Host species determines whether infection load increases beyond disease-causing thresholds following exposure to the amphibian chytrid fungus

Animal Conservation

Volumn 13, Issue SUPPL. 1, 2010, Pages 62-71

  Stockwell, M P ^a   Clulow, J ^a   Mahony, M J ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

Amphibian chytrid fungus; Batrachochytrium dendrobatidis; Host Species; Infection Threshold

Indexed keywords

DISEASE INCIDENCE; FROG; FUNGUS; HOST; HOST-PATHOGEN INTERACTION; PATHOGEN; POPULATION DECLINE; SURVIVAL;

AMPHIBIA; ANURA; BATRACHOCHYTRIUM DENDROBATIDIS; FUNGI; LIMNODYNASTES PERONII; LITORIA AUREA;

EID: 78149472669     PISSN: 13679430     EISSN: 14691795     Source Type: Journal    
DOI: 10.1111/j.1469-1795.2010.00407.x     Document Type: Article

References (62)

1. Anderson, R.M. & Crombie, J. (1984). Experimental studies of age-prevalence curves for Schistosoma mansoni infections in populations of Biomphalaria glabrata. Parasitology 89, 79-106.
2. Anderson, R.M. & May, R.M. (1978). Regulation and stability of host-parasite population interactions: I. Regulatory processes. J. Anim. Ecol. 47, 219-247.
3. Anderson, R.M. & May, R.M. (1980). Infectious diseases and population cycles of forest insects. Science 210, 658-661.
4. Apponyi, M.A., Pukala, T.L., Brinkworth, C.S., Maseli, V.M., Bowie, J.H., Tyler, M.J., Booker, G.W., Wallace, J.C., Carver, J.A., Separovic, F., Doyle, J. & Lewellyn, L.E. (2004). Host-defence peptides of Australian anurans: structure, mechanism of action and evolutionary significance. Peptides 25, 1035-1054.
5. Beldomenico, P.M. & Begon, M. (2010). Disease spread, susceptibility and infection intensity: vicious circles? Trends Ecol. Evol. 25, 21-27.
6. Berger, L., Speare, R., Daszak, P., Green, D.E., Cunningham, A.A., Goggin, C.L., Slocombe, R., Ragan, M.A., Hyatt, A.d., Mcdonald, K.R., Hines, H.B., Lips, K.R., Marantelli, G. & Parkes, H. (1998). Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of australia and central america. Proc. Natl. Acad. Sci. USA 95, 9031-9036.
7. Berger, L., Speare, R., Hines, H., Marantelli, G., Hyatt, A.D., Mcdonald, K.R., Skerratt, L.F., Oslen, V., Clarke, J.M., Gillespie, G., Mahony, M., Sheppard, N., Williams, C. & Tyler, M.J. (2004). Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Aust. Vet. J. 82, 434-440.
8. Berger, L, Marantelli, G., Skerratt, L. F. & Spear, R. (2005). Virulence of the amphibian chytrid fungus Batrachochytrium dendrobatidis varies with strain. Dis. Aquat. Org. 68, 47-50.
9. Blaustein, A.R., Romansic, J.M., Scheessele, E.A., Ham, B.A., Pessier, A.P. & Longcore, J.E. (2005). Interspecific variation in susceptability of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conserv. Biol. 19, 1460-1468.
10. Boyle, D.B., Boyle, D.B., Olsen, V., Morgan, J.A.T. & Hyatt, A.D. (2004). Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time taqman pcr assay. Dis. Aquat. Org. 60, 141-148.
11. Briggs, C.J., Knapp, R.A. & Vredenburg, V.T. (2010). Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. PNAS 107, 9695-9700.
12. Carey, C., Bruzgul, J.E., Livo, L.J., Walling, M.L., Kuehl, K.A., Dixon, B.F., Pessier, A.P., Alford, R. & Rogers, K.B. (2006). Experimental exposures of boreal toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 3, 5-21.
13. Daszak, P. (1999a). Extinction by infection. Trends Ecol. Evol. 14, 279.
14. Daszak, P., Berger, L., Cunningham, A.A., Hyatt, A.D., Green, D.E. & Speare, R. (1999b). Emerging infectious diseases and amphibian popultion declines. Emerg. Infect. Dis. 5, 735-748.
15. Daszak, P., Strieby, A., Cunningham, A., Longcore, J.E., Brown, C.C. & Porter, D. (2004). Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. Herpetol. J. 14, 201-207.
16. Daszak, P. & Cunningham, A.A. (1998). Wildlife disease biology comes of age. Oryx 32, 238-239.
17. Davidson, E.W., Parris, M.J., Collins, J.P., Longcore, J.E., Pessier, A.P. & Brunner, J. (2003). Pathogenicity and transmission of chytridiomycosis in tiger salamanders (Ambystoma tigrinum). Copeia 601-607.
