Volume 19, Number 3—March 2013
Parallels in Amphibian and Bat Declines from Pathogenic Fungi
|Area of knowledge||B. dendrobatidis
|Current knowledge||Unresolved research questions||Current knowledge||Unresolved research questions|
|Disease emergence||Multiple regions of endemism and 1 widely introduced hypervirulent lineage (7–9)||How and from where did the hypervirulent lineage emerge?||Limited genetic differentiation in North America (10)||How do strains from North America and Europe compare genetically, and is genetic variation greater in Europe, suggesting historic endemism?|
|Possibly endemic to Europe and introduced to North America (6,11,12)
||Can survive in water and soil (13,14)
||Can B. dendrobatidis form desiccation-resistant resting spores? Can B. dendrobatidis survive and reproduce as a saprophytic, nonparasitic form?
||Apparent persistence in soils and on cave walls (12,15)
||How widespread is G. destructans in the environment? Can G. destructans survive and reproduce as a saprophytic, nonparasitic form?
|Biotic reservoirs||Host generalist pathogen of amphibians (4,5)||Can B. dendrobatidis complete its life cycle on other vertebrate hosts?||Host generalist pathogen of bats (6)||Can G. destructans infect or persist on other vertebrates?|
|Can also infect reptiles, nematodes, and waterfowl (16–18)
|Life history and infection risk of the host
||Aquatic, biphasic, tropical amphibian species at greatest risk for chytridiomycosis (19)
||To what extent can life history characteristics of the host predict global patterns of disease-related population decline among amphibian species?
||Bat species that hibernate experience most deaths from WNS (20)
||Are only those species that hibernate susceptible to population decline from WNS? What role does life history of the host play in predicting species declines and extinctions from WNS?
|Host–pathogen interactions||Antimicrobial peptides and antifungal metabolites from skin-associated bacteria contribute to B. dendrobatidis resistance (21)||What is the immune response of B. dendrobatidis–tolerant hosts to infection?||Host immune down-regulation during hibernation probably important to WNS progression (24)||What is the host immune response to G. destructans infection?|
|Susceptible species appear to show little innate or adaptive immune response to B. dendrobatidis infection (22,23)||Does B. dendrobatidis evade the amphibian immune system through activity of secreted proteases?||How does host immunity vary seasonally? What role does immune function play in the observed winter season/hibernation mortality from WNS? Do proteases contribute to pathogenicity of G. destructans?|
*WNS, white-nose syndrome.
- Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol. 2004;19:535–44.
- Desprez-Loustau M-L, Robin C, Buée M, Courtecuisse R, Garbaye J, Suffert F, The fungal dimension of biological invasions. Trends Ecol Evol. 2007;22:472–80.
- Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Emerging fungal threats to animal, plant and ecosystem health. Nature. 2012;484:186–94.
- Fisher MC, Garner TWJ, Walker SF. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu Rev Microbiol. 2009;63:291–310 .
- Kilpatrick AM, Briggs CJ, Daszak P. The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol Evol. 2010;25:109–18.
- Puechmaille SJ, Frick WF, Kunz TH, Racey PA, Voigt CC, Wibbelt G, White-nose syndrome: is this emerging disease a threat to European bats? Trends Ecol Evol. 2011;26:570–6 .
- Goka K, Yokoyama J, Une Y, Kuroki T, Suzuki K, Nakahara M, Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan. Mol Ecol. 2009;18:4757–74.
- Bai C, Liu X, Fisher MC, Garner TWJ, Li Y. Global and endemic Asian lineages of the emerging pathogenic fungus Batrachochytrium dendrobatidis widely infect amphibians in China. Divers Distrib. 2012;18:307–18.
- Farrer RA, Weinert LA, Bielby J, Garner TWJ, Balloux F, Clare F, Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc Natl Acad Sci U S A. 2011;108:18732–6.
- Ren P, Haman KH, Last LA, Rajkumar SS, Keel MK, Chaturvedi V. Clonal spread of Geoymces destructans among bats, midwestern and southern United States. Emerg Infect Dis. 2012;18:883–5.
- Wibbelt G, Kurth A, Hellmann D, Weishaar M, Barlow A, Veith M, White-nose syndrome fungus (Geomyces destructans) in bats, Europe. Emerg Infect Dis. 2010;16:1237–43.
- Puechmaille SJ, Wibbelt G, Korn V, Fuller H, Forget F, Mühldorfer K, Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS ONE. 2011;6:e19167.
- Johnson ML, Speare R. Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerg Infect Dis. 2003;9:922–5.
- Johnson ML, Speare R. Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Dis Aquat Organ. 2005;65:181–6.
