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Host-parasite associations and host-specificity in haemoparasites of reed bed passerines

Published online by Cambridge University Press:  05 January 2012

RITA VENTIM ,
JOANA MORAIS ,
SARA PARDAL ,
LUÍSA MENDES ,
JAIME A. RAMOS  and
JAVIER PÉREZ-TRIS
RITA VENTIM*
Affiliation:
Institute of Marine Research (IMAR/CMA), Department of Life Sciences, University of Coimbra, Apartado 3046, 3001-401 Coimbra, Portugal Departamento de Zoología y Antropología Física, Facultad de Biología, Universidad Complutense, 28040 Madrid, Spain
JOANA MORAIS
Affiliation:
Institute of Marine Research (IMAR/CMA), Department of Life Sciences, University of Coimbra, Apartado 3046, 3001-401 Coimbra, Portugal
SARA PARDAL
Affiliation:
Institute of Marine Research (IMAR/CMA), Department of Life Sciences, University of Coimbra, Apartado 3046, 3001-401 Coimbra, Portugal
LUÍSA MENDES
Affiliation:
Institute of Marine Research (IMAR/CMA), Department of Life Sciences, University of Coimbra, Apartado 3046, 3001-401 Coimbra, Portugal
JAIME A. RAMOS
Affiliation:
Institute of Marine Research (IMAR/CMA), Department of Life Sciences, University of Coimbra, Apartado 3046, 3001-401 Coimbra, Portugal
JAVIER PÉREZ-TRIS
Affiliation:
Departamento de Zoología y Antropología Física, Facultad de Biología, Universidad Complutense, 28040 Madrid, Spain
*
*Corresponding author: Institute of Marine Research (IMAR/CMA), Department of Life Sciences, University of Coimbra, Apartado 3046, 3001-401 Coimbra, Portugal. Tel: +351 916343436. E-mail: ritaventim@gmail.com
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Summary

The host specificity and host sharing of avian haemoparasites (genera Haemoproteus and Plasmodium) is still poorly known, although they infect a large proportion of several studied bird populations. This study used molecular techniques to detect haemoparasites in marsh warblers and in other passerines that feed in reed beds, at 4 sites in Portugal. The host-specificity of the parasite lineages was analysed and compared with other cases described in the literature to assess whether apparent host specificity changes according to the studied system. Nine lineages of Haemoproteus and 15 of Plasmodium were found, of which only 10 Plasmodium were proven to have local transmission. Each lineage was confined to a distinct set of host species. The distribution of parasites in the host species was non-nested, meaning that specialist lineages did not always share hosts with generalists. The most prevalent lineages were those with a wider host range, indicating that the ability to infect more hosts will enhance a parasite's prevalence in its entire host range. We also found that in our areas, a specialist parasite (H. MW1) appears to have a more generalist character than described in the literature, suggesting that a parasite's apparent specialization can depend on the type of host species sampled.

