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Protection of wetlands as a strategy for reducing the spread of avian influenza from migratory waterfowl

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Abstract

Highly pathogenic avian influenza (HPAI) H5N1 has led to the death or destruction of millions of domesticated and wild birds and caused hundreds of human deaths worldwide. As with other HPAIs, H5N1 outbreaks among poultry have generally been caused by contact with infected migratory waterfowl at the interface of wildlands and human-dominated landscapes. Using a case–control epidemiological approach, we analyzed the relation between habitat protection and H5N1 outbreaks in China from 2004 to 2017. We found that while proximity to unprotected waterfowl habitats and rice paddy generally increased outbreak risk, proximity to the most highly protected habitats (e.g., Ramsar-designated lakes and wetlands) had the opposite effect. Protection likely involves two mechanisms: the separation of wild waterfowl and poultry populations and the diversion of wild waterfowl from human-dominated landscapes toward protected natural habitats. Wetland protection could therefore be an effective means to control avian influenza while also contributing to avian conservation.

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References

  • Amano, T., T. Székely, B. Sandel, S. Nagy, T. Mundkur, T. Langendoen, D. Blanco, C.U. Soykan, et al. 2018. Successful conservation of global waterbird populations depends on effective governance. Nature 553: 199.

    Article  CAS  Google Scholar 

  • Barnes, M.D., L. Glew, C. Wyborn, and I.D. Craigie. 2018. Prevent perverse outcomes from global protected area policy. Nature Ecology & Evolution 2: 759–762.

    Article  Google Scholar 

  • Beatty, W.S., D.C. Kesler, E.B. Webb, A.H. Raedeke, L.W. Naylor, and D.D. Humburg. 2014. The role of protected area wetlands in waterfowl habitat conservation: Implications for protected area network design. Biological Conservation 176: 144–152.

    Article  Google Scholar 

  • Bonter, D.N., S.A. Gauthreaux Jr., and T.M. Donovan. 2009. Characteristics of important stopover locations for migrating birds: Remote sensing with radar in the Great Lakes basin. Conservation Biology 23: 440–448.

    Article  Google Scholar 

  • Breslow, N.E. 1996. Statistics in epidemiology: The case-control study. Journal of the American Statistical Association 91: 14–28.

    Article  CAS  Google Scholar 

  • Brouwer, R., P. van Beukering, and E. Sultanian. 2008. The impact of the bird flu on public willingness to pay for the protection of migratory birds. Ecological Economics 64: 575–585.

    Article  Google Scholar 

  • Conan, A., F.L. Goutard, S. Sorn, and S. Vong. 2012. Biosecurity measures for backyard poultry in developing countries: A systematic review. BMC Veterinary Research 8: 240.

    Article  Google Scholar 

  • Daszak, P., A.A. Cunningham, and A.D. Hyatt. 2000. Wildlife ecology—Emerging infectious diseases of wildlife—Threats to biodiversity and human health. Science 287: 443–449.

    Article  CAS  Google Scholar 

  • Di Minin, E., and T. Toivonen. 2015. Global protected area expansion: Creating more than paper parks. BioScience 65: 637–638.

    Article  Google Scholar 

  • Fang, L.-Q., S.J. de Vlas, S. Liang, C.W.N. Looman, P. Gong, B. Xu, L. Yan, H. Yang, et al. 2008. Environmental factors contributing to the spread of H5N1 Avian influenza in mainland China. PLoS ONE 3: e2268.

    Article  CAS  Google Scholar 

  • Fang, L.Q., X.L. Li, K. Liu, Y.J. Li, H.W. Yao, S. Liang, Y. Yang, Z.J. Feng, et al. 2013. Mapping spread and risk of avian influenza A (H7N9) in China. Scientific Reports 3: 2722.

    Article  Google Scholar 

  • Finlayson, M., J. Harris, M. McCartney, Y. Lew, and C. Zhang. 2010. Report on Ramsar visit to Poyang Lake Ramsar site, P. R. China. Secretariat of the Ramsar Convention.

  • Fischer, J., B. Brosi, G.C. Daily, P.R. Ehrlich, G. Rebecca, J. Goldstein, D.B. Lindenmayer, A.D. Manning, et al. 2008. Should agricultural policies encourage land sparing or wildlife-friendly farming? Frontiers in Ecology and the Environment 6: 380–385.

    Article  Google Scholar 

  • Gill, J.A., K. Norris, P.M. Potts, T.G. Gunnarsson, P.W. Atkinson, and W.J. Sutherland. 2001. The buffer effect and large-scale population regulation in migratory birds. Nature 412: 436–438.

