Abstract
Greylag Geese (Anser anser, Anatidae) are associated with water throughout their life and are, therefore, frequently exposed to avian malaria vectors such as mosquitoes (Culicidae) and black flies (Simuliidae). Thus, they could serve as reservoir for avian malaria parasites (Haemosporida). We examined 143 blood samples from individually ringed geese in a sedentary flock in Stuttgart, southwestern Germany, for the prevalence of Haemosporida including Plasmodium, Haemoproteus and Leucocytozoon, using established and newly developed PCR protocols. Only one adult female goose was infected with Plasmodium sp. GRW04 (AF254975.1), a lineage that is part of the morphospecies Plasmodium (Haemamoeba) relictum, which has a worldwide distribution. This is the first time this parasite lineage was detected in the Anseriformes. Our findings support the hypothesis that the transmission of this strain occurred in mainland Europe and is not restricted to wintering areas outside Europe as previously suggested. We discuss the low haemosporidian prevalence detected in the examined goose population in the light of other studies on waterbirds.
Zusammenfassung
Geringe Prävalenz von Blutparasiten (Haemosporida) bei standorttreuen Graugänsen ( Anser anser ) in Südwestdeutschland
Graugänse (Anser anser, Anatidae) sind in ihrer Lebensweise an Wasser gebunden und in der Folge Vektoren der Vogelmalaria (Haemosporida) wie z.B. Mücken (Culicidae) und Kriebelmücken (Simuliidae) häufig ausgesetzt. Sie könnten daher ein Reservoir für diese parasitischen Einzeller darstellen. Daten zu Vogelmalariavorkommen bei Anatiden, insbesondere bei Standvögeln, liegen für Deutschland und auch Europa kaum vor. Mit molekulargenetischen Methoden untersuchten wir daher Blutproben von 143 farbberingten Graugänsen einer ortstreuen Grauganspopulation in Stuttgart, Südwestdeutschland auf Prävalenz von Haemosporidien insbesondere Plasmodium, Haemoproteus und Leucocytozoon. Dafür verwendeten wir für diese Fragestellung anerkannte sowie von uns neu entwickelte PCR-Protokolle. Nur bei einer einzigen weiblichen Gans gelang der Nachweis von Plasmodium sp. GRW04 (AF254975.1). Diese Linie ist Teil der Morphospezies Plasmodium (Haemamoeba) relictum und weltweit verbreitet. Es handelt sich um den ersten Nachweis dieser Linie bei den Anseriformes. Unser Ergebnis stützt die Hypothese anderer Autoren, dass die Übertragung dieser Malarialinie nicht wie ursprünglich angenommen auf die südlich gelegenen Überwinterungsgebiete wie z.B. Afrika beschränkt ist. Die niedrige Prävalenz der Haemosporidien bei den Graugänsen mag in Hinblick auf ihre aquatische Lebensweise zunächst erstaunlich erscheinen. Tatsächlich zeigen auch andere, an Gewässer gebundene Vogelfamilien wie Möwen oder Watvögel, eine ähnlich niedrige Prävalenz von Haemosporidien.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, Bensch S, Graves GR, Jhala YV, Peirce MA, Rahmani AR, Fonseca DM, Fleischer RC (2006) Global phylogeographic limits of Hawaii’s avian malaria. Proc R Soc B Biol Sci 273:2935–2944. https://doi.org/10.1098/rspb.2006.3671
Bensch S, Stjernman M, Hasselquist D, Ostman O, 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 B Biol Sci 267:1583–1589. https://doi.org/10.1098/rspb.2000.1181
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. https://doi.org/10.1111/j.1755-0998.2009.02692.x
Cumming GS, Shepard E, Okanga S, Caron A, Ndlovu M, Peters JL (2013) Host associations, biogeography, and phylogenetics of avian malaria in southern African waterfowl. Parasitology 140:193–201. https://doi.org/10.1017/S0031182012001461
