Skip to main content

Advertisement

SpringerLink
Log in

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

  • Short Note
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

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.

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

References

  • Bennett GF, Montgomerie R, Seutin G (1992) Scarcity of haematozoa in birds breeding on the arctic tundra of North America. Condor 94:289–292

    Article  Google Scholar 

  • 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 267:1583–1589

    Article  CAS  Google Scholar 

  • 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 9:1353–1358

    Article  Google Scholar 

  • 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 41:1041–1047

    Article  CAS  Google Scholar 

  • 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)

    Article  Google Scholar 

  • 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 8:528–531

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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):410–413

    Article  Google Scholar 

  • 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 137:523–525

    Article  Google Scholar 

  • 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 13:1915–1917

    Article  Google Scholar 

  • 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 132:39–46

    Article  CAS  Google Scholar 

  • 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 15:1651–1653

    Article  Google Scholar 

  • 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):61–68

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hubálek Z (2004) An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 40:639–659

    Article  Google Scholar 

  • 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 9:311–322

    Article  Google Scholar 

  • 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 77:358–364

    Article  Google Scholar 

  • 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 109:396–404

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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):39–50

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Valkiūnas G (2005) Avian malaria parasites and other Haemosporida. CRC, Boca Raton

    Google Scholar 

  • 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):637–645

    Article  Google Scholar 

  • 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 90:191–194

    Article  Google Scholar 

  • 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):652–656

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 23:147–156

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to the Farlington Ringing Group, Pedro Geraldes, Filipe Martinho, João Guilherme, and many other volunteers for their essential field assistance during bird capture sessions. The Portuguese Instituto para a Conservação da Natureza e das Florestas provided official permits for bird capturing and sampling. Sandra Antunes, Joana Morais, and Rita Ventim helped during laboratory analysis. This is a contribution from the Moncloa Campus of International Excellence of the Complutense and the Polytechnic Universities of Madrid (through J.P.T.). This project and S.P. were financed by the European Fund for Economic and Regional Development (FEDER) through the Program Operational Factors of Competitiveness (COMPETE) and National Funds through the Portuguese Foundation of Science and Technology (PTDC/BIA-BDE/64063/2006, FCOMP-01-0124-FEDER-007053). J.A.A. was supported by (Calouste Gulbenkian Foundation) and J.P.T. was supported by the Spanish Ministry of Science and Innovation (Grant CGL2010-15734/BOS). The experiments comply with the current laws of the country in which they were performed.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Life Sciences, IMAR, Marine and Environmental Research Center (IMAR/CMA), University of Coimbra, Apartado 3046, 3001-401, Coimbra, Portugal

    Sara Pardal, Afonso Rocha, Jaime A. Ramos & Luísa Mendes

  2. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK

    José A. Alves

  3. Centre for the Study of Vectors and Infectious Diseases Doutor Francisco Cambournac, National Health Institute Doutor Ricardo Jorge, IP, Av. Liberdade n°5, Apartado, 2965-575, Águas de Moura, Portugal

    Líbia Zé-Zé, Hugo Osório, Fátima Amaro & Maria J. Alves

  4. InBIO Laboratório Associado, CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, 4485-661, Vairão, Portugal

    Ricardo J. Lopes

  5. Farlington Ringing Group, Solent Court Cottage, Chilling Lane, Warsash, Southampton, SO31 9HF, UK

    Pete Potts

  6. Department of Anatomy, Cell Biology and Zoology, Faculty of Sciences, University of Extremadura, 06006, Badajoz, Spain

    Francisco Santiago-Quesada, Juan M. Sanchez-Guzman & José Masero

  7. Departamento de Zoología y Antropología Física, Facultad de Biología, Universidad Complutense, 28040, Madrid, Spain

    Javier Pérez-Tris

Authors
  1. Sara Pardal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José A. Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Líbia Zé-Zé
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hugo Osório
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Afonso Rocha
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ricardo J. Lopes
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pete Potts
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fátima Amaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Francisco Santiago-Quesada
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Juan M. Sanchez-Guzman
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. José Masero
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Maria J. Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Javier Pérez-Tris
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Jaime A. Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Luísa Mendes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sara Pardal.

Additional information

Communicated by K. C. Klasing.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10336_2013_1036_MOESM1_ESM.docx

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.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pardal, S., Alves, J.A., Zé-Zé, L. et al. Shorebird low spillover risk of mosquito-borne pathogens on Iberian wetlands. J Ornithol 155, 549–554 (2014). https://doi.org/10.1007/s10336-013-1036-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-013-1036-2

Keywords

Search

Navigation