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Use of a real-time PCR to explore the intensity of Plasmodium spp. infections in native, endemic and introduced New Zealand birds

Published online by Cambridge University Press:  10 July 2017

D. C. SIJBRANDA
Affiliation:
Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11 222, Palmerston North 4442, New Zealand
B. D. GARTRELL
Affiliation:
Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11 222, Palmerston North 4442, New Zealand
Z. L. GRANGE
Affiliation:
Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11 222, Palmerston North 4442, New Zealand
L. HOWE*
Affiliation:
Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11 222, Palmerston North 4442, New Zealand
*
*Corresponding author: Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11-222, Palmerston North 4442, New Zealand. E-mail: [email protected]

Summary

Avian malaria, caused by Plasmodium spp., is an emerging disease in New Zealand (NZ). To detect Plasmodium spp. infection and quantify parasite load in NZ birds, a real-time polymerase chain reaction (PCR) (qPCR) protocol was used and compared with a nested PCR (nPCR) assay. A total of 202 blood samples from 14 bird species with known nPCR results were tested. The qPCR prevalences for introduced, native and endemic species groups were 70, 11 and 21%, respectively, with a sensitivity and specificity of 96·7 and 98%, respectively, for the qPCR, while a sensitivity and specificity of 80·9 and 85·4% were determined for the nPCR. The qPCR appeared to be more sensitive in detecting lower levels of parasitaemia. The mean parasite load was significantly higher in introduced bird species (2245 parasites per 10 000 erythrocytes) compared with endemic species (31·5 parasites per 10 000 erythrocytes). In NZ robins (Petroica longipes), a significantly lower packed cell volume was found in birds that were positive for Plasmodium spp. compared with birds that were negative. Our data suggest that introduced bird species, such as blackbirds (Turdus merula), have a higher tolerance for circulating parasite stages of Plasmodium spp., indicating that introduced species are an important reservoir of avian malaria due to a high infection prevalence and parasite load.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Alley, M. R., Hale, K. A., Cash, W., Ha, H. J. and Howe, L. (2010). Concurrent avian malaria and avipox virus infection in translocated South Island saddlebacks (Philesturnus carunculatus carunculatus). New Zealand Veterinary Journal 58, 218–23. doi: 10.1080/00480169.2010.68868.CrossRefGoogle ScholarPubMed
Asghar, M., Hasselquist, D. and Bensch, S. (2011). Are chronic avian haemosporidian infections costly in wild birds? Journal of Avian Biology 42, 530537. doi: 10.1111/j.1600-048X.2011.05281.x.CrossRefGoogle Scholar
Asghar, M., Hasselquist, D., Hansson, B., Zehtindjiev, P., Westerdahl, H. and Bensch, S. (2015). Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347, 436438.CrossRefGoogle ScholarPubMed
Atkinson, C. T., Dusek, R. J., Woods, K. L. and Iko, W. M. (2000). Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi. Journal of Wildlife Diseases 36, 197204.CrossRefGoogle ScholarPubMed
Atkinson, C. T., Saili, K. S., Utzurrum, R. B. and Jarvi, S. I. (2013). Experimental evidence for evolved tolerance to avian malaria in a wild population of low elevation Hawai ‘i ‘Amakihi (Hemignathus virens). EcoHealth 10, 366375.CrossRefGoogle Scholar
Atkinson, C. T., Utzurrum, R. B., Lapointe, D. A., Camp, J., Crampton, L. H., Foster, J. T. and Giambelluca, T. W. (2014). Changing climate and the altitudinal range of avian malaria in the Hawaiian Islands – an ongoing conservation crisis on the island of Kaua'i. Global Change Biology 20, 24262436.CrossRefGoogle ScholarPubMed
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, 18431851. doi: 10.1017/s0031182011001491.CrossRefGoogle ScholarPubMed
Bensch, S., Stjernman, M., Hasselquist, D., Ostman, O., 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: Biological Sciences 267, 1583–589.Google ScholarPubMed
Branscum, A. J., Gardner, I. A. and Johnson, W. O. (2005). Estimation of diagnostic-test sensitivity and specificity through Bayesian modeling. Preventive Veterinary Medicine 68, 145163.CrossRefGoogle ScholarPubMed
Brown, L. D., Cai, T. T. and Anirban, D. (2001). Interval estimation for a binomial proportion. Statistical Science 16, 101117.CrossRefGoogle Scholar
