Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-28T00:20:37.373Z Has data issue: false hasContentIssue false

Interactions of Plasmodium juxtanucleare and chicken anaemia virus: establishing a model

Published online by Cambridge University Press:  19 August 2013

PATRICIA SILVEIRA
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil
SANDRA Y. G. MARIN
Affiliation:
Setor de Doenças das Aves, Departamento de Medicina Veterinária Preventiva, Escola de Veterinária, Belo Horizonte, MG 31270-901, Brazil
PATRICIA A. MOREIRA
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil
BÁRBARA B. TOCANTINS
Affiliation:
Faculdade de Agronomia e Medicina Veterinária, Universidade de Brasília, Campus Universitário Darcy Ribeiro, Brasília, DF 70910-900, Brazil
GUSTAVO LACORTE
Affiliation:
Departamento de Ciências Agrárias, Instituto Federal de Minas Gerais, Escola Agrotécnica Federal de Bambuí, MG 38900-000, Brazil
TATIANE A. PAIXÃO
Affiliation:
Departamento de Patologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil
NELSON R. S. MARTINS
Affiliation:
Setor de Doenças das Aves, Departamento de Medicina Veterinária Preventiva, Escola de Veterinária, Belo Horizonte, MG 31270-901, Brazil
ÈRIKA M. BRAGA*
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil
*
*Corresponding author: Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627. Instituto de Ciências Biológicas, Departamento de Parasitologia, Belo Horizonte, MG 31270-910, Brazil. E-mail: [email protected]

Summary

The pathogens Plasmodium juxtanucleare and chicken anaemia virus (CAV) are easily transmitted and potentially harmful to chickens. In this study, we established an experimental model to investigate the effects of avian malaria caused by P. juxtanucleare in white leghorn specific-pathogen-free (SPF) chicks previously immunosuppressed with CAV. Parasitaemia, haematological variables and clinical and pathological parameters were determined in four different experimental groups: chicks coinfected by CAV and P. juxtanucleare strain (Coinfected group), chicks exclusively infected by CAV (CAV group) or P. juxtanucleare (Malaria group) and uninfected chicks (Control group). Our data demonstrated that P. juxtanucleare parasitaemia was significantly higher in the Coinfected group. Furthermore, haematological parameters, including the RBC, haematocrit and haemoglobin concentration were significantly reduced in coinfected chicks. In agreement with the changes observed in haematological features, the mortality among coinfected chicks was higher compared with animals with single infections. Clinical analysis indicated moderate changes related to different organs size (bursa of Fabricius, heart and liver) in coinfected birds. The experimental coinfection of SPF chickens with P. juxtanucleare and CAV may represent a research tool for the study of avian malaria after CAV immunosuppression, enabling measurement of the impacts caused by different pathogens during malarial infection.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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

Al Dabagh, M. A. (1960). The effects of splenectomy on Plasmodium juxtanucleare infections in chicks. Transactions of the Royal Society of Tropical Medicine and Hygiene 54, 400405.CrossRefGoogle ScholarPubMed
Al Dabagh, M. A. (1961). Symptomatic partial paralysis in chicks with Plasmodium juxtanucleare. Journal of Comparative Pathology 71, 217221.CrossRefGoogle ScholarPubMed
