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Diversity and distribution of avian haematozoan parasites in the western Indian Ocean region: a molecular survey


The genetic diversity of haematozoan parasites in island avifauna has only recently begun to be explored, despite the potential insight that these data can provide into the history of association between hosts and parasites and the possible threat posed to island endemics. We used mitochondrial DNA sequencing to characterize the diversity of 2 genera of vector-mediated parasites (Plasmodium and Haemoproteus) in avian blood samples from the western Indian Ocean region and explored their relationship with parasites from continental Africa. We detected infections in 68 out of 150 (45 3%) individuals and cytochrome b sequences identified 9 genetically distinct lineages of Plasmodium spp. and 7 lineages of Haemoproteus spp. We found considerable heterogeneity in parasite lineage composition across islands, although limited sampling may, in part, be responsible for perceived differences. Two lineages of Plasmodium spp. and 2 lineages of Haemoproteus spp. were shared by hosts in the Indian Ocean and also on mainland Africa, suggesting that these lineages may have arrived relatively recently. Polyphyly of island parasites indicated that these parasites were unlikely to constitute an endemic radiation and instead probably represent multiple colonization events. This study represents the first molecular survey of vector-mediated parasites in the western Indian Ocean, and has uncovered a diversity of parasites. Full understanding of parasite community composition and possible threats to endemic avian hosts will require comprehensive surveys across the avifauna of this region.

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*Corresponding author: Center for Conservation and Evolutionary Genetics, National Zoological Park, Smithsonian Institution, 3001, Connecticut Avenue, NW Washington DC 20008-0551, USA. Tel: +1 202 603 4190. Fax: +1 202 673 0040. E-mail:
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Agresti, A. and Coull, B. (1998). Approximate is better than ‘exact’ for interval estimation of binomial proportions. The American Statistician 52, 119126.
Atkinson, C. T. and van Riper, C. III (1991). Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In Bird-Parasite Interactions: Ecology, Evolution and Behaviour (ed. Loye, J. E. and Zuk, M.), pp. 1948. Oxford University Press, New York, USA.
Apanius, V., Yorinks, N., Bermingham, E. and Ricklefs, R. E. (2000). Island and taxon effects in parasitism and resistance of Lesser Antilleanbirds. Ecology 81, 19591969.
Beadell, J. S., Covas, R., Gebhard, C., Ishtiaq, F., Melo, M., Schmidt, B. K., Perkins, S. L., Graves, G. R. and Fleischer, R. C. (2009). Host associations and evolutionary relationships of avian bloods parasite from west Africa. International Journal for Parasitology 39, 257266.
Beadell, J. S., Gering, E., Austin, J., Dumbacher, J. P., Peirce, M. A., Pratt, T. K., Atkinson, C. T. and Fleischer, R. C. (2004). Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Molecular Ecology 13, 38293844.
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, 29352944.
Bensch, S. and Ǻkesson, S. (2003). Temporal and spatial variation of haematozoans in Scandinavian willow warblers. Journal of Parasitology 89, 388391.
Bensch, S., Pérez-Tris, J., Waldenström, J. and Hellgren, O. (2004). Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58, 16171621.
Bensch, S., Stjernman, M., Hasselquist, D., Östman, Ö., 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, 15831589.
Bennett, G. F. and Blancou, J. (1974). A note on the blood parasites of some birds from the Republic of Madagascar. Journal of Wildlife Diseases 10, 239240.
Bennett, G. F., Campbell, A. G. and Cameron, M. (1974). Hematozoa of passeriform birds from insular Newfoundland. Canadian Journal of Zoology 52, 765772.
Biju, S. D. and Bossuyt, F. (2003). New frog family from India reveals an ancient biogeographical link with the Seychelles. Nature, London 425, 711714.
Bossuyt, F. and Milinkovitch, M. C. (2001). Amphibians as indicators of early Tertiary “out of India” dispersal of vertebrates. Science 292, 9395.
Cosgrove, C. L., Wood, M. J., Day, K. and Sheldon, B. C. (2008). Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. Journal of Animal Ecology 77, 540548.
Drummond, A. J., Ho, S. Y. W., Phillips, M. J. and Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology 4, e88.
