Abstract
Waterbirds represent the major natural reservoir for low pathogenic (LP) avian influenza viruses (AIV). Among the wide diversity of subtypes that have been described, two of them (H5 and H7) may become highly pathogenic (HP) after their introduction into domestic bird populations and cause severe outbreaks, as is the case for HP H5N1 in South-Eastern Asia. Recent experimental studies demonstrated that HP H5N1 AIV infection in ducks does not necessarily have significant pathological effects. These results suggest that wild migratory ducks may asymptomatically carry HP AIV and potentially spread viruses over large geographical distances. In this study, we investigated the potential spreading distance of HP AIV by common teal (Anas crecca), mallard (A. platyrhynchos), and Eurasian pochard (Aythya ferina). Based on capture-mark-recapture method, we characterized their wintering movements from a western Mediterranean wetland (Camargue, South of France) and identified the potential distance and direction of virus dispersal. Such data may be crucial in determining higher-risk areas in the case of HP AIV infection detection in this major wintering quarter, and may serve as a valuable reference for virus outbreaks elsewhere.
Similar content being viewed by others
References
Alerstam T (1990) Bird Migration. Cambridge: Cambridge University Press
Breban R, Drake JM, Stallknecht DE, Rohani P (2009) The role of environmental transmission in recurrent avian influenza epidemics. PLoS Computational Biology 5:e1000346
Brown JD, Stallknecht DE, Beck JR, Suarez DL, Swayne DE (2006) Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses. Emerging Infectious Diseases 12:1663-1670
Bub H (1991) Bird Trapping and Bird Banding: a Handbook for Trapping Methods all over the World. New York: Cornell University Press
Cramp S, Simmons KEL (1977) Handbook of the Birds of Europe the Middle East and North Africa, the Birds of Western Paleartic, Volume 1 Ostrich to Ducks. Oxford: Oxford University Press
Crawley MJ (1993) Glim for Ecologists. Oxford: Blackwell Scientific Publications
De Marco MA, Foni E, Campitelli L, Raffini E, Delogu M, Donatelli I (2003) Long-term monitoring for avian influenza viruses in wild bird species in Italy. Veterinary Research Communications 27(Suppl 1):107–114
Delany S, Scott D (2006) Waterbird Population Estimates, 4th Edition. Wageningen: Wetlands International.
Feare CJ (2007) The role of wild birds in the spread of HPAI H5N1. Avian Diseases 51:440-447
Gauthier-Clerc M, Le Maho Y (2001) Beyond bird marking with rings. Ardea 89:221-230
Gauthier-Clerc M, Lebarbenchon C, Thomas F (2007) Recent expansion of highly pathogenic avian influenza H5N1: a critical review. Ibis 149:202-214
Gilbert M, Xiao X, Domenech J, Lubroth J, Martin V, Lubroth J et al (2006) Anatidae migration in the western Palearctic and spread of highly pathogenic avian influenza H5N1 virus. Emerging Infectious Diseases 12:1650-1656
Globig A, Staubach C, Beer M, Köppen 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 and Emerging Diseases 56:57-72
Green AJ (1996) Analyses of globally threatened Anatidae in relation to threats, distribution, migration patterns, and habitat use. Conservation Biology 10:1435-1445
Guillemain M, Arzel C, Mondain-Monval JY, Schricke V, Johnson AR, Simon G (2006) Spring migration dates of teal Anas crecca ringed in the Camargue, southern France. Wildlife Biology 12:163-169
