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Host associations, biogeography, and phylogenetics of avian malaria in southern African waterfowl

Published online by Cambridge University Press:  12 October 2012

GRAEME S. CUMMING ,
ERIC SHEPARD ,
SHARON OKANGA ,
ALEXANDRE CARON ,
MDUDUZI NDLOVU  and
JEFFREY L. PETERS
GRAEME S. CUMMING*
Affiliation:
Percy FitzPatrick Institute, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch, Cape Town 7701, South Africa
ERIC SHEPARD
Affiliation:
Department of Biological Sciences, 3640 Colonel Glenn Highway, Wright State University, Dayton, OH 45435, USA
SHARON OKANGA
Affiliation:
Percy FitzPatrick Institute, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch, Cape Town 7701, South Africa
ALEXANDRE CARON
Affiliation:
Cirad, UPR AGIRs, Harare, Zimbabwe Cirad, UPR AGIRs, Montpellier, France
MDUDUZI NDLOVU
Affiliation:
Percy FitzPatrick Institute, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch, Cape Town 7701, South Africa
JEFFREY L. PETERS
Affiliation:
Department of Biological Sciences, 3640 Colonel Glenn Highway, Wright State University, Dayton, OH 45435, USA
*
*Corresponding author: Percy FitzPatrick Institute, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch, Cape Town 7701, South Africa. E-mail: gscumming@gmail.com
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Summary

The relevance of spatial variation in the environment and host communities for parasite community composition is poorly documented, creating a need for additional case studies from which general principles can be developed. Avian malaria in southern African waterfowl has not previously been studied. As a first step towards documenting and understanding its biogeography, we used PCR and molecular sequencing techniques to analyse 454 blood samples from Afrotropical ducks from 5 different locations (spread around the subregion) for avian malaria. Fifty-five blood samples were positive for one or more genera of haematozoa. The regional infection rate across all sites and sampling periods was 12·1%. Nine individuals carried dual infections containing multiple haematozoa. Fifteen different cytochrome b haplotypes among 52 positives (3 samples failed to sequence) and 61 total sequences were found. Eleven haplotypes closely matched Plasmodium, whereas 4 were more similar to Haemoproteus. Five distinct haematozoan clades were identified. Haemoproteus parasites appeared to be more host-specific than Plasmodium, which occurred at every sampling location and in every host species examined. There were no significant differences in overall parasite prevalence attributable to either site or species, although Plasmodium and Haemoproteus occurrences differed by site-species combination and the borderline significance of our test for between-site variation (P < 0·06) implied that with a larger sample size, differences in parasite prevalence among locations might be detectable.

