Avian malaria parasites (Haemosporida: Plasmodiidae) in mosquitoes (Diptera: Culicidae) of the Curonian Spit (South-East coast of the Baltic Sea)

Elena Platonova; Alexander Davydov; Maria Erokhina; Andrey Mukhin

doi:10.21638/spbu03.2024.306

Authors

Elena Platonova Biological Station Rybachy, Zoological Institute, Russian Academy of Sciences, ul. Pobedy, 32, Rybachy, Kaliningrad Region, 238535, Russian Federation https://orcid.org/0000-0002-9425-8998
Alexander Davydov Biological Station Rybachy, Zoological Institute, Russian Academy of Sciences, ul. Pobedy, 32, Rybachy, Kaliningrad Region, 238535, Russian Federation https://orcid.org/0000-0001-8577-503X
Maria Erokhina Biological Station Rybachy, Zoological Institute, Russian Academy of Sciences, ul. Pobedy, 32, Rybachy, Kaliningrad Region, 238535, Russian Federation; Department of Vertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University, ul. Kolmogorova, 1, Moscow, 119234, Russian Federation https://orcid.org/0000-0002-9905-8338
Andrey Mukhin Biological Station Rybachy, Zoological Institute, Russian Academy of Sciences, ul. Pobedy, 32, Rybachy, Kaliningrad Region, 238535, Russian Federation https://orcid.org/0000-0003-1238-4163

DOI:

https://doi.org/10.21638/spbu03.2024.306

Abstract

In recent years, numerous studies have shown an increasing prevalence of avian haemosporidian parasites in Europe. However, little is known about the vectors of these parasites, particularly specific dipterian species transmitting malaria parasites to birds. This study aims to identify vectors of avian malaria parasites on the South-East Baltic coast. Mosquito females were collected from 2020 to 2021 on the Curonian Spit of the Baltic Sea using traps with birds as bait. All insects were identified to the species level through morphological features and the PCR method. Subsequently, they were dissected to extract salivary glands for studying the presence of avian malaria infecting stages (the sporozoites). The remaining mosquito parts were used later for molecular analysis to detect haemosporidian parasite DNA. A total of 596 mosquitoes belonging to 8 species were collected. The analysis revealed that Culex pipiens is a competent vector of avian Plasmodium relictum (genetic lineages pGRW11 and pSGS1) and a potential vector for Plasmodium vaughani (genetic lineage pSYAT05) on the Curonian Spit of the Baltic Sea.

Keywords:

Avian malaria parasites, Plasmodium, mosquitoes, Culex pipiens, transmission, vectors

Downloads

Download data is not yet available.

References

Aželytė, J., Platonova, E., Bensch, S., Hellgren, O., and Palinauskas, V. 2022. A comparative analysis of the dynamics of Plasmodium relictum (GRW4) development in the blood during single and co-infections. Acta Tropica 226:106247. https://doi.org/10.1016/j.actatropica.2021.106247

Atkinson, C. T. 2008. Avian malaria; pp. 35–53 in Atkinson, C. T., Thomas, N. J., and Hunter, D. B. (eds), Parasitic Diseases of Wild Birds. Wiley-Blackwell. Ames, Iowa. https://doi.org/10.1002/9780813804620

Becker, N., Petrić, D., Zgomba, M., Boase, C., Madon, M., Dahl, C., and Kaiser, A. 2010. Mosquitoes and their control. Springer, Berlin; Heidelberg.

Bensch, S., Hellgren, O., and Pérez‐Tris, J. 2009. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9:1353–1358. https://doi.org/10.1111/j.1755-0998.2009.02692.x

Bernotienė, R. 2012. The fauna and seasonal activity of mosquitoes (Diptera: Culicidae) in the Curonian Spit (Russia, Lithuania). European Mosquito Bulletin 30:72–78.

Bernotienė, R., Iezhova, T. A., Bukauskaitė, D., Chagas, C. R. F., Kazak, M., and Valkiūnas, G. 2020. Development of Trypanosoma everetti in Culicoides biting midges. Acta Tropica 210:105555. https://doi.org/10.1016/j.actatropica.2020.105555

Bernotienė, R., Žiegytė, R., Vaitkutė, G., and Valkiūnas, G. 2019. Identification of a new vector species of avian haemoproteids, with a description of methodology for the determination of natural vectors of haemosporidian parasites. Parasites and Vectors 12:1–10. https://doi.org/10.1186/s13071-019-3559-8

Brugman, V. A., Medlock, J. M., Logan, J. G., Wilson, A. J., Lindsay, S. W., Fooks, A. R., Mertens, P. P., Johnson, N., and Carpenter, S. T. 2018. Bird-biting mosquitoes on farms in southern England. The Veterinary Record 183:474. https://doi.org/10.1136/vr.104830

Černý, O., Votýpka, J., and Svobodová, M. 2011. Spatial feeding preferences of ornithophilic mosquitoes, blackflies and biting midges. Medical and Veterinary Entomology 25:104–108. https://doi.org/10.1111/j.1365-2915.2010.00875.x

