, Volume 11, Issue 1, pp 53–62 | Cite as

Using Avian Surveillance in Ecuador to Assess the Imminence of West Nile Virus Incursion to Galápagos

  • Gillian Eastwood
  • Simon J. Goodman
  • Nancy Hilgert
  • Marilyn Cruz
  • Laura D. Kramer
  • Andrew A. Cunningham
Original Contribution


Infectious disease emergence represents a global threat to human, agricultural animal and wildlife health. West Nile virus (WNV) first emerged in the Americas in 1999 following its introduction to New York from the Old World. This flavivirus rapidly spread across much of North America, causing human, equine and avian mortalities and population declines of multiple wild bird species. It has now spread to Central and South America, and there is concern that the virus will reach the Galápagos Islands, a UNESCO World Heritage Site famous for its unique biodiversity, with potentially catastrophic results. Here, we use wild bird surveillance to examine the current WNV status in the Galapagos Islands and around the Ecuadorian city of Guayaquil (the main air and sea port serving Galápagos). We conducted serosurveys of wild birds on three Galápagos Islands (Baltra, San Cristobal and Santa Cruz) with direct transport links to the South American continent. In addition, dead birds killed by car collisions on Santa Cruz were tested for WNV infection. On mainland Ecuador, serosurveys of wild birds were conducted at three sites around Guayaquil. No evidence of WNV seropositivity or infection was detected. Although wider testing is recommended on the mainland, the study highlights a limit of WNV spread within South America. Our results indicate the continued absence of WNV on Galápagos and suggest the current likelihood of human-mediated transport of WNV to Galápagos to be low. The risk of emergence will almost certainly increase over time, however, and stringent biosecurity and surveillance measures should be put in place to minimise the risk of the introduction of WNV (and other alien pathogens) to Galápagos.


emerging infectious disease West Nile virus surveillance avifauna Ecuador Galápagos Infection prevalence 



This work was possible due to the generous funding of the Natural Environment Research Council, and to the 2011 Daisy Balloch Award (Zoological Society London—Institute of Zoology) awarded to GE. Additional financial support was provided by Darwin Initiative Grant EIDPO15 to SG, AC and Virna Cedeño. We thank Virna Cedeño for contributions instrumental to establishing the Galapagos Genetics Epidemiology and Pathology Laboratory, which made this work and other studies investigating disease emergence in Galapagos Islands possible. We are grateful to both the Galápagos National Park and the Ministry of Environment (MAE Guayaquil) for permissions to conduct sampling. Thank you to the administrators of Lago de Capeira, Pantanal Zoo, Parque Histórico Guayaquil and Fundación Ecológica Andrade for allowing us to collect on their properties. The field assistance of Julian Correa Pérez (UEES), Grace Loyola-Herrera and Pamela Martinez was greatly appreciated. Thank you also to Alan Dupuis for laboratory support and reviewing a draft manuscript.


