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Prevalence and diversity of Plasmodium and Haemoproteus parasites in the globally-threatened Aquatic Warbler Acrocephalus paludicola

Published online by Cambridge University Press:  30 April 2015

JÚLIO MANUEL NETO ,
ANTÓN PÉREZ-RODRÍGUEZ ,
MARTIN HAASE ,
MARTIN FLADE  and
STAFFAN BENSCH
JÚLIO MANUEL NETO*
Affiliation:
CIBIO/UP – Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas, P-4485-661 Vairão, Portugal Molecular Ecology and Evolution Lab, MEMEG, Department of Biology, Ecology Building, SE-223 62 Lund, Sweden
ANTÓN PÉREZ-RODRÍGUEZ
Affiliation:
Departamento de Zoología y Antropología Física, Universidad Complutense de Madrid, Madrid E-28040, Spain
MARTIN HAASE
Affiliation:
Lehrstuhl Allgemeine und Systematische Zoologie: AG Vogelwarte Hiddensee, Vogelwarte Hiddensee, Zoologisches Institut und Museum, Universität Greifswald, Soldmannstraße 23, D-17489 Greifswald, Germany
MARTIN FLADE
Affiliation:
BirdLife Aquatic Warbler Conservation Team, c/o Schorfheide-Chorin Biosphere Reserve, Hoher Steinweg 5-6, D – 16278 Angermünde, Germany
STAFFAN BENSCH
Affiliation:
Molecular Ecology and Evolution Lab, MEMEG, Department of Biology, Ecology Building, SE-223 62 Lund, Sweden
*
* Corresponding author. CIBIO/UP – Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas, P-4485-661 Vairão, Portugal. Tel: 0046733288090. E-mail: [email protected]
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Summary

The diversity and prevalence of malaria parasites of the genera Plasmodium and Haemoproteus were determined in the globally-threatened Aquatic Warbler Acrocephalus paludicola. Birds were sampled during migration in Portugal and at the wintering quarters in Senegal and parasites were detected using molecular methods. Only three generalist parasite lineages (Plasmodium) were found. There were no significant differences in the prevalence of parasites between sexes in Europe, but adults had higher prevalence than first-year birds, and birds in Europe had higher prevalence than those captured in Africa. When comparing with other Acrocephalus species and taking sample size into account, Aquatic Warblers had the lowest prevalence and, together with another threatened species, the Seychelles Warbler Acrocephalus sechellensis, the lowest diversity of malaria parasites. We hypothesize that the low diversity of parasites and absence of specialist lineages of Aquatic Warblers are caused by its small population size and fragmented distribution. Furthermore, Aquatic Warblers’ extreme habitat specialization may decrease their exposure to malaria parasites, but other explanations such as high mortality (which would constraint the sampling of infected birds) or, in contrast, very efficient immunological system in clearing the infections cannot be ruled out. This study contributes to explain variation in prevalence and diversity of malaria parasites among hosts.

