Skin peptide defences of New Zealand frogs against chytridiomycosis

Animal Conservation

Volumn 13, Issue SUPPL. 1, 2010, Pages 44-52

  Melzer, S ^a   Bishop, P J ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Batrachochytrium dendrobatidis; Conservation management; Inhibition assay; Leiopelma; Litoria; Skin peptides

Indexed keywords

ANTIMICROBIAL ACTIVITY; CONSERVATION MANAGEMENT; FROG; FUNGAL DISEASE; IMMUNE SYSTEM; INHIBITION; PEPTIDE; SECRETION; SKIN;

NEW ZEALAND;

AMPHIBIA; ANURA; BATRACHOCHYTRIUM DENDROBATIDIS; FUNGI; LEIOPELMA; LEIOPELMA ARCHEYI; LEIOPELMATIDAE; LITORIA;

EID: 78149489552     PISSN: 13679430     EISSN: 14691795     Source Type: Journal    
DOI: 10.1111/j.1469-1795.2009.00340.x     Document Type: Article

References (86)

1. Ali, M.F., Soto, A., Knoop, F.C. & Conlon, J.M. (2001). Antimicrobial peptides isolated from skin secretions of the diploid frog, Xenopus tropicalis (Pipidae). Biochim. Biophys. Acta 1550, 81-89.
2. Apponyi, M.A., Pukala, T.L., Brinkworth, C.S., Maselli, V.M., Bowie, J.H., Tyler, M.J., Booker, G.W., Wallace, J.C., Carver, J.A., Separovic, F., Doyle, J. & Llewellyn, L.E. (2004). Host-defence peptides of Australian anurans: structure, mechanism of action and evolutionary significance. Peptides 25, 1035-1054.
3. Banning, J.L., Weddle, A.L., Wahl, G.W., Simon, M.A., Lauer, A., Walters, R.L. & Harris, R.N. (2008). Antifungal skin bacteria, embryonic survival, and communal nesting in four-toed salamanders, Hemidactylium scutatum. Oecologia 156, 423-429.
4. Bell, B., Carer, S., Mitchell, N.J. & Pledger, S. (2004). The recent decline of a New Zealand endemic: how and why did populations of Archey's frog Leiopelma archeyi crash over 1996-2001? Biol. Conserv. 120, 189-199.
5. Berger, L. (2001). Diseases in Australian frogs. PhD thesis, James Cook University, Townsville.
6. Berger, L., Speare, R., Daszak, P., Green, D.E., Cunningham, A.A., Goggin, C.L., Slocombe, R., Ragan, M.A., Hyatt, A.H., 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. & Skerratt, L. (2005). Distribution of Batrachochytrium dendrobatidis and pathology in the skin of green tree frogs (Litoria caerulea) with severe chytridiomycosis. Dis. Aquat. Org. 68, 65-70.
8. Bishop, P. (1999). Declining frog populations in New Zealand - the New Zealand Frog Survey and possible future directions. N Z J. Zool. 26, 255-256.
9. Bishop, P., Speare, R., Poulter, R., Butler, M., Speare, B., Hyatt, A. & Haigh, A. (2009). Elimination of chytridiomycosis by Archey's frog, Leiopelma archeyi, a critically endangered New Zealand endemic species. Dis. Aquat. Org. 84, 9-15.
10. Boyle, D.G., Hyatt, A.D., Daszak, P., Berger, L., Longcore, J.E., Porter, D., Hengstberger, S.G. & Olsen, V. (2003). Cryo-archiving of Batrachochytrium dendrobatidis and other chytridiomycetes. Dis. Aquat. Org. 56, 59-64.
11. Carey, C., Cohen, N. & Rollins-Smith, L.A. (1999). Amphibian declines: an immunological perspective. Dev. Comp. Immunol. 23, 459-472.
12. Carver, S.S. (2004). Aspects of amphibian decline: the influence of stress on water balance; chytrid infection on skin function; plus biosecurity and chytrid pathogen pollution. MSc thesis, Ecology, Victoria University, Wellington.
13. Chinchar, V.G., Wang, J., Murti, G., Carey, C. & Rollins-Smith, L. (2001). Inactivation of Frog Virus 3 and Channel Catfish Virus by Esculentin-2P and Ranatuerin-2P, two antimicrobial peptides isolated from frog skin. Virology 288, 351-357.
14. Clarke, B.T. (1997). The natural history of amphibian skin secretions, their normal functioning and potential medical applications. Biol. Rev. 72, 365-379.
