, Volume 9, Issue 1, pp 80–88 | Cite as

The Ecology of Emerging Infectious Diseases in Migratory Birds: An Assessment of the Role of Climate Change and Priorities for Future Research

  • Trevon FullerEmail author
  • Staffan Bensch
  • Inge Müller
  • John Novembre
  • Javier Pérez-Tris
  • Robert E. Ricklefs
  • Thomas B. Smith
  • Jonas Waldenström


Pathogens that are maintained by wild birds occasionally jump to human hosts, causing considerable loss of life and disruption to global commerce. Preliminary evidence suggests that climate change and human movements and commerce may have played a role in recent range expansions of avian pathogens. Since the magnitude of climate change in the coming decades is predicted to exceed climatic changes in the recent past, there is an urgent need to determine the extent to which climate change may drive the spread of disease by avian migrants. In this review, we recommend actions intended to mitigate the impact of emergent pathogens of migratory birds on biodiversity and public health. Increased surveillance that builds upon existing bird banding networks is required to conclusively establish a link between climate and avian pathogens and to prevent pathogens with migratory bird reservoirs from spilling over to humans.


influenza A virus malaria salmonella West Nile virus zoonoses 



We thank three anonymous reviewers for comments that improved the manuscript. This work was supported by the US National Science Foundation Research Coordination Network Migration Interest Group: Research Applied Toward Education. JN was funded by the NSF (Grant number 0933731) and the Searle Scholars Program. JP was funded by the Spanish Ministry of Science and Technology (CGL2007-62937/BOS). JW was funded by the Swedish Research Council FORMAS (221-2008-326). SB was funded by the Swedish Research Council (621-2007-5193). TBS and TF were funded by the joint NSF-National Institutes of Health Ecology of Infectious Diseases Program (Grant number EF-0430146), by US Environmental Protection Agency grant (R 833778), and by the National Institute of Allergy and Infectious Diseases (Grant number EID-1R01AI074059-01).

Supplementary material

10393_2012_750_MOESM1_ESM.doc (370 kb)
Supplementary material 1 (DOC 370 kb)


