Prevalence and diversity of avian haematozoa in three species of Australian passerine
Shandiya Balasubramaniam A B D , Raoul A. Mulder A , Paul Sunnucks C , Alexandra Pavlova C , J. Nevil Amos C and Jane Melville B
+ Author Affiliations
- Author Affiliations
A Department of Zoology, University of Melbourne, Vic. 3010, Australia.
B Department of Sciences, Museum Victoria, Melbourne, Vic. 3001, Australia.
C School of Biological Sciences and Australian Centre for Biodiversity, Monash University, Clayton, Vic. 3800, Australia.
D Corresponding author. Email: shandiya@student.unimelb.edu.au
Emu 113(4) 353-358 https://doi.org/10.1071/MU13012
Submitted: 9 August 2012 Accepted: 10 April 2013 Published: 25 June 2013
Abstract
Avian haematozoa, or blood parasites, are extremely widespread and taxonomically diverse. They are known to infect a large number of avian species, making them ideal models for studying host–parasite interactions. Little is known about the prevalence or diversity of avian haematozoa in Australia because there have been fewer studies conducted in the southern hemisphere than the northern hemisphere. Here we assess the prevalence and diversity of avian haematozoa in three endemic Australian passerines using microscopy and molecular techniques. We identified four lineages of Haemoproteus infection among 32 individuals (of 1005 screened) and no Plasmodium infection. The four lineages clustered in three monophyletic groups within the larger Parahaemoproteus group, with 0.2–5.9% sequence divergence among these lineages. Three of the four lineages detected in this study are previously unreported and this is the first record of haematozoan infection in these species of passerine. This study provides valuable baseline data on the prevalence and diversity of haematozoan lineages in a poorly sampled region.
Additional keywords: cytochrome b, Haemoproteus, host–parasite, Plasmodium, Victoria.
References
Adlard, R., and O’Donoghue, P. J. (1998). Perspectives on the biodiversity of parasitic protozoa in Australia. International Journal for Parasitology 28, 887–897.| Perspectives on the biodiversity of parasitic protozoa in Australia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czjvVKmtA%3D%3D&md5=29c387c4f2bbe3e18fbfcfb82db368dbCAS | 9673868PubMed |
Adlard, R., Peirce, M., and Lederer, R. (2004). Blood parasites of birds from south-east Queensland. Emu 104, 191–196.
| Blood parasites of birds from south-east Queensland.Crossref | GoogleScholarGoogle Scholar |
Amos, J. N., Balasubramaniam, S., Grootendorst, L., Harrisson, K. A., Lill, A., Mac Nally, R., Pavlova, A., Radford, J. Q., Takeuchi, N., Thomson, J. R., and Sunnucks, P. (2013). Little evidence that condition, stress indicators, sex ratio, or homozygosity are related to landscape or habitat attributes in declining woodland birds. Journal of Avian Biology 44, 45–54.
| Little evidence that condition, stress indicators, sex ratio, or homozygosity are related to landscape or habitat attributes in declining woodland birds.Crossref | GoogleScholarGoogle Scholar |
Baillie, S. M., and Brunton, D. H. (2011). Diversity, distribution and biogeographical origins of Plasmodium parasites from the New Zealand Bellbird (Anthornis melanura). Parasitology 138, 1843–1851.
| Diversity, distribution and biogeographical origins of Plasmodium parasites from the New Zealand Bellbird (Anthornis melanura).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsV2hsL7O&md5=57f47ec4d25fc7fa28612b293ea684c0CAS |
Beadell, J., Gering, E., Austin, J., Dumbacher, J., Peirce, M., Pratt, T., Atkinson, C., and Fleischer, R. (2004). Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Molecular Ecology 13, 3829–3844.
| Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region.Crossref | GoogleScholarGoogle Scholar | 15548295PubMed |
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. Series B, Biological Sciences 273, 2935–2944.
| Global phylogeographic limits of Hawaii’s avian malaria.Crossref | GoogleScholarGoogle Scholar |
Bensch, S., Hellgren, O., and Peréz-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.
| MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages.Crossref | GoogleScholarGoogle Scholar | 21564906PubMed |
Drummond, A. J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T., and Wilson, A. (2011). Geneious, ver. 5.6. (Biomatters Ltd.) Available at: http://www.geneious.com/ [Verified 10 May 2013].