  1. Appler KK, Brown AN, Stewart BS, Behr MJ, Demarest VL, et al. (2010) Persistence of West Nile virus in the central nervous system and periphery of mice. PLoS ONE 5: e10649 doi: 10.1371/journal.pone.0010649 [Online May 14, 2010].PubMedCentralPubMedCrossRefGoogle Scholar
  2. Bataille A, Cunningham AA, Cedeño V, Cruz M, Eastwood G, Fonseca DM, Causton CE, Azuero R, Loayza J, Martinez JD, Goodman SJ (2009) Evidence for regular ongoing introductions of mosquito disease vectors into the Galápagos Islands. Proceedings of the Royal Society - Biological Sciences 276: 3769-3775.PubMedCentralPubMedCrossRefGoogle Scholar
  3. Berrocal L, Pena J, Gonzalez M, Mattar S (2006) West Nile virus - Ecology and epidemiology of an emerging pathogen in Colombia. Revista de Salud Pública 8: 218-228.PubMedCrossRefGoogle Scholar
  4. Beveroth TA, Ward MP, Lampman RL, Ringia AM, Novak RJ (2006) Changes in seroprevalence of West Nile virus across Illinois in free-ranging birds from 2001 through 2004. American Journal of Tropical Medicine and Hygiene 74: 174-179.PubMedGoogle Scholar
  5. Bosch I, Herrera F, Navarro JC, Lentino M, Dupuis A, Maffei J, Jones M, Fernandez E, Perez N, Perez-Eman J, Guimaraes AE, Barrera R, Valero N, Ruiz J, Velasquez G, Martinez J, Comach G, Komar N, Spielman A, Kramer L (2007) West Nile virus, Venezuela. Emerging Infectious Diseases 13: 651-653.PubMedCentralPubMedCrossRefGoogle Scholar
  6. CDC (2003) Epidemic/epizootic West Nile Virus in the United States: guidelines for surveillance, prevention, and control. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Infectious Diseases, Division of Vector-Borne Infectious Diseases, Fort Collins, CO.Google Scholar
  7. Cedeño V, Cunningham AA, Goodman SJ (2004) Proceedings of the Galápagos West Nile virus workshop: evaluating the threat posed by West Nile virus to Galápagos fauna, Galápagos National Park headquarters, Santa Cruz. Ecuador.Google Scholar
  8. Diaz LA, Komar N, Visintin A, Juri MJD, Stein M, Allende RL, Spinsanti L, Konigheim B, Aguilar J, Laurito M, Almirón W, Contigiani M (2008). West Nile virus in birds, Argentina. Letters to Editor. Emerging Infectious Diseases 14: 689-690.PubMedCentralCrossRefGoogle Scholar
  9. Dohoo IR, Martin W, Stryhn H (2003) Veterinary epidemiologic research. 2nd edition. AVC Incorporated, Charlottetown, PE, Canada.Google Scholar
  10. Dupuis AP, Marra PP, Reitsma R, Jones MJ, Louie KL, Kramer LD (2005) Short report: Serologic evidence for West Nile virus transmission in Puerto Rico and Cuba. American Journal of Tropical Medicine and Hygiene 73: 474-476.PubMedGoogle Scholar
  11. Eastwood G, Goodman SJ, Kramer LD, Cunningham AA (2013) Aedes taeniorhynchus vectorial capacity informs a pre-emptive assessment of West Nile virus establishment in Galápagos. Scientific Reports 3: 1519. doi: 10.1038/srep01519 [Online March 22, 2013].PubMedCentralPubMedCrossRefGoogle Scholar
  12. Eastwood G, Kramer LD, Goodman SJ, Cunningham AA (2011) West Nile virus vector competency of Culex quinquefasciatus mosquitoes in the Galápagos Islands. American Journal of Tropical Medicine and Hygiene 85: 426-433.PubMedCentralPubMedCrossRefGoogle Scholar
  13. Ebel GD, Dupuis II AP, Nicholas D, Young D, Maffei J, Kramer LD (2002) Detection by enzyme-linked immunosorbent assay of antibodies to West Nile virus in birds. Emerging Infectious Diseases 8: 979-982.PubMedCentralPubMedCrossRefGoogle Scholar
