Collapse of Amphibian Communities Due to an Introduced Ranavirus

Abstract

The emergence of infectious diseases with a broad host range can have a dramatic impact on entire communities and has become one of the main threats to biodiversity [1LaDeau S.L. Kilpatrick A.M. Marra P.P. West Nile virus emergence and large-scale declines of North American bird populations.Nature. 2007; 447: 710-713Crossref PubMed Scopus (368) Google Scholar, 2Fisher 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: 291-310Crossref PubMed Scopus (526) Google Scholar, 3Lembo T. Haydon D.T. Velasco-Villa A. Rupprecht C.E. Packer C. Brandão P.E. Kuzmin I.V. Fooks A.R. Barrat J. Cleaveland S. Molecular epidemiology identifies only a single rabies virus variant circulating in complex carnivore communities of the Serengeti.Proc. Biol. Sci. 2007; 274: 2123-2130Crossref PubMed Scopus (41) Google Scholar, 4Frick W.F. Pollock J.F. Hicks A.C. Langwig K.E. Reynolds D.S. Turner G.G. Butchkoski C.M. Kunz T.H. An emerging disease causes regional population collapse of a common North American bat species.Science. 2010; 329: 679-682Crossref PubMed Scopus (624) Google Scholar]. Here, we report the simultaneous exploitation of entire communities of potential hosts with associated severe declines following invasion by a novel viral pathogen. We found two phylogenetically related, highly virulent viruses (genus Ranavirus, family Iridoviridae) causing mass mortality in multiple, diverse amphibian hosts in northern Spain, as well as a third, relatively avirulent virus. We document host declines in multiple species at multiple sites in the region. Our work reveals a group of pathogens that seem to have preexisting capacity to infect and evade immunity in multiple diverse and novel hosts, and that are exerting massive impacts on host communities. This report provides an exceptional record of host population trends being tracked in real time following emergence of a wildlife disease and a striking example of a novel, generalist pathogen repeatedly crossing the species barrier with catastrophic consequences at the level of host communities.