- Lindner DL, Gargas A, Lorch JM, Banik MT, Glaeser J, Kunz TH, DNA-based detection of the fungal pathogen Geomyces destructans in soils from bat hibernacula. Mycologia. 2011;103:241–6.
- Kilburn VL, Ibáñez R, Green DM. Reptiles as potential vectors and hosts of the amphibian pathogen Batrachochytrium dendrobatidis in Panama. Dis Aquat Organ. 2011;97:127–34.
- Shapard EJ, Moss AS, San Francisco MJ. Batrachochytrium dendrobatidis can infect and cause mortality in the nematode Caenorhabditis elegans. Mycopathologia. 2012;173:121–6.
- Garmyn A, Van Rooij P, Pasmans F, Hellebuyck T, Van Den Broeck W, Haesebrouck F, Waterfowl: potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis. PLoS ONE. 2012;7:e35038.
- Lips KR, Reeve JD, Witters LR. Ecological traits predicting amphibian population declines in Central America. Conserv Biol. 2003;17:1078–88.
- Foley J, Clifford D, Castle K, Cryan P, Ostfeld RS. Investigating and managing the rapid emergence of white-nose syndrome, a novel, fatal, infectious disease of hibernating bats. Conserv Biol. 2011;25:223–31 .
- Rollins-Smith LA, Ramsey JP, Pask JD, Reinert LK, Woodhams DC. Amphibian immune defenses against chytridiomycosis: impacts of changing environments. Integr Comp Biol. 2011;51:552–62.
- Rosenblum EB, Poorten TJ, Settles M, Murdoch GK. Only skin deep: shared genetic response to the deadly chytrid fungus in susceptible frog species. Mol Ecol. 2012;21:3110–20.
- Ribas L, Li M-S, Doddington BJ, Robert J, Seidel JA, Kroll JS, Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis. PLoS ONE. 2009;4:e8408.
- Cryan PM, Meteyer CU, Boyles JG, Blehert DS. Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. BMC Biol. 2010;8:135.
- Rachowicz LJ, Hero J-M, Alford RA, Taylor JW, Morgan JAT, Vredenburg VT, The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conserv Biol. 2005;19:1441–8.
- Weldon C, du Preez LH, Hyatt AD, Muller R, Speare R. Origin of the amphibian chytrid fungus. Emerg Infect Dis. 2004;10:2100–5.
- Fisher MC, Farrer RA. Outbreaks and the emergence of novel fungal infections: lessons from the panzootic of amphibian chytridiomycosis. The Journal of Invasive Fungal Infections. 2011;5:73–81.
- Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misra V, Cryan PM, Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Natl Acad Sci U S A. 2012;109:6999–7003.
- de Castro F, Bolker B. Mechanisms of disease-induced extinction. Ecol Lett. 2005;8:117–26.
- Mitchell KM, Churcher TS, Garner TWJ, Fisher MC. Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction. Proc Biol Sci. 2008;275:329–34.
- Casadevall A. Fungal virulence, vertebrate endothermy, and dinosaur extinction: is there a connection? Fungal Genet Biol. 2005;42:98–106.
- Powell MJ. Looking at mycology with a Janus face: a glimpse at Chytridiomycetes active in the environment. Mycologia. 1993;85:1–20.
- Di Rosa I, Simoncelli F, Fagotti A, Pascolini R. The proximate cause of frog declines? Nature. 2007;447:E4–5.
- Chaturvedi V, Springer DJ, Behr MJ, Ramani R, Li X, Peck MK, Morphological and molecular characterizations of psychrophilic fungus Geomyces destructans from New York bats with white nose syndrome (WNS). PLoS ONE. 2010;5:e10783.
- Todd BD. Parasites lost? An overlooked hypothesis for the evolution of alternative reproductive strategies in amphibians. Am Nat. 2007;170:793–9.
- Ramsey JP, Reinert LK, Harper LK, Woodhams DC, Rollins-Smith LA. Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis. Infect Immun. 2010;78:3981–92.
- Joneson S, Stajich JE, Shiu S-H, Rosenblum EB. Genomic transition to pathogenicity in chytrid fungi. PLoS Pathog. 2011;7:e1002338.
- Clark RW, Marchand MN, Clifford BJ, Stechert R, Stephens S. Decline of an isolated timber rattlesnake (Crotalus horridus) population: interactions between climate change, disease, and loss of genetic diversity. Biol Conserv. 2011;144:886–91.
- Robert VA, Casadevall A. Vertebrate endothermy restricts most fungi as potential pathogens. J Infect Dis. 2009;200:1623–6.
- Garcia-Solache MA, Casadevall A. Global warming will bring new fungal diseases for mammals. MBio. 2010;1:e00061–10.
1Both authors contributed equally to this article.