, Volume 7, Issue 2, pp 226–236 | Cite as

The Cold European Winter of 2005–2006 Assisted the Spread and Persistence of H5N1 Influenza Virus in Wild Birds

  • Daniela Ottaviani
  • S. de la Rocque
  • S. Khomenko
  • M. Gilbert
  • S. H. Newman
  • B. Roche
  • K. Schwabenbauer
  • J. Pinto
  • T. P. Robinson
  • J. Slingenbergh
Original Contribution


In January 2006, a major cold spell affected Europe, coinciding with an increase of H5N1 influenza virus detected in wild birds, mostly dead mute swans, starting along the River Danube and the Mediterranean coast line. Subsequently H5N1 detections in wild birds were concentrated in central and western parts of Europe, reaching a peak in mid February. We tested the hypothesis that the geographic distribution of these H5N1 infections was modulated by the long-term wintering line, the 0°C isotherm marking the limit beyond which areas are largely unsuitable for wintering waterfowl. Given the particularly cold 2005–2006 European winter, we also considered the satellite-derived contemporary frost conditions. This brought us to select the long-term maximum rather than the mean January 0°C isotherm as the best approximation for the 2005–2006 wintering line. Our analysis shows that H5N1 detection sites were closer to the wintering line than would be expected by chance, even when the geographic distribution of water bird wintering sites was accounted for. We argue that partial frost conditions in water bodies are conducive to bird congregation, and this may have enhanced H5N1 transmission and local spread. Because the environmental virus load also would build up in these hot spots, H5N1 virus may have readily persisted during the spring, at least in cooler areas. We conclude that H5N1 introduction, spread, and persistence in Europe may have been enhanced by the cold 2005–2006 winter.


Avian influenza waterfowl outbreaks seasonality Europe 



The views expressed in the publication are those of the authors and do not necessarily reflect the views of the Food and Agriculture Organization of the United Nations.