Guillemain M, Fritz H, Klaassen M, Johnson AR, Hafner H (2004) Fuelling rates of Garganey (Anas querquedula) staging in the Camargue, southern France, during spring migration. Journal of Ornithology 145:152-158
Guillemain M, Sadoul N, Simon G (2005) European flyway permeability and abmigration in Teal Anas crecca, an analysis based on ringing recoveries. Ibis 147:688-696
Hulse-Post DJ, Sturm-Ramirez KM, Humberd J, Seiler P, Govorkova EA, Krauss S, et al. (2005) Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. Proceedings of the National Academy of Sciences of the USA 102:10682–10687
Jourdain E, Gauthier-Clerc M, Bicout DJ, Sabatier P (2007) Bird migration routes and risk for pathogen dispersion into western Mediterranean wetlands. Emerging Infectious Diseases 13:365-372
Kayser Y, Gauthier-Clerc M, Béchet A, Poulin B, Massez G, Chérain Y et al (2008) Compte rendu ornithologique camarguais pour les années 2001–2006 [in French]. Revue d’Ecologie (Terre Vie) 63: 299–349
Keawcharoen J, van Riel D, van Amerongen G, Besteboer T, Beyer WE, van Lavieren R et al (2008) Wild ducks as long-distance vectors of highly pathogenic avian influenza. Emerging Infectious Diseases 14:600-607
Keller I, Korner-Nievergelt F, Jenni L (2009). Within-winter movements: a common phenomenon in the Common Pochard Aythya ferina. Journal of Ornithology 150:483-494
Kilpatrick AM, Chmura AA, Gibbons DW, Fleischer RC, Marra P, Daszak P (2006) Predicting the global spread of H5N1 avian influenza. Proceedings of the National Academy Sciences of the USA 103:19368–19373
Latorre-Margalef N, Gunnarson G, Munster VJ, Fouchier RAM, Osterhaus ADME, Elmberg J, et al. (2009) Effects of influenza A virus infection on migrating mallard ducks. Proceedings of the Royal Society B 276:1029–1036
Lebarbenchon C, Albespy F, Brochet AL, Grandhomme V, Renaud F, Fritz H et al (2009) Spread of avian influenza viruses by Common Teal (Anas crecca) in Europe. PLoS ONE 4:e7289
Lebarbenchon C, Chang CM, Grandhomme V, Dietrich M, Kayser Y, Elguero E, et al. (in press) Avian influenza circulation in the Camargue (south of France) during the 2006–2007 season. Avian Diseases
Lebarbenchon C, van der Werf S, Thomas F, Aubin JT, Azebi S, Cuvelier F et al (2007) Absence of detection of highly pathogenic H5N1 in migratory waterfowl in southern France in 2005–2006. Infection, Genetics and Evolution 7:604-608
Nagy A, Vostinakova V, Pindova Z, Hornickova J, Cernikova L, Sedlak K et al (2009) Molecular and phylogenetic analysis of the H5N1 avian influenza virus caused the first highly pathogenic avian influenza outbreak in poultry in the Czech Republic in 2007. Veterinary Microbiology 133:257-263
Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus ADME, Fouchier RAM (2006) Global patterns of influenza A virus in wild birds. Science 312:384-388
Pradel R, Rioux N, Tamisier A, Lebreton JD (1997) Individual turnover among wintering teal in Camargue: a mark-recapture study. Journal of Wildlife Management 61:816-821
R Development Core Team (2008) R: a language and environment for statistical computing—R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL: http://www.R-project.org
Ridgill SC, Fox AD (1990) Cold weather movements of waterfowl in western Europe. Slimbridge: IWRB Publication 13
Roche B, Lebarbenchon C, Gauthier-Clerc M, Chang CM, Thomas F, Renaud F et al (2009) Water-borne transmission drives avian influenza dynamics in wild birds: the case of the 2005-2006 epidemics in the Camargue area. Infection, Genetics and Evolution 9: 800-805