Asghar, M., Westerdahl, H., Zehtindjiev, P., Ilieva, M., Hasselquist, D. and Bensch, S. (2012). Primary peak and chronic malaria infection levels are correlated in experimentally infected great reed warblers. Parasitology 139, 12461252.CrossRefGoogle ScholarPubMed
Atkinson, C. T. and Van Riper, C. III (1991). Pathogenicity and epizootiology of avian hematozoa: Plasmodium, Leucocytozoon and Haemoproteus. In Bird–Parasite Interactions: Ecology, Evolution, and Behavior (ed. Loye, J. and Zuk, M.), pp. 1948. Oxford University Press, New York, USA.CrossRefGoogle Scholar
Barrios, P. R., Marín, S. Y. G., Resende, M., Rios, R. L., Resende, J. S., Horta, R. S., Costa, M. P. and Martins, N. R. S. (2009). Occurrence of chicken anemia virus in backyard chickens of the metropolitan region of Belo Horizonte, Minas Gerais. Brazilian Journal of Poultry Science 11, 135138.CrossRefGoogle Scholar
Beirão, B. C., Fávaro, C. Jr., Nakao, L. S., Caron, L. F., Zanata, S. M. and Mercadante, A. F. (2012). Flow cytometric immune profiling of specific-pathogen-free chickens before and after infectious challenges. Veterinary Immunology Immunopathology 145, 3241.CrossRefGoogle ScholarPubMed
Belo, N. O., Pinheiro, R. T., Reis, E. S., Ricklefs, R. E. and Braga, E. M. (2011). Prevalence and lineage diversity of avian haemosporidians from three distinct cerrado habitats in Brazil. PLoS ONE 6, e17654.CrossRefGoogle ScholarPubMed
Belo, N. O., Rodríguez-Ferraro, A., Braga, E. M. and Ricklefs, R. E. (2012). Diversity of avian haemosporidians in arid zones of northern Venezuela. Parasitology 139, 10211028.CrossRefGoogle ScholarPubMed
Bennett, F. G. and Warren, M. (1966 a). Biology of the Malaysian strain of Plasmodium juxtanucleare Versiani and Gomes, 1941.I. Description of the stages in the vertebrate host. Journal of Parasitology 52, 565569.CrossRefGoogle ScholarPubMed
Bennett, F. G. and Warren, M. (1966 b). Biology of the Malaysian strain of Plasmodium juxtanucleare Versiani and Gomes, 1941.III. Life cycle of the erythrocytic parasite in the avian host. Journal of Parasitology 52, 653659.CrossRefGoogle ScholarPubMed
Bensch, S., Hellgren, O. and Pérez-Tris, J. (2009). A public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resource 9, 13531358.CrossRefGoogle ScholarPubMed
Boom, R., Sol, C. J., Salimans, M. M., Jansen, C. L., Wertheim-van, D. P. M. and van der Noordaa, J. (1990). Rapid and simple method for purification of nucleic acids. Journal of Clinical Microbiology 28, 495503.CrossRefGoogle ScholarPubMed
Brentano, L., Silva, B. G., Sayd, S. and Flores, S. W. (2000). Anticorpos Para o Vírus da Anemia das Galinhas (CAV) em Matrizes de Corte no Brasil. Brazilian Journal of Poultry Science 2, 163175.CrossRefGoogle Scholar
Campbell, T. W. (1995). Avian Hematology and Cytology, 1rd Edn. Iawa State Press, Ames, Iawa.Google Scholar
Chalwe, V., Van Geertruyden, J. P., Mukwamataba, D., Menten, J., Kamalamba, J., Mulenga, M. and D'Alessandro, U. (2009). Increased risk for severe malaria in HIV-1-infected adults, Zambia. Emerging Infectious Diseases 15, 749.CrossRefGoogle ScholarPubMed
Craig, M. I., Rimondi, A., Delamer, M., Sansalone, P., König, G., Vagnozzi, A. and Pereda, A. (2009). Molecular characterization of chicken infectious anemia virus circulating in Argentina during 2007. Avian Diseases 3, 331335.CrossRefGoogle Scholar
Ejiri, H., Sato, Y., Kim, K. S., Tsuda, Y., Murata, K., Saito, K., Watanabe, Y., Shimura, Y. and Yukawa, M. (2011). Blood meal identification and prevalence of avian malaria parasite in mosquitoes collected at Kushiro wetland, a subarctic zone of Japan. Journal of Medical Entomology 48, 904908.CrossRefGoogle ScholarPubMed