15. Collins, J.P. & Storfer, A. (2003). Global amphibian declines: sorting the hypotheses. Divers. Distrib. 9, 89-98.
16. Conlon, J., Iwamuro, S. & King, J. (2009). Dermal cytolytic peptides and the system of innate immunity in anurans. Trends Comp. Endocrinol. Neurobiol.: Ann. N. Y. Acad. Sci. 1163, 75-82.
17. Conlon, J.M., Woodhams, D.C., Raza, H., Coquet, L., Leprince, J., Jouenne, T., Vaudry, H. & Rollins-Smith, L.A. (2007). Peptides with differential cytolytic activity from skin secretions of the lemur leaf frog Hylomantis lemur (Hylidae: Phyllomedusinae). Toxicon 50, 489-506.
18. Daly, J.W., Spande, T.F. & Garraffo, H.M. (2005). Alkaloids from amphibian skin: a tabulation of over eight-hundred compounds. J. Nat. Prod. 68, 1556-1575.
19. Davidson, C., Benard, M.F., Shaffer, H.B., Parker, J.M., O'Leary, C., Conlon, J.M. & Rollins-Smith, L.A. (2007). Effects of chytrid and carbaryl exposure on survival, growth and skin peptide defenses in foothill yellow-legged frogs. Environ. Sci. Technol. 41, 1771-1776.
20. Duda, T.F., Vanhoye, D. & Nicolas, P. (2002). Roles of diversifying selection and coordinated evolution in the evolution of amphibian antimicrobial peptides. Mol. Biol. Evol. 19, 858-864.
21. Edge. (2009). The Zoological Society of London 2008: top 100 evolutionarily distinct and globally endangered amphibians. Available at (accessed 4 December 2009).
22. Harris, R.N., Brucker, R.M., Walke, J.B., Becker, M.H., Schwantes, C.R., Flaherty, D.C., Lam, B.A., Woodhams, D.C., Briggs, C.J., Vredenburg, V.T. & Minbiole, K.P. (2009). Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. Int. Soc. Microb. Ecol. J. 3, 818-824.
23. Harris, R.N., James, T.Y., Lauer, A., Simon, M.A. & Pate, A. (2006). Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth 3, 53-56.
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. Isaac, N.J.B., Turvey, S.T., Collen, B., Waterman, C. & Baillie, J.E.M. (2007). Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLoS ONE 2, e296. (Online DOI: DOI: 10.1371/journal.pone.0000296).
26. IUCN. (2008). An analysis of Amphibians on the 2008 IUCN Red List. Available at (accessed 4 December 2009).
27. Johnson, M., Berger, L., Phillips, L. & Speare, R. (2003). In vitro evaluation of chemical disinfectants and physical techniques against the amphibian chytrid, Batrachochytrium dendrobatidis. Dis. Aquat. Org. 57, 255-260.
28. Jones, M.E., Jarman, P.J., Lees, C.M., Hesterman, H., Hamede, R.K., Mooney, N.J., Mann, D., Pukk, C.E., Bergfeld, J. & McCallum, H. (2007). Conservation management of tasmanian devils in the context of an emerging, extinction-threatening disease: devil facial tumor disease. Ecohealth 4, 326-337.
29. Kriger, K.M. & Hero, J. (2006). Survivorship in wild frogs infected with chytridiomycosis. EcoHealth 3, 171-177.
30. Kriger, K.M. & Hero, J.-M. (2007). The chytrid fungus Batrachochytrium dendrobatidis is non-randomly distributed across amphibian breeding habitats. Divers. Distrib. 13, 781-788.
31. Lauer, A., Simon, M.A., Banning, J.L., Lam, B.A. & Harris, R.N. (2008). Diversity of cutaneous bacteria with antifungal activity isolated from female four-toed salamanders. Isme J. 2, 145-157.
32. Lips, K.R., Brem, F., Brenes, R., Reeve, J.D., Alford, R.A., Voyles, J., Carey, C., Livo, L., Pessier, A.P. & Collins, J.P. (2006). Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc. Natl. Acad. Sci. USA 102, 3165-3170.
33. Lips, K.R., Diffendorfer, J., Mendelson, J.R. III & Sears, M.W. (2008). Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biol. 6, 441-454.
