Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-13T01:58:11.122Z Has data issue: false hasContentIssue false

Serological and molecular surveys of influenza A viruses in Antarctic and sub-Antarctic wild birds

Published online by Cambridge University Press:  03 December 2019

Oliver Gittins
Affiliation:
School of Veterinary Medicine and Science (SVMS), University of Nottingham, Sutton Bonington Campus, LoughboroughLE12 5RD, UK
Llorenç Grau-Roma
Affiliation:
School of Veterinary Medicine and Science (SVMS), University of Nottingham, Sutton Bonington Campus, LoughboroughLE12 5RD, UK Current address: Institute of Animal Pathology, University of Bern, Länggassstrasse 122, 3012, Bern, Switzerland
Rosa Valle
Affiliation:
IRTA, Centre de Recerca en Sanitat Animal (CReSA, UAB-IRTA), Campus UAB, 08193Bellaterra, Spain
Francesc Xavier Abad
Affiliation:
IRTA, Centre de Recerca en Sanitat Animal (CReSA, UAB-IRTA), Campus UAB, 08193Bellaterra, Spain
Miquel Nofrarías
Affiliation:
IRTA, Centre de Recerca en Sanitat Animal (CReSA, UAB-IRTA), Campus UAB, 08193Bellaterra, Spain
Peter G. Ryan
Affiliation:
FitzPatrick Institute of African Ornithology, DST-NRF Centre of Excellence, University of Cape Town, Rondebosch7701, South Africa
Jacob González-Solís
Affiliation:
Institut de Recerca de la Biodiversitat (IRBio) and Dept Biologia Evolutiva, Ecologia i Ciències Ambientals, Universitat de Barcelona, Av. Diagonal 643, 08028Barcelona, Spain
Natàlia Majó*
Affiliation:
IRTA, Centre de Recerca en Sanitat Animal (CReSA, UAB-IRTA), Campus UAB, 08193Bellaterra, Spain Departament de Sanitat i Anatomia Animals, Universitat Autònoma de Barcelona, 08193Bellaterra, Barcelona, Spain

Abstract

To evaluate how avian influenza virus (AIV) circulates among the avifauna of the Antarctic and sub-Antarctic islands, we surveyed 14 species of birds from Marion, Livingston and Gough islands. A competitive enzyme-linked immunosorbent assay was carried out on the sera of 147 birds. Quantitative reverse transcription polymerase chain reaction was used to detect the AIV genome from 113 oropharyngeal and 122 cloacal swabs from these birds. The overall seroprevalence to AIV infection was 4.8%, with the only positive results coming from brown skuas (Catharacta antarctica) (4 out of 18, 22%) and southern giant petrels (Macronectes giganteus) (3 out of 24, 13%). Avian influenza virus antibodies were detected in birds sampled from Marion and Gough islands, with a higher seroprevalence on Marion Island (P = 0.014) and a risk ratio of 11.29 (95% confidence interval: 1.40–91.28) compared to Gough Island. The AIV genome was not detected in any of the birds sampled. These results confirm that AIV strains are uncommon among Antarctic and sub-Antarctic predatory seabirds, but they may suggest that scavenging seabirds are the main avian reservoirs and spreaders of this virus in the Southern Ocean. Further studies are necessary to determine the precise role of these species in the epidemiology of AIV.

