Journal of Ornithology

, Volume 155, Issue 2, pp 549–554 | Cite as

Shorebird low spillover risk of mosquito-borne pathogens on Iberian wetlands

  • Sara Pardal
  • José A. Alves
  • Líbia Zé-Zé
  • Hugo Osório
  • Afonso Rocha
  • Ricardo J. Lopes
  • Pete Potts
  • Fátima Amaro
  • Francisco Santiago-Quesada
  • Juan M. Sanchez-Guzman
  • José Masero
  • Maria J. Alves
  • Javier Pérez-Tris
  • Jaime A. Ramos
  • Luísa Mendes
Short Note

Abstract

Migratory shorebirds are exposed to a wide range of pathogens along their migratory flyways, but their capacity to acquire or spread pathogens beyond endemic areas is poorly known. We focused on the spillover and acquisition of mosquito-borne pathogens such as haemosporidians and West Nile virus (WNV) on key-staging Iberian wetlands during different seasons. We screened seven shorebird species (447 individuals), and detected low haemosporidian prevalence (0.6 %). Furthermore, no WNV infections could be detected, though 6.2 % revealed antibodies against flaviviruses. Although Iberian wetlands congregate numerous shorebirds of different species and origins, the potential introduction of foreign pathogens is not a common event.

Keywords

Migratory shorebirds Haemosporidians West Nile virus Spillover 

Zusammenfassung

Geringes Ansteckungsrisiko von durch Stechmücken übertragenen Krankheitserregern unter Watvögeln in Feuchtgebieten der iberischen Halbinsel

Obwohl wandernde Watvögel entlang ihrer Zugwege mit den verschiedensten Krankheitserregern in Kontakt treten, ist wenig darüber bekannt, in welchem Maße solche Krankheitserreger durch Watvögel aufgenommen und über die Grenzen endemischer Gebiete hinaus verbreitet werden. Während verschiedener Jahreszeiten haben wir die Aufnahme und Übertragung von durch Stechmücken übertragenen Krankheitserregern wie etwa Haemosporidia und das West-Nil-Virus (WNV) bei Watvögeln in Hauptrastgebieten der iberischen Halbinsel untersucht. Unter den sieben überprüften Watvogelarten (447 Individuen) fanden wir eine geringe Prävalenz von Haemosporidia (0.6 %). Des Weiteren konnten keine Infektionen des WNV festgestellt werden, jedoch trugen 6.2 % der untersuchten Vögel Antikörper gegen Flaviviren. Obgleich sich große Ansammlungen von Watvögeln verschiedenster Arten und Herkunftsgebiete in den Feuchtgebieten der iberischen Halbinsel aufhalten, ist das mögliche Einschleppen von fremden Krankheitserregern nicht verbreitet.

Supplementary material

10336_2013_1036_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 22 kb) Supplementary material - Fieldwork: detailed description of capture periods and sampling methods; Haemosporidians screening: detailed laboratory extraction and parasite screening protocols. ELISA assays and detailed respective results.