34. Longcore, J.E., Pessier, A.P. & Nichols, D.K. (1999). Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91, 219-227.
35. Mangoni, M.L., Maisetta, G., Luca, M.D., Gaddi, L.M.H., Esin, S., Florio, W., Brancatisano, F.L., Barra, D., Campa, M. & Batoni, G. (2008). Comparative analysis of the bactericidal activities of amphibian peptide analogues against multidrug-resistant nosocomial bacterial strains. Antimicrob. Agents Chemother. 52, 85-91.
36. Mangoni, M.L., Miele, R., Renda, T.G., Barra, D. & Simmaco, M. (2001). The synthesis of antimicrobial peptides in the skin of Rana esculenta is stimulated by microorganisms. FASEB J. 15, 1431-1432.
37. Matsuzaki, K., Mitani, Y., Akada, K.-y., Murase, O., Yoneyama, S., Zasloff, M. & Miyajima, K. (1998). Mechanism of synergism between antimicrobial peptides Magainin 2 and PGLa. Biochemistry 37, 15144-15153.
38. Matutte, B., Storey, K.B., Knoop, F.C. & Conlon, J.M. (2000). Induction of synthesis of an antimicrobial peptide in the skin of the freeze-tolerant frog, Rana sylvatica, in response to environmental stimuli. Febs Lett. 483, 135-138.
39. Mendelson, J.R.I., Lips, K.R., Gagliardo, R.W., Rabb, G.B., Collins, J.P., Diffendorfer, J.E. Daszak, P., Ibanez, R., Zippel, K.C., Lawson, D.P., Wright, K.M., Stuart, S.N., Gascon, C., Silva, H.R.d., Burrowes, P.A., Joglar, R.L., Marca, E.L., Lötters, S., Preez, L.H.d., Weldon, C., Hyatt, A., Rodriguez-Mahecha, J.V., Robertson, S.H.H., Lock, B., Raxworthy, C.J., Frost, D.R., Lacy, R.C., Alford, R.A., Campbell, J.A., Parra-Olea, G., Bolaños, F., Domingo, J.J.C., Halliday, T., Murphy, J.B., Wake, M.H., Coloma, L.A., Kuzmin, S.L., Price, M.S., Howell, K.M., Lau, M., Pethiyagoda, R., Boone, M., Lannoo, M.J., Blaustein, A.R., Dobson, A., Griffiths, R.A., Crump, M.L., Wake, D.B. & Brodie, E.D.J. (2006). Confronting amphibian declines and extinctions. Science 313, 47-48.
40. Nicolas, P. & Mor, A. (1995). Peptides as weapons against mircoorganisms in the chemical defense system of vertebrates. Annu. Rev. Microbiol. 49, 277-304.
41. Obendorf, D. & Dalton, A. (2006). A survey for the presence of the amphibian chytrid fungus (Batrachochytrium dendrobatidis) in Tasmania. Pap. Proc. Roy. Soc. T. 140, 25-29.
42. 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.
43. Parris, M.J., Reese, E. & Storfer, A. (2006). Antipredator behaviour of chytridiomycosis-infected northern leopard frog (Rana pipiens) tadpoles. Can. J. Zool. 84, 58-65.
44. Patrzykat, A. & Douglas, S.E. (2005). Antimicrobial peptides: cooperative approaches to protection. Protein Pep. Lett. 12, 19-25.
45. Pessier, A.P., Nichols, D.K., Longcore, J.E. & Fuller, M.S. (1999). Cutaneous chytridiomycosis in poison dart frogs (Dendrobates spp.) and White's tree frogs (Litoria caerulea). J. Vet. Diagn. Investig. 11, 194-199.
46. Piotrowski, J.S., Annis, S.L. & Longcore, J.F. (2004). Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96, 9-15.
47. Potter, J.S. & Norman, R.J.d. (2006). Veterinary care of captive Archey's frogs, Leiopelma archeyi, at Auckland Zoo. Kokako 13, 19-26.
48. Poulin, R. & Combes, C. (1999). The concept of virulence: interpretations and implications - comment. Parasitol. Today 15, 474-475.
49. Reading, C.J. (2006). Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia 151, 125-131.
50. Resnick, N.M., Maloy, W.L., Guy, H.R. & Zasloff, M. (1991). A novel endopeptidase from Xenopus that recognizes alpha-helical secondary structure. Cell 66, 541.