Type
Biological Sciences
Copyright
Copyright © Antarctic Science Ltd 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abad, F.X., Busquets, N., Sanchez, A., Ryan, P.G., Majó, N. & Gonzalez-Solís, J. 2013. Serological and virological surveys of the influenza A viruses in Antarctic and sub-Antarctic penguins. Antarctic Science, 25, 10.1017/S0954102012001228.CrossRefGoogle Scholar
Afanador-Villamizar, A., Gomez-Romero, C., Diaz, A. & Ruiz-Saenz, J. 2017. Avian influenza in Latin America: a systematic review of serological and molecular studies from 2000–2015. PloS One, 12, e0179573.CrossRefGoogle ScholarPubMed
Austin, F. & Webster, R. 1993. Evidence of ortho- and paramyxoviruses in fauna from Antarctica. Journal of Wildlife Diseases, 29, 568571.CrossRefGoogle ScholarPubMed
Barbosa, A. & Palacios, M.J. 2009. Health of Antarctic birds: a review of their parasites, pathogens and diseases. Polar Biology, 32, 10.1007/s00300-009-0640-3.CrossRefGoogle ScholarPubMed
Baumeister, E., Leotta, G., Pontoriero, A., Campos, A., Montalti, D., Vigo, G., Pecoraro, M. & Savy, V. 2004. Serological evidences of influenza A virus infection in Antarctica migratory birds. International Congress Series, 1263, 10.1016/j.ics.2004.02.099.CrossRefGoogle Scholar
Birdlife International. 2018. Data zone: Southern Giant petrel and Brown skuas. Available at http://datazone.birdlife.org/home (accessed September 2018).Google Scholar
Brown, J.D., Stallknecht, D.E., Beck, J.R., Suarez, D.L. & Swayne, D.E. 2006. Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses. Emerging Infectious Diseases, 12, 10.3201/eid1211.060652.CrossRefGoogle ScholarPubMed
Brown, J.D., Luttrell, M.P., Uhart, M.M., Ferreyra, H. del V., Romano, M.M., Rago, M.V. & Stallknecht, D.E. 2010. Antibodies to type A influenza virus in wild waterbirds from Argentina. Journal of Wildlife Diseases, 46, 10401045.CrossRefGoogle ScholarPubMed
Busquets, N., Alba, A., Napp, S., Sánchez, A., Serrano, E., Rivas, R., et al. 2010. Influenza A virus subtypes in wild birds in north-eastern Spain (Catalonia). Virus Research, 149, 10.1016/j.virusres.2009.12.005.CrossRefGoogle Scholar
Conroy, J. 1972. Ecological Aspects of the Biology of the Giant Petrel, Macronectes giganteus (Gmelin), in the Maritime Antarctic. Cambridge: British Antarctic Survey.Google Scholar
Egevang, C., Stenhouse, I.J., Phillips, R.A., Petersen, A., Fox, J.W. & Silk, J.R. 2010. Tracking of Arctic terns Sterna paradisaea reveals longest animal migration. Proceedings of the National Academy of Sciences of the United States of America, 107, 20782081.CrossRefGoogle ScholarPubMed
Ely, C.R., Hall, J.S., Schmutz, J.A., Pearce, J.M., Terenzi, J., Sedinger, J.S. & Ip, H.S. 2013. Evidence that life history characteristics of wild birds influence infection and exposure to influenza A viruses. PLoS One, 8, e57614.CrossRefGoogle ScholarPubMed
FAO. 2018. 2016–2018 spread of H5N8 highly pathogenic avian influenza (HPAI) in sub-Saharan Africa: epidemiological and ecological observations. Available at: http://www.fao.org/3/ca1209en/CA1209EN.pdf (accessed October 2018).Google Scholar
Grillo, V., Arzey, K., Hansbro, P., Hurt, A., Warner, S., Bergfeld, J., et al. 2015. Avian influenza in Australia: a summary of 5 years of wild bird surveillance. Australian Veterinary Journal, 93, 10.1111/avj.12379.CrossRefGoogle ScholarPubMed
Hunter, S. 1983. The food and feeding ecology of the giant petrels Macronectes halli and M. giganteus at South Georgia. Journal of Zoology, 200, 521538.Google Scholar
