
    [Google Scholar]
  117. 117. 
    Savage AE, Zamudio KR 2011. MHC genotypes associate with resistance to a frog-killing fungus. PNAS 108:16705–10
    [Google Scholar]
  118. 118. 
    Savage AE, Zamudio KR. 2016. Adaptive tolerance to a pathogenic fungus drives major histocompatibility complex evolution in natural amphibian populations. Proc. R. Soc. B 283:20153115
    [Google Scholar]
  119. 119. 
    Scheele B, Pasmans F, Skerratt LF, Berger L, Martel A et al. 2019. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363:1459–63
    [Google Scholar]
  120. 120. 
    Scheele BC, Skerratt LF, Grogan LF, Hunter DA, Clemann N et al. 2017. After the epidemic: ongoing declines, stabilizations and recoveries in amphibians afflicted by chytridiomycosis. Biol. Conserv. 206:37–46
    [Google Scholar]
  121. 121. 
    Schloegel LM, Ferreira CM, James TY, Hipolito M, Longcore JE et al. 2010. The North American bullfrog as a reservoir for the spread of Batrachochytrium dendrobatidis in Brazil. Anim. Conserv. 13:53–61
    [Google Scholar]
  122. 122. 
    Schmeller DS, Blooi M, Martel A, Garner TWJ, Fisher MC et al. 2014. Microscopic aquatic predators strongly affect infection dynamics of a globally emerged pathogen. Curr. Biol. 24:176–80
    [Google Scholar]
  123. 123. 
    Searle CL, Mendelson JR, Green LE, Duffy MA. 2013. Daphnia predation on the amphibian chytrid fungus and its impacts on disease risk in tadpoles. Ecol. Evol. 3:4129–38
    [Google Scholar]
  124. 124. 
    Shapard EJ, Moss AS, San Francisco MJ 2012. Batrachochytrium dendrobatidis can infect and cause mortality in the nematode Caenorhabditis elegans. Mycopathologia 173:121–26
    [Google Scholar]
  125. 125. 
    Smith HK, Pasmans F, Dhaenens M, Deforce D, Bonte D et al. 2018. Skin mucosome activity as an indicator of Batrachochytrium salamandrivorans susceptibility in salamanders. PLOS ONE 13:e0199295
    [Google Scholar]
  126. 126. 
    Spitzen-van der Sluijs A, Canessa S, Martel A, Pasmans F. 2017. Fragile coexistence of a global chytrid pathogen with amphibian populations is mediated by environment and demography. Proc. R. Soc. B 284:20171444
    [Google Scholar]
  127. 127. 
    Spitzen-Van der Sluijs A, Martel A, Hallmann CA, Bosman W, Garner TWJ et al. 2014. Environmental determinants of recent endemism of Batrachochytrium dendrobatidis infections in amphibian assemblages in the absence of disease outbreaks. Conserv. Biol. 28:1302–11
    [Google Scholar]
  128. 128. 
    Stegen G, Pasmans F, Schmidt BR, Rouffaer LO, Van Praet S et al. 2017. Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans. Nature 544:353–56
    [Google Scholar]
  129. 129. 
    Swafford AJM, Hussey SP, Fritz-Laylin LK. 2020. High-efficiency electroporation of chytrid fungi. Sci. Rep. 10:15145
    [Google Scholar]
  130. 130. 
    Symonds EP, Trott DJ, Bird PS, Mills P. 2008. Growth characteristics and enzyme activity in Batrachochytrium dendrobatidis isolates. Mycopathologia 166:143–47
    [Google Scholar]
  131. 131. 
    Talbot NJ. 2003. On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Annu. Rev. Microbiol. 57:177–202
    [Google Scholar]
  132. 132. 
    Valencia-Aguilar A, Toledo LF, Vital MVC, Mott T. 2016. Seasonality, environmental factors, and host behavior linked to disease risk in stream-dwelling tadpoles. Herpetologica 72:98–106
    [Google Scholar]
  133. 133. 
    Valenzuela-Sanchez A, Schmidt BR, Uribe-Rivera DE, Costas F, Cunningham AA, Soto-Azat C. 2017. Cryptic disease-induced mortality may cause host extinction in an apparently stable host-parasite system. Proc. R. Soc. B 284:20171176
    [Google Scholar]
  134. 134. 
    Van Rooij P, Martel A, Brutyn M, Maes S, Chiers K et al. 2010. Development of in vitro models for a better understanding of the early pathogenesis of Batrachochytrium dendrobatidis infections in amphibians. Altern. Lab. Anim. 38:519–28
    [Google Scholar]
  135. 135. 
    Van Rooij P, Martel A, D'Herde K, Brutyn M, Croubels S et al. 2012. Germ tube mediated invasion of Batrachochytrium dendrobatidis in amphibian skin is host dependent. PLOS ONE 7:e41481
    [Google Scholar]
  136. 136. 