51. Retallick, R.W., McCallum, H. & Speare, R. (2004). Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLoS Biol. 2, 1965-1971.
52. Richmond, J.Q., Savage, A.E., Zamudio, K.R. & Rosenblum, E.B. (2009). Toward immunogenetic studies of amphibian chytridiomycosis: linking innate and acquired immunity. BioScience 59, 311-320.
53. Rinaldi, A.C. (2002). Antimicrobial peptides from amphibian skin: an expanding scenario. Curr. Opin. Chem. Biol 6, 799-804.
54. Rohr, J.R., Raffel, T.R., Romansic, J.M., McCallum, H. & Hudson, P.J. (2008). Evaluating the links between climate, disease spread, and amphibian declines. Proc. Natl. Acad. Sci. USA 105, 17436-17441.
55. Rollins-Smith, L.A. (2009). The role of amphibian antimicrobial peptides in protection of amphibians from pathogens linked to global amphibian declines. Biochim. Biophys. Acta (BBA) - Biomembranes 1788, 1593-1599.
56. Rollins-Smith, L.A., Carey, C., Longcore, J., Doersam, J.K., Boutte, A., Bruzgal, J.E. & Conlon, J.M. (2002a). Activity of antimicrobial skin peptides from ranid frogs against Batrachochytrium dendrobatidis, the chytrid fungus associated with global amphibian declines. Dev. Comp. Immunol. 26, 471-479.
57. 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.
58. Rollins-Smith, L.A., Ramsey, J.P., Reinert, L.K., Woodhams, D.C., Livo, L.J. & Carey, C. (2009). Immune defenses of Xenopus laevis against Batrachochytrium dendrobatidis. Front. Biosci. S1, 68-91.
59. Rollins-Smith, L.A., Reinert, L.K., Miera, V. & Conlon, J.M. (2002c). Antimicrobial peptide defenses of the Tarahumara frog, Rana tarahumarae. Biochem. Biophys. Res. Commun. 297, 361-367.
60. Romani, L. (2004). Immunity to fungal infections. Nature Rev. Immunol. 4, 11-24.
61. Rozek, T., Bowie, J.H., Wallace, J.C. & Tyler, M.J. (2000a). The antibiotic and anticancer active aurein peptides from the Australian Bell Frogs Litoria aurea and Litoria raniformis. Part 2. Sequence determination using electrospray mass spectrometry. Rapid Commun. Mass Spectrom. 14, 2002-2011.
62. Rozek, T., Wegener, K.L., Bowie, J.H., Olver, I.N., Carver, J.A., Wallace, J. & Tyler, M. (2000b). The antibiotic and anticancer active aurein peptides from the Australian bell frogs Litoria aurea and Litoria raniformis. Eur. J. Biochem. 267, 5330-5341.
63. Sadic, E. & Waldman, B. (2004). Rapid detection of amphibian chytrid fungus by PCR assay. Captivity, reintroduction and disease control technologies for amphibians. Werribee: Amphibian Research Centre.
64. Sheafor, B., Davidson, E.W., Parr, L. & Rollins-Smith, L. (2008). Antimicrobial peptide defenses in the salamander, Ambystoma tigrinum, against emerging amphibian pathogens. J. Wildl. Dis. 44, 226-236.
65. 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.
66. Smale, A. (2006). Archey's frog emergency translocation-DOCDM-28159. Unpublished report. Department of Conservation, Waikato Conservancy, Hamilton.
67. Smith, B., Hayasaka, Y., Tyler, M. & Williams, B. (2004). Beta-caryophyllene in the skin secretion of the Australian green tree frog, Litoria caerulea: an investigation of dietary sources. Aust. J. Zool. 52, 521-530.
68. Smith, K.G., Weldon, C., Conradie, W. & Du Preez, L.H. (2005). Relationships among size, development, and Batrachochytrium dendrobatidis infection in African tadpoles. Dis. Aquat. Org. 74, 159-164.
69. Speare, R. & Berger, L. (2005). Chytridiomycosis status of wild amphibians in Australia. Available at (accessed 28 September 2009).
