Abstract
The amphibian fungal disease chytridiomycosis is considered one of the greatest threats to biodiversity. This lethal skin disease is caused by chytridiomycete fungi belonging to the genus Batrachochytrium. Although sudden amphibian population declines had occurred since the 1970s in the Americas and Australia, mass mortalities were not observed until the 1990s. The fungus Batrachochytrium dendrobatidis (Bd) was identified as the cause of these declines. It is estimated that Bd has caused the rapid decline or extinction of at least 200 amphibian species, which is probably an underestimation due to the cryptic behaviour of many amphibians such as many salamanders and also the lack of monitoring. A second chytrid species, B. salamandrivorans (Bsal), has recently emerged and caused mass mortality in salamanders in Belgium, the Netherlands and Germany, affecting most salamander and newt taxa in the amphibian community and is considered a major threat to the western Palearctic amphibian biodiversity. In this chapter we review the epidemiology, host pathogen interactions and mitigation strategies of both chytrid pathogens.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Abramyan J, Stajich JE (2012) Species-specific chitin binding module 18 expansion in the amphibian pathogen Batrachochytrium dendrobatidis. MBio 3:e00150–e00112
Annis SL, Dastoor FP, Ziel H et al (2004) A DNA-based assay identifies Batrachochytrium dendrobatidis in amphibians. J Wildl Dis 40:420–428
Bataille A, Cashins SD, Grogan L et al (2015) Susceptibility of amphibians to chytridiomycosis is associated with MHC class II conformation. Proc Biol Sci 22:282
Beard KH, O’Neill EM (2005) Infection of an invasive frog Eleutherodactylus coqui by the chytrid fungus Batrachochytrium dendrobatidis in Hawaii. Biol Conserv 126:591–595
Becker MH, Brucker RM, Schwantes CR et al (2009) The bacterially produced metabolite violacein is associated with survival of amphibians infected with a lethal fungus. Appl Environ Microbiol 75:6635–6638
Berger L, Skerratt L (2012) Disease strategy chytridiomycosis (infection with Batrachochytrium dendrobatidis) Version 1, 2012. Department of Sustainability, Environment, Water, Populations and Communities, Public Affairs, Commonwealth of Australia, Canberra. Available at: http://www.environment.gov.au/system/files/resources/387d3e66-3cdc-4676-8fed-759328277da4/files/chytrid-fungus-manual.pdf
Berger L, Speare R, Daszak P et al (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci U S A 95:9031–9036
Berger L, Speare R, Kent A (2000) Diagnosis of chytridiomycosis in amphibians by histological examination. Zoos Print J 15:184–190
Berger L, Hyatt AD, Olsen V et al (2002) Production of polyclonal antibodies to Batrachochytrium dendrobatidis and their use in an immunoperoxidase test for chytridiomycosis in amphibians. Dis Aquat Org 48:213–220
Berger L, Speare R, Hines HB et al (2004) Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Aust Vet J 82:434–439
Berger L, Hyatt AD, Speare R et al (2005) Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Dis Aquat Org 68:51–63
Berger L, Longcore J, Speare R, Hyatt A, Skerratt LF (2009) Fungal diseases in amphibians. In: Heatwole H, Wilkinson JW (eds) Amphibian biology, volume 8 amphibian decline: disease, parasites, maladies, and pollution. Surrey Beatty and Sons, Baulkham Hills, NSW, pp 2986–3052
Blaustein AR, Romansic JM, Scheessele EA et al (2005) Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conserv Biol 19:1460–1146
Blooi M, Pasmans F, Longcore JE et al (2013) Duplex real-time PCR for rapid simultaneous detection of Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans in amphibian samples. J Clin Microbiol 51:4173–4177