18. Garner, T.W.J., Walker, S., Bosch, J., Leech, S., Rowcliffe, J.M., Cunningham, A.A. & Fisher, M.C. (2009). Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118, 783-791.
19. Gosner, K.L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183-190.
20. Hamer, A.J., Lane, S.J. & Mahony, M.J. (2007). Life-history of an endangered amphibian challenges the declining species paradigm. Aust. J. Zool. 55, 79-88.
21. Harris, R.N., James, T.Y., Lauer, A., Simon, M.A. & Patel, A. (2006). Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth 3, 53-56.
22. Hassell, M.P., Anderson, R.M., Cohen, J.E., Cvjetanovic, B., Dobson, A.P., Gill, D.E., Holmes, J.C., May, R.M., Mckeown, T., Pereira, M.S. & Tyrell, D.A.J. (1982). Impact of infectious diseases on host populations. In Population biology of infectious diseases: 15-36. Anderson, R.M. & May, R.M. (Eds). New York: Springer-Verlag.
23. Hosmer, D.W. & Lemeshow, S. (1999). Applied survival analysis: regression modeling of time to event data. New York: Wiley.
24. Hyatt, A.D., Boyle, D.G., Olsen, V., Boyle, D.B., Berger, L., Obendorf, D., Dalton, A., Kriger, K., Hero, M., Hines, H., Phillott, R., Campbell, R., Marantelli, G., Gleason, F. & Colling, A. (2007). Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Dis. Aquat. Org. 73, 175-192.
25. IUCN. (2010). Summary statistics for globally threatened species. Available at
26. Johnson, M. (2003). Media for in-vitro cultivation of Batrachochytrium dendrobatidis. Available at (Accessed 11 November 2006)
27. Johnson, M.L., Berger, L., Phillips, L. & Speare, R. (2003). Fungicidal effects of chemical disinfectants, uv light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis. Dis. Aquat. Org. 57, 255-260.
28. Keymer, A. (1981). Population dynamics of Hymenolepis diminuta in the intermediate host. J. Anim. Ecol. 50, 941-950.
29. Kriger, K.M. & Hero, J.-M. (2006). Survivorship in wild frogs infected with chytridiomycosis. EcoHealth 3, 171-177.
30. Lamirande, E.W. & Nichols, D.K. (2002). Effects of host age on susceptability to cutaneous chytridiomycosis in blue-and-yellow poison dart frogs (Dendrobates tinctorius). In Proceeding of the sixth international symposium on the pathology of reptiles and amphibians: 3-13. Mckinnell, R.G. & Carlson, D.L. (Eds). University of Minnesota, Printing Services, Minnesota.
31. Marantelli, G., Berger, L., Speare, R. & Keegan, L. (2004). Distribution of the amphibian chytrid Batrachochytrium dendrobatidis and keratin during tadpole development. Pac. Conserv. Biol. 10, 173-179.
32. May, R.M. (1988). Conservation and disease. Conserv. Biol. 2, 28-30.
33. Mccallum, H. & Dobson, A. (1995). Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol. Evol. 10, 190-194.
34. Mcconnell, T.H. (2007). The nature of disease. Baltimore: Lippincott, Williams and Wilkins.
35. Nelson, K.E., Williams, C.M. & Graham, N.M.H. (2001). Infectious disease epidemiology: theory and practice. Maryland: Aspen Publishers.
36. Parker, J.M., Mikaelian, I., Hahn, N. & Diggs, H.E. (2002). Clinical diagnosis and treatment of epidermal chytridiomycosis in african clawed frogs (Xenopus tropicalis). Comp. Med. 52, 265-268.
37. Parris, M.J. & Baud, D.R. (2004). Interactive effects of a heavy metal and chytridiomycosis on gray treefrog larvae (Hyla chrysoscelis). Copeia 344-350.
38. Penman, T.D., Muir, G.W., Magerey, E.R. & Burns, E.L. (2008). Impact of a chytrid-related mortality event on a population of the green and golden bell frog Litoria aurea. Aust. Zool. 34, 314-318.
39. Pyke, G.H. & White, A.W. (1996). Habitat requirements for the green and golden bell frog Litoria aurea (anura: Hylidae). Aust. Zool. 30, 224-232.
40. Pyke, G.H. & White, A.W. (2001). A review of the biology of the green and golden bell frog Litoria aurea. Aust. Zool. 31, 563-598.
41. Rollins-Smith, L., Carey, C., Conlon, J.M., Reinert, L.K., Doersam, J.K., Bergman, T., Silberring, J., Lankinen, H. & Wade, D. (2003). Activities of temporin family peptides against the chytrid fungus (Batracochytrium dendrobatidis) associated with global amphibian declines. Antimicrob. Agents Chemother. 47, 1157-1160.
