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Detecting transmission areas of malaria parasites in a migratory bird species

Published online by Cambridge University Press:  13 May 2015

LUZ GARCIA-LONGORIA ,
OLOF HELLGREN ,
STAFFAN BENSCH ,
FLORENTINO DE LOPE  and
ALFONSO MARZAL
LUZ GARCIA-LONGORIA*
Affiliation:
Departamento de Biología Animal, Universidad de Extremadura, E-06071 Badajoz, Spain
OLOF HELLGREN
Affiliation:
Department of Biology, Molecular Ecology and Evolution Lab, Ecology Building, Lund University, SE- 22362 Lund, Sweden
STAFFAN BENSCH
Affiliation:
Department of Biology, Molecular Ecology and Evolution Lab, Ecology Building, Lund University, SE- 22362 Lund, Sweden
FLORENTINO DE LOPE
Affiliation:
Departamento de Biología Animal, Universidad de Extremadura, E-06071 Badajoz, Spain
ALFONSO MARZAL
Affiliation:
Departamento de Biología Animal, Universidad de Extremadura, E-06071 Badajoz, Spain
*
* Corresponding author: Departamento de Biología Animal, Universidad de Extremadura, E-06071 Badajoz, Spain. E-mail: luzlongoria@unex.es
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Summary

The identification of the regions where vector-borne diseases are transmitted is essential to study transmission patterns and to recognize future changes in environmental conditions that may potentially influence the transmission areas. SGS1, one of the lineages of Plasmodium relictum, is known to have active transmission in tropical Africa and temperate regions of Europe. Nuclear sequence data from isolates infected with SGS1 (based on merozoite surface protein 1 (MSP1) allelic diversity) have provided new insights on the distribution and transmission areas of these allelic variants. For example, MSP1 alleles transmitted in Africa differ from those transmitted in Europe, suggesting the existence of two populations of SGS1 lineages. However, no study has analysed the distribution of African and European transmitted alleles in Afro-Palearctic migratory birds. With this aim, we used a highly variable molecular marker to investigate whether juvenile house martins become infected in Europe before their first migration to Africa. We explored the MSP1 allelic diversity of P. relictum in adult and juvenile house martins. We found that juveniles were infected with SGS1 during their first weeks of life, confirming active transmission of SGS1 to house martins in Europe. Moreover, we found that all the juveniles and most of adults were infected with one European transmitted MSP1 allele, whereas two adult birds were infected with two African transmitted MSP1 alleles. These findings suggest that house martins are exposed to different strains of P. relictum in their winter and breeding quarters.

Keywords

avian malariaDelichon urbicajuvenilesMSP1Plasmodium relictum

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Type
Research Article
Information
Parasitology , Volume 142 , Issue 9 , August 2015 , pp. 1215 - 1220
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Copyright © Cambridge University Press 2015 

