Sane and sound: a serologic and molecular survey for selected infectious agents in neozootic Egyptian geese (Alopochen aegyptiacus) in Germany

  • Hanna PrüterEmail author
  • Gábor Árpád Czirják
  • Sönke Twietmeyer
  • Timm Harder
  • Christian Grund
  • Kristin Mühldorfer
  • Dörte Lüschow
Original Article


Aquatic birds can act as vectors and reservoir hosts for pathogens relevant for wild birds and poultry as well as human health. In this study, we address the questions (1) if the Egyptian goose (Alopochen aegyptiacus), as one of the most successful neozootic bird species in Europe, carry infectious agents that are relevant for poultry and wild birds and (2) if seasonal prevalences of these infectious agents differ from those of native geese species. In 2015 and 2016, up to 190 Egyptian geese from Western Germany were investigated serologically for antibodies (Ab) against influenza A viruses (IAV), Avian avulavirus 1 (AAvV-1), aviadenoviruses, Duck atadenovirus A (syn.: egg drop syndrome 1976 virus) (EDSV), and West Nile virus (WNV). Ab were detected against IAV in 6.1% (10/164), against AAvV-1 in 2.4% (4/165), against EDSV in 15.2% (16/105), and against aviadenoviruses in 0.86% (1/116) of the geese blood samples, respectively. None of the birds had Ab against WNV (0/84). PCR-based techniques (cloacal and/or pharyngeal swabs) were applied for the presence of IAV, AAvV-1, Mycoplasma spp., and Riemerella anatipestifer. Riemerella DNA was detected in the pharyngeal swabs with an overall prevalence of 70.3% (104/148). Neither Mycoplasma DNA nor IAV or AAvV-1 RNA could be detected in the pharynx or cloaca of the examined birds. Our study shows that Egyptian geese are frequent carriers of Riemerella anatipestifer and furthermore provides serological evidence of exposure to IAV, AAvV-1, and EDSV. It is one of very few studies on infectious agents of neozootic bird species. Comparing our results from a neozootic non-migratory goose species with published results from native migratory geese species (bean goose (Anser fabalis) and white-fronted goose (A. albifrons)) and another neozootic non-migratory goose species (Canada goose (Branta canadensis)), we found differences in the seroprevalence of viral pathogens. Native goose species show higher seroprevalences of IAV and AAvV-1, whereas neozootic non-migratory geese reveal higher seroprevalences for EDSV. The findings are discussed in the frame of seasonal variations in selected infectious agents, differences in sampling periods, and contrasting movement ecology of the different geese species.


Alopochen aegyptiacus Avian avulavirus Aviadenoviruses Influenza A virus Neozootic bird Riemerella anatipestifer 



This research was undertaken as part of the Graduate School IMPact-Vector funded by the Senate Competition Committee grant (SAW-2014-SGN-3) of the Leibniz Association and financially supported by the Ministry of Rhineland-Palatinate (Ministerium für Umwelt, Energie, Ernährung und Forsten, Project Nr: Gz. 105-63 313/2015-40). Hanna Prüter is also an associated doctoral student of the GRK2046 from the German Research Foundation (DFG). Additional support was received from the project AquaVir (Leibniz Association, SAW-2015-IZW-1 440), especially from Alex D. Greenwood, for which we are grateful. We are thankful to Lorena Derezanin, Elke Dyrks, Birgit Göllner, Gabriele Grotehenn, and Michaela Mann for their technical assistance; to Sarah Brüggemann-Schwarze for her help with the ELISA; to Niklas Böhm, Lorena Derezanin, Sophie Ewert, Lea Jäger, Oliver Krone, Manuela Merling de Chapa, Katja Pohle, Felix Prüter, and Jannis Twietmeyer for their assistance during field or laboratory work.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Supplementary material

10344_2018_1231_Fig1_ESM.png (370 kb)
Figure S1

Sampling sites in Western Germany (PNG 369 kb)

10344_2018_1231_MOESM1_ESM.tiff (24.6 mb)
High Resolution Image (TIFF 25186 kb)
10344_2018_1231_MOESM2_ESM.docx (14 kb)
Table S1 Serology results for antibody detection against influenza A virus (IAV), Avian avulavirus 1 (AAvV-1) and West Nile virus (WNV) in sera collected in 2015 and 2016 from Egyptian geese (DOCX 13 kb)