Elisei, C., Fernandes, K. R., Forlano, M. D., Madureira, R. C., Scofield, A., Yotoko, K. S. C., Soares, C. O., Araújo, F. R. and Massard, C. L. (2007). Morphology and morphometry of three Plasmodium juxtanucleare (Apicomplexa: Plasmodiidae) isolates. Revista Brasileira de Parasitologia Veterinaria 3, 139144.CrossRefGoogle Scholar
Eltahir, Y. M., Qian, K., Jin, W., Wang, P. and Qin, A. (2011). Molecular epidemiology of chicken anemia virus in commercial farms in China. Virology Journal 8, 145.CrossRefGoogle ScholarPubMed
Frevert, U., Späth, G. F. and Yee, H. (2008). Exoerythrocytic development of Plasmodium gallinaceum in the White Leghorn chicken. International Journal for Parasitology 6, 655672.CrossRefGoogle Scholar
Gallardo, R. A., van Santen, V. L. and Toro, H. (2012). Effects of chicken anaemia virus and infectious bursal disease virus-induced immunodeficiency on infectious bronchitis virus replication and genotypic drift. Avian Pathology 5, 451458.CrossRefGoogle Scholar
Garnham, P. C. C. (1966). Malaria Parasites and other Haemosporidia, 1st Edn. Blackwell Science, Oxford, UK.Google Scholar
Grim, K. C., van der Merwe, E., Sullivan, M., Parsons, N., Mc Cutchan, T. F. and Cranfield, M. (2003). Plasmodium juxtanucleare associated with mortality in black-footed penguin (Spheniscus demersus) admitted to a rehabilitation center. Journal Zoo Wildlife Medicine 34, 250255.CrossRefGoogle ScholarPubMed
Godfrey, R. D. Jr., Fedynich, A. M. and Pence, D. B. (1987). Quantification of hematozoa in blood smears. Journal of Wildlife Diseases 23, 558565.CrossRefGoogle ScholarPubMed
Goryo, M., Hayashi, S., Yoshizawa, K., Umemura, T., Itakura, C. and Yamashiro, S. (1989). Ultrastructure of the thymus in chicks inoculated with chicken anaemia agent (MSB1-TK5803 strain). Avian Pathology 18, 605617.CrossRefGoogle ScholarPubMed
Haridy, M., Sasaki, J., Ikezawa, M., Okada, K. and Goryo, M. (2012). Pathological and immunohistochemical studies of subclinical infection of chicken anemia virus in 4-week-old chickens. Journal of Veterinary Medical Science 6, 757764.CrossRefGoogle 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, 797802.CrossRefGoogle ScholarPubMed
Hoop, R. K. (1992). Persistence and vertical transmission of chicken anaemia agent in experimentally infected laying hens. Avian Pathology 21, 493501.CrossRefGoogle ScholarPubMed
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755.CrossRefGoogle ScholarPubMed
Juhl, J. and Permin, A. (2002). The effect of Plasmodium gallinaceum on a challenge infection with Ascaridia galli in chickens. Veterinary Parasitology 1, 1119.CrossRefGoogle Scholar
Khasnis, A. A. and Karnad, D. R. (2003). Human immunodeficiency virus type 1 infection in patients with severe falciparum malaria in urban India. Journal of Postgraduate Medicine 49, 114117.Google ScholarPubMed
Kimura, M., Darbro, J. M. and Harrington, L. C. (2010). Avian malaria parasites share congeneric mosquito vectors. Journal of Parasitology 96, 144151.CrossRefGoogle ScholarPubMed
Krettli, A. U. (1972). Plasmodium juxtanucleare in the state of Minas Gerais, Brazil. Studies on its prevalence and some aspects of its biology. Revista do Instituto de Medicina Tropical de São Paulo 14, 235245.Google Scholar
Kuscu, B. and Gurel, A. (2008). Lesions in the thymus and bone marrow in chicks with experimentally induced chicken infectious anemia disease. Journal of Veterinary Science 1, 1523.CrossRefGoogle Scholar