Keywords

avian malariaHaemoproteushaemosporidianhost–parasite associationhost rangelocal transmissionnestednessPlasmodiumspecialists versus generalists
Type
Research Article
Information
Parasitology , Volume 139 , Issue 3 , March 2012 , pp. 310 - 316
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Almeida-Neto, M., Guimarães, P., Guimarães, P. R., Loyola, R. D. and Ulrich, W. (2008). A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos, 117, 1227–1239. doi: 10.1111/j.2008.0030-1299.16644.x.CrossRefGoogle Scholar
Bascompte, J. and Jordano, P. (2007). Plant-animal mutualistic networks: The architecture of biodiversity. Annual Review of Ecology Evolution and Systematics, 38, 567–593. doi: 10.1146/annurev.ecolsys.38.091206.095818.CrossRefGoogle Scholar
Bascompte, J., Jordano, P., Melian, C. J. and Olesen, J. M. (2003). The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences, USA 100, 9383–9387. doi: 10.1073/pnas.1633576100.CrossRefGoogle ScholarPubMed
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. doi: 10.1098/rspb.2006.3671.Google ScholarPubMed
Bensch, S. and Akesson, A. (2003). Temporal and spatial variation of hematozoans in Scandinavian willow warblers. Journal of Parasitology 89, 388–391. doi: 10.1645/0022-3395(2003)089[0388:TASVOH]2.0.CO;2.CrossRefGoogle ScholarPubMed
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. doi: 10.1111/j.1755-0998.2009.02692.x.CrossRefGoogle ScholarPubMed
Bensch, S., Pérez-Tris, J., Waldenstrom, J. and Hellgren, O. (2004). Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: Multiple cases of cryptic speciation? Evolution 58, 1617–1621. doi: 10.1554/04-026.Google ScholarPubMed
Bensch, S., Stjernman, M., Hasselquist, D., Ostman, 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.CrossRefGoogle ScholarPubMed
Clarke, K. R. and Warwick, R. M. (1998). A taxonomic distinctness index and its statistical properties. Journal of Applied Ecology 35, 523–531. doi: 10.1046/j.1365-2664.1998.3540523.x.CrossRefGoogle Scholar
Combes, C. (1997). Fitness of parasites: Pathology and selection. International Journal for Parasitology 27, 1–10. doi: 10.1016/S0020-7519(96)00168-3.CrossRefGoogle ScholarPubMed
Dimitrov, D., Zehtindjiev, 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. doi: 10.2478/s11686-010-0029-z.CrossRefGoogle Scholar
Dobson, A. (2004). Population dynamics of pathogens with multiple host species. American Naturalist 164, S64–S78. doi: 10.1086/424681.CrossRefGoogle ScholarPubMed
Fallon, S. M., Bermingham, E. and Ricklefs, R. E. (2005). Host specialization and geographic localization of avian malaria parasites: A regional analysis in the Lesser Antilles. American Naturalist 165, 466–480.CrossRefGoogle ScholarPubMed
Graham, S. P., Hassan, H. K., Burkett-Cadena, N. D., Guyer, C. and Unnasch, T. R. (2009). Nestedness of ectoparasite-vertebrate host networks. PLoS One 4. doi: 10.1371/journal.pone.0007873.CrossRefGoogle ScholarPubMed
Guimarães, P. R. and Guimarães, P. (2006). Improving the analyses of nestedness for large sets of matrices. Environmental Modelling & Software 21, 1512–1513. doi: 10.1016/j.envsoft.2006.04.002.CrossRefGoogle Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.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. doi: 10.1890/08-1059.1.CrossRefGoogle Scholar
Hellgren, O., Waldenstrom, J., Pérez-Tris, J., Szollosi, 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. doi: 10.1111/j.1365-294X.2007.03277.x.CrossRefGoogle ScholarPubMed
Krizanauskiene, A., Hellgren, O., Kosarev, V., Sokolov, L., Bensch, S. and Valkiunas, 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.CrossRefGoogle ScholarPubMed
Palinauskas, V., Kosarev, V., Shapoval, A., Bensch, S. and Valkiūnas, G. (2007). Comparison of mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites of the subgenera Haemamoeba and Giovannolaia (Haemosporida: Plasmodiidae). Zootaxa 39–50.CrossRefGoogle Scholar
Pérez-Tris, J., Hellgren, O., Krizanauskiene, A., Waldenstrom, J., Secondi, J., Bonneaud, C., Fjeldsa, J., Hasselquist, D. and Bensch, S. (2007). Within-host speciation of malaria parasites. PloS One 2. doi: 10.1371/journal.pone.0000235.CrossRefGoogle ScholarPubMed
Poulin, R. and Mouillot, D. (2005). Combining phylogenetic and ecological information into a new index of host specificity. Journal of Parasitology 91, 511–514. doi: 10.1645/GE-398R.CrossRefGoogle ScholarPubMed
Ricklefs, R. E., Fallon, S. M. and Bermingham, E. (2004). Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology 53, 111–119. doi: 10.1080/10635150490264987.CrossRefGoogle ScholarPubMed
Ricklefs, R. E., Swanson, B. L., Fallon, S. M., Martinez-Abrain, A., Scheuerlein, A., Gray, J., and Latta, S. C. (2005). Community relationships of avian malaria parasites in southern Missouri. Ecological Monographs 75, 543–559. doi: 10.1890/04-1820.CrossRefGoogle Scholar
Svensson, L. (1992). Identification Guide to European Passerines, 4th Edn.Private Publisher, Stockholm, Sweden.Google Scholar
Thompson, J. N. (2006). Mutualistic webs of species. Science 312, 372–373. doi: 10.1126/science.1126904.CrossRefGoogle ScholarPubMed
Valkiunas, G. (2005). Avian Malaria Parasites and other Haemosporidia, 1st Edn.CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiunas, G., Bensch, S., Iezhova, T. A., Krizanauskiene, A., Hellgren, O. and Bolshakov, C. V. (2006). Nested cytochrome B polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: Microscopy is still essential. Journal of Parasitology 92, 418–422. doi: 10.1645/GE-3547RN.1.CrossRefGoogle ScholarPubMed
Waldenström, J., Bensch, S., Hasselquist, D. and Ostman, O. (2004). A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191–194. doi: 10.1645/GE-3221RN.CrossRefGoogle ScholarPubMed
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. doi: 10.1046/j.1365-294X.2002.01523.x.CrossRefGoogle ScholarPubMed
Zehtindjiev, P., Ilieva, M., Westerdahl, H., Hansson, B., Valkiunas, 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. doi: 10.1016/j.exppara.2007.12.018.CrossRefGoogle Scholar