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References

REFERENCES

Ambrosini, R., Orioli, V., Massimino, D. and Bani, L. (2011). Identification of putative wintering areas and ecological determinants of population dynamics of common house-martin (Delichon urbicum) and common swift (Apus apus) breeding in Northern Italy. Avian Conservation and Ecology 6, 3.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. Biological Sciences/The Royal Society 273, 2935–2944.CrossRefGoogle 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. Biological Sciences/The Royal Society 267, 1583–1589.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., Wood, M. J., Day, M. K. P. and Sheldon, B. C. (2008). Seasonal variation in Plasmodium prevalence in a population of blue tits Cysnistes caeruleus . Journal of Animal Ecology 77, 540–548.Google Scholar
Cramp, S. and Perrins, C. M. (1994). Handbook of the Birds of Europe, the Middle East, and North Africa: The Birds of the Western Palearctic Volume VIII: Crows to Finches. Oxford, Oxford University Press.Google Scholar
Davidar, P. and Morton, E. S. (1993). Living with parasites: prevalence of a blood parasite and its effect on survivorship in the Purple Martin. Auk 110, 116–119.Google Scholar
Dunn, J. C., Goodman, S. J., Benton, T. G. and Hamer, K. C. (2014). Active blood parasite infection is not limited to the breeding season in a declining farmland bird. The Journal of Parasitology 100, 260–266.CrossRefGoogle ScholarPubMed
Garvin, M. C., Szell, C. C. and Moore, F. R. (2006). Blood parasites of Nearctic-Neotropical migrant passerine birds during spring trans-Gulf migration: impact on host body condition. The Journal of Parasitology 92, 990–996.Google Scholar
Gerold, P., Schofieldb, L., Blackman, M. J., Holder, A. A. and Schwarz, R. T. (1996). Structural analysis of the glycosyl-phosphatidylinositol membrane anchor of the merozoite surface proteins-1 and -2 of Plasmodium falciparum . Molecular and Biochemical Parasitology 75, 131–143.CrossRefGoogle ScholarPubMed
Githeko, A. K., Lindsay, S. W., Confalonieri, U. E. and Patz, J. A. (2000). Climate change and vector-borne diseases: a regional analysis. Bulletin of the World Health Organization 78, 1136–1147.Google ScholarPubMed
Hall, T. (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., Waldenström, J., Peréz-Tris, J., Szöll Ösi, 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., Kutzer, M., Bensch, S., Valkiunas, G. and Palinauskas, V. (2013). Identification and characterization of the merozoite surface protein 1 (msp1) gene in a host-generalist avian malaria parasite, Plasmodium relictum (lineages SGS1 and GRW4) with the use of blood transcriptome. Malaria Journal 12, 381.Google Scholar
Hellgren, O., Carter, A., Bensch, S., Albayrak, T., Dimitrov, D., Ewen, J., Kim, K. S., Lima, M., Lynn, M., Palinauskas, V., Ricklefs, R. E., Sehgal, R. N. M., Valkiūnas, G., Tsuda, Y. and Marzal, A. (2015) Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity. Ecography 28, 001–009.Google Scholar
Howe, L., Castro, I. C., Schoener, E. R., Hunter, S., Barraclough, R. K. and Alley, M. R. (2012). Malaria parasites (Plasmodium spp.) infecting introduced, native and endemic New Zealand birds. Parasitology Research 110, 913–923.Google Scholar
Ilgunas, M., Palinauskas, V., Iezhova, T. A. and Valkiunas, G. (2013). Molecular and morphological characterization of two avian malaria parasites (Haemosporida: Plasmodiidae), with description of Plasmodium homonucleophilum n. Sp. Zootaxa 3666, 49–61.Google Scholar
Kazlauskiene, R., Bernotiene, R., Palinauskas, V., Iezhova, T. A. and Valkiunas, G. (2013). Plasmodium relictum (lineages pSGS1 and pGRW11): Complete synchronous sporogony in mosquitoes Culex pipiens pipiens. Experimental Parasitology 133, 454–461.Google Scholar
Lope, F. de. (1986). La biometría del avión común (Delichon urbica urbica L.) en Badajoz, España. Ardeola 33, 171–176.Google Scholar
Lope, F. de. and Silva, E. da. (1998). La fidelidad al lugar de nidificación o de nacimiento en el avión común (Delichon urbica urbica L.) en Badajoz, España. Ardeola 39, 51–58.Google Scholar
Lowe, S., Browne, M., Boudjelas, S. and De Poorter, M. (2000). 100 of the world's worst invasive alien species a selection from the global invasive species database. The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN) 12, 12.Google Scholar