  1. Abolnik C, Gerdes GH, Sinclair M, Ganzevoort BW, Kitching JP, Burger CE, Romito M, Dreyer M, Swanepoel S, Cumming GS, Olivier AJ (2010) Phylogenetic analysis of influenza A viruses (H6N8, H1N8, H4N2, H9N2, H10N7) isolated from wild birds, ducks and ostriches in South Africa from 2007 to 2009. Avian Dis 54:313–322CrossRefGoogle Scholar
  2. Arnold JM, Greiser G, Kampmann S and Martin I (2013) Status und Entwicklung ausgewählter Wildtierarten in Deutschland. Jahresbericht 2013. Wildtier-Informations- system der Länder Deutschlands (WILD). Deutscher Jagdverband; BerlinGoogle Scholar
  3. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48CrossRefGoogle Scholar
  4. Bauer H-G, Woog F (2008) Nichtheimische Vogelarten (Neozoen) in Deutschland, Teil I: Auftreten, Bestände und status - non-native and naturalized bird species (neozoa) in Germany, part I: occurrence, population size and status. Vogelwarte 46(2008):157–194Google Scholar
  5. Blackburn TM, Lockwood JL and Cassey P (2009) Avian invasions: the ecology and evolution of exotic birds. Oxford University press, Oxford ; New YorkGoogle Scholar
  6. Bönner BM, Jäger S, Reichel U, Lutz W, Wissing J, Knickmeier W et al (2003) Untersuchungen zum Gesundheitsstatus von Kanadagänsen (Branta canadensis, Linnaeus, 1758) in Nordrhein-Westfalen an Hand der Analyse von Eiern. Z Jagdwiss 49:61–76Google Scholar
  7. Brown JD, Luttrell MP, Berghaus RD, Kistler W, Keeler SP, Howey A, Wilcox B, Hall J, Niles L, Dey A, Knutsen G, Fritz K, Stallknecht DE (2010) Prevalence of antibodies to type A influenza virus in wild avian species using two serological assays. J Wildl Dis 46:896–911CrossRefGoogle Scholar
  8. Burger CE, Abolnik C, Fosgate GT (2012) Antibody response and viral shedding profile of Egyptian geese (Alopochen aegyptiacus) infected with low pathogenicity H7N1 and H6N8 avian influenza viruses. Avian Dis 56:341–346CrossRefGoogle Scholar
  9. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443CrossRefGoogle Scholar
  10. Cha S-Y, Kang M, Park C-K, Choi K-S, Jang H-K (2013) Epidemiology of egg drop syndrome virus in ducks from South Korea. Poult Sci 92:1783–1789CrossRefGoogle Scholar
  11. Cha S-Y, Seo H-S, Wei B, Kang M, Roh J-H, Yoon R-H, Kim JH, Jang HK (2015) Surveillance and characterization of Riemerella anatipestifer from wild birds in South Korea. J Wildl Dis 51:341–347CrossRefGoogle Scholar
  12. Cumming GS, Hockey PAR, Bruinzeel LW, Du Plessis MA (2008) Wild bird movements and avian influenza risk mapping in Southern Africa. Ecol Soc 13(2):26CrossRefGoogle Scholar
  13. Dietzen, C., Dolich, T., Grunwald, T., Keller, P. and Kunz, A. (2015) Die Vogelwelt von Rheinland-Pfalz. Band 2 Entenvögel bis Storchenvögel (Anseriformes-Ciconiformes). Gesellschaft für Ornithologie Rheinland-Pfalz LandauGoogle Scholar
  14. Dimitrov KM, Ramey AM, Qiu X, Bahl J, Afonso CL (2016) Temporal, geographic, and host distribution of avian paramyxovirus 1 (Newcastle disease virus). Infect Genet Evol 39:22–34CrossRefGoogle Scholar
  15. Fouchier RAM, Olsen B, Bestebroer TM, Herfst S, van der Kemp L, Rimmelzwaan GF, Osterhaus ADME (2003) Influenza A virus surveillance in wild birds in Northern Europe in 1999 and 2000. Avian Dis 47:857–860CrossRefGoogle Scholar
  16. Gedeon K, Sudfeldt C, Dougalis P (eds) (2015) Atlas Deutscher Brutvogelarten - Atlas of German Breeding Birds, neue Ausg. Dachverband Deutscher Avifaunisten, Münster, WestfGoogle Scholar
  17. Gulka CM, Piela TH, Yates VJ, Bagshaw C (1984) Evidence of exposure of waterfowl and other aquatic birds to the haemagglutinating duck adenovirus identical to EDS-76 virus. J Wildl Dis 20:1–5CrossRefGoogle Scholar