70. Speare, R., Skerratt, L., Hines, B.L.H., Hyatt, A., Mendez, D., McDonald, K., Hero, J., Marantelli, G., Muller, R., Alford, R. & Woods, R. (2005). A project that designs and trials a pilot survey to map the distribution of chytridiomycosis (caused by the amphibian chytrid) in Australian frogs. Vol. 64. Canberra: Department of Environment and Heritage.
71. Steinborner, S.T., Bowie, J.H., Tyler, M.J. & Wallace, J.C. (1997a). An unusual combination of peptides from the skin glands of Ewing's tree frog, Litoria ewingi. Sequence determination and antimicrobial activity. Aust. J. Chem. 50, 889-894.
72. Steinborner, S.T., Waugh, R.J., Bowie, J.H., Wallace, J.C., Tyler, M.J. & Ramsay, S.L. (1997b). New caerin antibacterial peptides from the skin glands of the Australian tree frog Litoria xanthomera. J. Pept. Sci. 3, 181-185.
73. Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L. & Waller, R.W. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783-1786.
74. Tennessen, J.A., Woodhams, D.C., Chaurand, P., Reinert, L.K., Billheimer, D., Shyr, Y., Caprioli, R.M., Blouin, M.S. & Rollins-Smith, L.A. (2009). Variations in the expressed antimicrobial peptide repertoire of northern leopard frog (Rana pipiens) populations suggest intraspecies differences in resistance to pathogens. Dev. Comp. Immunol. 33, 1247-1257.
75. Thurley, T. & Haigh, A. (2008). Hochstetter's frog amphibian chytrid fungus survey 2008. Hamilton: Waikato Conservancy, New Zealand Department of Conservation.
76. Tyler, M., Stone, D. & Bowie, J. (1992). A novel method for the release and collection of dermal, glandular secretions from the skin of frogs. J. Pharmacol. Toxicol. Methods 28, 199-200.
77. Urban, E., Nagy, E., Pal, T., Sonnevend, A. & Conlon, J.M. (2007). Activities of four frog skin-derived antimicrobial peptides (temporin-1DRa, temporin-1Va and the melittin-related peptides AR-23 and RV-23) against anaerobic bacteria. Int. J. Antimicrob. Agents 29, 317-321.
78. Wake, D.B. & Vredenburg, V.T. (2008). Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc. Natl. Acad. Sci. USA 105, 11466-11473.
79. Waldman, B., Van De Wolfshaar, K.E., Klena, J.D., Andjic, V., Bishop, P. & Norman, R. (2001). Chytridiomycosis in New Zealand frogs. Surveillance 28, 9-11.
80. Westerhoff, H.V., Zasloff, M., Rosner, J.L., Hendler, R.W., Waal, A.D., Gomes, A.V., Jongsma, A.P.M., Riethorst, A. & Juretic, D. (1995). Functional synergism of the magainins PGLa and magainin-2 in Escherichia coli, tumor cells and liposomes. Eur. J. Biochem. 228, 257-264.
81. Wolinska, J. & King, K.C. (2009). Environment can alter selection in host-parasite interactions. Trends Parasitol. 25, 236-244.
82. Woodhams, D.C., Alford, R.A., Briggs, C.J., Johnson, M. & Rollins-Smith, L.A. (2008). Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen. Ecology 89, 1627-1639.
83. Woodhams, D.C., Ardipradja, K., Alford, R.A., Marantelli, G., Reinert, L.K. & Rollins-Smith, L.A. (2007a). Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Anim. Conserv. 10, 409-417.
84. Woodhams, D.C., Rollins-Smith, L.A., Carey, C., Reinert, L., Tyler, M.J. & Alford, R.A. (2006a). Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs. Oecologia 146, 531-540.
85. Woodhams, D.C., Voyles, J., Lips, K.R., Carey, C. & Rollins-Smith, L.A. (2006b). Predicted disease susceptibility in a panamanian amphibian assemblage based on skin peptide defenses. J. Wildl. Dis. 42, 207-218.
86. Woodhams, D.C., Vredenburg, V.T., Simon, M.A., Billheimer, D., Shakhtour, B., Shyr, Y., Briggs, C.J., Rollins-Smith, L.A. & Harris, R.N. (2007b). Symbiotic bacteria contribute to innate immune defenses of the threatened mountain yellow-legged frog, Rana muscosa. Biol. Conserv. 138, 390-398.