Marzal, A., Bensch, S., Reviriego, M., Balbontin, J. and De Lope, F. (2008). Effects of malaria double infection in birds: one plus one is not two. Journal of Evolutionary Biology 21, 979–87.Google Scholar
Marzal, A., Ricklefs, R. E., Valkiūnas, G., Albayrak, T., Arriero, E., Bonneaud, C., Czirják, G. A., Ewen, J., Hellgren, O., Hořáková, D., Iezhova, T. A., Jensen, H., Križanauskienė, A., Lima, M. R., De Lope, F., Magnussen, E., Martin, L. B., Møller, A. P., Palinauskas, V., Pap, P. L., Pérez-Tris, J., Sehgal, R. N. M., Soler, M., Szöllősi, E., Westerdahl, H., Zetindjiev, P. and Bensch, S. (2011). Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS ONE 6, 8.CrossRefGoogle Scholar
Marzal, A., Reviriego, M., Hermosell, I. G., Balbontín, J., Bensch, S., Relinque, C., Rodríguez, L., Garcia-Longoria, L. and de Lope, F. (2013a). Malaria infection and feather growth rate predict reproductive success in house martins. Oecologia 171, 853–61.Google Scholar
Marzal, A., Asghar, M., Rodríguez, L., Reviriego, M., Hermosell, I. G., Balbontín, J., Garcia-Longoria, L., de Lope, F. and Bensch, S. (2013b). Co-infections by malaria parasites decrease feather growth but not feather quality in house martin. Journal of Avian Biology 44, 437–444.CrossRefGoogle Scholar
Marzal, A., García-Longoria, L., Cárdenas Callirgos, J. M. and Sehgal, R. N. (2015). Invasive avian malaria as an emerging parasitic disease in native birds of Peru. Biological Invasions 17, 39–45.Google Scholar
Miller, L. H., Roberts, T., Shahabuddin, M. and McCutchan, T. F. (1993). Analysis of sequence diversity in the Plasmodium falciparum merozoite surface protein-1 (MSP-1). Molecular and Biochemical Parasitology 59, 1–14.Google Scholar
Møller, A. P. (2005). Parasitism and the regulation of host populations. Parasitism and Ecosystems 75, 43–43.Google Scholar
Pajuelo, L., de Lope, F. and da Silva, E. (1992). Breeding biology of the House Martin (Delichon urbica) in Badajoz W Spain. Ardeola 39, 15–23.Google Scholar
Palinauskas, V., Kosarev, V., Shapoval, A., Bensch, S. and Valkiūnas, G. (2007). Comparison of mitochondrial cytochrome b lineages and morphospecies of twoavian malaria parasites of the subgenera Haemamoeba and Giovannolaia (Haemosporida: Plasmodiidae). Zootaxa 1626, 39–50.Google Scholar
Piersma, T. and van der Velde, M. (2012). Dutch House Martins Delichon urbicum gain blood parasite infections over their lifetime, but do not seem to suffer. Journal of Ornithology 153, 907–912.Google Scholar
Sambrook, J., Fritsch, E. F. and Maniatis, T. (2002). Molecular Cloning: A Laboratory Manual. Cold Spring, New York.Google Scholar
Samuel, M. D., Hobbelen, P. H. F., Decastro, F., Ahumada, J. A., Lapointe, D. A., Atkinson, C. T., Woodworth, B. L., Hart, P. J. and Duffy, D. C. (2011). The dynamics, transmission, and population impacts of avian malaria in native Hawaiian birds: a modeling approach. Ecological Applications 21, 2960–2973.Google Scholar
Schmid-Hempel, P. (2011). Evolutionary parasitology: The integrated study of infections, immunology, ecology and genetics. Oxford, Oxford University Press.Google Scholar
Sol, D., Jovani, R. and Torres, J. (2003). Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds. Oecologia 135, 542–547.CrossRefGoogle ScholarPubMed
Svensson, L., Grant, P. J. and Mullarney, K. (2009). Collins Bird Guide. HarperCollins, London.Google Scholar
Turner, A. K. and Rose, C. (1989). Swallows and Martins: An Identification Guide and Handbook. (ed Taylor, F. J. R.) Christopher Helm, London.Google Scholar
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton.Google Scholar
Valkiūnas, G., Zehtindjiev, P., Hellgren, O., Ilieva, M. and Iezhova, T. B. S., (2007). Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites, with a description of Plasmodium (Novyella) ashfordi sp. nov. Parasitology Research 100, 1311–1322.Google Scholar
Van Riper III, C., Van Riper, S. G., Goff, M. L. and Laird, M. (1986). The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 327–344.Google Scholar
Van Rooyen, J., Jenkins, T., Lahlah, N. and Christe, P. (2014). North-african house martins endure greater haemosporidian infection than their european counterparts. Journal of Avian Biology 45, 001–007.Google Scholar
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. The Journal of Parasitology 90, 191–194.Google Scholar