  1. Abdelwhab EM, Selim AA, Arafa A, Galal S, Kilany WH, Hassan MK, et al. (2010). Circulation of avian influenza H5N1 in live bird markets in Egypt. Avian Diseases 54:911-914.PubMedCrossRefGoogle Scholar
  2. Alerstam T (1990). Bird Migration. Cambridge University Press, Cambridge, UK.Google Scholar
  3. Altizer S, Bartel R, and Han BA (2011). Animal migration and infectious disease risk. Science 331:296-302.PubMedCrossRefGoogle Scholar
  4. Atkinson CT, and LaPointe DA (2009). Introduced avian diseases, climate change, and the future of Hawaiian Honeycreepers. Journal of Avian Medicine and Surgery 23:53-63.PubMedCrossRefGoogle Scholar
  5. Bensch S, and Akesson A (2003). Temporal and spatial variation of hematozoans in Scandinavian willow warblers. Journal of Parasitology 89:388-391.PubMedCrossRefGoogle Scholar
  6. Bensch S, Grahn M, Muller N, Gay L, and Akesson S (2009a). Genetic, morphological, and feather isotope variation of migratory willow warblers show gradual divergence in a ring. Molecular Ecology 18:3087-3096.PubMedCrossRefGoogle Scholar
  7. Bensch S, Hellgren O, and Perez-Tris J (2009b). MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9:1353-1358.PubMedCrossRefGoogle Scholar
  8. Berthold P (2001). Bird Migration: A General Survey. Second Edition. Oxford University Press, Oxford, UK.Google Scholar
  9. Both C, Bouwhuis S, Lessells CM, and Visser ME (2006). Climate change and population declines in a long-distance migratory bird. Nature 441:81-83.PubMedCrossRefGoogle Scholar
  10. Breban R, Drake JM, Stallknecht DE, and Rohani P (2009). The role of environmental transmission in recurrent avian influenza epidemics. Plos Computational Biology 5:e1000346.PubMedCrossRefGoogle Scholar
  11. Brooks DR, and Hoberg EP (2007). How will global climate change affect parasite-host assemblages? Trends in Parasitology 23:571-574.PubMedCrossRefGoogle Scholar
  12. Cattadori IM, Haydon DT, and Hudson PJ (2005). Parasites and climate synchronize red grouse populations. Nature 433:737-741.PubMedCrossRefGoogle Scholar
  13. Chamberlain CP, Bensch S, Feng X, Akesson S, and Andersson T (2000). Stable isotopes examined across a migratory divide in Scandinavian willow warblers (Phylloscopus trochilus trochilus and Phylloscopus trochilus acredula) reflect their African winter quarters. Proceedings of the Royal Society of London Series B-Biological Sciences 267:43-48.CrossRefGoogle Scholar
  14. Cooper CB, Hochachka WM, and Dhondt AA (2007). Contrasting natural experiments confirm competition between house finches and house sparrows. Ecology 88:864-870.PubMedCrossRefGoogle Scholar
  15. Danielova V, Daniel M, Schwarzova L, Materna J, Rudenko N, Golovchenko M, et al. (2010). Integration of a tick-borne encephalitis virus and Borrelia burgdorferi sensu lato into mountain ecosystems, following a shift in the altitudinal limit of distribution of their vector, Ixodes ricinus (Krkonose Mountains, Czech Republic). Vector-Borne and Zoonotic Diseases 10:223-230.PubMedCrossRefGoogle Scholar
  16. Daszak P, Cunningham AA, and Hyatt AD (2000). Wildlife ecology - Emerging infectious diseases of wildlife - Threats to biodiversity and human health. Science 287:443-449.PubMedCrossRefGoogle Scholar
  17. Devictor V, Julliard R, Couvet D, and Jiguet F (2008). Birds are tracking climate warming, but not fast enough. Proceedings of the Royal Society B-Biological Sciences 275:2743-2748.CrossRefGoogle Scholar
  18. Duval L, Robert V, Csorba G, Hassanin A, Randrianarivelojosia M, Walston J, et al. (2007). Multiple host-switching of Haemosporidia parasites in bats. Malaria Journal 6:157.PubMedCrossRefGoogle Scholar
  19. Faaborg J, Holmes RT, Anders AD, Bildstein KL, Dugger KM, Gauthreaux SA, et al. (2010). Conserving migratory land birds in the New World: Do we know enough? Ecological Applications 20:398-418.PubMedCrossRefGoogle Scholar
  20. Fallon SM, Bermingham E, and Ricklefs RE (2005). Host specialization and geographic localization of avian malaria parasites: A regional analysis in the Lesser Antilles. American Naturalist 165:466-480.PubMedCrossRefGoogle Scholar
  21. Fuller T, Saatchi S, Curd EE, Toffelmier E, Thomassen H, Buermann W, et al. (2010). Mapping the risk of avian influenza in wild birds in the US. BMC Infectious Diseases 10:187.PubMedCrossRefGoogle Scholar
  22. 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 large-scale satellite telemetry. Journal of Applied Ecology 47:1147-1157.CrossRefGoogle Scholar
  23. Garamszegi L (2011). Climate change increases the risk of malaria in birds. Global Change Biology 17:1751-1759.CrossRefGoogle Scholar
  24. Gilbert M, Slingenbergh J, and Xiao X (2008). Climate change and avian influenza. Revue scientifique et technique - Office international des epizooties 27:459-466.Google Scholar
  25. 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 and Emerging Diseases 56:57-72.PubMedCrossRefGoogle Scholar