  14. Ecuadorian Government Statute (April 22, 2010) concerning disinsection. Article number 016. Accessed March 5, 2013.
  15. Gibbs SE, Allison AB, Yabsley MJ, Mead DG, Wilcox BR, Stallknecht DE (2006) West Nile virus antibodies in avian species of Georgia, USA: 2000-2004. Vector-Borne and Zoonotic Diseases 6: 57-72.PubMedCrossRefGoogle Scholar
  16. Gottdenker NL, Walsh T, Vargas H, Merkel J, Jimenez GU, Miller RE, Dailey M, Parker PG (2005) Assessing the risks of introduced chickens and their pathogens to native birds in the Galápagos archipelago. Biological Conservation 126: 429-439.CrossRefGoogle Scholar
  17. Gottdenker NL, Walsh T, Jiménez-Uzcátegui G, Betancourt F, Cruz M, Soos C, Miller RE, Parker PG (2008) Causes of mortality of wild birds submitted to the Charles Darwin Research Station, Santa Cruz, Galápagos, Ecuador from 2002-2004. Journal of Wildlife Diseases 44: 1024-1031.PubMedCrossRefGoogle Scholar
  18. Gubler DJ (2002) The global emergence/resurgence of arboviral diseases as public health problems. Archives of Medical Research 33: 330-342.PubMedCrossRefGoogle Scholar
  19. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451: 990-993.PubMedCrossRefGoogle Scholar
  20. Kilpatrick AM, Daszak P, Goodman SJ, Rogg H, Kramer LD, Cedeno V, Cunningham AA (2006) Predicting pathogen introduction: West Nile virus spread to Galápagos. Conservation Biology 20: 1224-1231.PubMedCrossRefGoogle Scholar
  21. Kilpatrick AM, LaDeau SL, Marra PP (2007) Ecology of West Nile virus transmission and its impact on birds in the western hemisphere. Auk 124: 1121-1136.CrossRefGoogle Scholar
  22. Komar N (2003) West Nile virus: Vertebrate ecology and biology—Birds. In: Centers for Disease Control and Prevention [CDC] (editors), Fourth National Conference on West Nile Virus in the United States, New Orleans, LA.Google Scholar
  23. Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, Davis B, Bowen R, Bunning M (2003) Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerging Infectious Diseases 9: 311-322.PubMedCentralPubMedCrossRefGoogle Scholar
  24. Komar N (2003) West Nile virus: Epidemiology and ecology in North America. Advances in Virus Research 61: 185-234.PubMedCrossRefGoogle Scholar
  25. Komar N and Clark GG (2006) West Nile virus activity in Latin America and the Caribbean. Revista Panamericana De Salud Pública - Pan American Journal of Public Health 19: 112-117.PubMedCrossRefGoogle Scholar
  26. Komar O, Robbins MB, Contreras GG, Benz BW, Klenk K, Blitvich BJ, Marlenee NL, Burkhalter KL, Beckett S, Gonzallvez G, Pena CJ, Peterson AT, Komar N (2005) West Nile virus survey of birds and mosquitoes in the Dominican Republic. Vector-Borne and Zoonotic Diseases 5: 120-126.PubMedCrossRefGoogle Scholar
  27. Kauffman EB, Jones SA, Dupuis II AP, Ngo KA, Bernard KA, Kramer LD (2003) Virus detection protocols for West Nile virus in vertebrate and mosquito specimens. Journal of Clinical Microbiology 41: 3661-3667.PubMedCentralPubMedCrossRefGoogle Scholar
  28. Kramer LD and Bernard KA (2001) West Nile virus infection in birds and mammals. Annals of the New York Academy of Science. 951: 84-93.CrossRefGoogle Scholar
  29. Kramer LD, Li J, Shi P-Y (2007) West Nile virus. The Lancet Neurology 6: 171-181.CrossRefGoogle Scholar
  30. Kramer LD, Styer LM, Ebel GD (2008) A global perspective on the epidemiology of West Nile virus. Annual Review of Entomology 53: 61-81.PubMedCrossRefGoogle Scholar