    Van Rooij P, Martel A, Haesebrouck F, Pasmans F. 2015. Amphibian chytridiomycosis: a review with focus on fungus-host interactions. Vet. Res. 46:137
    [Google Scholar]
  137. 137. 
    Vandeputte D, Kathagen G, D'hoe K, Vieira-Silva S, Valles-Colomer M et al. 2017. Quantitative microbiome profiling links gut community variation to microbial load. Nature 551:507–11
    [Google Scholar]
  138. 138. 
    Venesky MD, Mendelson JR, Sears BF, Stiling P, Rohr JR. 2012. Selecting for tolerance against pathogens and herbivores to enhance success of reintroduction and translocation. Conserv. Biol. 26:586–92
    [Google Scholar]
  139. 139. 
    Verant ML, Meteyer CU, Speakman JR, Cryan PM, Lorch JM, Blehert DS. 2014. White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. BMC Physiol 14:10
    [Google Scholar]
  140. 140. 
    Verbrugghe E, Van Rooij P, Favoreel H, Martel A, Pasmans F. 2019. In vitro modeling of Batrachochytrium dendrobatidis infection of the amphibian skin. PLOS ONE 14:e0225224
    [Google Scholar]
  141. 141. 
    Voyles J, Berger L, Young S, Speare R, Webb R et al. 2007. Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Dis. Aquat. Organ. 77:113–18
    [Google Scholar]
  142. 142. 
    Voyles J, Johnson LR, Rohr J, Kelly R, Barron C et al. 2017. Diversity in growth patterns among strains of the lethal fungal pathogen Batrachochytrium dendrobatidis across extended thermal optima. Oecologia 184:363–73
    [Google Scholar]
  143. 143. 
    Voyles J, Kilpatrick AM, Collins JP, Fisher MC, Frick WF et al. 2015. Moving beyond too little, too late: managing emerging infectious diseases in wild populations requires international policy and partnerships. EcoHealth 12:404–7
    [Google Scholar]
  144. 144. 
    Voyles J, Woodhams DC, Saenz V, Byrne AQ, Perez R et al. 2018. Shifts in disease dynamics in a tropical amphibian assemblage are not due to pathogen attenuation. Science 359:1517–19
    [Google Scholar]
  145. 145. 
    Voyles J, Young S, Berger L, Campbell C, Voyles WF et al. 2009. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326:582–85
    [Google Scholar]
  146. 146. 
    Vredenburg VT, Briggs CJ, Harris R 2011. Host-pathogen dynamics of amphibian chytridiomycosis: the role of the skin microbiome in health and disease. Fungal Diseases: An Emerging Challenge to Human, Animal, and Plant Health L Olsen, ER Choffnes, DA Relman, L Pray 342–55 Washington, DC: Natl. Acad. Press
    [Google Scholar]
  147. 147. 
    Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ 2010. Dynamics of an emerging disease drive large-scale amphibian population extinctions. PNAS 107:9689–94
    [Google Scholar]
  148. 148. 
    Walker SF, Bosch J, Gomez V, Garner TWJ, Cunningham AA et al. 2010. Factors driving pathogenicity versus prevalence of amphibian panzootic chytridiomycosis in Iberia. Ecol. Lett. 13:372–82
    [Google Scholar]
  149. 149. 
    Weldon C, du Preez LH, Hyatt AD, Muller R, Speare R. 2004. Origin of the amphibian chytrid fungus. Emerg. Infect. Dis. 10:2100–5
    [Google Scholar]
  150. 150. 
    Woodhams DC, Ardipradja K, Alford RA, Marantelli G, Reinert LK, Rollins-Smith LA. 2007. Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Anim. Conserv. 10:409–17
    [Google Scholar]
  151. 151. 
    Woodhams DC, Brandt H, Baumgartner S, Kielgast J, Kupfer E et al. 2014. Interacting symbionts and immunity in the amphibian skin mucosome predict disease risk and probiotic effectiveness. PLOS ONE 9:e96375
    [Google Scholar]
  152. 152. 
    Woodhams DC, LaBumbard BC, Barnhart KL, Becker MH, Bletz MC et al. 2018. Prodigiosin, violacein, and volatile organic compounds produced by widespread cutaneous bacteria of amphibians can inhibit two Batrachochytrium fungal pathogens. Microb. Ecol. 75:1049–62
    [Google Scholar]
  153. 153. 
    Woodhams DC, Voyles J, Lips KR, Carey C, Rollins-Smith LA. 2006. Predicted disease susceptibility in a Panamanian amphibian assemblage based on skin peptide defenses. J. Wildlife Dis. 42:207–18
    [Google Scholar]
  154. 154. 
    Zamudio KR, McDonald CA, Belasen AM. 2020. High variability in infection mechanisms and host responses: a review of functional genomic studies of amphibian chytridiomycosis. Herpetologica 76:189–200
    [Google Scholar]
  155. 155. 
    Zipkin EF, DiRenzo GV, Ray JM, Rossman S, Lips KR. 2020. Tropical snake diversity collapses after widespread amphibian loss. Science 367:814–16
    [Google Scholar]
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