Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-20T18:27:07.290Z Has data issue: false hasContentIssue false
  • English
  • Français

Diversity, distribution and biogeographical origins of Plasmodium parasites from the New Zealand bellbird (Anthornis melanura)

Published online by Cambridge University Press:  09 September 2011

S. M. BAILLIE  and
D. H. BRUNTON
S. M. BAILLIE*
Affiliation:
Institute of Natural Sciences, Massey University, Private Bag 102-904, North Shore Mail Centre, Auckland, New Zealand
D. H. BRUNTON
Affiliation:
Institute of Natural Sciences, Massey University, Private Bag 102-904, North Shore Mail Centre, Auckland, New Zealand
*
*Corresponding author, present address: Department of Biology, Life Science Centre, Dalhousie University, 1459 Oxford Street, Halifax, Nova Scotia B3H 4R2, Canada. E-mail: s.m.baillie@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Understanding the origin of invasive parasites and ecological transmission barriers on the distribution of mosquito-borne pathogens is enriched by molecular phylogenetic approaches now that large databases are becoming available. Here we assess the biogeographical relationships among haemosporidian blood parasites and an avian host, the New Zealand bellbird (Meliphagidae, Anthornis melanura). Four Plasmodium haplotypes were identified among 93 infected bellbirds (693 screened) using nested PCR of a mitochondrial DNA cytochrome b gene fragment. The most common lineage, LIN1 (11%), is confined to northern New Zealand and falls within a known clade of Plasmodium (subgenus Novyella) sp. infecting Australian meliphagids. LIN1 differs within that clade by 4 9% sequence divergence suggestive of an endemic lineage to New Zealand. The most widespread lineage, LIN2 (2%), is an exact match with a global cosmopolitan (P. elongatum GRW06). Two rare lineages, LIN3 and LIN4 are less abundant, geographically restricted within New Zealand and have <1% sequence divergence with P. (Novyella) sp. (AFTRU08) and P. relictum (LINOLI01) documented from Africa. For the first time, we provide invaluable information on possible rates of entry of invading parasites in New Zealand and their distribution from temperate to cold environments.

Keywords

Plasmodiumavian malariabiogeographyNew Zealandhost-parasite distribution
Type
Research Article
Information
Parasitology , Volume 138 , Issue 14 , December 2011 , pp. 1843 - 1851
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