Supplementary material

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10393_2010_316_MOESM2_ESM.eps (674 kb)
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  1. Alerstam T (1990) Bird migration. Cambridge University Press, UKGoogle Scholar
  2. Arzel C, Elmberg J, Guillemain M (2006) Ecology of spring migrating Anatidae: a review. Journal of Ornithology 147:67-184CrossRefGoogle Scholar
  3. Atkinson PW, Clark JA, Delany S, Diagana CH, du Feu C, Fiedler W, et al. (2006) Urgent preliminary assessment of ornithological data relevant to the spread of Avian Influenza in Europe. In: Report to the European Commission, Delany S, Veen J, Clark JA (editors), Study contract: 07010401/2005/425926/MAR/B4Google Scholar
  4. Augustin NH, Mugglestone MA, Buckland ST (1996) An autologistic model for the spatial distribution of wildlife. Journal of Applied Ecology 33:339-347CrossRefGoogle Scholar
  5. Avram M (2008) The role of domestic waterfowl in H5N1 virus transmission in the Danube delta. Consultancy report. Food and Agriculture Organization of the United Nations. EMPRES. Rome, ItalyGoogle Scholar
  6. Baillie SR, Clark NA, Ogilvie MA (1986) Cold weather movements of waterfowl and waders: an analysis of ringing recoveries. BTO Research Report 19, Tring: British Trust for OrnithologyGoogle Scholar
  7. Baldassare GAR, Whyte RJ, Bolen EG (1986) Body weight and carcass composition of nonbreeding Green-winged Teal on Southern High Plains of Texas. Journal of Wildlife Management 50:420–426CrossRefGoogle Scholar
  8. BirdLife International (2006) BirdLife statement on avian influenza. BirdLife International. Available:
  9. Boos M, Zorn T, Le Maho Y, Groscolas R, Robin JP (2002) Sex differences in body composition of wintering mallards (Anas platyrhynchos): possible implications for survival and reproductive performance. Bird Study 49:212–218CrossRefGoogle Scholar
  10. Breban R, Drake JM, Stallknecht DE, Rohani P (2009) The role of environmental transmission in recurrent avian influenza epidemics. Plos 5:e1000346CrossRefGoogle Scholar
  11. Bregnballe T, Frederiksen M, Gregersen J (2006) Effects of distance to wintering area on arrival date and breeding performance in Great Cormorants Phalacrocorax carbo. Ardea 94:619-630Google Scholar
  12. Brown JD, Goekjian G, Poulson R, Valieka S, Stallknecht DE (2009) Avian influenza virus in water: infectivity is dependent on pH, salinity and temperature. Veterinary Microbiology 136:20-26CrossRefGoogle Scholar
  13. Cao C, Barter M, Lei G (2008) New Anatidae population estimates for eastern China: implications for current flyway estimates. Biological Conservation 141:2301-2309CrossRefGoogle Scholar
  14. Chen H, Li KS, Wang J, Fan XH, Rayner JM, et al. (2006) Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. Proceeding National Academy of Science USA 103:2845–2850CrossRefGoogle Scholar
  15. Choundhury S, Black JM (1991) Testing the behavioral dominance and dispersal hypothesis in Pochard. Ornis 22:155-159CrossRefGoogle Scholar
  16. Cramp S, Simmons K (1977) Birds of the Western Paleartic: Handbook of the Birds of Europe, the Middle East and North Africa. Vol I (Ostriches to Ducks). Oxford: Oxford University PressGoogle Scholar
  17. Crick HQP, Atkinson PW, Newson SE, Robinson RA, Snow L, Balmer DE, et al. (2006) Avian Influenza Incursion Analysis (through wild birds). BTO Research Report 448, Thetford: British Trust for OrnithologyGoogle Scholar
  18. Danish Veterinary and Food Administration (2007) Highly pathogenic avian influenza H5N1 in Denmark, Spring 2006- Report. Available: Accessed 22 March 2008
  19. Delany S, Scott D (2006) Waterbird Population estimates-Fourth Edition, Wageningen: Wetlands InternationalGoogle Scholar
  20. Dormann CF, Mc Pherson MJ, Araujo MB, Bivand R, Bolliger J, Carl G, et al. (2007) Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30:609-628CrossRefGoogle Scholar
  21. Drent RH, Fox AD, Stahl J (2006). Travel to breed. Journal of Ornithology 147:122–134CrossRefGoogle Scholar
