, Volume 817, Issue 1, pp 267–277 | Cite as

Host–pathogen dynamics among the invasive American bullfrog (Lithobates catesbeianus) and chytrid fungus (Batrachochytrium dendrobatidis)

  • Jenny Urbina
  • Evan M. Bredeweg
  • Tiffany S. Garcia
  • Andrew R. Blaustein


The combination of introduced host species and emerging pathogens can result in unanticipated disease dynamics and novel host–pathogen interactions. The American bullfrog (Lithobates catesbeianus) is a successful invasive amphibian in the western U.S. that can act as a host to the emerging fungal pathogen, Batrachochytrium dendrobatidis (Bd) implicated in the decline of amphibian populations worldwide. We examined if wild-caught invasive bullfrogs were differentially susceptible to two regionally distinct isolates of Bd. Newly metamorphosed bullfrog individuals were exposed to either a Bd strain originally isolated from bullfrogs in their endemic range or a strain from the invaded range in the western U.S. We quantified initial infection load and compared mortality rates and changes in infection load after 30 days to determine strain-specific susceptibility. Wild-caught bullfrogs from the western U.S. were particularly susceptible to an eastern Bd strain. Although infection loads were not different between strains, individuals exposed to the western strain survived, suggesting the ability to reduce their infection. Our findings highlight differences between strains and response variation of an invasive species host.


Bullfrogs Chytrid Invasive Strains Pathogen dynamics 


  1. Balaz, V., J. Voros, P. Civis, J. Vojar, A. Hettyey, E. Sos, R. Dankovics, R. Jehle, D. G. Christiansen, F. Clare, M. Fisher, T. Garner & J. Bielby, 2014. Assessing risk and guidance on monitoring of batrachochytrium dendrobatidis in Europe through identification of taxonomic selectivity of infection. Conservation Biology 28: 213–223.CrossRefPubMedGoogle Scholar
  2. Balvanera, P., A. B. Pfisterer, N. Buchmann, J.-S. He, T. Nakashizuka, D. Raffaelli & B. Schmid, 2006. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters 9: 1146–1156.CrossRefPubMedGoogle Scholar
  3. Băncilă, R., T. Hartel, J. Plăiaşu Rodica, J. Smets & D. Cogălniceanu, 2010. Comparing three body condition indices in amphibians: a case study of yellow-bellied toad Bombina variegata. Amphibia Reptilia 31: 558–562.CrossRefGoogle Scholar
  4. Barnosky, A. D., E. A. Hadly, J. Bascompte, E. L. Berlow, J. H. Brown, M. Fortelius, W. M. Getz, J. Harte, A. Hastings, P. A. Marquet, N. D. Martinez, A. Mooers, P. Roopnarine, G. Vermeij, J. W. Williams, R. Gillespie, J. Kitzes, C. Marshall, N. Matzke, D. P. Mindell, E. Revilla & A. B. Smith, 2012. Approaching a state shift in Earth’s biosphere. Nature 486: 52–58.CrossRefPubMedGoogle Scholar
  5. Beldomenico, P. M. & M. Begon, 2010. Disease spread, susceptibility and infection intensity: vicious circles? Trends in Ecology & Evolution 25: 21–27.CrossRefGoogle Scholar
  6. Berger, L., A. A. Roberts, J. Voyles, J. E. Longcore, K. A. Murray & L. F. Skerratt, 2016. History and recent progress on chytridiomycosis in amphibians. Fungal Ecology 19: 89–99.CrossRefGoogle Scholar
  7. Berger, L., R. Speare, P. Daszak, D. E. Green, A. A. Cunningham, C. L. Goggin, R. Slocombe, M. A. Ragan, A. D. Hyatt, K. R. McDonald, H. B. Hines, K. R. Lips, G. Marantelli & H. Parkes, 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences 95: 9031–9036.CrossRefGoogle Scholar