Blooi M, Martel A, Haesebrouck F et al (2015a) Treatment of urodelans based on temperature dependent infection dynamics of Batrachochytrium salamandrivorans. Sci Rep 5:8037
Blooi M, Pasmans F, Rouffaer L et al (2015b) Succesful treatment of Batrachochytrium salamandrivorans infections in salamanders requires synergy between voriconazole, polymyxin E and temperature. Sci Rep 5:11788
Blooi M, Pasmans F, Longcore JE et al (2016) Duplex real-time PCR for rapid simultaneous detection of Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans in amphibian samples. J Clin Microbiol 54:246–246
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 97:331–337
Bosch J, Sanchez-Tome E, Fernandez-Loras A et al (2015) Successful elimination of a lethal wildlife infectious disease in nature. Biol Lett 11(11):20150874
Boyle DG, Boyle DB, Olsen V et al (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Org 60:141–148
Brannelly LA, Richards-Zawacki CL et al (2012) Clinical trials with itraconazole as a treatment for chytrid fungal infections in amphibians. Dis Aquat Org 101:95–104
Brannelly LA, Hunter DA, Skerratt LF et al (2015) Chytrid infection and post-release fitness in the reintroduction of an endangered alpine tree frog. Anim Conserv 19(2):153–162. https://doi.org/10.1111/acv.12230
Brucker RM, Harris RN, Schwantes CR et al (2008) Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J Chem Ecol 34:1422–1429
Brutyn M, D’Herde K, Dhaenens M et al (2012) Batrachochytrium dendrobatidis zoospore secretions rapidly disturb intercellular junctions in frog skin. Fungal Genet Biol 49:830–837
Campbell CR, Voyles J, Cook DI et al (2012) Frog skin epithelium: electrolyte transport and chytridiomycosis. Int J Biochem Cell Biol 44:431–434
Cashins SD, Grogan LF, McFadden M et al (2013) Prior infection does not improve survival against the amphibian disease Chytridiomycosis. PLoS One 8:e56747
Chatfield MWH, Richards-Zawacki CL (2011) Elevated temperature as a treatment for Batrachochytrium dendrobatidis infection in captive frogs. Dis Aquat Org 94:235–238
Cheng TL, Rovito SM, Wake DB et al (2011) Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proc Natl Acad Sci U S A 108:9502–9507
Cunningham AA, Beckmann K, Perkins M et al (2015) Surveillance emerging disease in UK amphibians. Vet Rec 176:468–468
Daskin JH, Alford RA, Puschendorf R (2011) Short-term exposure to warm microhabitats could explain amphibian persistence with Batrachochytrium dendrobatidis. PLoS One 6:e26215
Davis AK, Keel MK, Ferreira A et al (2010) Effects of chytridiomycosis on circulating white blood cell distributions of bullfrog larvae (Rana catesbeiana). Comp Clin Pathol 19:49–55
Doddington BJ, Bosch J, Oliver JA et al (2013) Context dependent amphibian host population response to an invading pathogen. Ecology 94:1795–1804
Duellman WE, Trueb L (1994) Biology of amphibians. The Johns Hopkins University Press, Baltimore
Duffus ALJ (2009) Chytrid blinders: what other disease risks to amphibians are we missing? EcoHealth 6:335–339
Ellison AR, Savage AE, DiRenzo GV et al (2014) Fighting a losing battle: vigorous immune response countered by pathogen suppression of host defenses in the chytridiomycosis-susceptible frog Atelopus zeteki. G3 (Bethesda) 4:1275–1289
Ellison AR et al (2015) More than skin deep: functional genomic basis for resistance to amphibian chytridiomycosis. Genome Biol Evol 7:286–298. https://doi.org/10.1093/gbe/evu285
Farrer RA, Weinert LA, Bielby J et al (2011) Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc Natl Acad Sci U S A 108:18732–18736