  22. Feare CJ, Yasué M (2006) Asymptomatic infection with highly pathogenic avian influenza H5N1 in wild birds: how sound is the evidence? Virology Journal 3:96CrossRefGoogle Scholar
  23. Food and Agriculture Organization of the United Nations (2006) Emergency Prevention System Global animal disease information system. Available:
  24. Gaidet N, Dodman T, Caron A, Balanca G, Desvaux S, Goutard F, et al. (2007) Influenza surveillance in wild birds in Eastern Europe, the middle East and Africa: preliminary results from an ongoing FAO-led survey. Journal of Wildlife Disease 43:S22-S28Google Scholar
  25. Gaidet N, Cattoli G, Hammoumi S, Newman S, Hagemeijer W, Takekawa JY, et al. (2008) Evidence of infection by H5N2 highly pathogenic avian influenza viruses in healthy wild waterfowl. Plos Pathogen 4:e1000127CrossRefGoogle Scholar
  26. Gauthier-Clerc M, Lebarbenchon C, Thomas F (2007) Recent expansion of highly pathogenic avian influenza H5N1: a critical review. Ibis 149:202-214CrossRefGoogle Scholar
  27. Gill JS, Webby R, Gilchrist MJR, Gray GC (2006) Avian influenza among waterfowl hunters and wildlife professionals. Emergency Infectious Disease 12:1284-1286Google Scholar
  28. Gilbert M, Xia XM, Domenech J, Lubroth J, Martin V, Slingenbergh J (2006) Anatidae migration in the Western Paleartic and the spread of highly pathogenic avian influenza H5N1 virus. Emergency Infectious Disease 12:1650-1656Google Scholar
  29. Gilissen N, Haanstra L, Delany S, Boere G, Hagemeijer W (2002) Numbers and distribution of wintering waterbirds in the Western Palearctic and Southwest Asia in 1997, 1998 and 1999. Results from the International Waterbird Census. Wetlands International Global Series No. 11, Wageningen: Wetlands InternationalGoogle Scholar
  30. Globig A, Staubach C, Beer M, Koppen U, Fiedler W, Nieburg M, et al. (2009) Epidemiological and ornithological aspects of outbreaks of highly pathogenic avian influenza virus H5N1 of Asian lineage in wild birds in Germany, 2006 and 2007. Transboundary Emergency Disease 56:57-72CrossRefGoogle Scholar
  31. Hars J, Ruette S, Benmergui M, Fouque C, Fourneir J, Legouge A, et al. (2008) The epidemiology of the highly pathogenic H5N1 avian influenza in mute swan (Cygnus olor) and other Anatidae in the Dombes region (France), 2006. Journal Wildlife Disease 44:811-823Google Scholar
  32. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surface for Global Land areas. International Journal of Climatology 25:1965-1978CrossRefGoogle Scholar
  33. Hofmann MA, Renzullo S, Baumer A (2008) Phylogenetic characterization of H5N1 highly pathogenic avian influenza viruses isolated in Switzerland in 2006. Virus Genes 37:407-413CrossRefGoogle Scholar
  34. Kalthoff D, Breithaupt A, Teifke JP, Globig A, Harder T, Mettenleiter TC, Beer M (2008) Highly pathogenic avian influenza virus (H5N1) in experimentally infected adult mute swans. Emerging Infectious Diseases 14:1267-1270CrossRefGoogle Scholar
  35. Keawcharoen J, van Riel D, Amerongen G, Bestebroer T, Beyer WE, van Lavieren R, et al. (2008) wild ducks as long-distance vectors of highly pathogenic influenza (H5N1). Emerging Infectious Disease 12:1650-1656Google Scholar
  36. Keitt TH, Bjørnstad ON, Dixon PM, Citron-Pousty S (2002) Accounting for spatial pattern when modeling organism-environment interactions. Ecography 25:616–625CrossRefGoogle Scholar
  37. Keller I, Korner-Nievergelt F, Jenni L (2009) Within-winter movements: a common phenomenon in the common pochard Aythya farina. Journal of Ornithology 150:483-494CrossRefGoogle Scholar
  38. Kilpatrick AM, Chmura AA, Gibbons DW, Fleischer RC, Marra PP, Daszak P (2006) Predicting the global spread of H5N1 avian influenza. Pnas 103:19368-19373CrossRefGoogle Scholar
  39. Kreuzbergh-Mukhina EA (2006) The effect of habitat change on the distribution of waterbirds in Uzbekistan and the possible implications of climate change. In: Waterbirds Around the World, Boere GC, Galbraith CA, Stroud DA (editors), Edinburgh, UK: The Stationery Office, pp 277-282Google Scholar