Castro, I., Howe, L., Tompkins, D. M., Barraclough, R. K. and Slaney, D. (2011). Presence and seasonal prevalence of Plasmodium spp. in a rare endemic New Zealand passerine (Tieke or saddleback, Philesturnus carunculatus). Journal of Wildlife Disease 47, 860867.CrossRefGoogle Scholar
Dawson, R. D. and Bortolotti, G. R. (2000). Effects of hematozoan parasites on condition and return rates of American Kestrels. Auk 117, 373380. doi: 10.1642/0004-8038(2000)117[0373:eohpoc]2.0.co;2.CrossRefGoogle Scholar
Dimitrov, D., Palinauskas, V., Iezhova, T. A., Bernotienė, R., Ilgūnas, M., Bukauskaitė, D., Zehtindjiev, P., Ilieva, M., Shapoval, A. P., Bolshakov, C. V. and Markovets, M. Y. (2015). Plasmodium spp.: an experimental study on vertebrate host susceptibility to avian malaria. Experimental Parasitology 148, 116.CrossRefGoogle Scholar
Duncan, R. P. (1997). The role of competition and introduction effort in the success of passeriform birds introduced to New Zealand. American Naturalist 149, 903915.CrossRefGoogle ScholarPubMed
Ewen, J. G., Bensch, S., Blackburn, T. M., Bonneaud, C., Brown, R., Cassey, P., Clarke, R. H. and Perez-Tris, J. (2012 a). Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna. Ecology Letters 15, 11121119. doi: 10.1111/j.1461-0248.2012.01833.x.CrossRefGoogle Scholar
Ewen, J. G., Armstrong, D. P., Empson, R., Jack, S., Makan, T., McInnes, K., Parker, K. A., Richardson, K. and Alley, M. (2012 b). Parasite management in translocations: lessons from a threatened New Zealand bird. Oryx 46, 446456. doi: 10.1017/s0030605311001281.CrossRefGoogle Scholar
Fallon, S. M., Ricklefs, R. E., Swanson, B. L. and Bermingham, E. (2003). Detecting avian malaria: an improved polymerase chain reaction diagnostic. Journal of Parasitology 89, 10441047.CrossRefGoogle ScholarPubMed
Friedl, T. W. P. and Groscurth, E. (2012). A real-time PCR protocol for simple and fast quantification of blood parasite infections in evolutionary and ecological studies and some data on intensities of blood parasite infections in a subtropical weaverbird. Journal of Ornithology 153, 239247. doi: 10.1007/s10336-011-0735-9.CrossRefGoogle Scholar
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, 797802.CrossRefGoogle ScholarPubMed
Hill, A. G., Howe, L., Gartrell, B. D. and Alley, M. R. (2010). Prevalence of Leucocytozoon spp, in the endangered yellow-eyed penguin Megadyptes antipodes. Parasitology 137, 14771485.CrossRefGoogle ScholarPubMed
Howe, L., Castro, I. C., Schoener, E. R., Hunter, S., Barraclough, R. K. and Alley, M. R. (2012). Malaria parasites (Plasmodium spp.) infecting introduced, native and endemic New Zealand birds. Parasitology Research 110, 913923. doi: 10.1007/s00436-011-2577-z.CrossRefGoogle ScholarPubMed
Labocha, M. K. and Hayes, J. P. (2012). Morphometric indices of body condition in birds: a review. Journal of Ornithology 153, 122. doi: 10.1007/s10336-011-0706-1.CrossRefGoogle Scholar
Laird, M. (1950). Some blood parasites of New Zealand birds. Victoria University College Zoology Publications 5, 120.Google Scholar
Marzal, A., de Lope, F., Navarro, C. and Moller, A. P. (2005). Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142, 541545. doi: 10.1007/s00442-004-1757-2.CrossRefGoogle Scholar
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, 979987. doi: 10.1111/j.1420-9101.2008.01545.x.CrossRefGoogle Scholar
Marzal, A., Ricklefs, R. E., Valkiunas, G., Albayrak, T., Arriero, E., Bonneaud, C., Czirjak, G. A., Ewen, J., Hellgren, O., Horakova, D., Iezhova, T. A., Jensen, H., Krizanauskiene, A., Lima, M. R., de Lope, F., Magnussen, E., Martin, L. B., Moller, A. P., Palinauskas, V., Pap, P. L., Perez-Tris, J., Sehgal, R. N. M., Soler, M., Eszter, S., Westerdahl, H., Zetindjiev, P. and Bensch, S. (2011). Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS ONE 6, e21905. doi: 10.1371/journal.pone.0021905.CrossRefGoogle Scholar
Moller, A. P. and Nielsen, J. T. (2007). Malaria and risk of predation: a comparative study of birds. Ecology 88, 871881. doi: 10.1890/06-0747.CrossRefGoogle ScholarPubMed
Motta, R. O. C., Romero Marques, M. V., Ferreira Junior, F. C., de Assis Andery, D., Horta, R. S., Peixoto, R. B., Augusto, G., Lacorte, G. A., Moreira, P. D., Leme, F. D., Melo, M. M., Martins, N. R. D. and Braga, E. M. (2013). Does haemosporidian infection affect hematological and biochemical profiles of the endangered Black-fronted piping-guan (Aburria jacutinga)? PeerJ 1, e45.CrossRefGoogle ScholarPubMed
Nolan, M. J., Tomley, F. M., Kaiser, P. and Blake, D. P. (2015). Quantitative real-time PCR (qPCR) for Eimeria tenella replication – implications for experimental refinement and animal welfare. Parasitology International 64, 464470.CrossRefGoogle ScholarPubMed