  8. Bielby, J., M. C. Fisher, F. C. Clare, G. M. Rosa & T. W. J. Garner, 2015. Host species vary in infection probability, sub-lethal effects, and costs of immune response when exposed to an amphibian parasite. Scientific Reports 5: 10828.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Blaustein, A. R., J. M. Romansic, E. A. Scheessele, B. A. Han, A. P. Pessier & J. E. Longcore, 2005. Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conservation Biology 19: 1460–1468.CrossRefGoogle Scholar
  10. Both, C. & T. Grant, 2012. Biological invasions and the acoustic niche: the effect of bullfrog calls on the acoustic signals of white-banded tree frogs. Biology Letters 8: 714.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bowerman, J., C. Rombough, S. R. Weinstock & G. E. Padgett-Flohr, 2010. Terbinafine hydrochloride in ethanol effectively clears Batrachochytrium dendrobatidis in amphibians. Journal of Herpetological Medicine and Surgery 20: 24–28.CrossRefGoogle Scholar
  12. Boyle, D., D. Boyle, V. Olsen, J. Morgan & A. Hyatt, 2004. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of aquatic organisms 60: 141–148.CrossRefPubMedGoogle Scholar
  13. Bradley, P. W., S. S. Gervasi, J. Hua, R. D. Cothran, R. A. Relyea, D. H. Olson & A. R. Blaustein, 2015. Differences in sensitivity to the fungal pathogen Batrachochytrium dendrobatidis among amphibian populations. Conservation Biology 29: 1347–1356.CrossRefPubMedGoogle Scholar
  14. Briggs, C. J., R. A. Knapp & V. T. Vredenburg, 2010. Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences 107: 9695–9700.CrossRefGoogle Scholar
  15. Brook, B. W., N. S. Sodhi & C. J. A. Bradshaw, 2008. Synergies among extinction drivers under global change. Trends in Ecology & Evolution 23: 453–460.CrossRefGoogle Scholar
  16. Brutyn, M., K. D’Herde, M. Dhaenens, P. V. Rooij, E. Verbrugghe, A. D. Hyatt, S. Croubels, D. Deforce, R. Ducatelle, F. Haesebrouck, A. Martel & F. Pasmans, 2012. Batrachochytrium dendrobatidis zoospore secretions rapidly disturb intercellular junctions in frog skin. Fungal Genetics and Biology 49: 830–837.CrossRefPubMedGoogle Scholar
  17. Bucciarelli, G. M., A. R. Blaustein, T. S. Garcia & L. B. Kats, 2014. Invasion complexities: the diverse impacts of nonnative species on amphibians. Copeia 2014: 611–632.CrossRefGoogle Scholar
  18. Butchart, S. H. M., M. Walpole, B. Collen, A. van Strien, J. P. W. Scharlemann, R. E. A. Almond, J. E. M. Baillie, B. Bomhard, C. Brown, J. Bruno, K. E. Carpenter, G. M. Carr, J. Chanson, A. M. Chenery, J. Csirke, N. C. Davidson, F. Dentener, M. Foster, A. Galli, J. N. Galloway, P. Genovesi, R. D. Gregory, M. Hockings, V. Kapos, J.-F. Lamarque, F. Leverington, J. Loh, M. A. McGeoch, L. McRae, A. Minasyan, M. H. Morcillo, T. E. E. Oldfield, D. Pauly, S. Quader, C. Revenga, J. R. Sauer, B. Skolnik, D. Spear, D. Stanwell-Smith, S. N. Stuart, A. Symes, M. Tierney, T. D. Tyrrell, J.-C. Vié & R. Watson, 2010. Global biodiversity: indicators of recent declines. Science 328: 1164.CrossRefPubMedGoogle Scholar
  19. Crawford, A. J., K. R. Lips & E. Bermingham, 2010. Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proceedings of the National Academy of Sciences 107: 13777–13782.CrossRefGoogle Scholar
  20. D’Amore, A., E. Kirby & M. McNicholas, 2009. Invasive species shifts ontogenetic resource partitioning and microhabitat use of a threatened native amphibian. Aquatic Conservation: Marine and Freshwater Ecosystems 19: 534–541.CrossRefGoogle Scholar
  21. Daszak, P., A. A. Cunningham & A. D. Hyatt, 2000. Emerging infectious diseases of wildlife– threats to biodiversity and human health. Science 287: 443–449.CrossRefPubMedGoogle Scholar
  22. Daszak, P., A. Strieby, A. A. Cunningham, J. E. Longcore, C. C. Brown & D. Porter, 2004. Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. Herpetological Journal 14: 201–207.Google Scholar