  26. Hobson KA (2011). Isotopic ornithology: a perspective. Journal of Ornithology 152:49-66.CrossRefGoogle Scholar
  27. Hobson KA, and Wassenaar LI, editors. (2008). Tracking Animal Migration with Stable Isotopes. Elsevier, London.Google Scholar
  28. Hochachka WM, and Dhondt AA (2000). Density-dependent decline of host abundance resulting from a new infectious disease. Proceedings of the National Academy of Sciences of the United States of America 97:5303-5306.PubMedCrossRefGoogle Scholar
  29. Hosseini P, Sokolow SH, Vandegrift KJ, Kilpatrick AM, and Daszak P (2010). Predictive power of air travel and socio-economic data for early pandemic spread. Plos ONE 5: e12763.PubMedCrossRefGoogle Scholar
  30. Irwin DE, Irwin JH, and Smith TB (2011). Genetic variation and seasonal migratory connectivity in Wilson’s warblers (Wilsonia pusilla): species-level differences in nuclear DNA between western and eastern populations. Molecular Ecology 20:3102-3115.PubMedCrossRefGoogle Scholar
  31. Jiguet F, Devictor V, Ottvall R, Van Turnhout C, Van der Jeugd H, and Lindstrom A (2010). Bird population trends are linearly affected by climate change along species thermal ranges. Proceedings of the Royal Society B-Biological Sciences 277:3601-3608.CrossRefGoogle Scholar
  32. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. (2008). Global trends in emerging infectious diseases. Nature 451:990-993.PubMedCrossRefGoogle Scholar
  33. Kayser FH, Bienz KA, Eckert J, and Zinkernagel RM (2005). Medical Microbiology. Thieme, Stuttgart.Google Scholar
  34. Kearney M, and Porter W (2009). Mechanistic niche modelling: combining physiological and spatial data to predict species’ ranges. Ecology Letters 12:334-350.PubMedCrossRefGoogle Scholar
  35. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, et al. (2010). Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647-652.PubMedCrossRefGoogle Scholar
  36. Keller I, Korner-Nievergelt F, and Jenni L (2009). Within-winter movements: a common phenomenon in the Common Pochard Aythya ferina. Journal of Ornithology 150:483-494.CrossRefGoogle Scholar
  37. Kelly JF, Ruegg KC, and Smith TB (2005). Combining isotopic and genetic markers to identify breeding origins of migrant birds. Ecological Applications 15:1487-1494.CrossRefGoogle Scholar
  38. Keusch GT, Pappaioanou M, Gonzalez MC, Scott KA, and Tsai P (2009). Sustaining Global Surveillance and Response to Emerging Zoonotic Diseases. National Academies Press, Washington, DC.Google Scholar
  39. Kilpatrick AM (2011). Globalization, land use, and the invasion of West Nile virus. Science 334:323-327.PubMedCrossRefGoogle Scholar
  40. Kilpatrick AM, Daszak P, Goodman SJ, Rogg H, Kramer LD, Cedeno V, et al. (2006a). Predicting pathogen introduction: West Nile virus spread to Galapagos. Conservation Biology 20:1224-1231.PubMedCrossRefGoogle Scholar
  41. Kilpatrick AM, Daszak P, Jones MJ, Marra PP, and Kramer LD (2006b). Host heterogeneity dominates West Nile virus transmission. Proceedings of the Royal Society B-Biological Sciences 273:2327-2333.CrossRefGoogle Scholar
  42. Kilpatrick AM, Meola MA, Moudy RM, and Kramer LD (2008). Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. Plos Pathogens 4:e1000092.PubMedCrossRefGoogle Scholar
  43. Kilpatrick AM, Dupuis AP, Chang GJJ, and Kramer LD (2010). DNA vaccination of American Robins (Turdus migratorius) against West Nile Virus. Vector-Borne and Zoonotic Diseases 10:377-380.PubMedCrossRefGoogle Scholar
  44. King LJ, Anderson LR, Blackmore CG, Blackwell MJ, Lautner EA, Marcus LC, et al. (2008). Executive summary of the AVMA One Health Initiative Task Force report. Javma-Journal of the American Veterinary Medical Association 233:259-261.PubMedCrossRefGoogle Scholar
  45. Kistler AL, Gancz A, Clubb S, Skewes-Cox P, Fischer K, Sorber K, et al. (2008). Recovery of divergent avian bornaviruses from cases of proventricular dilatation disease: Identification of a candidate etiologic agent. Virology Journal 5:88.PubMedCrossRefGoogle Scholar
  46. La Sorte FA, and Thompson FR (2007). Poleward shifts in winter ranges of North American birds. Ecology 88:1803-1812.PubMedCrossRefGoogle Scholar
  47. Levin II, Outlaw DC, Vargas FH, and Parker PG (2009). Plasmodium blood parasite found in endangered Galapagos penguins (Spheniscus mendiculus). Biological Conservation 142:3191-3195.CrossRefGoogle Scholar
  48. Li YD, Li P, Lei FM, Guo S, Ding CQ, Xin Z, et al. (2010). Persistent circulation of highly pathogenic influenza H5N1 virus in Lake Qinghai area of China. Avian Diseases 54:821-829.PubMedCrossRefGoogle Scholar
  49. Liu WM, Li YY, Learn GH, Rudicell RS, Robertson JD, Keele BF, et al. (2010). Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467:420-425.PubMedCrossRefGoogle Scholar
  50. McKibbin WJ, and Sidorenki AA (2006). Global Macroeconomic Consequences of Pandemic Influenza. Lowry Institute for International Policy, Sydney, Australia.Google Scholar