Farrer RA, Henk DA, Garner TWJ et al (2013) Chromosomal copy number variation, selection and uneven rates of recombination reveal cryptic genome diversity linked to pathogenicity. PLoS Genet 9(8):e1003703
Fellers GM, Green DE, Longcore JE (2001) Oral chytridiomycosis in the mountain yellow-legged frog (Rana muscosa). Copeia 2001:945–953
Fisher MC, Garner TWJ, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu Rev Microbiol 63:291–310
Fites JS, Ramsey JP, Holden WM et al (2013) The invasive chytrid fungus of amphibians paralyzes lymphocyte responses. Science 342:366–369
Fites JS, Reinert LK, Chappell TM et al (2014) Inhibition of local immune responses by the frog-killing fungus Batrachochytrium dendrobatidis. Infect Immun 82:4698–4706
Fong JJ, Cheng TL, Bataille A et al (2015) Early 1900s detection of Batrachochytrium dendrobatidis in Korean amphibians. PLoS One 10(3):e0115656
Forzan MJ, Gunn H, Scott P (2008) Chytridiomycosis in an aquarium collection of frogs: diagnosis, treatment, and control. J Zoo Wildl Med 39:406–411
Garland S, Wood J, Skerratt LF (2011) Comparison of sensitivity between real-time detection of a TaqMan assay for Batrachochytrium dendrobatidis and conventional detection. Dis Aquat Organ 94:101–105
Garner TW, Perkins MW, Govindarajulu P et al (2006) The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the north American bullfrog, Rana catesbeiana. Biol Lett 2:455–459
Garner TW, Garcia G, Carroll B et al (2009) Using itraconazole to clear Batrachochytrium dendrobatidis infection, and subsequent depigmentation of Alytes muletensis tadpoles. Dis Aquat Organ 83:257–260
Geiger CC, Kupfer E, Schar S et al (2011) Elevated temperature clears chytrid fungus infections from tadpoles of the midwife toad, Alytes obstetricans. Amphibia-Reptilia 32:276–280
Georoff TA, Moore RP, Rodriguez C et al (2013) Efficacy of treatment and long-term follow-up of Batrachochytrium dendrobatidis PCR-positive anurans following itraconazole bath treatment. J Zoo Wildl Med 44:395–403
Goka K, Yokoyama J, Une Y et al (2009) Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan. Mol Ecol 18(23):4757–4774
Grant EHG, Muths E, Katz RA, et al (2016) Salamander chytrid fungus (Batrachochytrium salamandrivorans) in the United States—Developing research, monitoring, and management strategies. USGS Report https://doi.org/10.3133/ofr20151233
Greenspan SE, Longcore JE, Calhoun AJ (2012) Host invasion by Batrachochytrium dendrobatidis: fungal and epidermal ultrastructure in model anurans. Dis Aquat Org 100:201–210
Grogan LF (2014) Understanding host and environmental factors in the immunology and epidemiology of chytridiomycosis in anuran populations in Australia. PhD thesis, James Cook University
Grogan LF, Berger L, Rose K et al (2014) Surveillance for emerging biodiversity diseases of wildlife. PLoS Pathog 10:1–4
Harding KC, Hansen BJL, Goodman SJ (2005) Acquired immunity and stochasticity in epidemic intervals impede the evolution of host disease resistance. Am Nat 166:722–730
Harris RN, Lauer A, Simon MA et al (2009a) Addition of antifungal skin bacteria to salamanders ameliorates the effects of chytridiomycosis. Dis Aquat Org 83:11–16
Harris RN, Brucker RM, Walke JB et al (2009b) Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J 3:818–824
Heard GW, Thomas CD, Hodgson JA et al (2015) Refugia and connectivity sustain amphibian metapopulations afflicted by disease. Ecol Lett 18:853–863
Heringstad B, Klemetsdal G, Steine T (2007) Selection responses for disease resistance in two selection experiments with Norwegian red cows. J Dairy Sci 90:2419–2426
Hudson PJ, Dobson AP (1998) In: Grenfell BT, Dobson AP (eds) Ecology of infectious diseases in natural populations. Cambridge University Press, Cambridge