Rodrigues D, Figueiredo ME, Fabiao A, Encarnaçao V (2006) Ducks and the risk of avian influenza in Portugal. Airo 16:69-74
Scott DA, Rose PM (1996) Atlas of Anatidae populations in Africa and Western Eurasia. Wageningen: Wetlands International
Sturm-Ramirez KM, Hulse-Post DJ, Govorkova EA, Humberd J, Seiler P, Puthavathana P et al (2005) Are ducks contributing to the endemicity of highly pathogenic H5N1 influenza virus in Asia? Journal of Virology 79:11269-11279
Svazas S, Meissner W, Serebryakov V, Kozulin A, Grishanov G (2001) Changes of Wintering Sites of Waterfowl in Central and Eastern Europe. Vilnius: Oiseaux Migrateurs du Paléarctique Occidental “OMPO Vilnius” and Lithuanian Institute of Ecology
Tamisier A, Dehorter O (1999) Camargue, Ducks and Coots. Functioning and Gradual Change of a Prestigious Wintering Ground [in French]. Nîmes: Centre Ornithologique du Gard
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 1:e184
Weber TP, Stilianakis NI (2007) Ecologic immunology of avian influenza (H5N1) in migratory birds. Emerging Infectious Diseases 13:1139-1143
Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiological Reviews 56:152-179
Acknowledgments
The authors are most grateful to Luc Hoffmann, Hubert Kowalski, Heinz Hafner, Alan Johnson, and others who ringed ducks at the Tour du Valat for 25 years. We also thank Marc Lutz, Paul Isenmann, and the Centre de Recherche sur la Biologie des Populations d’Oiseaux (Muséum National d’Histoire Naturelle, Paris) for their help computerizing the Tour du Valat ringing database. Two anonymous referees provided useful comments on an earlier version of the manuscript. A.L. Brochet was funded by a Doctoral grant from Office National de la Chasse et de la Faune Sauvage, with additional funding from a research agreement between ONCFS, the Tour du Valat, Laboratoire de Biométrie et de Biologie Evolutive (UMR 5558 CNRS Université Lyon 1) and the Doñana Biological Station (CSIC). Camille Lebarbenchon was supported by a “Région Languedoc-Roussillon – Tour du Valat” PhD grant during this study. This work also received funding from the Agence Nationale de la Recherche through the Santé Environnement - Santé Travail scheme (contract number 2006-SEST-22), the European Union’s Framework Program for Research and Technological Development (FP6) (NEW-FLUBIRD project, contract number FP6-2005-SSP5B Influenza), and from the Agence Interorganisme pour la Recherche et le Développement.
Author information
Authors and Affiliations
Corresponding author
Appendix
Appendix
Median distance (D in km) and azimuth (A in decimal degrees) of recoveries for mallard (a), Eurasian pochard (b), and common teal (c), ringed during each month of the winter. Numbers in brackets give minimum and maximum values. Note that sample size (n) may be lower for azimuth than for distance travelled because, when birds were recovered at the ringing site itself, distance = 0 but azimuth could not be computed.
Month | No. of days since ringing | |||
---|---|---|---|---|
0–10 days | 11–20 days | 21–30 days | ||
(a) | ||||
September | D | 11.0 (0.0/19.6), n = 7 | 14.6 (0.0/,20.7) n = 4 | No data |
A | −90.0 (−106.4/144.3), n = 5 | −51.1 (−51.1/144.0), n = 3 | No data | |
October | D | 7.8 (0.0/24.0), n = 8 | 10.1 (5.5/45.1), n = 3 | 7.7 (5.5/7.7), n = 3 |
A | 111.5 (−89.9/111.5), n = 5 | 47.4 (23.5/47.4), n = 3 | 44.1 (44.0/47.4), n = 3 | |