  40. Lang AS, Kelly A Runstadler JA (2008) Prevalence and diversity of avian influenza viruses in environmental reservoirs. Journal of General Virology 89:509-519CrossRefGoogle Scholar
  41. Longcore JR, Gibbs JP (1988) Distribution and numbers of American Black ducks among the Maine coast during the severe winter of 1980–1981. In: Waterfowl in Winter, Weller MW (editor), Minneapolis: University of Minnesota Press, pp 377–389Google Scholar
  42. McPherson JM, Jetz W, Rogers DJ (2004) The effects of species’ range sizes on the accuracy of distribution models: ecological phenomenon or statistical artefact? Journal of Applied Ecology 41:811-823CrossRefGoogle Scholar
  43. Munoz MJ, Sanchez-Vizcaìno JM, Peris S (2006) Short communication. Can highly pathogenic influenza (HPAI) reach the Iberia peninsula from Asia by means of migratory birds? Spanish Journal of Agricultural Research 4:140-145Google Scholar
  44. Nagy A, Machova J, Hornickova J, Tomci M, Nagl I, Horyna B, Holko I (2007) Highly pathogenic avian influenza virus subtype H5N1in mute swans in the Czech Republic. Veterinary Microbiology 120:9–16CrossRefGoogle Scholar
  45. Nankinov DN (1996) Coastal parks and reserves along the Black Sea and their importance for seabirds. Marine Ornithology 24:29-34Google Scholar
  46. Newman SH, Honhold N, Erciyas K, Sanz-Alvarez J (2008) Investigation of the role of wild birds in highly pathogenic avian influenza outbreaks in Turkey between January and February 2008: Turkey Mission Report. Food and Agriculture Organization of the United Nations EMPRES, Rome, ItalyGoogle Scholar
  47. Nilsson L (1979) Variation in the production of young of swans wintering in Sweden. Wildfowl 30:129–134Google Scholar
  48. NOAA/NESDIS/OSDPD/SSD (2006) IMS Daily Northern Hemisphere Snow and Ice Analysis at 4 km and 24 km Resolution. Boulder, CO: National Snow and Ice Data Center. Digital mediaGoogle Scholar
  49. Owen M, Cook WA (1977) Variations in body weight, wing length and condition of Mallard Anas platyrhynchos and their relationship to environmental changes. Journal of Zoology 183:377–395CrossRefGoogle Scholar
  50. Pinto JG, Brücher T, Fink AH, Krüger A (2007) Extraordinary snow accumulations over parts of central Europe during the winter of 2005/06 and weather-related hazards. Royal Meteorological Society, Weather 62:16-21. doi:  10.1002/wea.19 Google Scholar
  51. Prosser D, Takekawa JY, Newman SH, Yan B, Douglas DC, Hou Y, et al. (2009) Satellite-marked waterfowl reveal migratory connection between H5N1 outbreak areas in China and Mongolia. Ibis 151:568-576CrossRefGoogle Scholar
  52. Ridgill SC, Fox AD (1990) Cold weather movements of waterfowl in Western Europe. Slim bridge: IWRB Special Publication 13Google Scholar
  53. Rinder M, Lang V, Fuchs C, Hafner-Marx A, Bogner K, Neubauer A, et al. (2007) Genetic evidence for multi-event imports of avian influenza virus A (H5N1) into Bavaria, Germany. Journal Veterinary Diagnostic Investigation 19:279-282Google Scholar
  54. Root T (1988) Environmental factors associated with avian distributional boundaries. Journal of Biogeography 15:489-505CrossRefGoogle Scholar
  55. Rustamov AN, Kovshar AF (2007) The Birds of Middle Asia, AlmatyGoogle Scholar
  56. Saad MD, Ahmed LS, Gamal-Eldein MA, Fouda MK, Khalil FM, et al. (2007) Possible avian influenza (H5N1) from migratory bird, Egypt. Emerging Infectious Disease 13:1120–1121Google Scholar
  57. Sabirovic M, Wilesmith J, Hall S, Coulson N, Landeg F (2006) Situation analysis – outbreaks of HPAI H5N1 virus in Europe during 2005/2006: an overview and commentary. London: Department of Environment, Food and Rural Affairs. Available:
  58. Scaife AA, Knight JR (2008) Ensemble simulations of the cold European winter of 2005–2006. Quarterly Journal of the Royal Meteorological Society. doi: 10.1002/qj.312
  59. Scott DA, Rose PM (1996) Atlas of Anatidae populations in Africa and western Eurasia Wageningen: Wetlands International. Available:
