, Volume 7, Issue 3, pp 283–293 | Cite as

Ecological Modeling of the Spatial Distribution of Wild Waterbirds to Identify the Main Areas Where Avian Influenza Viruses are Circulating in the Inner Niger Delta, Mali

  • Julien Cappelle
  • Olivier Girard
  • Bouba Fofana
  • Nicolas Gaidet
  • Marius Gilbert
Original Contribution


Predicting areas of disease emergence when no epidemiological data is available is essential for the implementation of efficient surveillance programs. The Inner Niger Delta (IND) in Mali is a major African wetland where >1 million Palearctic and African waterbirds congregate. Waterbirds are the main reservoir of Avian Influenza Viruses (AIV). Our objective was to model their spatial distribution in order to predict where these viruses would be more likely to circulate. We developed a generalized linear model (GLM) and a boosted regression trees (BRT) model based on total aerial bird counts taken in winter over 6 years. We used remotely sensed environmental variables with a high temporal resolution (10 days) to predict the spatial distribution of four waterbird groups. The predicted waterbird abundances were weighted with an epidemiological indicator based on the prevalence of low pathogenic AIV reported in the literature. The BRT model had the best predictive power and allowed prediction of the high variability of waterbird distribution. Years with low flood levels showed areas with a higher risk of circulation and had better spatial distribution predictions. Each year, the model identified a few areas with a higher risk of AIV circulation. This model can be applied every 10 days to evaluate the risk of AIV emergence in wild waterbirds. By taking into account the IND’s ecological variability, it allows better targeting of areas considered for surveillance. This could enhance the control of emerging diseases at a local and regional scale, especially when resources available for surveillance programs are scarce.


emerging infectious diseases surveillance wild birds distribution models AIV boosted regression trees 



We thank Bourama Niagate from the Direction Nationale des Eaux et Forêts du Mali, Jean-Marie Boutin and Jean Thal from the Office National de la Chasse et de la Faune Sauvage (ONCFS), and all the people that helped collect the data. We also thank Leo Zwartz and Jan Van der Kamp from Altenburg and Wymenga (A&W) for sharing their knowledge about the Inner Niger Delta, and for providing helpful advice on the spatial modeling. Finally, we thank Olivier Gimenez from the Centre National de Recherche Scientifique (CNRS) for advice during the early development of the models.