D’Amico VL, Baker AJ (2010) A rare case of Plasmodium (Haemamoeba) relictum infection in a free-living Red Knot (Calidris canutus rufa, Scolopacidae). J Ornithol 151:951–954. https://doi.org/10.1007/s10336-010-0566-0
Ejiri H, Sato Y, Sasaki E, Sumiyama D, Tsuda Y, Sawabe K, Matsui S, Horie S, Akatani K, Takagi M, Omori S, Murata K, Yukawa M (2008) Detection of avian Plasmodium spp. DNA sequences from mosquitoes captured in Minami Daito Island of Japan. J Vet Med Sci 70:1205–1210. https://doi.org/10.1292/jvms.70.1205
Farajollahi A, Fonseca DM, Kramer LD, Kilpatrick AM (2011) “Bird biting” mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. Infect Genet Evol 11:1577–1585. https://doi.org/10.1016/j.meegid.2011.08.013
Ferraguti M, Martínez-de la Puente J, Ruiz S, Soriguer R, Figuerola J (2013) On the study of the transmission networks of blood parasites from SW Spain: diversity of avian haemosporidians in the biting midge Culicoides circumscriptus and wild birds. Parasit Vectors 6:208. https://doi.org/10.1186/1756-3305-6-208
Ferrer ES, García-Navas V, Sanz JJ, Ortego J (2012) Molecular characterization of avian malaria parasites in three Mediterranean Blue Tit (Cyanistes caeruleus) populations. Parasitol Res 111:2137–2142. https://doi.org/10.1007/s00436-012-3062-z
Hellgren O, Waldenstrom J, Bensch S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium and Haemoproteus from avian blood. J Parasitol 90:797–802
Hellgren O, Bensch S, Malmqvist B (2008) Bird hosts, blood parasites and their vectors—associations uncovered by molecular analyses of blackfly blood meals. Mol Ecol 17:1605–1613. https://doi.org/10.1111/j.1365-294X.2007.03680.x
Hellgren O, Atkinson CT, Bensch S, Albayrak T, Dimitrov D, Ewen JG, Kim KS, Lima MR, Martin L, Palinauskas V, Ricklefs R, Sehgal RNM, Valkiunas G, Tsuda Y, Marzal A (2015) Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity. Ecography (Cop.) 38:842–850. https://doi.org/10.1111/ecog.01158
Kim K, Tsuda Y (2015) Sporogony and sporozoite rates of avian malaria parasites in wild Culex pipiens pallens and C. inatomii in Japan. Parasit Vectors 8:633. https://doi.org/10.1186/s13071-015-1251-1
Krams I, Suraka V, Rattiste K, Aboliņš-Abols M, Krama T, Rantala MJ, Mierauskas P, Cirule D, Saks L (2012) Comparative analysis reveals a possible immunity-related absence of blood parasites in Common Gulls (Larus canus) and Black-headed Gulls (Chroicocephalus ridibundus). J Ornithol 153:1245–1252. https://doi.org/10.1007/s10336-012-0859-6
Maier WA, Grunewald J, Habedank B, Hartelt K, Kampen H, Kimmig P, Naucke T, Oehme R, Vollmer A (2001) Mögliche Auswirkungen von Klimaveränderungen auf die Ausbreitung von primär humanmedizinisch relevanten Krankheitserregern über tierische Vektoren sowie auf die wichtigen Humanparasiten in Deutschland, Umweltbundesamt, Bonn. http://www.apug.de/archiv/pdf/Klima_Krankheitserreger_2004.pdf. Accessed 12 Dec 2017
Mendes L, Piersma T, Lecoq M, Spaans B, Ricklefs RE (2005) Disease-limited distributions? contrasts in the prevalence of avian malaria in shorebird species using marine and freshwater habitats. Oikos 109:396–404. https://doi.org/10.1111/j.0030-1299.2005.13509.x
Ramey AM, Reed JA, Schmutz JA, Fondell TF, Meixell BW, Hupp JW, Ward DH, Terenzi J, Ely CR (2014) Prevalence, transmission, and genetic diversity of blood parasites infecting tundra-nesting geese in Alaska. Can J Zool 92:699–706