Ejiri, H., Sato, Y., Sawai, R., Sasaki, E., Matsumoto, R., Ueda, M., Higa, Y., Tsuda, Y., Omori, S., Murata, K., and Yukawa, M. 2009. Prevalence of avian malaria parasite in mosquitoes collected at a zoological garden in Japan. Parasitology Research 105:629–633. https://doi.org/10.1007/s00436-009-1434-9

Fecchio, A., Chagas, C. R., Bell, J. A., and Kirchgatter, K. 2020. Evolutionary ecology, taxonomy, and systematics of avian malaria and related parasites. Acta Tropica 204:105364. https://doi.org/10.1016/j.actatropica.2020.105364

Ferraguti, M., Martinez-de la Puente, J., Munoz, J., Roiz, D., Ruiz, S., Soriguer, R., and Figuerola, J. 2013. Avian Plasmodium in Culex and Ochlerotatus mosquitoes from southern Spain: effects of season and host-feeding source on parasite dynamics. Plos One 8:e66237. https://doi.org/10.1371/journal.pone.0066237

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3(5):294–299.

Glaizot, O., Fumagalli, L., Iritano, K., Lalubin, F., Van Rooyen, J., and Christe, P. 2012. High prevalence and lineage diversity of avian malaria in wild populations of great tits (Parus major) and mosquitoes (Culex pipiens). Plos One 7:e34964. https://doi.org/10.1371/journal.pone.0034964

Hall, A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program of Windows 95/98/NT. Nucleic Acids Symposium Series 41:95–98.

Hellgren, O., Waldenström, J., and Bensch, S. 2004. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology 90:797–802. https://doi.org/10.1645/GE-184R1

Inci, A., Yildirim, A., Njabo, K., Duzlu, O., Biskin, Z., and Ciloglu, A. 2012. Detection and molecular characterization of avian Plasmodium from mosquitoes in central Turkey. Veterinary Parasitology 188:179–184. https://doi.org/10.1016/j.vetpar.2012.02.012

Kazlauskienė, R., Bernotienė, R., Palinauskas, V., Iezhova, T. A., and Valkiūnas, G. 2013. Plasmodium relictum (lineages pSGS1 and pGRW11): Complete synchronous sporogony in mosquitoes Culex pipiens pipiens. Experimental Parasitology 133:454–461. https://doi.org/10.1016/j.exppara.2013.01.008

Kim, K. and Tsuda, Y. 2015. Sporogony and sporozoite rates of avian malaria parasites in wild Culex pipiens pallens and C. inatomii in Japan. Parasites and Vectors 8:1–5. https://doi.org/10.1186/s13071-015-1251-1

Köchling, K., Schaub, G. A., Werner, D., and Kampen, H. 2023. Avian Plasmodium spp. and Haemoproteus spp. parasites in mosquitoes in Germany. Parasites and Vectors 16:369. https://doi.org/10.1186/s13071-023-05965-0

Križanauskienė, A., Hellgren, O., Kosarev, V., Sokolov, L., Bensch, S., and Valkiūnas, G. 2006. Variation in host specificity between species of avian hemosporidian parasites: evidence from parasite morphology and cytochrome B gene sequences. Journal of Parasitology 92:1319–1324. https://doi.org/10.1645/GE-873R.1

L’Ambert, G., Ferré, J. B., Schaffner, F., and Fontenille, D. 2012. Comparison of different trapping methods for surveillance of mosquito vectors of West Nile virus in Rhône Delta, France. Journal of Vector Ecology 37:269–275. https://doi.org/10.1111/j.1948-7134.2012.00227.x

Lalubin, F., Delédevant, A., Glaizot, O., and Christe, P. 2013. Temporal changes in mosquito abundance (Culex pipiens), avian malaria prevalence and lineage composition. Parasites and Vectors 6:1–8. https://doi.org/10.1186/1756-3305-6-307

Martínez-de la Puente, J., Muñoz, J., Capelli, G., Montarsi, F., Soriguer, R., Arnoldi, D., Rizzoli, A., and Figuerola, J. 2015. Avian malaria parasites in the last supper: Identifying encounters between parasites and the invasive Asian mosquito tiger and native mosquito species in Italy. Malaria Journal 14:1–7. https://doi.org/10.1186/s12936-015-0571-0

Njabo, K. Y., Cornel, A. J., Sehgal, R. N., Loiseau, C., Buermann, W., Harrigan, R. J., Pollinger, J., Valkiūnas, G., and Smith, T. B. 2009. Coquillettidia (Culicidae, Diptera) mosquitoes are natural vectors of avian malaria in Africa. Malaria Journal 8:1–12. https://doi.org/10.1186/1475-2875-8-193

Odagawa, T., Inumaru, M., Sato, Y., Murata, K., Higa, Y. and Tsuda, Y. 2022. A long-term field study on mosquito vectors of avian malaria parasites in Japan. Journal of Veterinary Medical Science 84:1391–1398. https://doi.org/10.1292/jvms.22-0211