    Article  CAS  Google Scholar 

  • Greenland, S., and D.C. Thomas. 1982. On the need for the rare disease assumption in case-control studies. American Journal of Epidemiology 116: 547–553.

    Article  CAS  Google Scholar 

  • Grimes, D.A., and K.F. Schulz. 2005. Compared to what? Finding controls for case-control studies. The Lancet 365: 1429–1433.

    Article  Google Scholar 

  • Gruber, K. 2017. Predicting zoonoses. Nature Ecology & Evolution 1: 1–4.

    Article  Google Scholar 

  • Haig, S.M., D.W. Mehlman, and L.W. Oring. 1998. Avian movements and wetland connectivity in landscape conservation. Conservation Biology 12: 749–758.

    Article  Google Scholar 

  • Han, X., X. Chen, and L. Feng. 2015. Four decades of winter wetland changes in Poyang Lake based on Landsat observations between 1973 and 2013. Remote Sensing of Environment 156: 426–437.

    Article  Google Scholar 

  • Hennessy, D.A., and T. Wang. 2012. Animal disease and the industrialization of agriculture. In Health and animal agriculture in developing countries, ed. D. Zilberman, J. Otte, D. Roland-Holst, and D. Pfeiffer. Heidelberg: Health and Animal Agriculture in Developing Countries. Food and Agriculture Organization of the United Nations and Springer Science & Business Media.

    Google Scholar 

  • Higuchi, H., J.P. Pierre, V. Krever, V. Andronov, G. Fujita, K. Ozaki, O. Goroshko, M. Ueta, et al. 2004. Using a remote technology in conservation: Satellite tracking white-naped cranes in Russia and Asia. Conservation Biology 18: 136–147.

    Article  Google Scholar 

  • Jha, P., B. Jacob, V. Gajalakshmi, P.C. Gupta, N. Dhingra, R. Kumar, D.N. Sinha, R.P. Dikshit, et al. 2008. A nationally representative case–control study of smoking and death in India. New England Journal of Medicine 358: 1137–1147.

    Article  CAS  Google Scholar 

  • Jiang, B., C.P. Wong, Y. Chen, L. Cui, and Z. Ouyang. 2015. Advancing wetland policies using ecosystem services–China’s way out. Wetlands 35: 983–995.

    Article  Google Scholar 

  • Jones, K.E., N.G. Patel, M.A. Levy, A. Storeygard, D. Balk, J.L. Gittleman, and P. Daszak. 2008. Global trends in emerging infectious diseases. Nature 451: 990–994.

    Article  CAS  Google Scholar 

  • Kilpatrick, A.M., D.J. Salkeld, G. Titcomb, and M.B. Hahn. 2017. Conservation of biodiversity as a strategy for improving human health and well-being. Philosophical Transactions of the Royal Society B: Biological Sciences 372: 20160131.

    Article  Google Scholar 

  • Kirkwood, B., and J. Sterne. 2003. Essential Medical Statistics, 2nd ed. London: Wiley-Blackwell.

    Google Scholar 

  • Kleijin, D., I. Cherkaoui, P.W. Goedhart, J. Hout, and D. Lammertsma. 2014. Waterbirds increase more rapidly in Ramsar-designated wetlands than in unprotected wetlands. Journal of Applied Ecology 51: 289–298.

    Article  Google Scholar 

  • Li, D., S. Chen, H. Lloyd, S. Zhu, K. Shan, and Z. Zhang. 2013. The importance of artificial habitats to migratory waterbirds within a natural/artificial wetland mosaic, Yellow River Delta, China. Bird Conservation International 23: 184–198.

    Article  CAS  Google Scholar 

  • Liu, J., H. Xiao, F. Lei, Q. Zhu, K. Qin, X.-W. Zhang, X.-L. Zhang, D. Zhao, et al. 2005. Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309: 1206.

    Article  CAS  Google Scholar 

  • Morin, C.W., B. Stoner-Duncan, K. Winker, M. Scotch, J.J. Hess, J.S. Meschke, K.L. Ebi, and P.M. Rabinowitz. 2018. Avian influenza virus ecology and evolution through a climatic lens. Environment International 119: 241–249.

    Article  CAS  Google Scholar 

  • Muzaffar, S.B., J.Y. Takekawa, D.J. Prosser, S.H. Newman, and X. Xiao. 2010. Rice production systems and avian influenza: Interactions between mixed-farming systems, poultry and wild birds. Waterbirds 33: 219–230.

    Article  Google Scholar 

  • National Bureau of Statistics. 2016. Chinese national statistics. China: Beijing.

