Low impact of chytridiomycosis on frog recruitment enables persistence in refuges despite high adult mortality

Biological Conservation

Volumn 182, Issue , 2015, Pages 36-43

  Scheele, Ben C ^a,b   Hunter, David A ^b   Skerratt, Lee F ^c   Brannelly, Laura A ^c   Driscoll, Don A ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b OFFICE OF ENVIRONMENT AND HERITAGE   (Australia)

^c JAMES COOK UNIVERSITY   (Australia)

Author keywords

Amphibian decline; Batrachochytrium dendrobatidis; Chytrid fungus; Recruitment; Wildlife disease

Indexed keywords

ADULT; BREEDING SEASON; CHRONOLOGY; DISEASE PREVALENCE; DISEASE TREATMENT; FROG; FUNGUS; HOST-PARASITE INTERACTION; MORTALITY; POPULATION STRUCTURE; RECRUITMENT (POPULATION DYNAMICS); SURVIVAL; WILD POPULATION;

AMPHIBIA; ANURA; BATRACHOCHYTRIUM DENDROBATIDIS; FUNGI; LITORIA VERREAUXII;

EID: 84949115576     PISSN: 00063207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocon.2014.11.032     Document Type: Article

References (50)

1. Altizer S., Harvell D., Friedle E. Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol. Evol. 2003, 18:589-596.
2. Anstis M. Breeding biology and larval development of Litoria verreauxii (Anura: Hylidae). Trans. R. Soc. S. Aust. 1976, 100:193-202.
3. Australian Government Department of the Environment, 2014. Litoria verreauxii alpina - Alpine Tree Frog, Verreaux's Alpine Tree Frog. Department of the Environment, Canberra. (accessed February 2014). http://www.environment.gov.au/cgi-bin/sprat/public/publicspecies.pl?taxon_id=66669.
4. Baitchman E.J., Pessier A.P. Pathogenesis, diagnosis, and treatment of amphibian chytridiomycosis. Vet. Clin. North Am. Exot. Anim. Pract. 2013, 16:669-685.
5. 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. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl. Acad. Sci. USA 1998, 95:9031-9036.
6. Böll S., Tobler U., Geiger C.C., Hansbauer G., Schmidt B.R. The amphibian chytrid fungus in Bavarian populations of Alytes obstetricans: past absence, current presence, and metamorph mortality. Amphibia-Reptilia 2012, 33:319-326.
7. BOM, 2014. (Bureau of Meteorology) Climate statistics for Australian locations. Australian Bureau of Meteorology, Melbourne. (accessed December 2013). http://www.bom.gov.au/climate/data/.
8. Boyle D.G., Boyle D.B., Olsen V., Morgan J.A.T., Hyatt A.D. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis. Aquat. Org. 2004, 60:141-148.
9. Briggs C.J., Knapp R.A., Vredenburg V.T. Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proc. Natl. Acad. Sci. USA 2010, 107:9695-9700.
10. Caughley G. Analysis of Vertebrate Populations 1977, Wiley, New York.
11. Chatfield M., Richards-Zawacki C. Elevated temperature as a treatment for Batrachochytrium dendrobatidis infection in captive frogs. Dis. Aquat. Org. 2011, 94:235-238.
12. Daskin J.H., Alford R.A., Puschendorf R. Short-term exposure to warm microhabitats could explain amphibian persistence with Batrachochytrium dendrobatidis. PLoS ONE 2011, 6:e26215.
13. Daszak P., Cunningham A.A., Hyatt A.D. Wildlife ecology - emerging infectious diseases of wildlife - threats to biodiversity and human health. Science 2000, 287:443-449.
14. Doddington B.J., Bosch J., Oliver J.A., Grassly N.C., Garcia G., Schmidt B.R., Garner T.W.J., Fisher M.C. Context-dependent amphibian host population response to an invading pathogen. Ecology 2013, 94:1795-1804.
15. Fisher M.C., Garner T.W.J., Walker S.F. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu. Rev. Microbiol. 2009, 63:291-310.
16. Fisher M.C., Henk D.A., Briggs C.J., Brownstein J.S., Madoff L.C., McCraw S.L., Gurr S.J. Emerging fungal threats to animal, plant and ecosystem health. Nature 2012, 484:186-194.
17. Forrest M.J., Schlaepfer M.A. Nothing a hot bath won't cure: infection rates of amphibian chytrid fungus correlate negatively with water temperature under natural field settings. PLoS ONE 2011, 6:e28444.
18. Geiger C.C., Kupfer E., Schar S., Wolf S., Schmidt B.R. Elevated temperature clears chytrid fungus infections from tadpoles of the midwife toad Alytes obstetricans. Amphibia-Reptilia 2011, 32:276-280.
19. Heard G.W., Scroggie M.P., Clemann N., Ramsey D.S.L. Wetland characteristics influence disease risk for a threatened amphibian. Ecol. Appl. 2014, 24:650-662.
20. Hossack B.R., Lowe W.H., Ware J.L., Corn P.S. Disease in a dynamic landscape: host behavior and wildfire reduce amphibian chytrid infection. Biol. Conserv. 2013, 157:293-299.
21. Hunter, D., 2000. The conservation and demography of the southern corroboree frog (Pseudophryne corroboree). Masters thesis. University of Canberra, Canberra, Australia. p. 138.
22. Hunter D.A., Speare R., Marantelli G., Mendez D., Pietsch R., Osborne W. Presence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in threatened corroboree frog populations in the Australian Alps. Dis. Aquat. Org. 2010, 92:209-216.
23. 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. Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Dis. Aquat. Org. 2007, 73:175-192.