Keywords

Haemosporidiacytochrome Bavian malariaEuropeAfrica
Type
Research Article
Information
Parasitology , Volume 142 , Issue 9 , August 2015 , pp. 1183 - 1189
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Altizer, S., Nunn, C. L. and Lindenfors, P. (2007). Do threatened hosts have fewer parasites? A comparative study in primates. Journal of Animal Ecology 76, 304–314.Google Scholar
Aquatic Warbler Conservation Team (1999). World population, trends and conservation status of the Aquatic Warbler Acrocephalus paludicola . Vogelwelt 120, 12–32.Google Scholar
Asghar, M., Hasselquist, D. and Bensch, S. (2011). Are chronic avian haemosporidian infections costly in wild birds? Journal of Avian Biology 42, 530–537.Google Scholar
Atkinson, C. T. and Samuel, M. D. (2010). Avian malaria Plasmodium relictum in native Hawaiian forest birds: epizootiology and demographic impacts on apapane Himatione sanguinea . Journal of Avian Biology 41, 357–366.Google Scholar
Beadell, J. S., Ishtiaq, F., Covas, R., Melo, M., Warren, B. H., Atkinson, C. T., Bensch, S., Graves, G. R., Jhala, Y. V., Peirce, M. A., Rahmani, A. R., Fonseca, D. M. and Fleischer, R. C. (2006). Global phylogeographic limits of Hawaii's avian malaria. Proceedings of the Royal Society of London B 273, 2935–2944.Google Scholar
Bensch, S., Sjernman, M., Hasselquist, D., Östman, O., Hansson, B., Westerdahl, H. and Pinheiro, R. T. (2000). Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society of London B 267, 1583–1589.Google Scholar
Bensch, S., Waldenström, J., Jonzén, N., Westerdahl, H., Hansson, B., Sejberg, D. and Hasselquist, D. (2007). Temporal dynamics and diversity of avian malaria parasites in a single host species. Journal of Animal Ecology 76, 112–122.Google Scholar
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.Google Scholar
Cosgrove, C. L., Knowles, S. C., Day, K. P. and Sheldon, B. C. (2006). No evidence for avian malaria infection during the nestling phase in a passerine bird. Journal of Parasitology 92, 1302–1304.Google Scholar
Cosgrove, C. L., Wood, M. J., Day, K. P. and Sheldon, B. C. (2008). Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus . Journal of Animal Ecology 77, 540–548.Google Scholar
Dawson, D. A. (2007). Genomic analysis of passerine birds using conserved microsatellite loci . Ph.D. thesis. University of Sheffield.Google Scholar
Dimitrov, D., Zahtindjiev, P. and Bensch, S. (2010). Genetic diversity of avian blood parasites in SE Europe: cytochrome b lineages of the genera Plasmodium and Haemoproteus (Haemosporida) from Bulgaria. Acta Parasitologica 55, 201–209.Google Scholar
Drovetski, S. V., Aghayan, S. A., Mata, V. A., Lopes, R. J., Mode, N. A., Harvey, J. A. and Volker, G. (2014). Does the niche breadth or trade-off hypothesis explain the abundance-occupancy relationship in avian Haemosporidia? Molecular Ecology 23, 3322–3329.Google Scholar
Fernández, M., Rojo, M. Á., Casanueva, P., Carrión, S., Hernández, M. Á. and Campos, F. (2010). High prevalence of haemosporidians in Reed Warbler Acrocephalus scirpaceus and Sedge Warbler Acrocephalus schoenobaenus in Spain. Journal of Ornithology 151, 27–32.Google Scholar
Flade, M., Diop, I., Haase, M., Le Neve, A., Oppel, S., Tegetmeyer, C., Vogel, A. and Salewski, V. (2011). Distribution, ecology and threat status of the Aquatic Warbler Acrocephalus paludicola wintering in West Africa. Journal of Ornithology 152, 129–140.Google Scholar
Foucher, J., Boucaux, M., Giraudot, É., André, A., Lorrillière, R. and Dougué, H. (2013). Nouveaux sites d'hivernage du Phragmite aquatique Acrocephalus paludicola . Ornithos 20, 1–9.Google Scholar
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.Google Scholar
Hellgren, O., Waldenström, J., Pérez-Tris, J., Szöllösi, E., Hasselquist, D., Krizanauskiene, A., Ottosson, U. and Bensch, S. (2007). Detecting shifts of transmission areas in avian blood parasites – a phylogenetic approach. Molecular Ecology 16, 1281–1290.Google Scholar
Hellgren, O., Pérez-Tris, J. and Bensch, S. (2009). A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90, 2840–2849.Google Scholar
Hellgren, O., Wood, M. J., Waldenström, D., Hasselquist, D., Ottosson, U., Stervander, M. and Bensch, S. (2013). Circannual variation in blood parasitism in a sub-Saharan migrant passerine bird, the garden warbler. Journal of Evolutionary Biology 26, 1047–1059.Google Scholar