  23. Dirzo, R., H. S. Young, M. Galetti, G. Ceballos, N. J. B. Isaac & B. Collen, 2014. Defaunation in the Anthropocene. Science 345: 401.CrossRefPubMedGoogle Scholar
  24. Doddington, B. J., J. Bosch, J. A. Oliver, N. C. Grassly, G. Garcia, B. R. Schmidt, T. W. J. Garner & M. C. Fisher, 2013. Context-dependent amphibian host population response to an invading pathogen. Ecology 94: 1795–1804.CrossRefPubMedGoogle Scholar
  25. Eskew, E. A., S. J. Worth, J. E. Foley & B. D. Todd, 2015. American bullfrogs (Lithobates catesbeianus) resist infection by multiple isolates of Batrachochytrium dendrobatidis, including one implicated in wild mass mortality. EcoHealth 12: 513–518.CrossRefPubMedGoogle Scholar
  26. Farrer, R. A., L. A. Weinert, J. Bielby, T. W. J. Garner, F. Balloux, F. Clare, J. Bosch, A. A. Cunningham, C. Weldon, L. H. du Preez, L. Anderson, S. L. K. Pond, R. Shahar-Golan, D. A. Henk & M. C. Fisher, 2011. Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proceedings of the National Academy of Sciences 108: 18732–18736.CrossRefGoogle Scholar
  27. Ficetola, G. F., C. Coïc, M. Detaint, M. Berroneau, O. Lorvelec & C. Miaud, 2007. Pattern of distribution of the American bullfrog Rana catesbeiana in Europe. Biological Invasions 9: 767–772.CrossRefGoogle Scholar
  28. Fisher, M. C., J. Bosch, Z. Yin, D. A. Stead, J. Walker, L. Selway, A. J. P. Brown, L. A. Walker, N. A. R. Gow, J. E. Stajich & T. W. J. Garner, 2009. Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Molecular Ecology 18: 415–429.CrossRefPubMedGoogle Scholar
  29. Fisher, M. C., D. A. Henk, C. J. Briggs, J. S. Brownstein, L. C. Madoff, S. L. McCraw & S. J. Gurr, 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484: 186–194.CrossRefPubMedGoogle Scholar
  30. Fites, J. S., J. P. Ramsey, W. M. Holden, S. P. Collier, D. M. Sutherland, L. K. Reinert, A. S. Gayek, T. S. Dermody, T. M. Aune, K. Oswald-Richter & L. A. Rollins-Smith, 2013. The invasive chytrid fungus of amphibians paralyzes lymphocyte responses. Science 342: 366.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Frick, W. F., J. F. Pollock, A. C. Hicks, K. E. Langwig, D. S. Reynolds, G. G. Turner, C. M. Butchkoski & T. H. Kunz, 2010. An emerging disease causes regional population collapse of a common North American bat species. Science 329: 679.CrossRefPubMedGoogle Scholar
  32. Gahl, M. K., J. E. Longcore & J. E. Houlahan, 2012. Varying responses of Northeastern North American amphibians to the chytrid pathogen Batrachochytrium dendrobatidis. Conservation Biology 26: 135–141.CrossRefPubMedGoogle Scholar
  33. Garner, T. W., M. W. Perkins, P. Govindarajulu, D. Seglie, S. Walker, A. A. Cunningham & M. C. Fisher, 2006. The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biology Letters 2: 455–459.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Garner, T. W. J., S. Walker, J. Bosch, S. Leech, J. Marcus Rowcliffe, A. A. Cunningham & M. C. Fisher, 2009. Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118: 783–791.CrossRefGoogle Scholar
  35. Gervasi, S., C. Gondhalekar, D. H. Olson & A. R. Blaustein, 2013a. Host identity matters in the amphibian-Batrachochytrium dendrobatidis system: fine-scale patterns of variation in responses to a multi-host pathogen. PLoS ONE 8: e54490.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Gervasi, S. S., J. Urbina, J. Hua, T. Chestnut, R. A. Relyea & A. R. Blaustein, 2013b. Experimental evidence for American bullfrog (Lithobates catesbeianus) susceptibility to chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 10: 166–171.CrossRefPubMedGoogle Scholar