  60. Si Y, Skidmoire AK, Wang T, de Boer WF, Debba P, Toxopeus AG, et al. (2009) Spatio-temporal dynamics of global H5N1 outbreaks match bird migration patterns. Geospatial Health 4:65-78Google Scholar
  61. Spencer R (1982) Birds in winter: an outline. Bird Study 29:169-182CrossRefGoogle Scholar
  62. Starick E, Beer M, Hoffmann B, Staubach C, Werner O, Globig A, et al. (2008) Phylogenetic analyses of highly pathogenic avian influenza virus isolates from Germany in 2006 and 2007 suggest at least three separate introductions of H5N1 virus. Veterinary Microbiology 128:243-252CrossRefGoogle Scholar
  63. Steffen O, Powell AN, Dickson DL (2008) Timing and distance of king eider migration and winter movements. The Condor 110:296–305. DOI  10.1525/cond.2008.8502 CrossRefGoogle Scholar
  64. Stumberger B (1999) Results of the mid-winter waterfowl counts in January 1999 in Slovenia. Acrocephalus 20:6-22Google Scholar
  65. Stumberger B (2000) Results of the mid-winter waterfowl counts in January 2001 in Slovenia. Acrocephalus 21:261-274Google Scholar
  66. Stumberger B (2001) Results of the mid-winter waterfowl counts in January 2001 in Slovenia. Acrocephalus 22:171-174Google Scholar
  67. Stumberger B (2002) Results of the mid-winter waterfowl counts in January 2002 in Slovenia. Acrocephalus 23:43-47Google Scholar
  68. Stumberger B (2005) Results of the mid-winter waterfowl counts in January 2001 in Slovenia. Acrocephalus 26:99-103Google Scholar
  69. Suter W, Van Eerden MR (1992). Simultaneous mass starvation of wintering diving ducks in Switzerland and the Netherlands: a wrong decision in the right strategy? Ardea 80:229-242Google Scholar
  70. Szeleczky Z, Dán A, Ursu K, Ivanics E, Kiss I, Erdélyi K (2009) Four different sublineages of highly pathogenic avian influenza H5N1 introduced in Hungary in 2006–2007. Veterinary Microbiology 139:24-33CrossRefGoogle Scholar
  71. Tucakov M (2005) Numbers and seasonal activity of the mute swan (Cygnus olor) on the Kolut fishpond (NW Serbia). Ring 27:221-226CrossRefGoogle Scholar
  72. Van Gils JA, Munster VJ, Radersma R, Liefhebber D, Fouchier RAM, Klaassen M (2007) Hampered foraging and migratory performance in swans infected with low-pathogenic avian influenza A virus. Plos one 2:e184CrossRefGoogle Scholar
  73. Ward P, Maftei D, Apostu C, Suru A (2008) Geostatistical visualisation and spatial statistics foe evaluation of the dispersion of epidemic highly pathogenic avian influenza subtype H5N1. Veterinary Research 39:22CrossRefGoogle Scholar
  74. Weber TP, Stilianakis NI (2007) Ecological immunology of avian influenza (H5N1) in migratory birds. Emerging Infectious Disease 13:1139-1143Google Scholar
  75. Weber TP, Stilianakis NI (2008) Migratory birds, the H5N1 influenza virus and the scientific method. Virology Journal 5:1-3CrossRefGoogle Scholar
  76. White RJ, Bolen EG (1984) Impact of winter stress on mallard body composition. Condor 86:477-482CrossRefGoogle Scholar
  77. Wilking H, Ziller M, Staubach C, Globig A, Harder TC, Conraths FJ (2009) Chances and limitations of wild bird monitoring for the avian influenza virus H5N1. Detection of pathogens highly mobile in time and space. Plos 4:e6639CrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2010

Authors and Affiliations

  • Daniela Ottaviani
    • 1
  • S. de la Rocque
    • 1
    • 2
  • S. Khomenko
    • 1
  • M. Gilbert
    • 3
  • S. H. Newman
    • 1
  • B. Roche
    • 4
    • 5
  • K. Schwabenbauer
    • 6
  • J. Pinto
    • 1
  • T. P. Robinson
    • 1
  • J. Slingenbergh
    • 1
  1. 1.Food and Agriculture Organization of the United NationsRomeItaly
  2. 2.Centre de Coopération Internationale en Recherche Agronomique pour le DéveloppementMontpellierFrance
  3. 3.Biological control and spatial ecologyUniversité Libre de BruxellesBrusselsBelgium
  4. 4.Department of Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA
  5. 5.UMI IRD/UPMC UMMISCOBondy CedexFrance
  6. 6.Federal Ministry of Food, Agriculture and Consumer ProtectionBonnGermany

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