Palinauskas, V., Žiegytė, R., Šengaut, J., and Bernotienė, R. 2018. Different paths–the same virulence: Experimental study on avian single and co-infections with Plasmodium relictum and Plasmodium elongatum. International Journal for Parasitology 48:1089–1096. https://doi.org/10.1016/j.ijpara.2018.08.003

Platonova, E. and Palinauskas, V. 2021. The impact of temperature on the sporogonic development of the tropical avian malaria parasite Plasmodium relictum (Genetic Lineage pGRW4) in Culex pipiens form molestus mosquitoes. Microorganisms 9:2240. https://doi.org/10.3390/microorganisms9112240

Schoener, E., Uebleis, S. S., Butter, J., Nawratil, M., Cuk, C., Flechl, E., Kothmayer, M., Obwaller, A. G., Zechmeister, T., Rubel, F. and Lebl, K. 2017. Avian Plasmodium in eastern Austrian mosquitoes. Malaria Journal 16:1–12. https://doi.org/10.1186/s12936-017-2035-1

Sokolov, L. V., Markovets, M. J., and Shapoval, A. P. 2017. Long-term monitoring of breeding and migratory bird populations on the Curonian Spit of the Baltic Sea. Trudy Zoologicheskogo instituta RAN 321:72–88. (In Russian)

Synek, P., Munclinger, P., Albrecht, T., and Votýpka, J. 2013. Avian haemosporidians in haematophagous insects in the Czech Republic. Parasitology Research 112:839–845. https://doi.org/10.1007/s00436-012-3204-3

Valkiūnas, G. 2005. Avian Malaria Parasites and Other Haemosporidia. Boca Raton, Florida, CRC Press. https://doi.org/10.1201/9780203643792

Valkiūnas, G. and Iezhova, T. A. 2018. Keys to the avian malaria parasites. Malaria Journal 17:1–24. https://doi.org/10.1186/s12936-018-2359-5

Valkiūnas, G., Ilgūnas, M., Bukauskaitė, D., Fragner, K., Weissenböck, H., Atkinson, C. T., and Iezhova, T. A. 2018. Characterization of Plasmodium relictum, a cosmopolitan agent of avian malaria. Malaria Journal 17:1–21. https://doi.org/10.1186/s12936-018-2325-2

Valkiūnas, G., Žiegytė, R., Palinauskas, V., Bernotienė, R., Bukauskaitė, D., Ilgūnas, M., Dimitrov, D., and Iezhova, T. A. 2015. Complete sporogony of Plasmodium relictum (lineage pGRW4) in mosquitoes Culex pipiens pipiens, with implications on avian malaria epidemiology. Parasitology Research 114:3075–3085. https://doi.org/10.1007/s00436-015-4510-3

Ventim, R., Ramos, J. A., Osório, H., Lopes, R. J., Pérez-Tris, J., and Mendes, L. 2012. Avian malaria infections in western European mosquitoes. Parasitology Research 111:637–645. https://doi.org/10.1007/s00436-012-2880-3

Vinogradova, E. B. 2000. Culex pipiens pipiens mosquitoes: Taxonomy, distribution, ecology, physiology, genetic, applied importance and control. Pensoft Publishers, Sofia; Moscow.

Zélé, F., Vézilier, J., L’ambert, G., Nicot, A., Gandon, S., Rivero, A., and Duron, O. 2014. Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: The effects of Wolbachia, filarial nematodes and insecticide resistance. Parasites and Vectors 7:1–16. https://doi.org/10.1186/1756-3305-7-437

Žiegytė, R. and Bernotienė, R. 2022. Contribution to the knowledge on black flies (Diptera: Simuliidae) as vectors of Leucocytozoon (Haemosporida) parasites in Lithuania. Parasitology International 87:102515. https://doi.org/10.1016/j.parint.2021.102515

Žiegytė, R., Bernotienė, R., and Palinauskas, V. 2022. Culicoides segnis and Culicoides pictipennis biting midges (Diptera, Ceratopogonidae), new reported vectors of Haemoproteus parasites. Microorganisms 10:898. https://doi.org/10.3390/microorganisms10050898

Žiegytė, R., Platonova, E., Kinderis, E., Mukhin, A., Palinauskas, V., and Bernotienė, R. 2021. Culicoides biting midges involved in transmission of haemoproteids. Parasites and Vectors 14:1–9. https://doi.org/10.1186/s13071-020-04516-1

Žiegytė, R. and Valkiūnas, G. 2014. Recent advances in vector studies of avian haemosporidian parasites. Ekologija 60:73–83. https://doi.org/10.6001/ekologija.v60i4.3042

Zittra, C., Kocziha, Z., Pinnyei, S., Harl, J., Kieser, K., Laciny, A., Eigner, B., Silbermayr, K., Duscher, G. G., Fok, É., and Fuehrer, H. P. 2015. Screening blood-fed mosquitoes for the diagnosis of filarioid helminths and avian malaria. Parasites and Vectors 8:1–6. https://doi.org/10.1186/s13071-015-0637-4