Hunter D, Osborne W, Marantelli G et al (1999) Implementation of a population augmentation project for remnant populations of the southern corroboree frog (Pseudophryne corroboree). In: Campbell A (ed) Declines and disappearances of Australian frogs. Environment Australia, Canberra
Hyatt AD, Boyle DG, Olsen V et al (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Dis Aquat Org 73:175–192
James TY, Kauf F, Schoch CL et al (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443:818–822
Johnson ML, Berger L, Philips L et al (2003) Fungicidal effects of chemical disinfectans, UV light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis. Dis Aquat Org 57:255–260
Johnson PTJ, Hoverman JT (2014) Heterogeneous hosts: how variation in host size, behaviour and immunity affects parasite aggregation. J Anim Ecol 83:1103–1112
Jones ME, Paddock D, Bender L et al (2012) Treatment of chytridiomycosis with reduced-dose itraconazole. Dis Aquat Org 99:243–249
Joneson S, Stajich JE, Shiu SH et al (2011) Genomic transition to pathogenicity in Chytrid fungi. PLoS Pathog 7:e1002338
Kindermann C, Narayan EJ, Hero JM (2012) Urinary corticosterone metabolites and chytridiomycosis disease prevalence in a free-living population of male Stony Creek frogs (Litoria wilcoxii). Comp Biochem Physiol A 162:171–176
Kolby JE, Smith KM, Berger L et al (2014) First evidence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) and ranavirus in Hong Kong amphibian trade. PLoS One 9:e90750
Kriger KM, Hines HB, Hyatt AD et al (2006) Techniques for detecting chytridiomycosis in wild frogs: comparing histology with real-time Taqman PCR. Dis Aquat Org 71:141–148
La Marca E, Lips KR, Lötters S et al (2005) Catastrophic population declines and extinctions in Neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica 37:190–201
Lam BA, Walke JB, Vredenburg VT et al (2010) Proportion of individuals with anti-Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa. Biol Conserv 143:529–531
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
Lauer A et al (2007) Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia 3:630–640
Lips KR, Brem F, Brenes R et al (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci U S A 103:3165–3170
Lips KR, Diffendorfer J, Mendelson JR et al (2008) Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biol 6:e72
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
Longcore J, Pessier A, Nichols D (1999) Batrachochytrium dendrobatidis gen et sp nov, a chytrid pathogenic to amphibians. Mycologia 91:219–227
Loudon AH, Holland JA, Umile TP et al (2014) Interactions between amphibians’ symbiotic bacteria cause the production of emergent anti-fungal metabolites. Front Microbiol 5:441
Marantelli G, Berger L, Speare R et al (2004) Distribution of the amphibian chytrid Batrachochytrium dendrobatidis and keratin during tadpole development. Pac Conserv Biol 10:173–179
Martel A, Van Rooij P, Vercauteren G et al (2011) Developing a safe antifungal treatment protocol to eliminate Batrachochytrium dendrobatidis from amphibians. Med Mycol 49:143–149
Martel A, Spitzen-van der Sluijs A, Blooi M et al (2013) Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proc Natl Acad Sci U S A 110:15325–15329
Martel A, Blooi M, Adriaensen C et al (2014) Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346:630–631
McFadden M, Hobbs R, Marantelli G et al (2013) Captive management and breeding of the critically endangered southern corroboree frog (Pseudophryne corroboree) (Moore 1953) at Taronga and Melbourne zoos. Amphib Reptile Conserv 5:70–87
McMahon TA, Rohr JR (2015) Transition of chytrid dungus infection from mouthparts to hind limbs during amphibian metamorphosis. EcoHealth 12:88–193
