title: Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages.
abstract: Emerging diseases have been increasingly associated with population declines, with co-infections exhibiting many types of interactions. The chytrid fungus (Batrachochytrium dendrobatidis) and ranaviruses have extraordinarily broad host ranges, however co-infection dynamics have been largely overlooked. We investigated the pattern of co-occurrence of these two pathogens in an amphibian assemblage in Serra da Estrela (Portugal). The detection of chytridiomycosis in Portugal was linked to population declines of midwife-toads (Alytes obstetricans). The asynchronous and subsequent emergence of a second pathogen - ranavirus - caused episodes of lethal ranavirosis. Chytrid effects were limited to high altitudes and a single host, while ranavirus was highly pathogenic across multiple hosts, life-stages and altitudinal range. This new strain (Portuguese newt and toad ranavirus - member of the CMTV clade) caused annual mass die-offs, similar in host range and rapidity of declines to other locations in Iberia affected by CMTV-like ranaviruses. However, ranavirus was not always associated with disease, mortality and declines, contrasting with previous reports on Iberian CMTV-like ranavirosis. We found little evidence that pre-existing chytrid emergence was associated with ranavirus and the emergence of ranavirosis. Despite the lack of cumulative or amplified effects, ranavirus drove declines of host assemblages and changed host community composition and structure, posing a grave threat to all amphibian populations.
authors.affiliation: Durrell Institute of Conservation and Ecology, School of Anthropology and Conservation, University of Kent, Canterbury, Kent, CT2 7NR, UK.|Institute of Zoology, Zoological Society of London, Regent's Park, NW1 4RY, London, UK.|Centre for Ecology, Evolution and Environmental Changes (CE3C), Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal.|Department of Biology, University of Nevada, Reno, NV 89557, USA.
authors.forename: Gonçalo M
authors.initials: GM
authors.lastname: Rosa
authors.affiliation: Technische Universität Braunschweig, Division of Evolutionary Biology, Zoological Institute, Mendelssohnstr. 4, 38106 Braunschweig, Germany.
authors.forename: Joana
authors.initials: J
authors.lastname: Sabino-Pinto
authors.affiliation: Computational Biology and Population Genomics Group, Centre for Ecology, Evolution and Environmental Changes (CE3C), Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal.|Zoological Institute, University of Basel, Vesalgasse 1, Basel, Switzerland.
authors.forename: Telma G
authors.initials: TG
authors.lastname: Laurentino
authors.affiliation: Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Ghent, Belgium.
authors.forename: An
authors.initials: A
authors.lastname: Martel
authors.affiliation: Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Ghent, Belgium.
authors.forename: Frank
authors.initials: F
authors.lastname: Pasmans
authors.affiliation: Centre for Ecology, Evolution and Environmental Changes (CE3C), Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal.
authors.forename: Rui
authors.initials: R
authors.lastname: Rebelo
authors.affiliation: Durrell Institute of Conservation and Ecology, School of Anthropology and Conservation, University of Kent, Canterbury, Kent, CT2 7NR, UK.
authors.forename: Richard A
authors.initials: RA
authors.lastname: Griffiths
authors.affiliation: Fachgebiet für Umwelt- und Tierhygiene, Universität Hohenheim, Stuttgart, Germany.
authors.forename: Anke C
authors.initials: AC
authors.lastname: Stöhr
authors.affiliation: Fachgebiet für Umwelt- und Tierhygiene, Universität Hohenheim, Stuttgart, Germany.|Laboklin GmbH &Co. KG, Laboratory for Clinical Diagnostics, Bad Kissingen, Germany.
authors.forename: Rachel E
authors.initials: RE
authors.lastname: Marschang
authors.affiliation: Institute of Zoology, Zoological Society of London, Regent's Park, NW1 4RY, London, UK.|UCL Genetics Institute, Gower Street, London, WC1E 6BT, UK.
authors.forename: Stephen J
authors.initials: SJ
authors.lastname: Price
authors.affiliation: Institute of Zoology, Zoological Society of London, Regent's Park, NW1 4RY, London, UK.
authors.forename: Trenton W J
authors.initials: TW
authors.lastname: Garner
authors.affiliation: Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain.
authors.forename: Jaime
authors.initials: J
authors.lastname: Bosch
mesh_terms: D000531:Altitude; D000818:Animals; D001001:Anura / Q000254:growth & development / Q000382:microbiology / Q000821:virology; D008411:Chytridiomycota / Q000472:pathogenicity* / Q000502:physiology; D060085:Coinfection; D004266:DNA Virus Infections / Q000453:epidemiology / Q000401:mortality / Q000662:veterinary* / Q000821:virology; D008018:Life Cycle Stages; D009181:Mycoses / Q000453:epidemiology / Q000382:microbiology / Q000401:mortality / Q000662:veterinary*; D011174:Portugal / Q000453:epidemiology; D015995:Prevalence; D017995:Ranavirus / Q000472:pathogenicity* / Q000502:physiology; D012455:Salamandridae / Q000254:growth & development / Q000382:microbiology / Q000821:virology; D016019:Survival Analysis