Renner SC, Lüdtke B, Kaiser S, Kienle J, Schaefer HM, Segelbacher G, Tschapka M, Santiago-Alarcon D (2016) Forests of opportunities and mischief: disentangling the interactions between forests, parasites and immune responses. Int J Parasit 46:571–579
Schmid S, Fachet K, Dinkel A, Mackenstedt U, Woog F (2017) Carrion crows (Corvus corone) of southwest Germany: important hosts for haemosporidian parasites. Malar J 16:369. https://doi.org/10.1186/s12936-017-2023-5
Seimon TA, Gilbert M, Neabore S, Hollinger C, Tomaszewicz A, Newton A, Chang T, McAloose D (2008) Avian haemosporidian parasite lineages in four species of free-ranging migratory water birds from Mongolia. J Wildl Dis 52:2015-11–2015-311. https://doi.org/10.7589/2015-11-311
Soares L, Escudero G, Penha VAS, Ricklefs RE (2016) Low prevalence of haemosporidian parasites in Shorebirds. Ardea 104:129–141. https://doi.org/10.5253/arde.v104i2.a8
Valkiunas G (2005) Avian malaria parasites and other haemosporidia. CRC Ress, London
Valkiunas G, Zehtindjiev P, Hellgren O, Ilieva M, Iezhova TA, Bensch S (2007) Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites, with a description of Plasmodium (Novyella) ashfordi sp. nov. Parasitol Res 100:1311–1322. https://doi.org/10.1007/s00436-006-0409-3
Valkiūnas G, Žiegytė R, Palinauskas V, Bernotienė R, Bukauskaitė D, Ilgūnas M, Dimitrov D, Iezhova TA (2015) Complete sporogony of Plasmodium relictum (lineage pGRW4) in mosquitoes Culex pipiens pipiens, with implications on avian malaria epidemiology. Parasitol Res 114:3075–3085. https://doi.org/10.1007/s00436-015-4510-3
Waldenström AJ, 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
Wink M (2006) Use of DNA markers to study bird migration. J Ornithol 147:234–244. https://doi.org/10.1007/s10336-006-0065-5
Wood MJ, Childs DZ, Davies AS, Hellgren O, Cornwallis CK, Perrins CM, Sheldon BC (2013) The epidemiology underlying age-related avian malaria infection in a long-lived host: the mute swan Cygnus olor. J Avian Biol 44:347–358. https://doi.org/10.1111/j.1600-048X.2013.00091.x
Woog F, Schmolz M, Lachenmaier K (2008) Die bestandsentwicklung der graugans (Anser anser) im stadtkreis stuttgart. Ornithol Jh Bad-Württ 24:141–146
Woog F, Maierhofer J, Haag H (2011) Endoparasites in the annual cycle of feral Greylag Geese Anser anser. Wildfowl 61:166–181
Yohannes E, Krizanauskiene A, Valcu M, Bensch S, Kempenaers B (2009) Prevalence of malaria and related haemosporidian parasites in two shorebird species with different winter habitat distribution. J Ornithol 150:287–291. https://doi.org/10.1007/s10336-008-0349-z
Acknowledgements
We sincerely thank all volunteers assisting in the annual moult catches and the “Ministerium für Ländlichen Raum und Verbraucherschutz Baden-Württemberg” and the “Ministerium für Wissenschaft, Forschung und Kunst Baden-Württemberg“(Kap. 1499 Titel 547 71) for financial support. We are indebted to Markus Weinhardt who did the molecular sexing.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical standards
All applicable federal, state and institutional guidelines for the care and use of animals were followed in this study and 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.
Additional information
Communicated by K. C. Klasing.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Musa, S., Fachet, K., Dinkel, A. et al. Low prevalence of haemosporidian parasites in resident Greylag Geese (Anser anser) in southwestern Germany. J Ornithol 159, 1099–1103 (2018). https://doi.org/10.1007/s10336-018-1580-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-018-1580-x