  18. Gyimesi A, Lensink R (2010) Risk analysis of the Egyptian goose in the Netherlands. Bureau Waardenburg BV Culomborg, The NetherlandsGoogle Scholar
  19. Hess C, Enichlmayr H, Jandreski-Cvetkovic D, Liebhart D, Bilic I, Hess M (2013) Riemerella anatipestifer outbreaks in commercial goose flocks and identification of isolates by MALDI-TOF mass spectrometry. Avian Pathology 42:151–156CrossRefGoogle Scholar
  20. Hinz K, Ryll M, Köhler B, Glünder G (1998) Phenotypic characteristics of Riemerella anatipestifer and similar micro-organisms from various hosts. Avian Pathology 27:33–42CrossRefGoogle Scholar
  21. Hoffmann B, Harder T, Lange E, Kalthoff D, Reimann I, Grund C et al (2010) New real-time reverse transcriptase polymerase chain reactions facilitate detection and differentiation of novel a/H1N1 influenza virus in porcine and human samples. Berliner und Muenchener Tierarztliche Wochenschrift 123:286–292Google Scholar
  22. Hubálek Z (2004) An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 40:639–659CrossRefGoogle Scholar
  23. Ivanics E, Palya V, Glavits R, Dan A, Palfi V, Reeesz T et al (2001) The role of egg drop syndrome virus in acute respiratory disease of goslings. Avian Pathology 30:201–208CrossRefGoogle Scholar
  24. Kistler WM, Stallknecht DE, Deliberto TJ, Swafford S, Pedersen K, Why KV, Wolf PC, Hill JA, Bruning DL, Cumbee JC, Mickley RM, Betsill CW, Randall AR, Berghaus RD, Yabsley MJ (2012) Antibodies to avian influenza viruses in Canada geese (Branta canadensis): a potential surveillance tool? J Wildl Dis 48:1097–1101CrossRefGoogle Scholar
  25. Kruckenberg H, Müller T, Freuling C, Mühle R-U, Globig A, Schirrmeier H, Buss M, Harder T, Kramer M, Teske K, Polderdijk K, Wallschläger D, Hlinak A (2011) Serological and virological survey and resighting of marked wild geese in Germany. Eur J Wildl Res 57:1025–1032CrossRefGoogle Scholar
  26. Latorre-Margalef N, Tolf C, Grosbois V, Avril A, Bengtsson D, Wille M, Osterhaus ADME, Fouchier RAM, Olsen B, Waldenström J (2014) Long-term variation in influenza A virus prevalence and subtype diversity in migratory mallards in northern Europe. Proc R Soc B Biol Sci 281:20140098CrossRefGoogle Scholar
  27. Leggewie M, Badusche M, Rudolf M, Jansen S, Börstler J, Krumkamp R, Huber K, Krüger A, Schmidt-Chanasit J, Tannich E, Becker SC (2016) Culex pipiens and Culex torrentiumpopulations from Central Europe are susceptible to West Nile virus infection. One Health 2:88–94CrossRefGoogle Scholar
  28. Lierz M, Hagen N, Harcourt-Brown N, Hernandez-Divers SJ, Lüschow D, Hafez HM (2007) Prevalence of mycoplasmas in eggs from birds of prey using culture and a genus-specific mycoplasma polymerase chain reaction. Avian Pathology 36:145–150CrossRefGoogle Scholar
  29. Lillehaug A, Monceyron Jonassen C, Bergsjø B, Hofshagen M, Tharaldsen J, Nesse LL et al (2005) Screening of feral pigeon (Colomba livia), mallard (Anas platyrhynchos) and graylag goose (Anser anser) populations for Campylobacter spp., Salmonella spp., avian influenza virus and avian paramyxovirus. Acta Vet Scand 46:193–202CrossRefGoogle Scholar
  30. Linke S, Niedrig M, Kaiser A, Ellerbrok H, Müller K, Müller T et al (2007) Serologic evidence of West Nile Virus infections in wild birds captured in Germany. Am J Trop Med Hyg 77:358–364CrossRefGoogle Scholar
  31. McFerran JB, Smyth JA (2000) Avian adenoviruses. Revue Scientifique Et Technique (International Office of Epizootics) 19:589–601Google Scholar