Fallon, S. M., and Ricklefs, R. (2008). Parasitemia in PCR-detected Plasmodium and Haemoproteus infections in birds. Journal of Avian Biology 39, 514–522.
| Parasitemia in PCR-detected Plasmodium and Haemoproteus infections in birds.Crossref | GoogleScholarGoogle Scholar |
Freed, L. A., and Cann, R. L. (2003). On polymerase chain reaction tests for estimating prevalence of malaria in birds. Journal of Parasitology 89, 1261–1264.
| On polymerase chain reaction tests for estimating prevalence of malaria in birds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWrur8%3D&md5=0884a2a63e715bd78c12f2c677239ff5CAS | 14740926PubMed |
Garamszegi, L. Z. (2010). The sensitivity of microscopy and PCR-based detection methods affecting estimates of prevalence of blood parasites in birds. Journal of Parasitology 96, 1197–1203.
| The sensitivity of microscopy and PCR-based detection methods affecting estimates of prevalence of blood parasites in birds.Crossref | GoogleScholarGoogle Scholar | 21158636PubMed |
Garvin, M., and Remsen, J. (1997). An alternative hypothesis for heavier parasite loads of brightly coloured birds: exposure at the nest. Auk 114, 179–191.
| An alternative hypothesis for heavier parasite loads of brightly coloured birds: exposure at the nest.Crossref | GoogleScholarGoogle Scholar |
Gill, F., and Donsker, D. (Eds) (2013). IOC World Bird List, v. 3.3. (International Ornithologists’ Union.) Available at http://www.worldbirdnames.org [Verified 10 May 2013].
Godfrey, R., Fedynich, A., and Pence, D. (1987). Quantification of hematozoa in blood smears. Journal of Wildlife Diseases 23, 558–565.
| 3119870PubMed |
Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
| A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.Crossref | GoogleScholarGoogle Scholar | 14530136PubMed |
Harrisson, K. A., Pavlova, A., Amos, J. N., Takeuchi, N., Lill, A., Radford, J. Q., and Sunnucks, P. (2012). Fine-scale effects of habitat loss and fragmentation despite large-scale gene flow for some regionally declining woodland bird species. Landscape Ecology 27, 813–827.
| Fine-scale effects of habitat loss and fragmentation despite large-scale gene flow for some regionally declining woodland bird species.Crossref | GoogleScholarGoogle Scholar |
Hellgren, O., Waldenström, 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.
| A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVyjs78%3D&md5=9557f66a894af02a8db52482307ee85dCAS | 15357072PubMed |
Hellgren, O., Krizanauskiene, A., Valkiunas, G., and Bensch, S. (2007). Diversity and phylogeny of mitochondrial cytochrome b lineages from six morphospecies of avian Haemoproteus (Haemosporida : Haemoproteidae). Journal of Parasitology 93, 889–896.
| Diversity and phylogeny of mitochondrial cytochrome b lineages from six morphospecies of avian Haemoproteus (Haemosporida : Haemoproteidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFOnt77P&md5=1d706d46a0efcc4da316e08d85d9c74aCAS | 17918371PubMed |
Higgins, P. J. (Ed.) (1999) ‘Handbook of Australian, New Zealand and Antarctic Birds. Vol. 4: Parrots to Dollarbird.’ (Oxford University Press: Melbourne.)
Higgins, P. J., and Peter, J. M. (Eds) (2002). ‘Handbook of Australian, New Zealand and Antarctic Birds. Vol. 6: Pardalotes to Shrike-thrushes ’ (Oxford University Press: Melbourne.).
Higgins, P. J., Peter, J. M., and Steele, W. K. (Eds) (2001). ‘Handbook of Australian, New Zealand and Antarctic Birds. Vol. 5: Tyrant-flycatchers to Chats.’ (Oxford University Press: Melbourne.).
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.
| 17699077PubMed |
Ishtiaq, F., Clegg, S., Phillimore, A., Black, R., Owens, I., and Sheldon, B. (2010). Biogeographical patterns of blood parasite lineage diversity in avian hosts from southern Melanesian islands. Journal of Biogeography 37, 120–132.
| Biogeographical patterns of blood parasite lineage diversity in avian hosts from southern Melanesian islands.Crossref | GoogleScholarGoogle Scholar |
Jarvi, S., 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.
| 12053956PubMed |
Kleindorfer, S., Lambert, S., and Paton, D. (2006). Ticks (Ixodes sp.) and blood parasites (Haemoproteus spp.) in New Holland Honeyeaters (Phylidonyris novaehollandiae): evidence for site specificity and fitness costs. Emu 106, 113–118.
| Ticks (Ixodes sp.) and blood parasites (Haemoproteus spp.) in New Holland Honeyeaters (Phylidonyris novaehollandiae): evidence for site specificity and fitness costs.Crossref | GoogleScholarGoogle Scholar |
Krone, O., and Cooper, J. E. (2002). Parasitic diseases. In ‘Birds of Prey: Health & Disease’. 3rd edn. (Ed. J. E. Cooper.) pp. 105–120. (Blackwell Science: Malden, MA.)