Keywords

malariawaterfowlsouthern Africaparasitepathogenevolutionbiogeographyecology
Type
Research Article
Information
Parasitology , Volume 140 , Issue 2 , February 2013 , pp. 193 - 201
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual., M. and Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467–484.CrossRefGoogle ScholarPubMed
Beadell, J. S., Covas, R., Gebhard, C. F., Ishtiaq, C., Gebhard, M., Melo, M., Schmidt, B. K., Perkins, S. L., Graves, G. and Fleischer, R. (2009). Host associations and evolutionary relationships of avian blood parasites from West Africa. International Journal for Parasitology 39, 257–266.CrossRefGoogle ScholarPubMed
Beadell, J. S., Gering, E., Austin, J., Dumbacher, J. and Peirce, M. (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., Hellgren, O. and Perez-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.CrossRefGoogle ScholarPubMed
Bensch, S., Waldenström, J., Jonsén, 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.CrossRefGoogle Scholar
Cumming, G. S., Caron, A., Abolnik, C., Cattoli, G., Bruinzeel, L. W., Burger, C. E., Cecchettin, K., Chiweshe, N., Mochotlhoane, B., Mutumi, G. L. and Ndlovu, M. (2011). The ecology of Influenza A viruses in wild birds in southern Africa. Ecohealth 8, 4–13.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 levels in the red-billed quelea Quelea quelea. Journal of Avian Biology 38, 662–671.CrossRefGoogle Scholar
Ewers, R. M. and Didham, R. K. (2006). Confounding factors in the detection of species’ responses to habitat fragmentation. Biological Reviews 81, 117–142.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. and Schneider, S. (2005). Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
Excoffier, L., Smouse, P. E. and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131, 479–491.CrossRefGoogle ScholarPubMed
Fallon, S., Bermingham, E. and Ricklefs, R. E. (2005). Hose specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. The American Naturalist 165, 466–480.CrossRefGoogle Scholar
Gaston, K. (2000). Global patterns in biodiversity. Nature, London 405, 220–227.CrossRefGoogle ScholarPubMed
Hanski, I. (1998). Metapopulation dynamics. Nature, London 396, 41–49.CrossRefGoogle Scholar
Hay, S. I. J., Cox, J., Rogers, D. J., Randolph, S. E., Stern, D. I., Shanks, G. D., Myers, M. F. and Snow, R. W. (2002). Climate change and the resurgence of malaria in the East African highlands. Nature, London 415, 905–909.CrossRefGoogle ScholarPubMed
Hellgren, O., Perez-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.CrossRefGoogle Scholar
Hockey, P. A. R. (2000). Patterns and correlates of bird migrations in sub-saharan Africa. Emu 100, 401–417.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 introduced populations of common myna Acridotheres tristis. Proceedings of the Royal Society of London, B 273, 587–594.Google ScholarPubMed
Ishtiaq, F., Beadell, J. S., Warren, B. H. and Fleischer, R. C. (2012). Diversity and distribution of avian haematozoan parasites in the western Indian Ocean region: a molecular survey. Parasitology 139, 221–231.CrossRefGoogle ScholarPubMed
Keesing, F., Holt, R. D. and Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485–498.CrossRefGoogle ScholarPubMed
Lambin, E., Tran, A., Vanwambeke, S. O., Linard, C. and Soti, V. (2010). Pathogenic landscapes: Interactions between land, people, disease vectors and their animal hosts. International Journal of Health Geographics 9, 54.CrossRefGoogle ScholarPubMed
Loiseau, C., Harrington, R. J., Robert, A., Bowie, R. C. K., Thomassen, H. A., Smith, T. B. and Sehgal, R. N. M. (2012). Host and habitat specialization of avian malaria in Africa. Molecular Ecology 21, 431–441.CrossRefGoogle ScholarPubMed
Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J. P., Hector, A., Hooper, D. U., Huston, M. A., Raffaelli, D., Schmid, B., Tilman, D. and Wardle, D. A. (2001). Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804–808.CrossRefGoogle ScholarPubMed
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, 979–987.CrossRefGoogle Scholar
Mathworks (2010). Matlab® Version 2010b. The MathWorks, Inc., Natick, MA, USA.Google Scholar
Rahbek, C. (2005). The role of spatial scale and the perception of large-scale species-richness patterns. Ecology Letters 8, 224–239.CrossRefGoogle Scholar
Randolph, S. E. and Dobson, A. D. M. (2012). Pangloss revisited: a critique of the dilution effect and biodiversity-buffers-disease paradigm. Parasitology 139, 847–863.CrossRefGoogle ScholarPubMed
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A. and Huelsenbeck, J. P. (2012). MrBayes 3·2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Schultz, A., Underhill, L. G., Earle, R. and Underhill, G. (2011). Seasonality, distribution and taxonomic status of avian haemosporidian parasites within the Greater Cape Town area, South Africa. Ostrich 82, 141–153.CrossRefGoogle Scholar
Valkiūnas, G. (2005). Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Raton, FL, USA.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.CrossRefGoogle ScholarPubMed
White, N. J. (2011). Determinants of relapse periodicitiy in Plasmodium vivax malaria. Malaria Journal 10, 297.CrossRefGoogle ScholarPubMed