42. Rollins-Smith, L.A., Carey, C., Longcore, J.E., Doersam, J.K., Boutte, A., Bruzal, J.E. & Conlon, J.M. (2002a). Activity of antimicrobial skin peptides from ranid frogs against Batrachochytrium dendrobatidis, the fungus associated with global amphibian declines. Dev. Comp. Immunol. 26, 471-479.
43. Rollins-Smith, L.A., Doersam, J.K., Longcore, J.E., Taylor, S.K., Shamblin, J.C., Carey, C. & Zasloff, M.A. (2002b). Antimicrobial peptide defenses against pathogens associated with global amphibian declines. Dev. Comp. Immunol. 26, 63-72.
44. Rollins-Smith, L.A., Woodhams, D.C., Reinert, L.K., Vredenburg, V.T., Briggs, C.J., Nielsen, P.F. & Conlon, J.M. (2006). Antimicrobial defenses of the mountain yellow-legged frog (Rana muscosa). Dev. Comp. Immunol. 30, 831-842.
45. Rowley, J.J.L. & Alford, R.A. (2007). Behaviour of Australian rainforest stream frogs may affect the transmission of chytridiomycosis. Dis. Aquat. Org. 77, 1-9.
46. Scott, M.E. (1987). Regulation of mouse colony abundance by Heligmosomoides polygyrus. Parasitology 95, 111-128.
47. Scott, M.E. (1988). The impact of infection and disease on animal populations: implications for conservation biology. Conserv. Biol. 2, 40-56.
48. Scott, M.E. & Anderson, R.M. (1984). The population dynamics of Gyrodactylus bullatarudis (monogenea) within laboratory populations of the fish host Poecilia reticulata. Parasitology 89, 159-194.
49. Skerratt, L.F., Berger, L., Speare, R., Cashins, S., Mcdonald, K.R., Phillott, A.D., Hines, H.B. & Kenyon, N. (2007). Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125-134.
50. Speare, R. & Berger, L. (2004). Global distribution of chytridiomycosis in amphibians. Available at (Accessed 15 April 2005)
51. Stockwell, M.P., Clulow, S., Clulow, J. & Mahony, M. (2008). The impact of the amphibian chytrid fungus Batrachochytrium dendrobatidis on a green and golden bell frog Litoria aurea reintroduction program at the hunter wetlands centre australia in the hunter region of NSW. Aust. Zool. 34, 379-386.
52. Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L. & Walker, R.W. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783-1786.
53. Thompkins, D.M. & Begon, M. (1999). Parasites can regulate wildlife populations. Parasitol. Today 15, 311-313.
54. Voyles, J., Berger, L., Young, S., Speare, R., Webb, R., Warner, J., Rudd, D., Campbell, R. & Skerratt, L.F. (2007). Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Dis. Aquat. Org. 77, 113-118.
55. Voyles, J., Young, S., Berger, L., Campbell, C., Voyles, W.F., Dinudom, A., Cook, D., Webb, R., Alford, R.A., Skerratt, L.F. & Speare, R. (2009). Pathogenesis of chytridiomycosis, a cause of catastrphic amphibian declines. Science 326, 582-585.
56. Vredenburg, V.T., Knapp, R.A., Tunstall, T.S. & Briggs, C.J. (2010). Dynamics of an emerging disease drive large-scale amphibian population extinctions. PNAS 107, 9689-9694.
57. White, A.W. & Pyke, G.H. (1996). Distribution and conservation status of the green and golden bell frog Litoria aurea in new south wales. Aust. Zool. 30, 177-189.
58. Woodhams, D.C., Rollins-Smith, L.A., Carey, C., Reinert, L., Tyler, M.J. & Alford, R.A. (2006). Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs. Oecologia 146, 531-540.
59. Woodhams, D.C., Ardipraja, K., Alford, R.A., Marantelli, G., Reinert, L.K. & Rollins-Smith, L.A. (2007). Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Anim. Conserv. 10, 409-417.
60. Woodhams, D.C., Alford, R.A. & Marantelli, G. (2003). Emerging disease of amphibians cured by elevated body temperature. Dis. Aquat. Org. 55, 65-67.
61. Wright, K.M. & Whitaker, B.R. (2001). Pharmacotherapeutics. In Amphibian medicine and captive husbandry: 309-319. Wright, K.M. & Whitaker, B.R. (Eds). Malabar: Krieger Publishing Company.
62. Zou, K.H., O'malley, A.J. & Mauri, L. (2007). Receiver operating characteristic analysis for evaluating diagnostic tests and predictive models. J. Am. Heart Assoc. 115, 645-657.