McMahon TA, Brannelly LA, Chatfield MWH et al (2013) Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in absence of infection. Proc Natl Acad Sci U S A 110:210–215
McMahon TA, Sears BF, Venesky MD et al (2014) Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature 511:224–227
Meng P, Yang S, Shen C et al (2013) The first salamander defensing antimicrobial peptide. PLoS One 8:e83044
Meyer W, Seegers U, Schnapper A et al (2007) Possible antimicrobial defense by free sugars on the epidermal surface of aquatic vertebrates. Aquat Biol 1:167–175
Miedaner T, Korzun V (2012) Marker-assisted selection for disease resistance in wheat and barley breeding. Phytopathology 102:560–566
Moss AS, Reddy NS, Dortaj IM et al (2008) Chemotaxis of the amphibian pathogen Batrachochytrium dendrobatidis and its response to a variety of attractants. Mycologia 100:1–5
Muletz CR, Myers JM, Domangue RJ et al (2012) Soil bioaugmentation with amphibian cutaneous bacteria protects amphibian hosts from infection by Batrachochytrium dendrobatidis. Biol Conserv 152:119–126
Murphy PJ, St-Hilaire S, Corn PS (2011) Temperature, hydric environment, and prior pathogen exposure alter the experimental severity of chytridiomycosis in boreal toads. Dis Aquat Org 95:31–42
Murray KA, Skerratt LF, Garland S et al (2013) Whether the weather drives patterns of endemic amphibian chytridiomycosis: a pathogen proliferation approach. PLoS One 8(4):e61061
Myers JM, Ramsey JP, Blackman AL et al (2012) Synergistic inhibition of the lethal fungal pathogen Batrachochytrium dendrobatidis: the combined effect of symbiotic bacterial metabolites and antimicrobial peptides of the frog Rana muscosa. J Chem Ecol 38:958–965
Newell DA, Goldingay RL, Brooks LO (2013) Population recovery following decline in an endangered stream-breeding frog (Mixophyes fleayi) from subtropical Australia. PLoS One 8:e58559
Nichols DK, Lamirande EW, Pessier AP et al (2000) Experimental transmission and treatment of cutaneous chytridiomycosis in poison dart frogs (Dendrobates auratus and Dendrobates tinctorius). In: Proceedings of the Joint Conference of American Association of Zoo Veterinarians and International Association for Aquatic Animal Medicine, pp 42–44
Nichols DK, Lamirande EW, Pessier AP et al (2001) Experimental transmission of cutaneous chytridiomycosis in dendrobatid frogs. J Wildl Dis 37:1–11
Olson DH, Aanensen DM, Ronnenberg KL et al (2013) Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS One 8:e56802
Parris MJ, Beaudoin JG (2004) Chytridiomycosis impacts predator-prey interactions in larval amphibian communities. Oecologia 140:626–632
Pask JD, Cary TL, Rollins-Smith LA (2013) Skin peptides protect juvenile leopard frogs (Rana pipiens) against chytridiomycosis. J Exp Biol 216:2908–2916
Pasmans F, Van Rooij P, Blooi M et al (2013) Resistance to chytridiomycosis in European plethodontid salamanders of the genus Speleomantes. PLoS One 8:e63639
Pessier AP, Mendelson JR (2010) A manual for control of infectious diseases in amphibian survival assurance colonies and reintroduction programs. IUCN/SSC Conservation Breeding Specialist Group
Pessier AP, Nichols DK, Longcore JE et al (1999) Cutaneous chytridiomycosis in poison dart frogs (Dendrobates spp.) and White's tree frogs (Litoria caerulea). J Vet Diagn Investig 11:194–199
Peterson JD, Steffen JE, Reinert LK et al (2013) Host stress response is important for the pathogenesis of the deadly amphibian disease, chytridiomycosis, in Litoria caerulea. PLoS One 8:e62146
Phillott AD, Speare R, Hines HB et al (2010) Minimising exposure of amphibians to pathogens during field studies. Dis Aquat Org 92:175–185
