Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-24T04:31:16.428Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  11 November 2011

FARAH ISHTIAQ ,
JON S. BEADELL ,
BEN H.WARREN  and
ROBERT C. FLEISCHER
FARAH ISHTIAQ*
Affiliation:
Center for Conservation and Evolutionary Genetics, National Zoological Park, Smithsonian Institution, 3001, Connecticut Avenue, NW Washington DC 20008-0551, USA
JON S. BEADELL
Affiliation:
Center for Conservation and Evolutionary Genetics, National Zoological Park, Smithsonian Institution, 3001, Connecticut Avenue, NW Washington DC 20008-0551, USA
BEN H.WARREN
Affiliation:
UMR C53 PVBMT, CIRAD-Université de La Réunion, 7 chemin de l'IRAT, Ligne Paradis, 97410 Saint Pierre, Réunion, France
ROBERT C. FLEISCHER
Affiliation:
Center for Conservation and Evolutionary Genetics, National Zoological Park, Smithsonian Institution, 3001, Connecticut Avenue, NW Washington DC 20008-0551, USA
*
*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: farahishtiaq@yahoo.com
Get access Rights & Permissions [Opens in a new window]

Summary

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.

Keywords

AfricaHaemoproteushaematozoan parasiteswestern Indian OceanPlasmodium
Type
Research Article
Information
Parasitology , Volume 139 , Issue 2 , February 2012 , pp. 221 - 231
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Agresti, A. and Coull, B. (1998). Approximate is better than ‘exact’ for interval estimation of binomial proportions. The American Statistician 52, 119–126.Google Scholar
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. 19–48. Oxford University Press, New York, USA.CrossRefGoogle Scholar
Apanius, V., Yorinks, N., Bermingham, E. and Ricklefs, R. E. (2000). Island and taxon effects in parasitism and resistance of Lesser Antilleanbirds. Ecology 81, 1959–1969.CrossRefGoogle Scholar
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, 257–266.CrossRefGoogle ScholarPubMed
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, 3829–3844.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.Google ScholarPubMed
Bensch, S. and Ǻkesson, S. (2003). Temporal and spatial variation of haematozoans in Scandinavian willow warblers. Journal of Parasitology 89, 388–391.CrossRefGoogle Scholar
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, 1617–1621.Google ScholarPubMed
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, 1583–1589.CrossRefGoogle ScholarPubMed
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, 239–240.CrossRefGoogle ScholarPubMed
Bennett, G. F., Campbell, A. G. and Cameron, M. (1974). Hematozoa of passeriform birds from insular Newfoundland. Canadian Journal of Zoology 52, 765–772.CrossRefGoogle ScholarPubMed
Biju, S. D. and Bossuyt, F. (2003). New frog family from India reveals an ancient biogeographical link with the Seychelles. Nature, London 425, 711–714.CrossRefGoogle ScholarPubMed
Bossuyt, F. and Milinkovitch, M. C. (2001). Amphibians as indicators of early Tertiary “out of India” dispersal of vertebrates. Science 292, 93–95.CrossRefGoogle ScholarPubMed
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, 540–548.CrossRefGoogle Scholar
Drummond, A. J., Ho, S. Y. W., Phillips, M. J. and Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology 4, e88.CrossRefGoogle ScholarPubMed
Drummond, A. J. and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.CrossRefGoogle ScholarPubMed
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, 662–671.CrossRefGoogle Scholar
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, 606–615.Google 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
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, 517–521.CrossRefGoogle ScholarPubMed
Gerberg, E. J. and Arnett, R. H. (1976). A pictorial key to the mosquito larvae of the Seychelles. Mosquito Systematics 8, 343–346.Google Scholar
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, 307–316.CrossRefGoogle ScholarPubMed
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, 889–896.CrossRefGoogle Scholar
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, 587–594.Google ScholarPubMed
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, 120–132.CrossRefGoogle Scholar
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, 382–398.CrossRefGoogle Scholar
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, 4545–4555.CrossRefGoogle ScholarPubMed
Killick-Kendrick, R. (1978). Taxonomy, zoogeography and evolution. In Rodent Malaria (ed. Killick-Kendrick, R. and Peters, W.), pp. 1–52. Academic Press, London, UK.CrossRefGoogle Scholar
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, 6196–6200.CrossRefGoogle ScholarPubMed
Lajeunesse, M. J. and Forbes, M. R. (2002). Host range and local parasite adaptation. Proceedings of the Royal Society of London, B 269, 703–710.CrossRefGoogle ScholarPubMed
Lowery, R. S. (1971). Blood parasites of vertebrates of Aldabra. Philosophical Transactions of the Royal Society of London, B 260, 577–580.Google Scholar
MacArthur, R. H. and Wilson, E. O. (1967). The Theory of Island Biogeography. Princeton University Press, Princeton, NJ, USA.Google Scholar
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. 217–232. Oxford University Press, New York, USA.Google Scholar
Mayr, E. (1942). Systematics and the Origin of Species. Colombia University Press, New York, USA.Google Scholar
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.CrossRefGoogle Scholar
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, 451–461.CrossRefGoogle Scholar
Perkins, S. L. (2001). Phylogeography of Caribbean lizard malaria: tracing the history of vector-borne parasites. Journal of Evolutionary Biology 14, 34–45.CrossRefGoogle ScholarPubMed
Perkins, S. L. and Schall, J. J. (2002). A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology 88, 972–978.CrossRefGoogle ScholarPubMed
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Rambaut, A. and Drummond, A. J. (2003). Tracer v1.3, available from http://evolve.zoo.ox.ac.uk/.Google Scholar
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, 1427–1435.CrossRefGoogle ScholarPubMed
Renner, S. S. (2004 b). Multiple Miocene Melastomataceae dispersal between Madagascar, Africa and India. Philosophical Transactions of the Royal Society of London, B 359, 1485–1494.CrossRefGoogle ScholarPubMed
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, 885–892.CrossRefGoogle ScholarPubMed
Ricklefs, R. E. and Outlaw, D. C. (2010). A molecular clock for malaria parasites. Science 329, 226–229.CrossRefGoogle ScholarPubMed
Savage, A. F. (2003). Identity and prevalence of blood parasites in wild-caught birds from Madagascar. M.S. thesis, University of Florida, FL, USA.Google Scholar
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, 907–920.CrossRefGoogle ScholarPubMed
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, 177–185.CrossRefGoogle Scholar
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, 511–515.CrossRefGoogle Scholar
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, 117–126.Google Scholar
Seutin, G., White, B. and Boag, P. (1991). Preservation of avian blood and tissue samples for DNA analyses. Canadian Journal of Zoology 69, 82–90.CrossRefGoogle Scholar
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.Google Scholar
Valkiũnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
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, 327–344.CrossRefGoogle Scholar
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, 1545–1554.CrossRefGoogle ScholarPubMed
Warner, R. E. (1968). The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. Condor 70, 101–120.CrossRefGoogle Scholar
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, 67–85.CrossRefGoogle ScholarPubMed
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, 271–287.CrossRefGoogle Scholar
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, 3769–3786.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed