No evidence that migratory geese disperse avian influenza viruses from breeding to wintering ground

RESEARCH ARTICLE No evidence that migratory geese disperse avian influenza viruses from breeding to wintering ground Shenglai Yin1*, David Kleijn2, Gerard J. D. M. Müskens3, Ron A. M. Fouchier4, Josanne H. Verhagen5, Petr M. Glazov6, Yali Si1,7, Herbert H. T. Prins1, Willem Frederik de Boer1* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Resource Ecology Group, Wageningen University and Research, Wageningen, The Netherlands, 2 Plant Ecology and Nature Conservation Group, Wageningen University and Research, Wageningen, The Netherlands, 3 Alterra, Centre for Ecosystem Studies, Wageningen University and Research, Wageningen, The Netherlands, 4 Department of Viroscience, Erasmus MC, Rotterdam, the Netherlands, 5 Department Biology and Environmental Sciences, Linnaeus University, Kalmar, Sweden, 6 Laboratory of Biogeography, Institute of Geography Russian Academy of Sciences, Moscow, Russia, 7 Ministry of Education Key Laboratory for Earth System Modelling, and Department of Earth System Science, Tsinghua University, Beijing, China * (SY); (WFdB) OPEN ACCESS Citation: Yin S, Kleijn D, Müskens GJDM, Fouchier RAM, Verhagen JH, Glazov PM, et al. (2017) No evidence that migratory geese disperse avian influenza viruses from breeding to wintering ground. PLoS ONE 12(5): e0177790. https://doi. org/10.1371/journal.pone.0177790 Editor: Jonas Waldenström, Lund University, SWEDEN Received: January 13, 2017 Accepted: May 3, 2017 Published: May 18, 2017 Copyright: © 2017 Yin 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. Abstract Low pathogenic avian influenza virus can mutate to a highly pathogenic strain that causes severe clinical signs in birds and humans. Migratory waterfowl, especially ducks, are considered the main hosts of low pathogenic avian influenza virus, but the role of geese in dispersing the virus over long-distances is still unclear. We collected throat and cloaca samples from three goose species, Bean goose (Anser fabalis), Barnacle goose (Branta leucopsis) and Greater white-fronted goose (Anser albifrons), from their breeding grounds, spring stopover sites, and wintering grounds. We tested if the geese were infected with low pathogenic avian influenza virus outside of their wintering grounds, and analysed the spatial and temporal patterns of infection prevalence on their wintering grounds. Our results show that geese were not infected before their arrival on wintering grounds. Barnacle geese and Greater white-fronted geese had low prevalence of infection just after their arrival on wintering grounds in the Netherlands, but the prevalence increased in successive months, and peaked after December. This suggests that migratory geese are exposed to the virus after their arrival on wintering grounds, indicating that migratory geese might not disperse low pathogenic avian influenza virus during autumn migration. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This work was carried out in the framework of the projects ‘Flyway conservation of migratory waterbirds’, BO-10-003-002, and ‘Voortzetting monitoring ganzen en Smienten ivm het voorkomen van vogelgriepvirussen in 2008/ 2009’, Verpl. Nr. 2001126, funded by the Dutch Ministry of Agriculture, Nature Conservation and Food Quality. The study is supported by a Ph.D. Introduction Pathogens can strongly influence host populations by reducing activity, reproduction or survival [1–3]. Many pathogens are capable of infecting more than one host species. The avian influenza viruses (AIVs), for example, are highly infectious to a wide range of wildlife, domestic animals, and humans [4–8]. In 2016, a highly pathogenic AIV (HPAIV) H5N8 was isolated from water birds in Russia, rapidly followed by isolations in India and Europe [9]. The highly PLOS ONE | https://doi.org/10.1371/journal.pone.0177790 May 18, 2017 1 / 11 Migratory geese do not disperse AIV scholarship to Shenglai Yin from the Chinese Scholarship Council (Nr. 201406190178), and by the Dutch Ministry of Economic Affairs, European Research Council project FLUPLAN [250136] and NIAID/NIH contract HHSN272201400008C. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: Co-author Ron A.M. Fouchier is a member of the PLOS ONE Editorial Board. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials. The authors have declared that no competing interests exist. infectious and fast spread of AIV has boosted research into the presence and dynamics of this pathogen in wild birds. Based on their ability to cause disease in chickens, AIVs are characterized by two types: HPAIV, such as the one isolated in 2016, and LPAIV (low pathogenic AIV). The latter occurs more frequently in wild birds. When they are infected with LPAIV, wild birds do not show any clinical signs. Therefore, the migration of wild birds might contribute to the dispersal of LPAIV. Insights into the dynamics of LPAIV infection in migratory wild birds can help us to better understand and predict the spatial and temporal distribution of LPAIV outbreaks. Most of what is known about the ecology of LPAIV prevalence is based on information from duck species such as mallard (Anas platyrhynchos). Ducks are considered the main hosts of LPAIV, because their aquatic habits facilitate transmission, spread, and persistence of LPAIV [10,11]. Previous studies from Northern Hemisphere have shown that LPAIV circulates year-round in ducks, and the infection peaks just after the breeding season when the population comprises many immunologically naive juveniles [12,13]. LPAIV prevalence typically declines after the breeding season, from as high as 60% during the post-breeding migration to as low as 0.25% during spring migration [14]. Many ducks are long-distance migrants. They encounter migratory birds from other flyways and aggregate in large numbers at stopover sites during migration. Aggregation may facilitate outbreaks of LPAIV infection because the virus can be more rapidly transmitted between individuals that occur in high density [12,15]. Longdistance migrations, encounters with other birds, and aggregation of many duck species such as mallard could provide an explanation for why AIV disperse over long distances so fast [16,17]. However, it is unlikely that all migratory waterfowl have a similar role in the dispersal of LPAIV. Other waterfowl, such as geese, might only be secondary hosts [18]. Geese may become infected after exposure to LPAIV from a primary host, but lose the LPAIV rapidly [18]. Furthermore, some species, such as Greater white-fronted goose, breed at higher latitudes than mallard. These mor (...truncated)