November | D | 0.0 (0.0/20.6), n = 19 | 8.6 (0.0/30.3), n = 14 | 0.0 (0.0/18.3), n = 3 |
A | 154.2 (−90.0/154.2), n = 9 | −90.0 (−90.0/154.2), n = 11 | 144.0, n = 1 | |
December | D | 3.3 (0.0/225.5), n = 35 | 2.7 (0.0/134.9), n = 13 | 3.9 (0.0/153.1), n = 14 |
A | −90.0 (−137.8/180.0), n = 23 | −90.0 (−114.7/−23.5), n = 10 | 115.0 (-115.3/144), n = 10 | |
January | D | 7.9 (0.0/369.5), n = 24 | 11.0 (0.0/450.7), n = 18 | 11.1 (0.0/488.4), n = 15 |
A | −175.9 (−160.0/168.3), n = 18 | 149.8 (−90.0/149.8), n = 15 | 149.8 (−106.4/154.2), n = 12 | |
February | D | 2.7 (0.0/19.1), n = 7 | 1.3 (0.0/5.5), n = 6 | 201.2 (10.7/391.8), n = 2 |
A | −90.0 (−144.0/39.1), n = 6 | −90.0 (−90.0/47.4), n = 4 | 98.7 (47.6/149.8), n = 2 | |
March | D | 2.3 (0.0/644.9), n = 7 | No data | No data |
A | 141.9 (−144.0/67.9), n = 4 | No data | No data | |
(b) | ||||
September | D | No data | No data | No data |
A | No data | No data | No data | |
October | D | 4.6, n = 1 | No data | No data |
A | −35.9, n = 1 | No data | No data | |
November | D | 16.3 (6.2/20.9), n = 5 | 16.3 (16.3/16.3), n = 2 | 382.5, n = 1 |
A | −55.3 (−105.3/154.2), n = 5 | −55.3 (−55.3/−55.3), n = 2 | −78.9, n = 1 | |
December | D | 9.2 (3.3/74.2), n = 5 | 2.7 (1.9/252.4), n = 3 | 4.6, n = 1 |
A | 154.2 (−105.3/154.2), n = 4 | 2.9 (−90.0/ 2.9), n = 3 | −35.9, n = 1 | |
January | D | 11.3 (0.0/19.7), n = 6 | 12.7 (4.6/20.9), n = 4 | 19.8 (0.0/39.7), n = 2 |
A | −54.3 (−160.1/−48.6), n = 4 | −70.971.1 (−105.3/−35.9), n = 4 | −79.1, n = 1 | |
February | D | 1.9 (0.0/14.8), n = 5 | 0.0 n = 1 | 17.6 (3.3/20.7), n = 3 |
A | 89.9 (-55.4/89.9), n = 3 | No data | 55.4 (−51.1/55.4), n = 3 | |
March | D | 0.7 (0.0/2.7), n = 4 | 0.9 (0.0/1.9), n = 2, n = 1 | 6.2, n = 1 |
A | −90.0, n = 1 | No data | −25.8, n = 1 | |
(c) | ||||
September | D | 11.4 (4.4/18.3), n = 2 | 32.6 (13.2/51.9), n = 2 | 268.8 (54.6/483.6), n = 2 |
A | −165.3 (−114.7/144.0), n = 2 | −135.6 (−79.5/168.3), n = 2 | −80.3 (−84.6/−75.9), n = 2 | |
October | D | 8.3 (0.0/99.1), n = 8 | 10.9 (2.7/18.6), n = 5 | 2.7, n = 1 |
A | −95.7 (−101.5/168.3), n = 6 | −90.0 (−90.0/168.3), n = 5 | −90.0, n = 1 | |
November | D | 2.5 (0.0/26.4), n = 18 | 165.8 (0.0/1149.1), n = 18 | 169.3 (2.7/482.9), n = 26 |
A | −144.0 (−144.0/154.2), n = 11 | −92.7 (−104.1/88.1), n = 17 | −115.3 (−138.1/173.1), n = 26 | |
December | D | 6.7 (0.0/911.0), n = 169 | 146.3 (0.0/578.5), n = 103 | 216.1 (0.0/1004.0), n = 71 |
A | −103.3 (−144/180.0), n = 107 | −99.4 (−151.0/171.7), n = 94 | −93.7 (−139.2/171.1), n = 68 | |
January | D | 24.2 (0.0/807.9), n = 200 | 171.9 (0.0/940.7), n = 128 | 252.1 (0.0/894.4), n = 143 |
A | −117.7 (−160.0/173.1), n = 192 | −125.3 (−162.1/173.1), n = 118 | 161.2 (−141.8/168.3), n = 136 | |
February | D | 18.6 (0.0/843.1), n = 155 | 170.7 (0.0/726.6), n = 57 | 282.1 (0.0/738.7), n = 53 |
A | 95.5 (−160.0/168.3), n = 139 | 90.7 (−144.0/168.3), n = 54 | 73.4 (−160.0/180), n = 51 | |
March | D | 22.8 (2.1/711.4), n = 43 | 416.2 (0.0/1107.1), n = 29 | 424.9 (2.3/930.7), n = 11 |
A | 75.7 (−144.7/171.7), n = 43 | 66.4 (−144.0/154.2), n = 28 | 64.9 (−144.0/173.1), n = 11 |
Rights and permissions
About this article
Cite this article
Brochet, AL., Guillemain, M., Lebarbenchon, C. et al. The Potential Distance of Highly Pathogenic Avian Influenza Virus Dispersal by Mallard, Common Teal and Eurasian Pochard. EcoHealth 6, 449–457 (2009). https://doi.org/10.1007/s10393-010-0275-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-010-0275-4