  32. Morand S, Bordes F, Chen H-W, Claude J, Cosson J-F, Galan M et al (2015) Global parasite and Rattus rodent invasions: the consequences for rodent-borne diseases. Integr Zool 10:409–423CrossRefGoogle Scholar
  33. OIE World Animal Health Information System. URL [accessed 21 June 2017]
  34. Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus ADME, Fouchier RAM (2006) Global patterns of influenza A virus in wild birds. Science 312:384–388CrossRefGoogle Scholar
  35. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891CrossRefGoogle Scholar
  36. Pfitzer S, Verwoerd DJ, Gerdes GH, Labuschagne AE, Erasmus A, Manvell RJ, Grund C (2000) Newcastle disease and avian influenza A virus in wild waterfowl in South Africa. Avian Dis 44:655–660CrossRefGoogle Scholar
  37. R Core Team. (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  38. Ryll M, Christensen H, Bisgaard M, Christensen JP, Hinz KH, Köhler B (2001) Studies on the prevalence of Riemerella anatipestifer in the upper respiratory tract of clinically healthy ducklings and characterization of untypable strains. J Vet Med B Infect Dis Vet Public Health 48:537–546CrossRefGoogle Scholar
  39. Shihmanter E, Weisman Y, Lublin A, Mechani S, Gruenberg R, Horowith H, Lipkind M (1998) Avian paramyxoviruses serotype 3 isolated from captive birds in Israel: clinical signs, pathology, and antigenic characterization. Avian Dis 42:418–422CrossRefGoogle Scholar
  40. Suarez DL, Schultz-Cherry S (2000) Immunology of avian influenza virus: a review. Dev Comp Immunol 24:269–283CrossRefGoogle Scholar
  41. Thompson PN, Sinclair M, Ganzevoort B (2008) Risk factors for seropositivity to H5 avian influenza virus in ostrich farms in the Western Cape Province, South Africa. Prev Vet Med 86:139–152CrossRefGoogle Scholar
  42. Tolf C, Latorre-Margalef N, Wille M, Bengtsson D, Gunnarsson G, Grosbois V, Hasselquist D, Olsen B, Elmberg J, Waldenström J (2013) Individual variation in influenza A virus infection histories and long-term immune responses in mallards. PLoS One 8:e61201CrossRefGoogle Scholar
  43. Tsai H-J, Liu Y-T, Tseng C-S, Pan M-J (2005) Genetic variation of the ompA and 16S rRNA genes of Riemerella anatipestifer. Avian Pathology 34:55–64CrossRefGoogle Scholar
  44. Wahl J, Dröschmeister R, Langgemach T and Sudfeldt (Hrsg.) C (2011) Vögel in Deutschland - 2011. DDA, BfN, LAG VSW, MünsterGoogle Scholar
  45. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179PubMedPubMedCentralGoogle Scholar
  46. Wille M, Avril A, Tolf C, Schager A, Larsson S, Borg O, Olsen B, Waldenström J (2015) Temporal dynamics, diversity, and interplay in three components of the virodiversity of a mallard population: influenza A virus, avian paramyxovirus and avian coronavirus. Infect Genet Evol 29:129–137CrossRefGoogle Scholar
  47. Wise MG, Suarez DL, Seal BS, Pedersen JC, Senne DA, King DJ, Kapczynski DR, Spackman E (2004) Development of a real-time reverse-transcription PCR for detection of Newcastle disease virus RNA in clinical samples. J Clin Microbiol 42:329–338CrossRefGoogle Scholar
  48. Woernle H (1959) Diagnose der infektiösen Bronchitis der Hühner mit Hilfe der Präzipitationsreaktion im festen Agarmedium. Monatshefte für Tierheilkunde, Stuttgart 11:154–167Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Wildlife DiseasesLeibniz Institute for Zoo and Wildlife ResearchBerlinGermany
  2. 2.Department of Research and DocumentationEifel National ParkSchleidenGermany
  3. 3.Friedrich-Loeffler-InstitutFederal Research Institute for Animal HealthGreifswaldGermany
  4. 4.Freie Universität BerlinInstitute of Poultry DiseasesBerlinGermany

Personalised recommendations