Drummond, A. J. and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
Durrant, K. L., Reed, J. L., Jones, P. J., Dallimer, M., Cheke, R. A., McWilliam, A. N. and Fleischer, R. C. (2007). Variation in haematozoan parasitism at local and landscape level in the red-billed quelea Quelea quelea. Journal of Avian Biology 38, 662671.
Fallon, S. M., Bermingham, E. and Ricklefs, R. E. (2003). Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles. Evolution 57, 606615.
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, 466480.
Freeman-Gallant, C. R., O'Connor, K. D. and Breuer, M. E. (2001). Sexual selection and the geography of Plasmodium infection in savannah sparrows (Passerculus sandwichensis). Oecologia 127, 517521.
Gerberg, E. J. and Arnett, R. H. (1976). A pictorial key to the mosquito larvae of the Seychelles. Mosquito Systematics 8, 343346.
Githeko, A. K., Service, M. W., Mbogo, C. M., Atieli, F. K. and Juma, F. O. (1994). Origin of blood meals in indoor and outdoor resting malaria vectors in western Kenya. Acta Tropica 58, 307316.
Hellgren, O., Kristanauskiene, A., Valkiunas, G. and Bensch, S. (2007). Diversity and phylogeny of mitochondrial cytochrome b lineages from six morphospecies of avian Haemoproteus (Haemosporidia: Haemoproteidae). Journal of Parasitology 93, 889896.
Ishtiaq, F., Beadell, J. S., Baker, A. J., Rahmani, A. R., Jhala, Y. V. and Fleischer, R. C. (2006). Prevalence and evolutionary relationships of haematozoan parasites in native versus and introduced populations of common myna Acridotheres tristis. Proceedings of the Royal Society of London, B 273, 587594.
Ishtiaq, F., Clegg, S. M., Phillimore, A. B., Black, R. A., Owens, I. P. F. and Sheldon, B. C. (2010). Biogeographical patterns of blood parasite lineage diversity in avian hosts from southern Melanesian islands. Journal of Biogeography 37, 120132.
Ishtiaq, F., Gering, E., Rappole, J. H., Rahmani, A. R., Jhala, Y. V., Dove, C. J., Milensky, C., Olson, S. L., Peirce, M. and Fleischer, R. C. (2007). Prevalence and diversity of avian haematozoan parasites in Asia: a regional survey. Journal of Wildlife Diseases 43, 382398.
Ishtiaq, F., Guillaumot, L., Clegg, S. M., Phillimore, A. B., Black, R. A., Owens, I. P. F., Mundy, N. I. and Sheldon, B. C. (2008). Avian haematozoan parasites and their associations with mosquitoes across southwest Pacific Islands. Molecular Ecology 17, 45454555.
Killick-Kendrick, R. (1978). Taxonomy, zoogeography and evolution. In Rodent Malaria (ed. Killick-Kendrick, R. and Peters, W.), pp. 152. Academic Press, London, UK.
Kocher, T. D., Thomas, W. K., Meyer, A., Edwards, S. V., Pāābo, S., Villablanca, F. X. and Wilson, A. C. (1989). Dynamics of mtDNA evolution in animals: amplification and sequencing with conserved primers. Proceedings of National Academy of Sciences, USA 86, 61966200.
Lajeunesse, M. J. and Forbes, M. R. (2002). Host range and local parasite adaptation. Proceedings of the Royal Society of London, B 269, 703710.
Lowery, R. S. (1971). Blood parasites of vertebrates of Aldabra. Philosophical Transactions of the Royal Society of London, B 260, 577580.
MacArthur, R. H. and Wilson, E. O. (1967). The Theory of Island Biogeography. Princeton University Press, Princeton, NJ, USA.
Matson, K. and Beadell, J. (2010). Infection, immunity, and island adaptation in birds. In The Biogeography of Host-Parasite Interactions (ed. Morand, S. and Krasnov, B. R.), pp. 217232. Oxford University Press, New York, USA.
Mayr, E. (1942). Systematics and the Origin of Species. Colombia University Press, New York, USA.
Mila, B., Warren, B. H., Heeb, P. and Thébaud, C. (2010). The geographic scale of diversification on islands: genetic and morphological divergence at a very small spatial scale in the Mascarene grey white-eye (Aves: Zosterops borbonicus). BMC Evolutionary Biology 10, 158.