  51. Meltzer MI, Cox NJ, and Fukuda K (1999). The economic impact of pandemic influenza in the United States: Priorities for intervention. Emerging Infectious Diseases 5:659-671.PubMedCrossRefGoogle Scholar
  52. Moreau RE, and Monk JF (1972). Palaearctic-African Birds Migration System. Academic Press, London.Google Scholar
  53. Newton I (2008). The Migration Ecology of Birds. Elsevier, Amsterdam.Google Scholar
  54. Novembre J, Johnson T, Bryc K, Kutalik Z, Boyko AR, Auton A, et al. (2008). Genes mirror geography within Europe. Nature 456:98-101.PubMedCrossRefGoogle Scholar
  55. Parrish CR, Holmes EC, Morens DM, Park EC, Burke DS, Calisher CH, et al. (2008). Cross-species virus transmission and the emergence of new epidemic diseases. Microbiology and Molecular Biology Reviews 72:457-470.PubMedCrossRefGoogle Scholar
  56. Pepin KM, Lass S, Pulliam JRC, Read AF, and Lloyd-Smith JO (2010). Identifying genetic markers of adaptation for surveillance of viral host jumps. Nature Reviews Microbiology 8:802-813.PubMedCrossRefGoogle Scholar
  57. Reed KD, Melski JW, Graham MB, Regnery RL, Sotir MJ, Wegner MV, et al. (2004). The detection of monkeypox in humans in the Western Hemisphere. New England Journal of Medicine 350:342-350.PubMedCrossRefGoogle Scholar
  58. Reperant LA, Fuckar NS, Osterhaus A, Dobson AP, and Kuiken T (2010). Spatial and temporal association of outbreaks of H5N1 influenza virus infection in wild birds with the 0 degrees C isotherm. Plos Pathogens 6:e1000854.PubMedCrossRefGoogle Scholar
  59. Ricklefs RE, and Outlaw DC (2010). A molecular clock for malaria parasites. Science 329:226-229.PubMedCrossRefGoogle Scholar
  60. Robinson RA, Lawson B, Toms MP, Peck KM, Kirkwood JK, Chantrey J, et al. (2010). Emerging infectious disease leads to rapid population declines of common British birds. Plos One 5:e12215.PubMedCrossRefGoogle Scholar
  61. 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.CrossRefGoogle Scholar
  62. Rolshausen G, Hobson KA, and Schaefer HM (2010). Spring arrival along a migratory divide of sympatric blackcaps (Sylvia atricapilla). Oecologia 162:175-183.PubMedCrossRefGoogle Scholar
  63. Rvachev LA, and Longini IM (1985). A mathematical model for the global spread of influenza. Mathematical Biosciences 75:3-23.CrossRefGoogle Scholar
  64. Saino N, Ambrosini R, Rubolini D, von Hardenberg J, Provenzale A, Huppop K, et al. (2011). Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proceedings of the Royal Society B-Biological Sciences 278:835-842.CrossRefGoogle Scholar
  65. Salomon R, and Webster RG (2009). The influenza virus enigma. Cell 136:402-410.PubMedCrossRefGoogle Scholar
  66. Slenning BD (2010). Global climate change and implications for disease emergence. Veterinary Pathology 47:28-33.PubMedCrossRefGoogle Scholar
  67. Smith TB, Clegg SM, Kimura M, Ruegg K, Mila B, and Lovette I (2005). Molecular genetic approaches to linking breeding and overwintering areas in five Neotropical migrant passerines. Pages 222-234 in R. Greenberg and P. P. Marra, editors. Birds of Two Worlds: The Ecology and Evolution of Migration. Johns Hopkins University Press, Baltimore.Google Scholar
  68. Stutchbury BJM, Tarof SA, Done T, Gow E, Kramer PM, Tautin J, et al. (2009). Tracking long-distance songbird migration by using geolocators. Science 323:896.PubMedCrossRefGoogle Scholar
  69. Swaddle JP, and Calos SE (2008). Increased avian diversity is associated with lower incidence of human West Nile infection: observation of the dilution effect. Plos One 3:e2488.PubMedCrossRefGoogle Scholar
  70. Tomkiewicz SM, Fuller MR, Kie JG, and Bates KK (2010). Global positioning system and associated technologies in animal behaviour and ecological research. Philosophical Transactions of the Royal Society B-Biological Sciences 365:2163-2176.CrossRefGoogle Scholar
  71. Traill LW, Bradshaw CJA, Field HE, and Brook BW (2009). Climate change enhances the potential impact of infectious disease and harvest on tropical waterfowl. Biotropica 41:414-423.CrossRefGoogle Scholar
  72. Ulbert S (2011). West Nile virus: the complex biology of an emerging pathogen. Intervirology 54:171-184.PubMedCrossRefGoogle Scholar
  73. Van Riper III C, Van Riper SG, Goff ML, and Laird M (1986). The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56:327-344.CrossRefGoogle Scholar
  74. Vandegrift KJ, Sokolow SH, Daszak P, Kilpatrick AM (2010) Ecology of avian influenza viruses in a changing world. Pages 113-128 in R. S. Ostfeld and W. H. Schlesinger, editors. Year in Ecology and Conservation Biology 2010. New York Academy of Sciences, New York.Google Scholar
  75. Webster MS, Marra PP, Haig SM, Bensch S, and Holmes RT (2002). Links between worlds: unraveling migratory connectivity. Trends in Ecology & Evolution 17:76-83.CrossRefGoogle Scholar
  76. Woolhouse MEJ, and Gowtage-Sequeria S (2005). Host range and emerging and reemerging pathogens. Emerging Infectious Diseases 11:1842-1847.PubMedCrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2012