    Google Scholar 

  • O’Donnell, M.J., S.L. Chin, S. Rangarajan, D. Xavier, L. Liu, H. Zhang, P. Rao-Melacini, X. Zhang, et al. 2016. Global and regional effects of potentially modifiable risk factors associated with acute stroke in 32 countries (INTERSTROKE): A case-control study. The Lancet 388: 761–775.

    Article  Google Scholar 

  • Olsen, B., V.J. Munster, A. Wallensten, J. Waldenstrom, A.D.M.E. Osterhaus, and R.A.M. Fouchier. 2006. Global patterns of influenza A virus in wild birds. Science 312: 384–388.

    Article  CAS  Google Scholar 

  • Pike, J., T. Bogich, S. Elwood, D.C. Finnoff, and P. Daszak. 2014. Economic optimization of a global strategy to address the pandemic threat. Proceedings of the National Academy of Sciences 111: 18519–18523.

    Article  CAS  Google Scholar 

  • Poetri, O.N., M.V. Boven, I. Claassen, G. Koch, I.W. Wibawan, A. Stegeman, J. Van den Broek, and A. Bouma. 2014. Silent spread of highly pathogenic avian influenza H5N1 virus amongst vaccinated commercial layers. Research in Veterinary Science 97: 637–641.

    Article  Google Scholar 

  • Prosser, D.J., L.L. Hungerford, R.M. Erwin, M.A. Ottinger, J.Y. Takekawa, and E.C. Ellis. 2013. Mapping avian influenza transmission risk at the interface of domestic poultry and wild birds. Frontiers in Public Health 1: 28.

    Article  Google Scholar 

  • Railsback, S.F., and M.D. Johnson. 2014. Effects of land use on bird populations and pest control services on coffee farms. Proceedings of the National Academy of Sciences 111: 6109–6114.

    Article  CAS  Google Scholar 

  • Ramsar Convention Secretariat. 2010a. Avian influenza and wetlands: Guidance on control of and responses to highly pathogenic avian influenza. Gland: Ramsar Convention Secretariat.

    Google Scholar 

  • Ramsar Convention Secretariat. 2010b. Managing wetlands: Frameworks for managing Ramsar Sites and other wetlands. Gland: Ramsar Convention Secretariat.

    Google Scholar 

  • Ramsar Convention Secretariat. 2019. The Ramsar Sites Criteria. Gland: The Ramsar Convention Secretariat.

    Google Scholar 

  • Schulz, K.F., and D.A. Grimes. 2002. Case-control studies: Research in reverse. The lancet 359: 431–434.

    Article  Google Scholar 

  • Si, Y., W. de Boer, and P. Gong. 2013. Different environmental drivers of highly pathogenic avian influenza H5N1 outbreaks in poultry and wild birds. PLoS ONE 8: e53362.

    Article  CAS  Google Scholar 

  • Si, Y., T. Wang, A.K. Skidmore, W.F. de Boer, L. Li, and H.H.T. Prins. 2010. Environmental factors influencing the spread of the highly pathogenic avian influenza H5N1 virus in wild birds in Europe. Ecology and Society 15: 26.

    Article  Google Scholar 

  • Takekawa, J.Y., S.H. Newman, X. Xiao, D.J. Prosser, K.A. Spragens, E.C. Palm, B. Yan, T. Li, et al. 2010. Migration of waterfowl in the East Asian flyway and spatial relationship to HPAI H5N1 outbreaks. Avian Diseases 54: 466–476.

    Article  Google Scholar 

  • Tian, H., S. Zhou, L. Dong, T.P. Van Boeckel, Y. Cui, Y. Wu, B. Cazelles, S. Huang, et al. 2015. Avian influenza H5N1 viral and bird migration networks in Asia. Proceedings of the National Academy of Sciences 112: 172–177.

    Article  CAS  Google Scholar 

  • USDA Foreign Agricultural Service. 2017. China—Peoples Republic of Poultry and Products Semi-annual 2017 GAIN Report Number: CH17005. Washington DC: USDA Foreign Agricultural Service.

    Google Scholar 

  • Wang, Z., J. Wu, M. Madden, and D. Mao. 2012. China’s wetlands: Conservation plans and policy impacts. Ambio 41: 782–786.

    Article  Google Scholar 

  • Welte, V.R., and M.V. Teran. 2004. Emergency Prevention System (EMPRES) for transboundary animal and plant pests and diseases. The EMPRES-Livestock: An FAO initiative. Annals of the New York Academy of Sciences 1026: 19–31.

    Article  Google Scholar 

  • Wilson, E.O. 2016. Half-earth: Our planet’s fight for life. New York: WW Norton & Company.