Peirce, M. A., Cheke, A. S. and Cheke, R. A. (1977). A survey of blood parasites of birds in the Mascarene Islands, Indian Ocean: with descriptions of two new species and taxonomic discussion. Ibis 119, 451461.
Perkins, S. L. (2001). Phylogeography of Caribbean lizard malaria: tracing the history of vector-borne parasites. Journal of Evolutionary Biology 14, 3445.
Perkins, S. L. and Schall, J. J. (2002). A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology 88, 972978.
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.
Rambaut, A. and Drummond, A. J. (2003). Tracer v1.3, available from
Renner, S. S. (2004 a). Bayesian analysis of combined chloroplast loci, using multiple calibrations, supports the recent arrival of Melastomataceae in Africa and Madagascar. American Journal of Botany 91, 14271435.
Renner, S. S. (2004 b). Multiple Miocene Melastomataceae dispersal between Madagascar, Africa and India. Philosophical Transactions of the Royal Society of London, B 359, 14851494.
Ricklefs, R. E. and Fallon, S. M. (2002). Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London, B 269, 885892.
Ricklefs, R. E. and Outlaw, D. C. (2010). A molecular clock for malaria parasites. Science 329, 226229.
Savage, A. F. (2003). Identity and prevalence of blood parasites in wild-caught birds from Madagascar. M.S. thesis, University of Florida, FL, USA.
Savage, A. F., Robert, V., Goodman, S. M., Raharimanga, V., Raherilalao, M. J., Andrianarimisa, A., Ariey, F. and Greiner, E. (2009). Blood parasites in birds from Madagascar. Journal of Wildlife Diseases 45, 907920.
Schall, J. J. and Marghoob, A. B. (1995). Prevalence of a malarial parasite over time and space: Plasmodium mexicanum in its vertebrate host, the western fence lizard Sceloporus occidentalis. Journal of Animal Ecology 64, 177185.
Schall, J. J., Pearson, A. R. and Perkins, S. L. (2000). Prevalence of malaria parasite (Plasmodium floridense and Plasmodium azurophilum) infecting a Puerto Rican lizard (Anolis gundlachi): a nine year study. Journal of Parasitology 86, 511515.
Seutin, G., Brawn, J., Ricklefs, R. E. and Bermingham, E. (1993). Genetic divergence among populations of a tropical passerine, the Streaked Saltator (Saltator albicollis). Auk 110, 117126.
Seutin, G., White, B. and Boag, P. (1991). Preservation of avian blood and tissue samples for DNA analyses. Canadian Journal of Zoology 69, 8290.
Sibley, C. G. and Monroe, B. L. (1996). Birds of the World. On diskette, Windows version 2.0. Charles G. Sibley, Santa Rosa, CA, USA.
Valkiũnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.
van Riper, C. III, van Riper, S. G., Goff, M. L. and Laird, M. (1986). The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monograph 56, 327344.
Waldenström, J., Bensch, S., Kiboi, S., Hasselquist, D. and Ottoson, U. (2002). Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology 11, 15451554.
Warner, R. E. (1968). The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. Condor 70, 101120.
Warren, B. H., Bermingham, E., Bowie, C. K. R., Prys-Jones, R. P. and Thebaud, C. (2003). Molecular phylogeography reveals island colonization history and diversification of western Indian Ocean sunbirds (Nectarinia: Nectariniidae). Molecular Phylogentics and Evolution 29, 6785.
Warren, B. H., Bermingham, E., Prys-Jones, R. P. and Thebaud, C. (2005). Tracking island colonization history and phenotypic shifts in Indian Ocean bulbuls (Hypsipetes: Pycnonotidae). Biological Journal of Linnean Society 85, 271287.
Warren, B. H., Bermingham, E., Prys-Jones, R. P. and Thebaud, C. (2006). Immigration, species radiation and extinction in a highly diverse songbird lineage: white-eyes on Indian Ocean islands. Molecular Ecology 15, 37693786.
Wood, M. J., Cosgrove, C. L., Wilkin, T. A., Knowles, S. C. L., Day, K. P. and Sheldon, B. C. (2007). Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology 16, 3263–73.
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