Phillott AD, Grogan LF, Cashins SD et al (2013) Chytridiomycosis and seasonal mortality of tropical stream-associated frogs 15 years after introduction of Batrachochytrium dendrobatidis. Conserv Biol 27:1058–1068
Pilliod DS, Muths E, Scherer RD et al (2010) Effects of amphibian chytrid fungus on individual survival probability in wild boreal toads. Conserv Biol 24:1259–1267
Plehn M (1920) Neue Parasiten in Haut and Kiemen von Fischen. Ichthyochytrium und Mucophilus Zentralblatt für Bakteriologie und Parasitenkunde Abteilung, vol 1, pp 275–281
Puschendorf R, Hoskin CJ, Cashins SD et al (2011) Environmental refuge from disease-driven amphibian extinction. Conserv Biol 25:956–964
Rachowicz LJ, Vredenburg VT (2004) Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Dis Aquat Org 61:75–83
Ramsey JP, Reinert LK, Harper LK et al (2010) Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the south African clawed frog, Xenopus laevis. Infect Immun 78:3981–3992
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
Retallick RWR, McCallum H, Speare R (2004) Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLoS Biol 2:1965–1971
Ribas L, Li MS, Doddington BJ, Robert J et al (2009) Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis. PLoS One 4:e8408
Ricardo H (2006) Distribution and ecology of chytrid in Tasmania. Honours thesis, University of Tasmania
Richards-Zawacki CL (2010) Thermoregulatory behaviour affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs. Proc R Soc Lond B Biol Sci 277:519–528
Rivas LR (1964) A reinterpretation of the concepts “sympatric” and “allopatric” with proposal of the additional terms “syntopic” and “allotopic”. Syst Zool 13:42–43
Rodriguez D, Becker CG, Pupin NC et al (2014) Long-term endemism of two highly divergent lineages of the amphibian-killing fungus in the Atlantic Forest of Brazil. Mol Ecol 23:774–787
Rollins-Smith LA (2009) The role of amphibian antimicrobial peptides in protection of amphibians from pathogens linked to global amphibian declines. Biochim Biophys Acta 1788:1593–1599
Rollins-Smith LA, Woodhams DC, Reinert LK et al (2006) Antimicrobial peptide defenses of the mountain yellow-legged frog (Rana muscosa). Dev Comp Immunol 30:831–842
Rollins-Smith LA, Ramsey JP, Pask JD et al (2011) Amphibian immune defenses against chytridiomycosis: impacts of changing environments. Integr Comp Biol 51:552–562
Rosenblum EB, Stajich JE, Maddox N et al (2008) Global gene expression profiles for life stages of the deadly amphibian pathogen Batrachochytrium dendrobatidis. Proc Natl Acad Sci U S A 105:17034–17039
Rosenblum EB, Poorten TJ, Settles M et al (2009) Genome-wide transcriptional response of Silurana (Xenopus) tropicalis to infection with the deadly chytrid fungus. PLoS One 4:e6494
Rosenblum EB, Poorten TJ, Settles M et al (2012) Only skin deep: shared genetic response to the deadly chytrid fungus in susceptible frog species. Mol Ecol 21:3110–3120
Rosenblum EB, James TY, Zamudio KR et al (2013) Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proc Natl Acad Sci U S A 110:9385–9390
Rovito SM, Parra-Olea G, Vasquez-Almazan CR et al (2009) Dramatic declines in neotropical salamander populations are an important part of the global amphibian crisis. Proc Natl Acad Sci U S A 106:3231–3236
Rowley JJL, Alford RA (2007) Behaviour of Australian rain forest stream frogs may affect the transmission of chytridiomycosis. Dis Aquat Org 77:1–9
Rowley JJL, Skerratt LF, Alford RA et al (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
Sabino-Pinto JS, Bletz M, Hendrix R et al (2015) First detection of the emerging fungal pathogen in Batrachochytrium salamandrivorans in Germany. Amphibia-Reptilia 36(4):411–416. https://doi.org/10.1163/15685381-00003008
