Climate forcing of an emerging pathogenic fungus across a montane multi-host community

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 371, Issue 1709, 2016, Pages

  Clare, Frances C ^a,b   Halder, Julia B ^b   Daniel, Olivia ^b   Bielby, Jon ^a   Semenov, Mikhail A ^c   Jombart, Thibaut ^b   Loyau, Adeline ^d,e   Schmeller, Dirk S ^d,e   Cunningham, Andrew A ^a   Rowcliffe, Marcus ^a   Garner, Trenton W J ^a   Bosch, Jaime ^f   Fisher, Matthew C ^b  

^a INSTITUTE OF ZOOLOGY   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c ROTHAMSTED RESEARCH   (United Kingdom)

^d UNIVERSITÉ DE TOULOUSE   (France)

^e HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^f MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

Author keywords

Chytridiomycosis; Climate change; Epidemiology; Host pathogen environment interaction; Mountain ecosystems; Multi host communities

Indexed keywords

AMPHIBIAN; ANTHROPOGENIC EFFECT; BIODIVERSITY; CLIMATE CHANGE; CLIMATE FORCING; COMMUNITY DYNAMICS; DISEASE PREVALENCE; DISEASE SEVERITY; EPIDEMIOLOGY; FUNGUS; HOST-PATHOGEN INTERACTION; INFECTIOUS DISEASE; MOUNTAIN ENVIRONMENT; PATHOGENICITY; POPULATION DECLINE; SEASONALITY;

ALYTES OBSTETRICANS; AMPHIBIA; BATRACHOCHYTRIUM DENDROBATIDIS; FUNGI;

ANIMAL; ANURA; CHYTRIDIOMYCETES; CLIMATE; CLIMATE CHANGE; DISEASE CARRIER; FRANCE; GROWTH, DEVELOPMENT AND AGING; LAKE; LARVA; MICROBIOLOGY; MYCOSIS; PHYSIOLOGY; PREVALENCE; VETERINARY;

ANIMALS; ANURA; CHYTRIDIOMYCOTA; CLIMATE; CLIMATE CHANGE; DISEASE RESERVOIRS; FRANCE; LAKES; LARVA; MYCOSES; PREVALENCE;

EID: 84992467403     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2015.0454     Document Type: Article

References (38)

1. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD. 2002 Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162. (doi:10.1126/science.1063699)
2. Epstein P. 2010 The ecology of climate change and infectious diseases: comment. Ecology 91, 925–928. (doi:10.1890/09-0761.1)
3. Rodó X et al. 2013 Climate change and infectious diseases: can we meet the needs for better prediction? Clim. Change 118, 625–640. (doi:10.1007/s10584-013-0744-1)
4. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues AS, Fischman DL, Waller RW. 2004 Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786. (doi:10.1126/science.1103538)
5. 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.(doi:10.1146/annurev.micro.091208.073435)
6. Pounds AJ et al. 2006 Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439, 161–167. (doi:10.1038/nature04246)
7. Bosch J, Carrascal LM, Duran L, Walker S, Fisher MC. 2007 Climate change and outbreaks of amphibian chytridiomycosis in a montane area of Central Spain; is there a link? Proc. R. Soc. B 274, 253–260. (doi:10.1098/rspb.2006.3713)
8. Voyles J, Johnson LR, Briggs CJ, Cashins SD, Alford RA, Berger L, Skerratt LF, Speare R, Bree Rosenblum E. 2012 Temperature alters reproductive life history patterns in Batrachochytrium dendrobatidis, a lethal pathogen associated with the global loss of amphibians. Ecol. Evol. 2, 2241–2249. (doi:10.1002/ece3.334)
9. Ribas L et al. 2009 Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis. PLoS ONE 4, e8408. (doi:10.1371/journal.pone.0008408)
10. Garner TWJ, Rowcliffe JM, Fisher MC. 2011 Climate change, chytridiomycosis or condition: an experimental test of amphibian survival. Glob. Change Biol. 17, 667–675. (doi:10.1111/j.1365-2486.2010.02272.x)
11. Rohr JR, Raffel TR. 2010 Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proc. Natl Acad. Sci. USA 107, 8269–8274. (doi:10.1073/pnas.0912883107)
12. Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ. 2008 Evaluating the links between climate, disease spread, and amphibian declines. Proc. Natl Acad. Sci. USA 105, 17 436–17 441. (doi:10.1073/pnas.0806368105)
13. Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, Garner TWJ. 2013 Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS ONE 8, e56802. (doi:10.1371/journal.pone.0056802)
14. Baláž V et al. 2014 Assessing risk and guidance on monitoring of Batrachochytrium dendrobatidis in Europe through identification of taxonomic selectivity of infection. Conserv. Biol. 28, 213–223. (doi:10.1111/cobi.12128)
15. Bielby J, Bovero S, Angelini C, Favelli M, Gazzaniga E, Perkins M, Sotgiu G, Tessa G, Garner TWJ 2013 Geographic and taxonomic variation in Batrachochytrium dendrobatidis infection and transmission within a highly endemic amphibian community. Divers. Distrib. 19, 1153–1163. (doi:10.1111/ddi.12085)
16. Doddington BJ, Bosch J, Oliver JA, Grassly NC, Garcia G, Schmidt BR, Garner TWJ, Fisher MC. 2013 Context-dependent amphibian host population response to an invading pathogen. Ecology 94, 1795–1804. (doi:10.1890/12-1270.1)
17. 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. (doi:10.1016/S0006-3207(00)00132-4)
18. Whiles MR et al. 2006 The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. Front. Ecol. Environ. 4, 27–34. (doi:10.1890/1540-9295(2006)004 [0027:TEOAPD]2.0.CO;2)
19. Briggs CJ, Knapp RA, Vredenburg VT. 2010 Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proc. Natl Acad. Sci. USA 107, 9695–9700. (doi:10.1073/pnas.0912886107)
20. Walker SF et al. 2010 Factors driving pathogenicity vs. prevalence of amphibian panzootic chytridiomycosis in Iberia. Ecol. Lett. 13, 372–382. (doi:10.1111/j.1461-0248.2009.01434.x)
21. Recuero E et al. 2012 Multilocus species tree analyses resolve the radiation of the widespread Bufo bufo species group (Anura, Bufonidae). Mol. Phylogenet. Evol. 62, 71–86. (doi:10.1016/j.ympev.2011.09.008)
22. Garner TWJ, Walker S, Bosch J, Leech S, Rowcliffe JM, Cunningham AA, Fisher MC. 2009 Life history trade-offs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118, 783–791. (doi:10.1111/j.1600-0706.2008.17202.x)
23. Bielby J, Fisher MC, Clare FC, Rosa GM, Garner TWJ. 2015 Host species vary in infection probability, sublethal effects, and costs of immune response when exposed to an amphibian parasite. Sci. Rep.-UK 5, 10828. (doi:10.1038/srep10828)
24. Briggs CJ, Vredenburg VT, Knapp RA, Rachowicz LJ. 2005 Investigating the population-level effects of chytridiomycosis: an emerging infectious disease of amphibians. Ecology 86, 3149–3159. (doi:10.1890/04-1428)
25. Bradley GA, Rosen PC, Sredl MJ, Jones TR, Longcore JE. 2002 Chytridiomycosis in native Arizona frogs. J. Wildl. Dis. 38, 206–212. (doi:10.7589/0090-3558-38.1.206)
26. Rachowicz LJ, Vredenburg VT. 2004 Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Dis. Aquat. Organ. 61, 75–83. (doi:10.3354/dao061075)
27. Semenov MA, Stratonovitch P. 2010 Use of multimodel ensembles from global climate models for assessment of climate change impacts. Clim. Res. 41, 1–14. (doi:10.3354/cr00836)
28. Stocker T. 2014 Climate change 2013, the physical science basis: Working Group I contribution to the Fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press.
29. Raffel TR, Romansic JM, Halstead NT, McMahon TA, Venesky MD, Rohr JR. 2013 Disease and thermal acclimation in a more variable and unpredictable climate. Nat. Clim. Change 3, 146–151. (doi:10.1038/nclimate1659)
30. Schmeller DS et al. 2014 Microscopic aquatic predators strongly affect infection dynamics of a globally emerged pathogen. Curr. Biol. 24, 176–180. (doi:10.1016/j.cub.2013.11.032)
31. Scheffer M, Rinaldi S, Kuznetsov YA, van Nes EH. 1997 Seasonal dynamics of Daphnia and algae explained as a periodically forced predatorprey system. Oikos 80, 519–532. (doi:10.2307/3546625)
32. Bosch J, Rincon PA. 2008 Chytridiomycosis-mediated expansion of Bufo bufo in a montane area of Central Spain: an indirect effect of the disease. Divers. Distrib. 14, 637–643. (doi:10.1111/j.1472-4642.2007.00461.x)
33. Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD. 2004 Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis. Aquat. Organ. 60, 141–148. (doi:10.3354/dao060141)
34. Reading CJ. 1998 The effect of winter temperatures on the timing of breeding activity in the common toad Bufo bufo. Oecologia 117, 469–475. (doi:10.1007/s004420050682)
35. Thompson R, Ventura M, Camarero L. 2009 On the climate and weather of mountain and sub-arctic lakes in Europe and their susceptibility to future climate change. Freshwater Biol. 54, 2433–2451. (doi:10.1111/j.1365-2427.2009.02236.x)
36. Thompson R et al. 2005 Quantitative calibration of remote mountain-lake sediments as climatic recorders of air temperature and ice-cover duration. Arct. Antarct. Alp. Res. 37, 626–635. (doi:10.1657/1523-0430(2005)037[0626:QCORMS]2.0.CO;2)
37. Semenov MA, Stratonovitch P. 2015 Adapting wheat ideotypes for climate change: accounting for uncertainties in CMIP5 climate projections. Clim. Res. 65, 123–139. (doi:10.3354/cr01297)
38. Heinzl H, Mittlbock M. 2003 Pseudo R-squared measures for Poisson regression models with overor underdispersion. Comput. Stat. Data Anal. 44, 253–271. (doi:10.1016/S0167-9473(03)00062-8)