  31. LaDeau SL, Kilpatrick AM, Marra PP (2007) West Nile virus emergence and large-scale declines of North American bird populations. Nature 447: 710-713.PubMedCrossRefGoogle Scholar
  32. Mattar S, Edwards E, Laguado J, Gonzalez M, Alvarez J, Komar N (2005) West Nile virus antibodies in Colombian horses. Emerging Infectious Diseases 11: 1497-1498.PubMedCentralPubMedCrossRefGoogle Scholar
  33. Morales MA, Barrandeguy M, Fabbri C, Garcia JB, Vissani A, Trono K, Gutierrez G, Pigretti S, Menchaca H, Garrido N, Taylor N, Fernandez F, Levis S, Enria D (2006) West Nile virus isolation from equines in Argentina, 2006. Emerging Infectious Diseases 12: 1559-1561.PubMedCentralPubMedCrossRefGoogle Scholar
  34. National Research Council (2008) Vector-Borne Diseases: Understanding the Environmental, Human Health, and Ecological Connections, Workshop Summary (Forum on Microbial Threats). Washington, DC: The National Academies Press.Google Scholar
  35. Pauvolid-Corrêa A, Morales MA, Levis S, Moraes Figueiredo LT, Couto-Lima D, Campos Z, Furlan Nogueira M, Elias da Silva E, Ribeiro Nogueira RM, Gonçalves Schatzmayr H (2011) Neutralising antibodies for West Nile virus in horses from Brazilian Pantanal. Memόrias do Instituto Oswaldo Cruz 106: 467-474.CrossRefGoogle Scholar
  36. Rios-Ibarra C, Blitvich BJ, Farfan-Ale J, Ramos-Jimenez J, Muro-Escobedo S, Martínez-Rodriguez HR, Ortiz-López R, Torres-López E, Rivas-Estill AM (2010). Fatal human case of West Nile virus disease, Mexico, 2009. Emerging Infectious Diseases 16: 741-743.PubMedCentralPubMedCrossRefGoogle Scholar
  37. Travis EK, Vargas FH, Merkel J, Gottdenker N, Miller RE, Parker PG (2006) Hematology, serum chemistry, and serology of Galápagos penguins (Sphenicus mendiculus) in the Galápagos Islands, Ecuador. Journal of Wildlife Diseases. 42: 625–632.PubMedCrossRefGoogle Scholar
  38. Ulloa A, Langevin SA, Mendez-Sanchez JD, Arredondo-Jimenez JI, Raetz JL, Powers AM, Villarreal-Treviño C, Gubler DJ, Komar N (2003) Serologic survey of domestic animals for zoonotic arbovirus infections in the Lacandón Forest region of Chiapas, Mexico. Vector-Borne and Zoonotic Diseases 3: 3-9.PubMedCrossRefGoogle Scholar
  39. University of California Davis (2004) Species affected by West Nile virus. Accessed October 1, 2011.
  40. Wheeler SS, Barker CM, Fang Y, Veronica Armijos M, Carroll BD, Husted S, Johnson WO, Reisen WK (2009) Differential impact of West Nile virus on California birds. The Condor 111: 1-20.PubMedCentralPubMedCrossRefGoogle Scholar
  41. Yamshchikov G, Borisevich V, Kwok CW, Nistler R, Kohlmeier J, Seregin A, Chaporgina E, Benedict S, Yamschikov V (2005) The suitability of Yellow fever and Japanese encephalitis vaccines for immunization against West Nile virus. Vaccine 23: 4785-4792.PubMedCrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2014

Authors and Affiliations

  • Gillian Eastwood
    • 1
    • 2
    • 3
  • Simon J. Goodman
    • 2
    • 3
  • Nancy Hilgert
    • 4
  • Marilyn Cruz
    • 2
  • Laura D. Kramer
    • 5
  • Andrew A. Cunningham
    • 1
    • 2
  1. 1.Institute of ZoologyZoological Society of LondonLondonUK
  2. 2.Galápagos Genetics, Epidemiology and Pathology LaboratorySanta Cruz, GalápagosEcuador
  3. 3.School of BiologyUniversity of LeedsLeedsUK
  4. 4.University of Espiritu Santo (UEES)SamborondónEcuador
  5. 5.Wadsworth CenterNew York State Department of HealthSlingerlandsUSA

Personalised recommendations