  37. Gervasi, S. S., P. R. Stephens, J. Hua, C. L. Searle, G. Y. Xie, J. Urbina, D. H. Olson, B. A. Bancroft, V. Weis, J. I. Hammond, R. A. Relyea & A. R. Blaustein, 2017. Linking ecology and epidemiology to understand predictors of multi-host responses to an emerging pathogen, the amphibian chytrid fungus. PLOS ONE 12: e0167882.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Gold, K. K., P. D. Reed, D. A. Bemis, D. L. Miller, M. Gray & M. J. Souza, 2013. Efficacy of common disinfectants and terbinafine in inactivating the growth of Batrachochytrium dendrobatidis in culture. Diseases of aquatic organisms 107: 77–81.CrossRefPubMedGoogle Scholar
  39. Gosner, K. L., 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183–190.Google Scholar
  40. Greenspan, S. E., A. J. K. Calhoun, J. E. Longcore & M. G. Levy, 2012. Transmission of Batrachochytrium dendrobatidis to wood frogs (Lithobates sylvaticus) via a bullfrog (L. catesbeianus) vector. Journal of Wildlife Diseases 48: 575–582.CrossRefPubMedGoogle Scholar
  41. Hatcher, M. J., J. T. A. Dick & A. M. Dunn, 2012. Disease emergence and invasions. Functional Ecology 26: 1275–1287.CrossRefGoogle Scholar
  42. Huss, M., L. Huntley, V. Vredenburg, J. Johns & S. Green, 2013. Prevalence of Batrachochytrium dendrobatidis in 120 Archived Specimens of Lithobates catesbeianus (American Bullfrog) Collected in California, 1924–2007. EcoHealth 10: 339–343.CrossRefPubMedGoogle Scholar
  43. Hyatt, A. D., D. G. Boyle, V. Olsen, D. B. Boyle, L. Berger, D. Obendorf, A. Dalton, K. Kriger, M. Hero, H. Hines, R. Phillott, R. Campbell, G. Marantelli, F. Gleason & A. Colling, 2007. Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Diseases Aquatic Organisms 73: 175–192.CrossRefGoogle Scholar
  44. James, T. Y., A. P. Litvintseva, R. Vilgalys, J. A. T. Morgan, J. W. Taylor, M. C. Fisher, L. Berger, C. Weldon, L. du Preez & J. E. Longcore, 2009. Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PLOS Pathogens 5: e1000458.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kats, L. B. & R. P. Ferrer, 2003. Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Diversity and Distributions 9: 99–110.CrossRefGoogle Scholar
  46. Kiesecker, J. M. & A. R. Blaustein, 1997. Population differences in responses of Red legged frogs (Rana aurora) to introduced bullfrogs. Ecology 78: 1752–1760.CrossRefGoogle Scholar
  47. Kiesecker, J. M. & A. R. Blaustein, 1998. Effects of introduced bullfrogs and smallmouth bass on microhabitat use, growth, and survival of native red-legged frogs (Rana aurora). Conservation Biology 12: 776–787.CrossRefGoogle Scholar
  48. Kiesecker, J. M., A. R. Blaustein & C. Miller, 2001. Potential mechanisms underlying the displacement of native Red-legged frogs by introduced bullfrogs. Ecology 82: 1964–1970.CrossRefGoogle Scholar
  49. Langhammer, P. F., K. R. Lips, P. A. Burrowes, T. Tunstall, C. M. Palmer & J. P. Collins, 2013. A fungal pathogen of amphibians, Batrachochytrium dendrobatidis, attenuates in pathogenicity with in vitro passages. PLOS ONE 8: e77630.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Lever, C., 2003. Naturalized reptiles and amphibians of the world. Oxford University Press, Oxford and New York.Google Scholar
  51. Liu, X., J. R. Rohr & Y. Li, 2012. Climate, vegetation, introduced hosts and trade shape a global wildlife pandemic. Proceedings of the Royal Society B: Biological Sciences 280: 20122506.CrossRefPubMedGoogle Scholar
  52. Lorch, J. M., J. Lankton, K. Werner, E. A. Falendysz, K. McCurley & D. S. Blehert, 2015. Experimental infection of snakes with Ophidiomyces ophiodiicola causes pathological changes that typify snake fungal disease. MBio 6: 1534.CrossRefGoogle Scholar