  1. Artois M, Bicout D, Doctrinal D, Fouchier R, Gavier-Widen D, Globig A, et al. (2009) Outbreaks of highly pathogenic avian influenza in Europe: the risks associated with wild birds. Revue Scientifique Et Technique–Office International Des Epizooties 28:69–92Google Scholar
  2. Augustin NH, Mugglestone MA, Buckland ST (1996) An autologistic model for the spatial distribution of wildlife. Journal of Applied Ecology 33:339–347.CrossRefGoogle Scholar
  3. Barry SC, Welsh AH (2002) Generalized additive modelling and zero inflated count data. Ecological Modelling 157:179–188.CrossRefGoogle Scholar
  4. Brochet A-L, Guillemain M, Lebarbenchon C, Simon G, Fritz H, Green A, et al. (2009) The potential distance of highly pathogenic avian influenza virus dispersal by mallard, common teal and Eurasian pochard. EcoHealth 6:449–457CrossRefGoogle Scholar
  5. 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.Google Scholar
  6. Brown JD, Stallknecht DE, Swaynet DE (2008) Experimental infection of swans and geese with highly pathogenic avian influenza virus (H5N1) of Asian lineage. Emerging Infectious Diseases 14:136–142.CrossRefGoogle Scholar
  7. Chen H, Li Y, Li Z, Shi J, Shinya K, Deng G, et al. (2006) Properties and dissemination of H5N1 viruses isolated during an influenza outbreak in migratory waterfowl in western China. Journal of Virology 80:5976–5983.CrossRefGoogle Scholar
  8. Chen JM, Liu J, Cihlar J, Goulden ML (1999) Daily canopy photosynthesis model through temporal and spatial scaling for remote sensing applications. Ecological Modelling 124:99–119.CrossRefGoogle Scholar
  9. CIESIN (2005) Gridded Population of the World, Version 3 (GPWv3): Population Density Grids. Socioeconomic Data and Applications Center (SEDAC), Columbia University. Accessed 10 October 2009
  10. Clements ACA, Pfeiffer DU (2009) Emerging viral zoonoses: frameworks for spatial and spatiotemporal risk assessment and resource planning. Veterinary Journal 182:21–30.CrossRefGoogle Scholar
  11. Cumming G, Hockey PAR, Bruinzeel LW, Du Plessis MA (2008) Wild birds movements and avian influenza risk mapping in Southern Africa. Ecology and Society 13:26Google Scholar
  12. Elith J, Graham CH, Anderson RP, Dudik M, Ferrier S, Guisan A, Hijmans RJ, et al. (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151.CrossRefGoogle Scholar
  13. Elith J, Leathwick JR, Hastie T (2008) A working guide to boosted regression trees. Journal of Animal Ecology 77:802–813.CrossRefGoogle Scholar
  14. Fusaro A, Joannis T, Monne I, Salviato A, Yakubu B, Meseko C, Oladokun T, et al. (2009) Introduction into Nigeria of a distinct genotype of avian influenza virus (H5N1). Emerging Infectious Diseases 15:445–447.CrossRefGoogle Scholar
  15. Gaidet N, Dodman T, Caron A, Balanca G, Desvaux S, Goutard F, et al. (2007) Avian influenza viruses in water birds, Africa. Emerging Infectious Diseases 13:626–629.CrossRefGoogle Scholar
  16. Gaidet N, Cattoli G, Hammoumi S, Newman SH, Hagemeijer W, Takekawa JY, et al. (2008) Evidence of infection by H5N2 highly pathogenic avian influenza viruses in healthy wild waterfowl. PLoS Pathogens 4:e1000127Google Scholar
  17. Gaidet N, Cappelle J, Takekawa JY, Prosser DJ, Iverson SA, Douglas DC, et al. (2010) Potential spread of highly pathogenic avian influenza H5N1 by wildfowl: dispersal ranges and rates determined from largescale satellite telemetry. Journal of Applied Ecology 47:1147–1157CrossRefGoogle Scholar
  18. Gao BC (1996) NDWI—a normalized difference water index for remote sensing of vegetation liquid water from space. Remote Sensing of Environment 58:257–266.CrossRefGoogle Scholar
  19. Girard O (2006) Anatidae wintering in the Inner Niger Delta, Mali. In: Waterbirds Around the World, Boere GC, Galbraith CA, Stroud DA (editors), Edinburgh, UK: The Stationery Office, p 960Google Scholar
  20. Girard O, Thal J, Niagate B (2004) The Antadis (Anatidae) wintering in the Inner Niger Delta. Game and Wildlife Science 21:107–137.Google Scholar
  21. Gond V, Bartholome E, Ouattara F, Nonguierma A, Bado L (2004) Monitoring and mapping of waters and wetlands in arid regions using the SPOT-4 VEGETATION imaging system. International Journal of Remote Sensing 25:987–1004.CrossRefGoogle Scholar
  22. Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecological Modelling 135:147–186.CrossRefGoogle Scholar
  23. Hastie T, Tibshirani R, Friedman JH (2001) The Elements of Statistical Learning: Data Mining, Inference, and Prediction, New York: Springer-Verlag.Google Scholar
  24. Hesterberg U, Harris K, Stroud DA, Guberti V, Busani L, Pittman, M, et al. (2009) Avian influenza surveillance in wild birds in the European Union in 2006. Influenza and Other Respiratory Viruses 3:1–14.CrossRefGoogle Scholar
  25. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. (2008) Global trends in emerging infectious diseases. Nature 451:990–993CrossRefGoogle Scholar
  26. Keawcharoen J, van Riel D, van Amerongen G, Bestebroer T, Beyer WE, van Lavieren R, et al. (2008) Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5NI). Emerging Infectious Diseases 14:600–607.CrossRefGoogle Scholar