24. Kinney V.C., Heemeyer J.L., Pessier A.P., Lannoo M.J. Seasonal pattern of Batrachochytrium dendrobatidis infection and mortality in Lithobates areolatus: affirmation of Vredenburg's "10,000 Zoospore Rule". PLoS ONE 2011, 6:e16708.
25. 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. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc. Natl. Acad. Sci. USA 2006, 103:3165-3170.
26. Louca S., Lampo M., Doebeli M. Assessing host extinction risk following exposure to Batrachochytrium dendrobatidis. Proc. R. Soc. Lond. B Biol. Sci. 2014, 281:20132783.
27. Muths E., Scherer R.D., Pilliod D.S. Compensatory effects of recruitment and survival when amphibian populations are perturbed by disease. J. Appl. Ecol. 2011, 48:873-879.
28. Osborne, W., Hunter, D., 2003. Frog declines in the Snowy Mountains: what do we know after fifteen years? In: Proceedings of an International Year of Mountains Conference. Australian Alps Liaison Committee.
29. Osborne W., Hunter D., Hollis G. Population declines and range contraction in Australian alpine frogs. Declines and Disappearances of Australian Frogs 1999, 145-157. Environment Australia, Canberra. A. Campbell (Ed.).
30. Phillott A.D., Grogan L.F., Cashins S.D., McDonald K.R., Berger L., Skerratt L.F. Chytridiomycosis and seasonal mortality of tropical stream-associated frogs 15 years after introduction of Batrachochytrium dendrobatidis. Conserv. Biol. 2013, 27:1058-1068.
31. Piotrowski J.S., Annis S.L., Longcore J.E. Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 2004, 96:9-15.
32. Puschendorf R., Hoskin C.J., Cashins S.D., McDonald K., Skerratt L.F., VanDerWal J., Alford R.A. Environmental refuge from disease-driven amphibian extinction. Conserv. Biol. 2011, 25:956-964.
33. R Development Core Team, 2014. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. ISBN 3-900051-07-0. http://www.R-project.org.
34. Ripley, B., Venables, B., Bates, D.M., Hornik, K., 2013. MASS. R package, version 7.3-33. (accessed December 2013). http://cran.r-project.org/web/packages/MASS/index.html.
35. Rowley J.J.L., Alford R.A. Hot bodies protect amphibians against chytrid infection in nature. Sci. Rep. 2013, 3:e1515.
36. Savage A.E., Zamudio K.R. MHC genotypes associate with resistance to a frog-killing fungus. Proc. Natl. Acad. Sci. USA 2011, 108:16705-16710.
37. Scheele B., Driscoll D., Fischer J., Hunter D. Decline of an endangered amphibian during an extreme climatic event. Ecosphere 2012, 3:e101.
38. Scheele B.C., Guarino F., Osborne W., Hunter D.A., Skerratt L.F., Driscoll D.A. Decline and re-expansion of an amphibian with high prevalence of chytrid fungus. Biol. Conserv. 2014, 170:86-91.
39. Scheele B.C., Hunter D.A., Grogan L., Berger L., Kolby J., McFadden M., Marantelli G., Skerratt L.F., Driscoll D.A. Interventions for reducing extinction risk in chytridiomycosis-threatened amphibians. Conserv. Biol. 2014, 28:1195-1205.
40. Schmeller D.S., Blooi M., Martel A., Garner T.W., Fisher M.C., Azemar F., Clare F.C., Leclerc C., Jäger L., Guevara-Nieto M. Microscopic aquatic predators strongly affect infection dynamics of a globally emerged pathogen. Curr. Biol. 2013, 24:176-180.
41. Shoo L.P., Olson D.H., McMenamin S.K., Murray K.A., Van Sluys M., Donnelly M.A., Stratford D., Terhivuo J., Merino-Viteri A., Herbert S.M., Bishop P.J., Corn P.S., Dovey L., Griffiths R.A., Lowe K., Mahony M., McCallum H., Shuker J.D., Simpkins C., Skerratt L.F., Williams S.E., Hero J.M. Engineering a future for amphibians under climate change. J. Appl. Ecol. 2011, 48:487-492.
42. Skerratt L.F., Berger L., Speare R., Cashins S., McDonald K.R., Phillott A.D., Hines H.B., Kenyon N. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 2007, 4:125-134.
43. Skerratt L.F., McDonald K.R., Hines H.B., Berger L., Mendez D., Phillott A.D., Cashins S.D., Murray K.A., Speare R. Application of the survey protocol for chytridiomycosis to Queensland. Australia. Dis. Aquat. Org. 2010, 92:117-129.
44. Smirina E. Age determination and longevity in amphibians. Gerontology 1994, 40:133-146.
45. Tobler U., Borgula A., Schmidt B.R. Populations of a susceptible amphibian species can grow despite the presence of a pathogenic chytrid fungus. PLoS ONE 2012, 7:e34667.
46. 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. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 2009, 326:582-585.
47. Vredenburg V.T., Knapp R.A., Tunstall T.S., Briggs C.J. Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc. Natl. Acad. Sci. USA 2010, 107:9689-9694.
48. Wilbur H.M. Complex life cycles. Annu. Rev. Ecol. Syst. 1980, 11:67-93.
49. Woodhams D.C., Bosch J., Briggs C.J., Cashins S., Davis L.R., Lauer A., Muths E., Puschendorf R., Schmidt B.R., Sheafor B., Voyles J. Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Front. Zool. 2011, 8. 10.1186/1742-9994-1188-1188.
50. Zuur A.F., Ieno E.N., Smith G.M. Analysing Ecological Data 2007, Springer, New York.