  53. Mazzoni, R., A. A. Cunningham, P. Daszak, A. Apolo, E. Perdomo & G. Speranza, 2003. Emerging pathogen in wild amphibians and frogs (Rana catesbeiana) farmed for international trade. Emerging Infectious Diseases 9: 995–998.CrossRefPubMedPubMedCentralGoogle Scholar
  54. McConnell, T. H., 2007. The nature of disease: pathology for the health professions. Lippincott Williams & Wilkins, Baltimore.Google Scholar
  55. Medeiros, C. I., C. Both, T. Grant & S. M. Hartz, 2017. Invasion of the acoustic niche: variable responses by native species to invasive American bullfrog calls. Biological Invasions 19: 675–690.CrossRefGoogle Scholar
  56. Morehouse, E. A., T. Y. James, A. R. D. Ganley, R. Vilgalys, L. Berger, P. J. Murphy & J. E. Longcore, 2003. Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone. Molecular Ecology 12: 395–403.CrossRefPubMedGoogle Scholar
  57. Moyle, P. B., 1973. Effects of introduced bullfrogs, Rana catesbeiana, on the native frogs of the San Joaquin Valley, California. Copeia 1973: 18–22.CrossRefGoogle Scholar
  58. Naeem, S., F. Chapin III, R. Costanza, P. R. Ehrlich, F. B. Golley, D. U. Hooper, J. H. Lawton, R. V. O’Neill, H. A. Mooney & O. E. Sala, 1999. Biodiversity and ecosystem functioning: maintaining natural life support processes. Issues in ecology 4: 1–11.Google Scholar
  59. Nori, J., J. N. Urbina-Cardona, R. D. Loyola, J. N. Lescano & G. C. Leynaud, 2011. Climate change and American bullfrog invasion: what could we expect in South America? PLoS ONE 6: e25718.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Oliver, T. H., N. J. B. Isaac, T. A. August, B. A. Woodcock, D. B. Roy & J. M. Bullock, 2015. Declining resilience of ecosystem functions under biodiversity loss. Nature Communications 6: 10122.CrossRefPubMedPubMedCentralGoogle Scholar
  61. Olson, D. H., D. M. Aanensen, K. L. Ronnenberg, C. I. Powell, S. F. Walker, J. Bielby, T. W. J. Garner, G. Weaver, M. C. Fisher & The Bd Mapping Group, 2013. Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS ONE 8: e56802.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Ortiz-Santaliestra, M. E., T. A. G. Rittenhouse, T. L. Cary & W. H. Karasov, 2013. Interspecific and postmetamorphic variation in susceptibility of three North American anurans to Batrachochytrium dendrobatidis. Journal of Herpetology 47: 286–292.CrossRefGoogle Scholar
  63. Piovia-Scott, J., K. Pope, S. Joy Worth, E. B. Rosenblum, T. Poorten, J. Refsnider, L. A. Rollins-Smith, L. K. Reinert, H. L. Wells, D. Rejmanek, S. Lawler & J. Foley, 2015. Correlates of virulence in a frog-killing fungal pathogen: evidence from a California amphibian decline. ISME J 9: 1570–1578.CrossRefPubMedGoogle Scholar
  64. Poulin, R. & C. Combes, 1999. The concept of virulence: interpretations and implications. Parasitology Today 15: 474–475.CrossRefPubMedGoogle Scholar
  65. Preston, D. L., J. S. Henderson & P. T. J. Johnson, 2012. Community ecology of invasions: direct and indirect effects of multiple invasive species on aquatic communities. Ecology 93: 1254–1261.CrossRefPubMedGoogle Scholar
  66. Retallick, R. W. R. & V. Miera, 2007. Strain differences in the amphibian chytrid Batrachochytrium dendrobatidis and non-permanent, sub-lethal effects of infection. Diseases of Aquatic Organisms 75: 201–207.CrossRefPubMedGoogle Scholar
  67. Retallick, R. W. R., H. McCallum & R. Speare, 2004. Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLOS Biology 2: e351.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Rogers, C. S. & J. Miller, 2013. Coral diseases cause reef decline. Science 340: 1522.CrossRefPubMedGoogle Scholar