References

  1. Bennett GF, Montgomerie R, Seutin G (1992) Scarcity of haematozoa in birds breeding on the arctic tundra of North America. Condor 94:289–292CrossRefGoogle Scholar
  2. Bensch S, Stjernam M, Hasselquist D, Östman Ö, Hansson B, Westerdahl H, Pinheiro RT (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc Lond B 267:1583–1589CrossRefGoogle Scholar
  3. Bensch S, Hellgren O, Pérez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353–1358PubMedCrossRefGoogle Scholar
  4. Blitvich BJ, Marlenee NL, Hall RA, Calisher CH, Bowen RA, Roehrig JT, Komar N, Langevin SA, Beaty BJ (2003) Epitope-blocking enzyme-linked immunosorbent assays for the detection of serum antibodies to West Nile virus in multiple avian species. J Clin Microbiol 41:1041–1047PubMedCentralPubMedCrossRefGoogle Scholar
  5. Boulinier T, Staszewski V (2007) Maternal transfer of antibodies: raising immune-ecology issues. Trends Ecol Evol 23(5):282–288. doi:10.1016/j.tree.2007.12.006 (Epub 2008 April 2)CrossRefGoogle Scholar
  6. Briese T, Rambaut A, Pathmajeyan M, Bishara J, Weinberger M, Pitlik S, Lipkin WI (2002) Phylogenetic analysis of a human isolate from the 2000 Israel West Nile virus epidemic. Emerg Infect Dis 8:528–531PubMedCentralPubMedCrossRefGoogle Scholar
  7. Catry T, Alves JA, Andrade J, Costa H, Dias MP, Fernandes P, Leal A, Lourenço PM, Martins RC, Moniz F, Pardal S, Rocha A, Santos CD, Encarnação V, Granadeiro JP (2011) Long-term declines of wader populations at the Tagus estuary, Portugal: a response to global or local factors? Bird Conserv Int 21:438–453. doi:10.1017/S0959270910000626 CrossRefGoogle Scholar
  8. Connel J, McKeown P, Garvey P, Cotter S, Conway A, O′Flanagan D, O′Herlihy B P, Morgan D, Nicoll A and Lloyd G (2004) Two linked cases of West Nile virus (WNV) acquired by Irish tourists in the Algarve, Portugal. Euro Surveill 8(32):pii 2517. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=2517 Accessed 20 Oct 2012
  9. Esteves A, Almeida APG, Galão RP, Parreira R, Piedade J, Rodrigues JC, Sousa CA, Novo MT (2005) West Nile Virus in Southern Portugal, 2004. Vector-borne Zoonotic Dis 5(4):410–413PubMedCrossRefGoogle Scholar
  10. Figuerola J, Velarde R, Bertolero A, Cerda F (1996) Absence of haematozoa in a breeding population of Kentish plover Charadrius alexandrinus in Northeast Spain. J Ornithol 137:523–525CrossRefGoogle Scholar
  11. Figuerola J, Soringer R, Rojo G, Gómez-Tejedor C, Jiménez-Clavero MA (2007) Seroconversion in wild birds and local circulation of West Nile virus, Spain. Emerg Infect Dis 13:1915–1917PubMedCentralPubMedCrossRefGoogle Scholar
  12. Figuerola J, Jiménez-Clavero MA, Lopez G, Rubio C, Soriguer R, Gómez-Tejedor C, Tenorio A (2008) Size matters: West Nile virus neutralizing antibodies in resident and migratory birds in Spain. Vet Microbiol 132:39–46PubMedCrossRefGoogle Scholar
  13. Figuerola J, Baouab RE, Soringer R, Fassi-Fihri O, Llorente F, Jiménez-Clavero MA (2009) West Nile virus antibodies in wild birds, Morocco, 2008. Emerg Infect Dis 15:1651–1653PubMedCentralPubMedCrossRefGoogle Scholar
  14. Formosinho P, Santos-Silva MM, Santos A, Melo P, Encarnação V, Santos N, Nunes T, Agrícola R, Portas M (2006) West Nile virus in Portugal—epidemiological surveys. RPCV 101(557–558):61–68Google Scholar
  15. Gibbs SEJ, Hoffman DM, Stark LM, Marlenee NL, Blitvich BJ, Beaty BJ, Stallknecht DE (2005) Persistence of antibodies to West Nile Virus in naturally infected Rock Pigeons (Columba livia). Clin Vaccine Immunol 12(5):665–667. doi:10.1128/CDLI.12.5.665-667.2005 CrossRefGoogle Scholar
  16. Hubálek Z (2004) An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 40:639–659PubMedCrossRefGoogle Scholar
  17. 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. Emerg Infect Dis 9:311–322PubMedCentralPubMedCrossRefGoogle Scholar
  18. Linke S, Niedrig M, Kaiser A, Ellerbrok H, Müller K, Müller T, Conraths FJ, Mühle RU, Schimdt D, Köppen U, Bairlein F, Berthold P, Pauli G (2007) Serologic evidence of West Nile virus infections in wild birds captured in Germany. Am J Trop Med Hyg 77:358–364PubMedGoogle Scholar
  19. Mendes L, Piersma T, Lecoq M, Spaans B, Ricklefs RE (2005) Disease-limited distributions? Contrast in the prevalence of avian malaria in shorebird species using marine and freshwater habitats. Oikos 109:396–404CrossRefGoogle Scholar
  20. Mendes L, Pardal S, Morais J, Antunes S, Ramos JA, Pérez-Tris J, Piersma T (2013) Hidden haemosporidian infections in ruffs, Philomachus pugnax, staging in northwest Europe en route from Africa to arctic Europe. Parasitol Res 112(5):2037–2043. doi:10.1007/s00436-013-3362-y PubMedCrossRefGoogle Scholar
  21. Muñoz J, Ruiz S, Soriguer R, Alcaide M, Viana DS, Roiz D, Vázquez A, Figuerola J (2012) Feeding patterns of potential West Nile virus vectors in South-West Spain. PLoS ONE 7(6):e39549. doi:10.1371/journal.pone.0039549 PubMedCentralPubMedCrossRefGoogle Scholar
  22. Palinauskas V, Kosarev V, Shapoval A, Bensch S, Valkiunas G (2007) Comparison of mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites of the subgenera Haemamoeba and Giovannolaia (Haemosporida: Plasmodiidae). Zootaxa 32(1626):39–50Google Scholar
  23. Pérez-Tris J, Bensch S (2005) Dispersal increases local transmission of avian malarial parasites. Ecol Lett 8:838–845. doi:10.1111/j.1461-0248.2005.00788.x CrossRefGoogle Scholar
  24. Valkiūnas G (2005) Avian malaria parasites and other Haemosporida. CRC, Boca RatonGoogle Scholar
  25. Ventim R, Ramos JA, Osório H, Lopes RJ, Pérez-Tris J, Mendes L (2012) Avian malaria infections in western European mosquitoes. Parasitol Res 111(2):637–645PubMedCrossRefGoogle Scholar
  26. Waldeström MJ, Bensch S, Hasselquist D, Östman Ö (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol 90:191–194CrossRefGoogle Scholar
  27. Weissenböck H, Kolodziejek J, Url A, Lussy H, Rebel-Bauder B, Nowotny N (2002) Emergence of Usutu virus, an African Mosquito-Borne Flavivirus of the Japanese Encephalitis Virus Group, Central Europe. Emerg Infect Dis 8(7):652–656PubMedCentralPubMedCrossRefGoogle Scholar
  28. Yohannes E, Križanauskiené A, Valcu M, Bensch S, Kempenaers B (2009) Prevalence of malaria and related haemosporidians parasites in two shorebirds species with different winter habitat distribution. J Ornithol 150(1):287–291. doi:10.1007/s10336-008-0349-z CrossRefGoogle Scholar
  29. Zeller HG, Schuffenecker I (2004) West Nile virus: an overview of its spread in Europe and the Mediterranean basin in contrast to its spread in the Americas. Eur J Clin Microbiol Infec Dis 23:147–156CrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2013