Leblanc, M. J., Tregoning, P., Ramillien, G., Tweed, S. O., and Fakes, A. (2009). Basin‐scale, integrated observations of the early 21st century multiyear drought in southeast Australia. Water Resources Research 45, W04408.
| Basin‐scale, integrated observations of the early 21st century multiyear drought in southeast Australia.Crossref | GoogleScholarGoogle Scholar |
Martinsen, E. S., Perkins, S. L., and Schall, J. J. (2008). A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Molecular Phylogenetics and Evolution 47, 261–273.
| A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktV2jtrs%3D&md5=27b9aa05fe06d696902eaa15d5dfcce9CAS | 18248741PubMed |
Merino, S., Moreno, J., Váaquez, R., Martinez, J., Sánchez-Monsálvez, I., Estades, C., Ippi, S., Sabat, P., Rozzi, R., and McGehee, S. (2008). Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. Austral Ecology 33, 329–340.
| Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness.Crossref | GoogleScholarGoogle Scholar |
Ots, I., and Hõrak, P. (1998). Health impact of blood parasites in breeding Great Tits. Oecologia 116, 441–448.
| Health impact of blood parasites in breeding Great Tits.Crossref | GoogleScholarGoogle Scholar |
Perkins, S., and Schall, J. (2002). A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology 88, 972–978.
| 1:CAS:528:DC%2BD38XptVOjtrc%3D&md5=1a4e193c0be40ac47f2c35c15dd363c7CAS | 12435139PubMed |
Poiani, A. (1992). Ectoparasitism as a possible cost of social life: a comparative analysis using Australian passerines (Passeriformes). Oecologia 92, 429–441.
| Ectoparasitism as a possible cost of social life: a comparative analysis using Australian passerines (Passeriformes).Crossref | GoogleScholarGoogle Scholar |
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
| jModelTest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlKgsb4%3D&md5=93c07cb89d20df1f435a6ee229b8528eCAS | 18397919PubMed |
Rambaut, A. (2009). ‘FigTree, ver. 1.3.1.’ Available at http://tree.bio.ed.ac.uk/software/figtree [Verified 10 May 2013].
Ricklefs, R. (1992). Embryonic development period and the prevalence of avian blood parasites. Proceedings of the National Academy of Sciences of the United States of America 89, 4722–4725.
| Embryonic development period and the prevalence of avian blood parasites.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383mt1Gisw%3D%3D&md5=566fe6789e15ea4a2aebbbce6dc8cea1CAS | 1584808PubMed |
Ricklefs, R., and Fallon, S. (2002). Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London – B. Biological Sciences 269, 885–892.
| Diversification and host switching in avian malaria parasites.Crossref | GoogleScholarGoogle Scholar |
Rogers, K., Rogers, A., and Rogers, D. (1986). ‘Bander’s Aid: A Guide to Ageing and Sexing Bush Birds.’ (A. Rogers: St Andrews, Vic.)
Ronquist, F., Teslenko, M., Van der Mark, P., Ayres, D. L., Darling, A., Hohna, 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.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |
Sol, D., Jovani, R., and Torres, J. (2000). Geographical variation in blood parasites in Feral Pigeons: the role of vectors. Ecography 23, 307–314.
| Geographical variation in blood parasites in Feral Pigeons: the role of vectors.Crossref | GoogleScholarGoogle Scholar |
Stjernman, M., Raberg, L., and Nilsson, J. (2004). Survival costs of reproduction in the Blue Tit (Parus caeruleus): a role for blood parasites? Proceedings of the Royal Society of London – B. Biological Sciences 271, 2387–2394.
| Survival costs of reproduction in the Blue Tit (Parus caeruleus): a role for blood parasites?Crossref | GoogleScholarGoogle Scholar |
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 28, 2731–2739.
| MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=2b0500328212dce711161963a0c1b8ffCAS | 21546353PubMed |
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.
| Relationship between avian malaria distribution and an exotic invasive mosquito in New Zealand.Crossref | GoogleScholarGoogle Scholar |
Valkiūnas, G. (2005). ‘Avian Malaria Parasites and Other Haemosporidia.’ (CRC Press: Boca Raton, FL.)
Valkiūnas, G., Iezhova, T., Krizanauskiene, A., Palinauskas, V., Seghal, R. N. M., and Bensch, S. (2008). A comparative analysis of microscopy and PCR-based detection methods for blood parasites. Journal of Parasitology 94, 1395–1401.
| A comparative analysis of microscopy and PCR-based detection methods for blood parasites.Crossref | GoogleScholarGoogle Scholar | 18576856PubMed |
van Riper, C., van Riper, S. G., Geoff, M. L., and Laird, M. (1986). The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 327–344.
| The epizootiology and ecological significance of malaria in Hawaiian land birds.Crossref | GoogleScholarGoogle Scholar |
Waldenström, J., Bensch, S., Hasselquist, D., and Östman, Ö. (2004). A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191–194.
| A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood.Crossref | GoogleScholarGoogle Scholar | 15040694PubMed |
Warner, R. E. (1968). The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. Condor 70, 101–120.
| The role of introduced diseases in the extinction of the endemic Hawaiian avifauna.Crossref | GoogleScholarGoogle Scholar |
Zamora-Vilchis, I., Williams, S. E., and Johnson, C. N. (2012). Environmental temperature affects prevalence of blood parasites of birds on an elevation gradient: implications for disease in a warming climate. PLoS ONE 7, e39208.
| Environmental temperature affects prevalence of blood parasites of birds on an elevation gradient: implications for disease in a warming climate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XptlSns7k%3D&md5=99dc50074373c3a654b288d17b7803afCAS | 22723966PubMed |