    Google Scholar 

  • Wu, X., M. Lv, Z. Jin, R. Michishita, J. Chen, H. Tian, X. Tu, H. Zhao, et al. 2014. Normalized difference vegetation index dynamic and spatiotemporal distribution of migratory birds in the Poyang Lake wetland, China. Ecological Indicators 47: 219–230.

    Article  Google Scholar 

  • Wu, T., and C. Perrings. 2017. Conservation, development and the management of infectious disease: Avian influenza in China, 2004–2012. Philosophical Transactions of the Royal Society B: Biological Sciences 372: 20160126.

    Article  Google Scholar 

  • Xiao, X., S. H. Newman, T. McCracken, and C. Ding. 2010. Wild waterfowl—Domestic poultry—Human Interfaces An Integrated Pilot Study in Poyang Lake, Jiangxi, China. The 2nd international workshop on community-based data synthesis, analysis and modelling of highly pathogenic avian influenza H5N1 in Asia.

  • Xu, W., Y. Xiao, J. Zhang, W. Yang, L. Zhang, V. Hull, Z. Wang, H. Zheng, et al. 2017. Strengthening protected areas for biodiversity and ecosystem services in China. Proceedings of the National Academy of Sciences 114: 1601–1606.

    Article  CAS  Google Scholar 

  • Yan, D., U.A. Schneider, E. Schmid, H. Huang, L. Pan, and O. Dilly. 2013. Interactions between land use change, regional development, and climate change in the Poyang Lake district from 1985 to 2035. Agricultural Systems 119: 10–21.

    Article  Google Scholar 

  • Yong, D.L., A. Jain, Y. Liu, M. Iqbal, C.Y. Choi, N.J. Crockford, S. Millington, and J. Provencher. 2018. Challenges and opportunities for transboundary conservation of migratory birds in the East Asian-Australasian flyway. Conservation Biology 32: 740–743.

    Article  Google Scholar 

  • Yusuf, S., S. Hawken, S. Ôunpuu, T. Dans, A. Avezum, F. Lanas, M. McQueen, A. Budaj, et al. 2004. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): Case-control study. The Lancet 364: 937–952.

    Article  Google Scholar 

  • Zhang, Y., A.D. Fox, L. Cao, Q. Jia, C. Lu, H.H.T. Prins, and W.F. de Boer. 2019. Effects of ecological and anthropogenic factors on waterbird abundance at a Ramsar Site in the Yangtze River Floodplain. Ambio 48: 293–303.

    Article  Google Scholar 

  • Zhang, Y., Q. Jia, H.H.T. Prins, L. Cao, and W. de Boer. 2015. Individual-area relationship best explains goose species density in wetlands. PLoS ONE 10: e0124972.

    Article  CAS  Google Scholar 

  • Zhang, L., X. Wang, J. Zhang, Z. Ouyang, S. Chan, M. Crosby, D. Watkins, J. Martinez, et al. 2017. Formulating a list of sites of waterbird conservation significance to contribute to China’s Ecological Protection Red Line. Bird Conservation International 27: 153–166.

    Article  Google Scholar 

  • Zhang, Z., X. Wang, X. Zhao, B. Liu, L. Yi, L. Zuo, Q. Wen, F. Liu, et al. 2014. A 2010 update of national land use/cover database of China at 1:100000 scale using medium spatial resolution satellite images. Remote Sensing of Environment 149: 142–154.

    Article  Google Scholar 

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Acknowledgments

Funding was provided by NSF-NIH-USDA Ecology and Evolution of Infectious Diseases Program (Grant Number 1414374).

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Authors and Affiliations

  1. State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100875, China

    Tong Wu

  2. School of Life Sciences, Arizona State University, 427 East Tyler Mall, Tempe, AZ, 85287, USA

    Tong Wu, Charles Perrings, Chenwei Shang, James P. Collins, Ann Kinzig & Ben A. Minteer

  3. Center for Human-Environment System Sustainability (CHESS), State Key Laboratory of Earth Surface Processes and Resource Ecology (ESPRE), Beijing Normal University, Beijing, 100875, China

    Chenwei Shang

  4. EcoHealth Alliance, 460 West 34th Street - 17th Floor, New York, NY, 10001, USA

    Peter Daszak

  5. Global Institute of Sustainability, Arizona State University, 800 South Cady Mall, Tempe, AZ, 85287, USA

    Ann Kinzig

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Wu, T., Perrings, C., Shang, C. et al. Protection of wetlands as a strategy for reducing the spread of avian influenza from migratory waterfowl. Ambio 49, 939–949 (2020). https://doi.org/10.1007/s13280-019-01238-2

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