Hurt, A.C., Su, Y.C.F., Aban, M., Peck, H., Lau, H., Baas, C., et al. 2016. Evidence for the introduction, reassortment, and persistence of diverse influenza A viruses in Antarctica. Journal of Virology, 90, 10.1128/JVI.01404-16.CrossRefGoogle ScholarPubMed
Hurt, A.C., Vijaykrishna, D., Butler, J., Baas, C., Maurer-Stroh, S., Silva-de-la-Fuente, M.C., et al. 2014. Detection of evolutionarily distinct avian influenza A viruses in Antarctica. mBio, 5, 10.1128/mBio.01098-14.CrossRefGoogle ScholarPubMed
Kilpatrick, A.M., Chmura, A.A., Gibbons, D.W., Fleischer, R.C., Marra, P.P. & Daszak, P. 2006. Predicting the global spread of H5N1 avian influenza. Proceedings of the National Academy of Sciences of the United States of America, 103, 1936819373.CrossRefGoogle ScholarPubMed
McMahon, C.R. 2010. Health of Antarctic wildlife: a challenge for science and policy. Polar Research, 29, 10.1111/j.1751-8369.2010.00182.x.Google Scholar
Miller, G.D., Watts, J.M. & Shellam, G.R. 2008. Viral antibodies in south polar skuas around Davis Station, Antarctica. Antarctic Science, 20, 10.1017/S0954102008001259.CrossRefGoogle Scholar
Olsen, B., Munster, V.J., Wallensten, A., Waldenström, J., Osterhaus, A.D.M.E. & Fouchier, R.A.M. 2006. Global patterns of influenza A virus in wild birds. Science, 312, 10.1126/science.1122438.CrossRefGoogle ScholarPubMed
Ramos i Garcia, R., Garnier, R., González-Solís, J. & Boulinier, T. 2014. Long antibody persistence and transgenerational immonoresponse in a long-lived vertebrate. American Naturalist, 185, 764776.CrossRefGoogle Scholar
Renata, H. & Thijl, V.R.E. 2016. Avian influenza in wild birds from South America: review, implications and perspectives. Exploratory Research and Hypothesis in Medicine, 1, 6274.Google Scholar
Roscales, J.L., González-Solís, J., Zango, L., Ryan, P.G. & Jiménez, B. 2016. Latitudinal exposure to DDTs, HCB, PCBs, PBDEs and DP in giant petrels (Macronectes spp.) across the Southern Ocean. Environmental Research, 148, 285294.CrossRefGoogle ScholarPubMed
Shirihai, H. 2008. The Complete Guide to the Antarctic Wildlife. Princeton, NJ: Princeton University Press.Google Scholar
Silva, M.P., Favero, M., Casaux, R. & Baroni, A. 1998. The status of breeding birds at Harmony Point, Nelson Island, Antarctica in summer 1995/96. Marine Ornithology, 26, 7578.Google Scholar
Souza Petersen, E., Araujo, J., Krüger, L., Seixas, M., Ometto, T., Thomazelli, L., et al. 2017. First detection of avian influenza virus (H4N7) in giant petrel monitored by geolocators in the Antarctic region. International Journal on Life in Oceans and Coastal Waters, 164, 10.1007/s00227-017-3086-0.Google Scholar
Spackman, E., Senne, D.A., Myers, T., Bulaga, L.L., Garber, L.P., Perdue, M.L., et al. 2002. Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. Journal of Clinical Microbiology, 40, 32563260.CrossRefGoogle ScholarPubMed
Stonehouse, B. 1956. The Brown Skua (Catharacta skua lönnbergi, Mathews) of South Georgia. Richmond: Her Majesty's Stationery Office.Google Scholar
Webster, R.G., Bean, W.J., Gorman, O.T., Chambers, T.M. & Kawaoka, Y. 1992. Evolution and ecology of influenza A viruses. Microbiological Reviews, 56, 152179.CrossRefGoogle ScholarPubMed
Weimerskirch, H., Tarroux, A., Chastel, O., Delord, K., Cherel, Y. & Descamps, S. 2015. Population-specific wintering distributions of adult south polar skuas over three oceans. Marine Ecology Progress Series, 538, 229237.CrossRefGoogle Scholar