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      Emerging Infectious Disease Leads to Rapid Population Declines of Common British Birds

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          Abstract

          Emerging infectious diseases are increasingly cited as threats to wildlife, livestock and humans alike. They can threaten geographically isolated or critically endangered wildlife populations; however, relatively few studies have clearly demonstrated the extent to which emerging diseases can impact populations of common wildlife species. Here, we report the impact of an emerging protozoal disease on British populations of greenfinch Carduelis chloris and chaffinch Fringilla coelebs, two of the most common birds in Britain. Morphological and molecular analyses showed this to be due to Trichomonas gallinae. Trichomonosis emerged as a novel fatal disease of finches in Britain in 2005 and rapidly became epidemic within greenfinch, and to a lesser extent chaffinch, populations in 2006. By 2007, breeding populations of greenfinches and chaffinches in the geographic region of highest disease incidence had decreased by 35% and 21% respectively, representing mortality in excess of half a million birds. In contrast, declines were less pronounced or absent in these species in regions where the disease was found in intermediate or low incidence. Also, populations of dunnock Prunella modularis, which similarly feeds in gardens, but in which T. gallinae was rarely recorded, did not decline. This is the first trichomonosis epidemic reported in the scientific literature to negatively impact populations of free-ranging non-columbiform species, and such levels of mortality and decline due to an emerging infectious disease are unprecedented in British wild bird populations. This disease emergence event demonstrates the potential for a protozoan parasite to jump avian host taxonomic groups with dramatic effect over a short time period.

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          Most cited references26

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          Spatial population dynamics: analyzing patterns and processes of population synchrony.

          The search for mechanisms behind spatial population synchrony is currently a major issue in population ecology. Theoretical studies highlight how synchronizing mechanisms such as dispersal, regionally correlated climatic variables and mobile enemies might interact with local dynamics to produce different patterns of spatial covariance. Specialized statistical methods, applied to large-scale survey data, aid in testing the theoretical predictions with empirical estimates. Observational studies and experiments on the demography of local populations are paramount to identify the true ecological mechanisms. The recent achievements illustrate the power of combining theory, observation and/or experimentation and statistical modeling in the ecological research protocol.
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            West Nile virus emergence and large-scale declines of North American bird populations.

            Emerging infectious diseases present a formidable challenge to the conservation of native species in the twenty-first century. Diseases caused by introduced pathogens have had large impacts on species abundances, including the American chestnut, Hawaiian bird species and many amphibians. Changes in host population sizes can lead to marked shifts in community composition and ecosystem functioning. However, identifying the impacts of an introduced disease and distinguishing it from other forces that influence population dynamics (for example, climate) is challenging and requires abundance data that extend before and after the introduction. Here we use 26 yr of Breeding Bird Survey (BBS) data to determine the impact of West Nile virus (WNV) on 20 potential avian hosts across North America. We demonstrate significant changes in population trajectories for seven species from four families that concur with a priori predictions and the spatio-temporal intensity of pathogen transmission. The American crow population declined by up to 45% since WNV arrival, and only two of the seven species with documented impact recovered to pre-WNV levels by 2005. Our findings demonstrate the potential impacts of an invasive species on a diverse faunal assemblage across broad geographical scales, and underscore the complexity of subsequent community response.
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              Density-dependent decline of host abundance resulting from a new infectious disease.

              Although many new diseases have emerged within the past 2 decades [Cohen, M. L. (1998) Brit. Med. Bull. 54, 523-532], attributing low numbers of animal hosts to the existence of even a new pathogen is problematic. This is because very rarely does one have data on host abundance before and after the epizootic as well as detailed descriptions of pathogen prevalence [Dobson, A. P. & Hudson, P. J. (1985) in Ecology of Infectious Diseases in Natural Populations, eds. Grenfell, B. T. & Dobson, A. P. (Cambridge Univ. Press, Cambridge, U.K.), pp. 52-89]. Month by month we tracked the spread of the epizootic of an apparently novel strain of a widespread poultry pathogen, Mycoplasma gallisepticum, through a previously unknown host, the house finch, whose abundance has been monitored over past decades. Here we are able to demonstrate a causal relationship between high disease prevalence and declining house finch abundance throughout the eastern half of North America because the epizootic reached different parts of the house finch range at different times. Three years after the epizootic arrived, house finch abundance stabilized at similar levels, although house finch abundance had been high and stable in some areas but low and rapidly increasing in others. This result, not previously documented in wild populations, is as expected from theory if transmission of the disease was density dependent.

                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                18 August 2010
                : 5
                : 8
                : e12215
                Affiliations
                [1 ]British Trust for Ornithology, Thetford, Norfolk, United Kingdom
                [2 ]Institute of Zoology, Zoological Society of London, London, United Kingdom
                [3 ]The Royal Society for the Protection of Birds, Sandy, United Kingdom
                [4 ]Universities Federation for Animal Welfare, Wheathampstead, United Kingdom
                [5 ]Department of Veterinary Pathology, University of Liverpool, South Wirral, United Kingdom
                [6 ]Electron Microscopy Unit, UCL Medical School, London, United Kingdom
                [7 ]Disease Surveillance Centre, Scottish Agricultural College, Ayr, United Kingdom
                [8 ]Wildlife Veterinary Investigation Centre, Truro, United Kingdom
                [9 ]Biomedical Research Centre, School of Medicine, Health Policy and Practice, University of East Anglia, Norwich, United Kingdom
                University of Bristol, United Kingdom
                Author notes

                Conceived and designed the experiments: RR BL JKK AAC. Performed the experiments: BL MPT KMP JC IC ADE LAH SKJ TWP MWP PRR VRS. Analyzed the data: RR. Contributed reagents/materials/analysis tools: OCH KT. Wrote the paper: RR BL AAC. Data collection: BL MPT KMP JC IC LAH SKJ TWP MWP PRR VRS. Modelling of data: RR. Research design and coordination: JKK AAC. Supervision of RSPB data collection: ADE. Development of new molecular analytic tools: OCH. Technical assistance: MWP. Supervision of molecular analyses: KT.

                Article
                09-PONE-RA-11022R3
                10.1371/journal.pone.0012215
                2923595
                20805869
                f8d7dae7-0d8c-4dc2-8f26-5d8d0a98d969
                Robinson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 15 June 2009
                : 12 July 2010
                Page count
                Pages: 12
                Categories
                Research Article
                Pathology
                Ecology/Population Ecology
                Infectious Diseases/Protozoal Infections

                Uncategorized
                Uncategorized

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