Ortiz-Catedral, L., Prada, D., Gleeson, D. and Brunton, D. H. (2011). Avian malaria in a remnant population of red-fronted parakeets on Little Barrier Island, New Zealand. New Zealand Journal of Zoology 38, 261268. doi: 10.1080/03014223.2011.584540.CrossRefGoogle Scholar
Palinauskas, V., Valkiūnas, G., Bolshakov, C. V. and Bensch, S. (2008). Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Experimental Parasitology, 120, 372380.CrossRefGoogle ScholarPubMed
Paulman, A. and McAllister, M. M. (2005). Plasmodium gallinaceum: clinical progression, recovery, and resistance to disease in chickens infected via mosquito bite. American Journal of Tropical Medicine and Hygiene 73, 11041107.CrossRefGoogle ScholarPubMed
Perandin, F., Manca, N., Calderaro, A., Piccolo, G., Galati, L., Ricci, L., Medici, M. C., Arcangeletti, M. C., Snounou, G., Dettori, G. and Chezzi, C. (2004). Development of a real-time PCR assay for detection of Plasmodium falciparum, Plasmodium vivax, and Plasmodium ovale for routine clinical diagnosis. Journal of Clinical Microbiology 42, 12141219. doi: 10.1128/jcm.42.31.214-1219.2004.CrossRefGoogle ScholarPubMed
Preacher, K. J. (2001). Calculation for the chi-square test: an interactive calculation tool for chi-square tests of goodness of fit and independence [Computer software]. Available from http://quantpsy.org.Google Scholar
Preacher, K. J. and Briggs, N. E. (2001). Calculation for Fisher's Exact Test: an interactive calculation tool for Fisher's exact probability test for 2 × 2 tables [Computer software]. Available from http://quantpsy.org.Google Scholar
Rook, G. A. W. (2009). Review series on helminths, immune modulation and the hygiene hypothesis: the broader implications of the hygiene hypothesis. Immunology 126, 311. doi: 10.1111/j.1365-2567.2008.03007.x.CrossRefGoogle ScholarPubMed
Roth, J. M., Korevaar, D. A., Leeflang, M. M. G. and Mens, P. F. (2016) Molecular malaria diagnostics: a systematic review and meta-analysis. Critical Reviews in Clinical Laboratory Sciences, 53, 87105.CrossRefGoogle ScholarPubMed
Schoener, E., Banda, M., Howe, L., Castro, I. and Alley, M. (2014). Avian malaria in New Zealand. New Zealand Veterinary Journal 62, 189198. doi: 10.1080/00480169.2013.871195.CrossRefGoogle ScholarPubMed
Sijbranda, D. C., Campbell, J., Gartrell, B. D. and Howe, L. (2016). Avian malaria in introduced, native and endemic New Zealand bird species in a mixed eco-system. New Zealand Journal of Ecology 40, 7279.CrossRefGoogle Scholar
Tan, T. M. C., Nelson, J. S., Ng, H. C., Ting, R. C. Y. and Kara, U. A. K. (1997). Direct PCR amplification and sequence analysis of extrachromosomal Plasmodium DNA from dried blood spots. Acta Tropica 68, 105114.CrossRefGoogle ScholarPubMed
Tiersch, T. R. and Wachtel, S. S. (1991). On the evolution of genome size of birds. Journal of Heredity 82, 363368.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, 5162. doi: 10.1080/03014223.2006.9517799.CrossRefGoogle Scholar
Valkiunas, G. (2005). Avian Malaria Parasites and Other Haemosporidia. Boca Raton, Florida, USA: CRC Press.Google Scholar
Valkiūnas, G., Bensch, S., Iezhova, T. A., Krizanauskiené, A., Hellgren, O. and Bolshakov, C. V. (2006) Nested cytochrome b polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential. Journal of Parasitology 92, 418422.CrossRefGoogle ScholarPubMed
Westerdahl, H. (2012). Quantitative disease resistance: to better understand parasite mediated selection on major histocompatibility complex. Proceedings of the Royal Society B: Biological sciences 279, 577584.CrossRefGoogle ScholarPubMed
Wickham, H. (2009). ggplot2, Elegant Graphics for Data Analysis, 1st edn. Springer-Verlag, New York.CrossRefGoogle Scholar
Wilson, R. J., Denny, P. W., Preiser, P. R., Rangachari, K., Roberts, K., Roy, A., Whyte, A., Strath, M., Moore, D. J., Moore, P. W. and Williamson, D. H. (1996). Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum . Journal of Molecular Biology 261, 155172.CrossRefGoogle ScholarPubMed
Yorinks, N. and Atkinson, C. T. (2000). Effects of malaria on activity budgets of experimentally infected juvenile Apapane (Himatione sanguinea). Auk 117, 731738. doi: 10.1642/0004-8038(2000)117[0731:eomoab]2.0.co;2.CrossRefGoogle Scholar
Zehtindjiev, P., Ilieva, M., Westerdahl, H., Hansson, B., Valkiunas, G. and Bensch, S. (2008). Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus . Experimental Parasitology 119, 99110. doi: 10.1016/j.exppara.2007.12.018.CrossRefGoogle Scholar