Alley, M. R., Fairley, R. A., Martin, D. G., Howe, L. and Atkinson, T. (2008). An outbreak of avian malaria in captive yellowheads/mohua (Mohoua ochrocephala). New Zealand Veterinary Journal 56, 247–251.CrossRefGoogle ScholarPubMed
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 blood parasites 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., 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., Waldenstrom, J., Jonzen, 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, 12–122.CrossRefGoogle Scholar
Cosgrove, C. L., Wood, M. J., Day, K. P. 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
Dawkins, R. and Krebs, J. R. (1979). Arms races between and within species. Proceedings of the Royal Society of London, B 205, 489–511.Google ScholarPubMed
Derraik, J. G. B. (2004). Exotic mosquitoes in New Zealand: a review of species intercepted, their pathways and ports of entry. Australian and New Zealand Journal of Public Health 28, 433–444.CrossRefGoogle ScholarPubMed
Derraik, J. G. B., Tompkins, D. M., Alley, M. R., Holder, P. and Atkinson, T. (2008). Epidemiology of an avian malaria outbreak in a native bird species (Mohoua ochrocephala) in New Zealand. Journal of the Royal Society of New Zealand 38, 237–242.CrossRefGoogle Scholar
Driskell, A. C. and Christidis, L. (2004). Phylogeny and evolution of the Australo-Papuan honeyeaters (Passeriformes, Meliphagidae). Molecular Phylogenetics and Evolution 31, 943–960.CrossRefGoogle ScholarPubMed
Driskell, A. C., Christidis, L., Gill, B. J., Boles, W. E., Barker, F. K. and Longmore, N. W. (2007). A new endemic family of New Zealand passerine birds: adding heat to a biodiversity hotspot. Australian Journal of Zoology 55, 73–78.CrossRefGoogle Scholar
Fallon, S. M., Ricklefs, R. E., Latta, S. C. and Bermingham, E. (2004). Temporal stability of insular avian malarial parasite communities. Proceedings of the Royal Society of London, B 271, 493–500.CrossRefGoogle ScholarPubMed
Fernandez, M., Rojo, M. A., Casanueva, P., Carrion, S., Hernandez, M. A. and Campos, F. (2010). High prevalence of haemosporidians in Reed Warbler Acrocephalus scirpaceus and Sedge Warbler Acrocephalus schoenobaenus in Spain. Journal of Ornithology 151, 27–32.CrossRefGoogle Scholar
Garamszegi, L. Z. (2011). Climate change increases the risk of malaria in birds. Global Change Biology 17, 1751–1759. doi: 10.1111/j.1365-2486.2010.02346.X.CrossRefGoogle Scholar
Guindon, S. and Gascuel, O. (2003). A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Hellgren, O., Bensch, S. and Malmqvist, B. (2008). Bird hosts, blood parasites and their vectors - associations uncovered by molecular analyses of blackfly blood meals. Molecular Ecology 17, 1605–1613.CrossRefGoogle ScholarPubMed
Hellgren, O., Waldenstrom, J. and Bensch, S. (2004). A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology 90, 797–802.CrossRefGoogle ScholarPubMed
Hellgren, O., Waldenstrom, J., Perez-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.CrossRefGoogle ScholarPubMed
Ishak, H. D., Dumbacher, J. P., Anderson, N. L., Keane, J. J., Valkiunas, G., Haig, S. M., Tell, L. A. and Sehgal, R. N. M. (2008). Blood parasites in owls with conservation implications for the spotted owl (Strix occidentalis). PLoS ONE 3, e2304. doi: 10.1371/journal.pone.0002304.CrossRefGoogle ScholarPubMed
Ishtiaq, F., Clegg, S. M., Phillimore, A. B., Black, R. A. and Owens, I. P. F. (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. A. and Fleischer, R. C. (2007). Prevalence and diversity of avian hematozoan 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
Jarvi, S. I., Farias, M. E. M., Baker, H., Freifeld, H. B., Baker, P. E., Van Gelder, E., Massey, J. G. and Atkinson, C. T. (2003). Detection of avian malaria (Plasmodium spp.) in native land birds of American Samoa. Conservation Genetics 4, 29–637.CrossRefGoogle Scholar
Jarvi, S. I., Schultz, J. J. and Atkinson, C. T. (2002). PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. Journal of Parasitology 88, 153–158.CrossRefGoogle ScholarPubMed
Kimura, M., Dhondt, A. A. and Lovette, I. J. (2006). Phylogeographic structuring of Plasmodium lineages across the North American range of the house finch (Carpodacus mexicanus). Journal of Parasitology 92, 1043–1049.CrossRefGoogle ScholarPubMed
Knowles, S. C. L., Wood, M. J., Alves, R., Wilkin, T. A., Bensch, S. and Sheldon, B. C. (2011). Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Molecular Ecology 20, 1062–1076.CrossRefGoogle Scholar
Lockhart, P. J., Steel, M. A., Hendy, M. D. and Penny, D. (1994). Recovering evolutionary trees under a more realistic model of sequence evolution. Molecular Biology and Evolution 11, 605–612.Google Scholar
MacArthur, R. H. and Wilson, E. O. (1967). The Theory of Island Biogeography. Princeton University Press, Princeton, New Jersey, USA.Google Scholar
Norte, A. C., Araujo, P. M., Sampaio, H. L., Sousa, J. P. and Ramos, J. A. (2009). Haematozoa infections in a Great tit Parus major population in central Portugal: relationships with breeding effort and health. Ibis 151, 677–688.CrossRefGoogle Scholar
Outlaw, D. C. and Ricklefs, R. E. (2009). On the phylogenetic relationships of haemosporidian parasites from raptorial birds (Falconiformes and Strigiformes). Journal of Parasitology 95, 1171–1176.CrossRefGoogle ScholarPubMed
Perez-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, E235. doi: 10.1371/journal.pone.0000235.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. (2008). jModelTest: phylogenetic model averaging. Molecular Biology Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Ricklefs, R. E. and Outlaw, D. C. (2010). A molecular clock for malaria parasites. Science 329, 226–229.CrossRefGoogle ScholarPubMed
Robertson, C. J. R., Hyvonen, P., Fraser, M. J. and Pickard, C. R. (2007). Atlas of Bird Distribution in New Zealand 1999–2004. The Ornithological Society of New Zealand, Inc., Nelson, New Zealand.Google Scholar
Santiago-Alarcon, D., Outlaw, D. C., Ricklefs, R. E. and Parker, P. G. (2010). Phylogenetic relationships of haemosporidian parasites in New World Columbiformes, with emphasis on the endemic Galapagos dove. International Journal for Parasitology 40, 463–470.CrossRefGoogle ScholarPubMed
Santiago-Alarcon, D., Whiteman, N. K., Parker, P. G., Ricklefs, R. E. and Valkiunas, G. (2008). Patterns of parasite abundance and distribution in island populations of Galapagos endemic birds. Journal of Parasitology 94, 584–590.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution. doi: 10.1093/molbev/msr121.CrossRefGoogle ScholarPubMed
Tompkins, D. M. and Gleeson, D. M. (2006). Relationship between avian malaria distribution and an exotic invasive mosquito in New Zealand. Journal of the Royal Society of New Zealand 36, 51–62.CrossRefGoogle Scholar
Valkiunas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, Florida USA.Google Scholar
Valkiunas, G., Iezhova, T. A., Krizanauskiene, A., Palinauskas, V., Sehgal, R. N. M. and Bensch, S. (2008 b). A comparative analysis of microscopy and PCR-based detection methods for blood parasites. Journal of Parasitology 94, 1395–1401.CrossRefGoogle ScholarPubMed
Valkiunas, G., Zehtindjiev, P., Dimitrov, D., Krizanauskiene, A., Iezhova, T. A. and Bensch, S. (2008 a). Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank. Parasitology Research 102, 1185–1193.CrossRefGoogle ScholarPubMed
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, 3263–3273.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Baillie Supplementary Figure 1

Baillie Supplementary Figure 1

Download Baillie Supplementary Figure 1(Image)
Image 12.4 MB
Supplementary material: Image

Baillie Supplementary Figure 2

Baillie Supplementary Figure 2

Download Baillie Supplementary Figure 2(Image)
Image 16.3 MB