Savage AE, Zamudio KR (2011) MHC genotypes associate with resistance to a frog-killing fungus. Proc Natl Acad Sci U S A 108:16705–16710
Scheele BC, Guarino F, Osbourne W et al (2014) Decline and re-expansion of an amphibian with high prevalence of chytrid fungus. Biol Conserv 170:86–91
Scheele BC, Hunter DA, Skerratt LF et al (2015) Low impact of chytridiomycosis on frog recruitment enables persistence in refuges despite high adult mortality. Biol Conserv 182:36–43
Schloegel LM, Ferreira CM, James TY et al (2010) The north American bullfrog as a reservoir for the spread of Batrachochytrium dendrobatidis in Brazil. Anim Conserv 13:53–61
Schloegel LM, Toledo LF, Longcore JE et al (2012) Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Mol Ecol 21:5162–5177
Schmeller DS, Blooi M, Martel A et al (2014) Microscopic aquatic predatorsstrongly affect infection dynamics of a globally emerged pathogen. Curr Biol 24:176–180
Searle CL, Gervasi SS, Hua J et al (2011) Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen. Conserv Biol 25:965–974
Sheafor B, Davidson EW, Parr L et al (2008) Antimicrobial peptide defenses in the salamander Ambystoma tigrinum, against emerging amphibian pathogens. J Wildl Dis 44:226–236
Skerratt L, Speare R, Berger L (2011a) Mitigating the impact of diseases affecting biodiversity—retrospective on the outbreak investigation for chytridiomycosis. Ecohealth 7:S26
Skerratt LF, Berger L, Hines HB et al (2008) Survey protocol for detecting chytridiomycosis in all Australian frog populations. Dis Aquat Org 80:85–94
Skerratt LF, Mendez D, McDonald KR et al (2011b) Validation of diagnostic tests in wildlife: the case of chytridiomycosis in wild amphibians. J Herpetol 45:444–450
Skerratt LF, Berger L, Clemann N et al (2016) Priorities for management of chytridiomycosis in Australia: saving frogs from extinction. Wildlife Res 43(2):105–120
Smith KG, Weldon C, Conradie W et al (2007) Relationships among size, development, and Batrachochytrium dendrobatidis infection in African tadpoles. Dis Aquat Organ 74:159–164
Soto-Azat C, Clarke BT, Poynton JC (2010) Widespread historical presence of Batrachochytrium dendrobatidis in African pipid frogs. Divers Distrib 16:126–131
Stice MJ, Briggs CJ (2010) Immunization is ineffective at preventing infection and mortality due to the amphibian chytrid fungus Batrachochytrium dendrobatidis. J Wildl Dis 46:70–77
Stockwell MP, Clulow J, Mahony MJ (2015a) Evidence of a salt refuge: chytrid infection loads are suppressed in hosts exposed to salt. Oecologia 177:901–910
Stockwell MP, Storrie LJ, Pollard CJ et al (2015b) Effects of pond salinization on survival rate of amphibian hosts infected with the chytrid fungus. Conserv Biol 29:391–399
Swei A, Rowley JJL, Rodder D et al (2011) Is chytridiomycosis an emerging infectious disease in Asia? PLoS One 6(8):e23179
Talley BL, Muletz CR, Vredenburg VT et al (2015) A century of Batrachochytrium dendrobatidis in Illinois amphibians (1888–1989). Biol Conserv 182:254–261
Tamukai K, Une Y, Tominaga A et al (2011) Treatment of spontaneous chytridiomycosis in captive amphibians using itraconazole. J Vet Med Sci 73:155–159
Tennessen JA, Woodhams DC, Chaurand P et al (2009) Variations in the expresses antimicrobial peptide repertoire of northern leopard frog (Rana pipiens) populations suggest intraspecies differences in resistance to pathogens. Dev Comp Immunol 33:1247–1257
Thekkiniath JC, Zabet-Moghaddam M, San Francisco SK et al (2013) A novel subtilisin-like serine protease of Batrachochytrium dendrobatidis is induced by thyroid hormone and degrades antimicrobial peptides. Fungal Biol 117:451–461