  27. Koopmans M, Wilbrink B, Conyn M, Natrop G, van der Nat H, Vennema H, et al. (2004) Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. The Lancet 363:587–593.CrossRefGoogle Scholar
  28. Leathwick JR, Elith J, Rowe D, Julian K (2009) Robust planning for restoring diadromous fish species in New Zealand’s lowland rivers and streams. New Zealand Journal of Marine and Freshwater Research 43:659–671.CrossRefGoogle Scholar
  29. Leyrer J, Spaans B, Camara M, Piersma T (2006) Small home ranges and high site fidelity in red knots (Calidris c. canutus) wintering on the Banc d’Arguin, Mauritania. Journal of Ornithology 147:376–384.CrossRefGoogle Scholar
  30. Manel S, Williams HC, Ormerod SJ (2001) Evaluating presence–absence models in ecology: the need to account for prevalence. Journal of Applied Ecology 38:921–931.CrossRefGoogle Scholar
  31. McCullagh P, Nelder JA (1989) Generalized Linear Models, London: Chapman & Hall.Google Scholar
  32. Morens DM, Folkers GK, Fauci AS (2004) The challenge of emerging and re-emerging infectious diseases. Nature 430:242–249.CrossRefGoogle Scholar
  33. Morens DM, Folkers GK, Fauci AS (2008) Emerging infections: a perpetual challenge. Lancet Infectious Diseases 8:710–719.CrossRefGoogle Scholar
  34. Morse SS (1995) Factors in the emergence of infectious-diseases. Emerging Infectious Diseases 1:7–15.CrossRefGoogle Scholar
  35. Munster VJ, Baas C, Lexmond P, Waldenström J, Wallensten A, Fransson T, et al. (2007) Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathogens 3:e61.CrossRefGoogle Scholar
  36. OIE (2009) Highly Pathogenic Avian Influenza, Germany. World Organization for Animal Health. Accessed 12 July 2010
  37. Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus A, Fouchier RAM (2006) Global patterns of influenza A virus in wild birds. Science 312:384–388.CrossRefGoogle Scholar
  38. Pearce J, Ferrier S (2000) Evaluating the predictive performance of habitat models developed using logistic regression. Ecological Modelling 133:225–245.CrossRefGoogle Scholar
  39. R Development Core Team (2009) R: A Language and Environment for Statistical Computing, v. 2.9.0, Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
  40. Reed BC, Brown JF, VanderZee D, Loveland TR, Merchant JW, Ohlen DO (1994) Measuring phenological variability from satellite imagery. Journal of Vegetation Science 5:703–714.CrossRefGoogle Scholar
  41. Roche B, Lebarbenchon C, Gauthier-Clerc M, Chang C-M, 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.CrossRefGoogle Scholar
  42. Saad MD, Ahmed LS, Gamal-Eldein MA, Fouda MK, Khalil FM, Yingst SL (2007) Possible avian influenza (H5N1) from migratory bird, Egypt. Emerging Infectious Diseases 13:1120–1121.Google Scholar
  43. Seoane J, Carrascal LM, Alonso CL, Palomino D (2005) Species-specific traits associated to prediction errors in bird habitat suitability modelling. Ecological Modelling 185:299–308.CrossRefGoogle Scholar
  44. Siembieda JL, Johnson CK, Cardona C, Anchell N, Dao N, Reisen W, et al. (2010) Influenza A viruses in wild birds of the Pacific flyway, 2005–2008. Vector-Borne and Zoonotic Diseases. doi: 10.1089/vbz.2009.0095. Online 8 January 2010
  45. Smith KF, Dobson AP, McKenzie FE, Real LA, Smith DL, Wilson ML (2005) Ecological theory to enhance infectious disease control and public health policy. Frontiers in Ecology and the Environment 3:29–37.CrossRefGoogle Scholar
  46. Stallknecht DE, Kearney MT, Shane SM, Zwank PJ (1990) Effects of pH, temperature, and salinity on persistence of avian influenza viruses in water. Avian Disease 34:412–418.CrossRefGoogle Scholar
  47. Trolliet B, Girard O, Benmergui M, Schricke V, Boutin JM, Fouquet M, Triplet P (2008) Oiseaux d’eau en Afrique subsaharienne: Bilan des dénombrements de janvier 2007. Faune Sauvage 279:4–11.Google Scholar
  48. Vgt4Africa (2006) VGT4Africa project. VITO NV. Accessed 8 March 2010
  49. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza-A viruses. Microbiological Reviews 56:152–179.Google Scholar
  50. Zwarts L, Grigoras I (2005) Flooding of the Inner Niger Delta. In: The Niger, a Lifeline, Zwarts L, Beukering vP, Kone B, Wymenga E (editors), Lelystad, The Netherlands: RIZA/Wetlands International/IVM/A&W, pp 43–77 Google Scholar
  51. Zwarts L, Bijlsma RG, van der Kamp J, Wymenga E (2009) Living on the Edge: Wetlands and Birds in a Changing Sahel, Zeist, The Netherlands: KNNV Publishing.Google Scholar

Copyright information

© International Association for Ecology and Health 2010

Authors and Affiliations

  • Julien Cappelle
    • 1
  • Olivier Girard
    • 2
  • Bouba Fofana
    • 3
    • 4
  • Nicolas Gaidet
    • 1
  • Marius Gilbert
    • 5
    • 6
  1. 1.CIRAD ESUR Animal et Gestion intégrée des risques (AGIR)Montpellier Cedex 5France
  2. 2.ONCFS, Réserve de Chanteloupl’Ile d’OlonneFrance
  3. 3.Direction Nationale des Eaux et Forêts du MaliBamakoMali
  4. 4.Wetlands InternationalMopti-SevareMali
  5. 5.Biological Control and Spatial EcologyUniversité Libre de BruxellesBrusselsBelgium
  6. 6.Fonds National de la Recherche ScientifiquesBrusselsBelgium

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