Authors and Affiliations

  • Trevon Fuller
    • 1
    Email author
  • Staffan Bensch
    • 2
  • Inge Müller
    • 3
  • John Novembre
    • 4
    • 5
  • Javier Pérez-Tris
    • 6
  • Robert E. Ricklefs
    • 7
  • Thomas B. Smith
    • 1
    • 4
  • Jonas Waldenström
    • 8
  1. 1.Center for Tropical Research, Institute of the Environment and SustainabilityUniversity of California, Los AngelesLos AngelesUSA
  2. 2.Department of EcologyLund UniversityLundSweden
  3. 3.Max Planck Institute for OrnithologyVogelwarte RadolfzellRadolfzellGermany
  4. 4.Department of Ecology and Evolutionary BiologyUniversity of California, Los AngelesLos AngelesUSA
  5. 5.Interdepartmental Program in BioinformaticsUniversity of California, Los AngelesLos AngelesUSA
  6. 6.Departamento de Zoología y Antropología Física, Facultad de BiologíaUniversidad Complutense de MadridMadridSpain
  7. 7.Department of BiologyUniversity of Missouri-St. LouisSt. LouisUSA
  8. 8.Section for Zoonotic Ecology and Epidemiology, School of Natural SciencesLinnaeus UniversityKalmarSweden

Personalised recommendations