  69. Rosenblum, E. B., T. Y. James, K. R. Zamudio, T. J. Poorten, D. Ilut, D. Rodriguez, J. M. Eastman, K. Richards-Hrdlicka, S. Joneson, T. S. Jenkinson, J. E. Longcore, G. Parra Olea, L. F. Toledo, M. L. Arellano, E. M. Medina, S. Restrepo, S. V. Flechas, L. Berger, C. J. Briggs & J. E. Stajich, 2013. Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proceedings of the National Academy of Sciences 110: 9385–9390.CrossRefGoogle Scholar
  70. Schloegel, L. M., A. M. Picco, A. M. Kilpatrick, A. J. Davies, A. D. Hyatt & P. Daszak, 2009. Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biological Conservation 142: 1420–1426.CrossRefGoogle Scholar
  71. Schloegel, L. M., L. F. Toledo, J. E. Longcore, S. E. Greenspan, C. Vieira, M. Lee, S. Zhao, C. Wangen, C. M. Ferreira, M. Hipolito, A. J. Davies, C. A. Cuomo, P. Daszak & T. Y. James, 2012. Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology 21: 5162–5177.CrossRefPubMedGoogle Scholar
  72. Searle, C. L., S. S. Gervasi, J. Hua, J. I. Hammond, R. A. Relyea, D. H. Olson & A. R. Blaustein, 2011. Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen. Conservation Biology 25: 965–974.CrossRefPubMedGoogle Scholar
  73. Searle, C. L., G. Y. Xie & A. R. Blaustein, 2013. Development and infectious disease in hosts with complex life cycles. PLoS ONE 8: e60920.CrossRefPubMedPubMedCentralGoogle Scholar
  74. Simberloff, D. & B. Von Holle, 1999. Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions 1: 21–32.CrossRefGoogle Scholar
  75. Skerratt, L., L. Berger, R. Speare, S. Cashins, K. McDonald, A. Phillott, H. Hines & N. Kenyon, 2007. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4: 125–134.CrossRefGoogle Scholar
  76. Stuart, S. N., J. S. Chanson, N. A. Cox, B. E. Young, A. S. L. Rodrigues, D. L. Fischman & R. W. Waller, 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783–1786.CrossRefPubMedGoogle Scholar
  77. Tobler, U. & B. R. Schmidt, 2010. Within- and among-population variation in chytridiomycosis-induced mortality in the toad Alytes obstetricans. PLOS ONE 5: e10927.CrossRefPubMedPubMedCentralGoogle Scholar
  78. Tompkins, D. M., S. Carver, M. E. Jones, M. Krkošek & L. F. Skerratt, 2015. Emerging infectious diseases of wildlife: a critical perspective. Trends in Parasitology 31: 149–159.CrossRefPubMedGoogle Scholar
  79. Van Rooij, P., A. Martel, F. Haesebrouck & F. Pasmans, 2015. Amphibian chytridiomycosis: a review with focus on fungus-host interactions. Veterinary Research 46: 137.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Voyles, J., S. Young, L. Berger, C. Campbell, W. F. Voyles, A. Dinudom, D. Cook, R. Webb, R. A. Alford, L. F. Skerratt & R. Speare, 2009. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326: 582–585.CrossRefPubMedGoogle Scholar
  81. Walke, J. B., M. H. Becker, S. C. Loftus, L. L. House, T. L. Teotonio, K. P. C. Minbiole & L. K. Belden, 2015. Community structure and function of amphibian skin microbes: an experiment with bullfrogs exposed to a chytrid fungus. PLoS One 10: 1–18.CrossRefGoogle Scholar
  82. Xie, G. Y., D. H. Olson & A. R. Blaustein, 2016. Projecting the global distribution of the emerging amphibian fungal pathogen, Batrachochytrium dendrobatidis, based on IPCC climate futures. PLoS One 11: e0160746.CrossRefPubMedPubMedCentralGoogle Scholar
  83. Young, S., P. Whitehorn, L. Berger, L. F. Skerratt, R. Speare, S. Garland & R. Webb, 2014. Defects in host immune function in tree frogs with chronic chytridiomycosis. PLoS One 9: e107284.CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Environmental Sciences Graduate ProgramOregon State UniversityCorvallisUSA
  2. 2.Department of Fisheries and WildlifeOregon State UniversityCorvallisUSA
  3. 3.Department of Integrative BiologyOregon State UniversityCorvallisUSA

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