Lacorte, G. A., Félix, G. M., Pinheiro, R. R., Chaves, A. V., Almeida-Neto, G., Neves, F. S., Leite, L. O., Santos, F. R. and Braga, E. M. (2013). Exploring the diversity and distribution of neotropical avian malaria parasites – a molecular survey from southeast Brazil. PLoS ONE 8, e57770.CrossRefGoogle ScholarPubMed
Lapointe, D. A., Atkinson, C. T. and Samuel, M. D. (2012). Ecology and conservation biology of avian malaria. Annals of the New York Academy of Sciences 1249, 211226.CrossRefGoogle ScholarPubMed
Liang, M., Zhao, Q., Liu, G., Yang, S., Zuo, X., Cui, G., Zhong, S., Sun, J., Liu, J. and Zhu, R. (2013). Pathogenicity of Bordetella avium under immunosuppression induced by Reticuloendotheliosis virus in specific-pathogen-free chickens. Microbial Pathogenesis 54, 4045.CrossRefGoogle ScholarPubMed
Lyimo, I. N., Keegan, S. P., Ranford-Cartwright, L. C. and Ferguson, H. M. (2012). The impact of uniform and mixed species blood meals on the fitness of the mosquito vector Anopheles gambiae: does a specialist pay for diversifying its host species diet? Journal of Evolutionary Biology 3, 452460.CrossRefGoogle Scholar
Lourenço-de-Oliveira, R. and Castro, F. A. (1991). Culex saltanensis Dyar, 1928 Natural Vetor of Plasmodium juxtanucleare in Rio de Janeiro, Brazil. Memorias Instituto Oswaldo Cruz 86, 8794.CrossRefGoogle Scholar
Loving, C. L., Brockmeier, S. L., Vincent, A. L., Palmer, M. V., Sacco, R. E. and Nicholson, T. L. (2010). Influenza virus coinfection with Bordetella bronchiseptica enhances bacterial colonization and host responses exacerbating pulmonary lesions. Microbial Pathogenesis 49, 237245.CrossRefGoogle ScholarPubMed
Macchi, B. M., Quaresma, J. A., Herculano, A. M., Crespo-López, M. E., DaMatta, R. A. and Nascimento, J. L. (2010). Pathogenic action of Plasmodium gallinaceum in chickens: brain histology and nitric oxide production by blood monocyte-derived macrophages. Veterinary Parasitology 2, 1622.CrossRefGoogle Scholar
Marin, S. Y. G., Barrios, P. R., Rios, R. L., Resende, M., Resende, J. S., Santos, B. M. and Martins, N. R. S. (2013). Molecular characterization of contaminating infectious anemia virus of chickens in live commercial vaccines produced in the 1990's. Avian Diseases 57, 1521.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.CrossRefGoogle Scholar
Marzal, A., Ricklefs, R. E., Valkiūnas, G., Albayrak, T., Arriero, E., Bonneaud, C., Czirják, G. A., Ewen, J., Hellgren, O., Hořáková, D., Iezhova, T. A., Jensen, H., Križanauskienė, A., Lima, M. R., de Lope, F., Magnussen, E., Martin, L. B., Møller, A. P., Palinauskas, V., Pap, P. L., Pérez-Tris, J., Sehgal, R. N., Soler, M., Szöllosi, E., Westerdahl, H., Zetindjiev, P. and Bensch, S. (2011). Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS ONE 7, e21905.CrossRefGoogle Scholar
McNulty, M. S., McIlroy, S. G., Bruce, D. W. and Todd, D. (1991). Economic effects of subclinical chicken anemia agent infection in broiler chickens. Avian Diseases 35, 263268.CrossRefGoogle ScholarPubMed
Murata, K., Nii, R., Sasaki, E., Ishikawa, S., Sato, Y., Sawabe, K., Tsuda, Y., Matsumoto, R., Suda, A. and Ueda, M. (2008). Plasmodium (Bennettinia) juxtanucleare infection in a captive white eared-pheasant (Crossoptilon crossoptilon) at a Japanese zoo. Journal of Veterinary Medical Science 70, 203205.CrossRefGoogle Scholar