Tobler U, Schmidt BR (2010) Within- and among-population variation in chytridiomycosis-induced mortality in the toad Alytes obstetricans. PLoS One 5:e10927
Une Y, Kadekaru S, Tamukai K et al (2008) First report of spontaneous chytridiomycosis in frogs in Asia. Dis Aquat Organ 82:157–160
Van Ells T, Stanton J, Strieby A et al (2003) Use of immunohistochemistry to diagnose chytridiomycosis in dyeing poison dart frogs (Dendrobates tinctorius). J Wildl Dis 39:742–745
Van Rooij P, Martel A, D’Herde K et al (2012) Germ tube mediated invasion of Batrachochytrium dendrobatidis in amphibian skin is host dependent. PLoS One 7:1–8
Van Rooij P, Martel A, Haesebrouck F et al (2015) Amphibian chytridiomycosis: a review with focus on fungus-host interactions. Vet Res 46:137
Venesky MD, Mendelson JR, Sears BF et al (2012) Selecting for tolerance against pathogens and herbivores to enhance success of reintroduction and translocation. Conserv Biol 26:586–592
Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, Cook D, Webb R, Alford RA, Skerratt LF, Speare R (2009) Pathogenesis of Chytridiomycosis, a Cause of Catastrophic Amphibian Declines. Science 326: 582–585.
Vredenburg VT, Knapp RA, Tunstall TS et al (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc Nat Acad Sci U S A 107:9689–9694
Vredenburg VT, Briggs CJ, Harris RN (2011) Host-pathogen dynamics of amphibian chytridiomycosis: the role of the skin microbiome in health and disease. In: Fungal diseases: an emerging threat to human, animal and plant health: workshop summary. National Academy Press, Washington
Walker S, Bosch J, James TY et al (2008) Invasive pathogens threaten species recovery programs. Curr Biol 18:853–R854
Walker SF, Bosch J, Gomez V et al (2010) Factors driving pathogenicity vs. prevalence of amphibian panzootic chytridiomycosis in Iberia. Ecol Lett 13(3):372–382
Weldon C, du Preez LH, Hyatt AD et al (2004) Origin of the amphibian chytrid fungus. Emerg Infect Dis 10:2100–2105
Woodhams DC, Alford RA, Marantelli G (2003) Emerging disease of amphibians cured by elevated body temperature. Dis Aquat Org 55:65–67
Woodhams DC, Ardipradja K, Alford RA et al (2007) Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Anim Conserv 10:409–417
Woodhams DC, Bosch J, Briggs CJ et al (2011) Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Front Zool 8(1):8
Woodhams DC, Bell SC, Kenyon N et al (2012a) Immune evasion or avoidance: fungal skin infection linked to reduced defence peptides in Australian green-eyed treefrogs, Litoria serrata. Fungal Biol 116:1203–1211
Woodhams DC, Geiger CC, Reinert LK et al (2012b) Treatment of amphibians infected with chytrid fungus: learning from failed trials with itraconazole, antimicrobial peptides, bacteria, and heat therapy. Dis Aquat Organ 98:11–25
Woodward A, Berger L, Skerratt LF (2014) In vitro sensitivity of the amphibian pathogen Batrachochytrium dendrobatidis to antifungal therapeutics. Res Vet Sci 97:364–366
Young S, Whitehorn P, Berger L et al (2014) Defects in host immune function in tree frogs with chronic chytridiomycosis. PLoS One 9:e107284
Acknowledgements
LB was supported by the Australian Research Council (grant FT100100375).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Martel, A., Pasmans, F., Fisher, M.C., Grogan, L.F., Skerratt, L.F., Berger, L. (2018). Chytridiomycosis. In: Seyedmousavi, S., de Hoog, G., Guillot, J., Verweij, P. (eds) Emerging and Epizootic Fungal Infections in Animals. Springer, Cham. https://doi.org/10.1007/978-3-319-72093-7_14
Download citation
DOI: https://doi.org/10.1007/978-3-319-72093-7_14
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-72091-3
Online ISBN: 978-3-319-72093-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)