Hutchings, K. (2009). Parasite-mediated selection in an island endemic, the Seychelles warbler (Acrocephalus sechellensis) . Ph.D. thesis. University of East Anglia, UK.Google Scholar
Ishtiaq, F., Gering, E., Rappole, J. H., Rahmani, A. R., Jhala, Y. V., Dove, C. J., Milensky, C., Olson, S. L., Peirce, M. A. and Fleischer, R. C. (2007). Prevalence and diversity of avian hematozoan parasites in Asia: a regional survey. Journal of Wildlife Diseases 43, 382–398.Google Scholar
Julliard, R., Bargain, B., Dubos, A. and Jiguet, F. (2006). Identifying autumn migration routes for the globally threatened Aquatic Warbler Acrocephalus paludicola . Ibis 148, 735–743.CrossRefGoogle Scholar
Kamiya, T., O'Dwyer, K., Nakagawa, S. and Poulin, R. (2014). What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biological Reviews 89, 123–134.Google Scholar
Kim, K. S. and Tsuda, Y. (2012). Avian Plasmodium lineages found in spot surveys of mosquitoes from 2007 to 2010 at Sakata wetland, Japan: do dominant lineages persist multiple years? Molecular Ecology 21, 5374–5385.Google Scholar
Neto, J. M., Encarnação, V. and Fearon, P. (2010). Distribution, phenology and condition of Aquatic Warblers Acrocephalus paludicola migrating through Portugal. Ardeola 57, 181–189.Google Scholar
Neto, J. M., Hansson, B. and Hasselquist, D. (2011). Sex allocation in Savi's Warblers Locustella luscinioides: multiple factors affect seasonal trends in brood sex ratios. Behavioural Ecology and Sociobiology 65, 297–304.CrossRefGoogle Scholar
Ortego, J., Cordero, P. J., Aparicio, J. M. and Calabuig, G. (2008). Consequences of chronic infections with three different avian malaria lineages on reproductive performance of Lesser Kestrels (Falco naumanni). Journal of Ornithology 149, 337–343.Google Scholar
Podmokła, E., Dubiec, A., Drobniak, S. M., Arct, A., Gustafsson, L. and Cichoń, M. (2014). Determinants of prevalence and intensity of infection with malaria parasites in the Blue Tit. Journal of Ornithology 155, 721–727.Google Scholar
Reullier, J., Pérez-Tris, J., Bensch, S. and Secondi, J. (2006). Diversity, distribution and exchange of blood parasites meeting at an avian moving contact zone. Molecular Ecology 15, 753–763.Google Scholar
Scheuerlein, A. and Ricklefs, R. E. (2004). Prevalence of blood parasites in European passeriform birds. Proceedings of the Royal Society of London B 271, 1363–1370.Google Scholar
Svensson, L. (1992). Identification Guide to European Passerines, 4th Edn. Lars Svensson, Stockolm.Google Scholar
Svoboda, A., Mathinsen, G., Turčoková, L., Lifjeld, J. T. and Johnsen, A. (2009). Identification of blood parasites in old world warbler species from the Danube river delta. Avian Diseases 53, 634–636.Google Scholar
van Oers, K., Richardson, D. S., Sæther, S. A. and Komdeur, J. (2010). Reduced blood parasite prevalence with age in the Seychelles Warbler: selective mortality or suppression of infection? Journal of Ornithology 151, 69–77.Google Scholar
Ventim, R., Morais, J., Pardal, S., Mendes, L., Ramos, J. A. and Peréz-Tris, J. (2012). Host-parasite associations and host-specificity in haemoparasites of reed bed passerines. Parasitology 139, 310–316.Google Scholar
Waldenström, J., Bensch, S., Kiboi, S., Hasselquist, D. and Ottosson, U. (2002). Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology 11, 1545–1554.Google Scholar
Weatherhead, P. J. and Bennett, G. F. (1991). Ecology of red-winged blackbird parasitism by hematozoa. Canadian Journal of Zoology 69, 2352–2359.Google Scholar
Yohannes, E., Hansson, B., Lee, R. W., Waldenström, J., Westerdahl, H., Åkesson, M., Haselquist, D. and Bensch, S. (2008). Isotope signatures in winter moulted feathers predict malaria prevalence in a breeding avian host. Oecologia 158, 299–306.Google Scholar
Zehtindjiev, P., Ilieva, M., Westerdahl, H., Hansson, B., Valkiūnas, G. and Bensch, S. (2008). Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus . Experimental Parasitology 119, 99–110.Google Scholar
Zehtindjiev, P., Ilieva, M., Krizanauskiene, A., Oparina, O., Oparn, M. and Bensch, S. (2009). Occurrence of haemosporidian parasites in the paddyfield warbler, Acrocephalus Agricola (Passeriformes, Sylviidae). Acta Parasitologica 54, 295–300.Google Scholar