Authors and Affiliations

  • Sara Pardal
    • 1
  • José A. Alves
    • 2
  • Líbia Zé-Zé
    • 3
  • Hugo Osório
    • 3
  • Afonso Rocha
    • 1
  • Ricardo J. Lopes
    • 4
  • Pete Potts
    • 5
  • Fátima Amaro
    • 3
  • Francisco Santiago-Quesada
    • 6
  • Juan M. Sanchez-Guzman
    • 6
  • José Masero
    • 6
  • Maria J. Alves
    • 3
  • Javier Pérez-Tris
    • 7
  • Jaime A. Ramos
    • 1
  • Luísa Mendes
    • 1
  1. 1.Department of Life Sciences, IMAR, Marine and Environmental Research Center (IMAR/CMA)University of CoimbraCoimbraPortugal
  2. 2.School of Biological SciencesUniversity of East AngliaNorwichUK
  3. 3.Centre for the Study of Vectors and Infectious Diseases Doutor Francisco CambournacNational Health Institute Doutor Ricardo JorgeÁguas de MouraPortugal
  4. 4.InBIO Laboratório Associado, CIBIO, Centro de Investigação em Biodiversidade e Recursos GenéticosUniversidade do PortoVairãoPortugal
  5. 5.Farlington Ringing GroupSouthamptonUK
  6. 6.Department of Anatomy, Cell Biology and Zoology, Faculty of SciencesUniversity of ExtremaduraBadajozSpain
  7. 7.Departamento de Zoología y Antropología Física, Facultad de BiologíaUniversidad ComplutenseMadridSpain

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