Nagao, E., Arie, T., Dorward, D. W., Fairhurst, R. M. and Dvorak, J. A. (2008). The avian malaria parasite Plasmodium gallinaceum causes marked structural changes on the surface of its host erythrocyte. Journal of Structural Biology 3, 460467.CrossRefGoogle Scholar
Natt, M. P. and Herrick, C. A. (1952). A new blood diluent for counting erythrocytes and leukocytes of the chickens. Poultry Science 31, 182.CrossRefGoogle Scholar
Niikura, M., Kim, T., Hunt, H. D., Burnside, J., Morgan, R. W., Dodgson, J. B. and Cheng, H. H. (2007). Marek's disease virus up-regulates major histocompatibility complex class II cell surface expression in infected cells. Virology 359, 212219.CrossRefGoogle ScholarPubMed
Njabo, K. Y., Cornel, A. J., Bonneaud, C., Toffelmier, E., Sehgal, R. N. M., Valkiūnas, G., Russell, A. F. and Smith, T. B. (2011). Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Molecular Ecology 20, 10491061.CrossRefGoogle Scholar
Nogueira, E. O., Piantino, F. A., Martins, S. R., Luiz, D. E., Lazzarin, S. and Brentano, L. (2007). Genome sequencing analysis of Brazilian chicken anemia virus isolates that lack MSB-1 cell culture tropism. Comparative Immunology, Microbiology and Infectious Diseases 30, 8196.CrossRefGoogle ScholarPubMed
Pacheco, M. A., Escalante, A. A., Garner, M. M., Bradley, G. A. and Aguilar, R. F. (2011). Haemosporidian infection in captive masked bobwhite quail (Colinus virginianus ridgwayi), an endangered subspecies of the northern bobwhite quail. Veterinary Parasitology 4, 113120.CrossRefGoogle Scholar
Palinauskas, V., Valkiūnas, G., Krizanauskiene, A., Bensch, S. and Bolshakov, C. V. (2009). Plasmodium relictum (lineage P-SGS1): further observation of effects on experimentally infected passeriform birds, with remarks on treatment with Malarone. Experimental Parasitology 123, 134139.CrossRefGoogle ScholarPubMed
Palinauskas, V., Valkiūnas, G., Bolshakov, C. V. and Bensch, S. (2011). Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): the effects of the co-infection on experimentally infected passerine birds. Experimental Parasitology 127, 527533.CrossRefGoogle ScholarPubMed
Peters, M. A., Crabb, B., Tivendale, K. and Browning, G. F. (2007). Attenuation of chicken anemia virus by site-directed mutagenesis of VP2. Journal of General Virology 88, 21682175.CrossRefGoogle ScholarPubMed
Pope, C. R. (1991). Pathology of lymphoid organs with emphasis on imunosuppression. Veterinary Immunology Immunopathology 30, 3144.CrossRefGoogle Scholar
Ragland, W. L., Mazija, H., Cvelic-Cabrilo, V., Savic, V., Novak, R. and Pogacnik, M. (1998). Immune suppression of commercial broilers in Croatia, Slovenia, and Bosnia and Herzegovina from 1981 to 1991. Avian Pathology 2, 200204.CrossRefGoogle Scholar
Rosenberger, J. K. and Cloud, S. S. (1998). Chicken anemia virus. Poultry Science 8, 11901192.CrossRefGoogle Scholar
Santiago-Alarcon, D., Havelka, P., Schaefer, H. M. and Segelbacher, G. (2012). Bloodmeal analysis reveals avian Plasmodium infections and broad host preferences of Culicoides (Diptera: Ceratopogonidae) vectors. PLoS ONE 7, e31098.CrossRefGoogle ScholarPubMed
Santos-Prezoto, H. H., D'Agosto, M. and Daemom, E. (2004). Prevalência e variação dos estádios eritrocíticos do Plasmodium (Novyella) juxtanucleare em Gallus gallus sob condições naturais, no período de um ano. Parasitologia Latinoamericana 59, 1420.Google Scholar
Schat, K. A. (2009). Chicken anemia virus. Current Topics in Microbiology and Immunology 331, 151183.Google ScholarPubMed
Sehgal, R. N. M. (2010). Deforestation and avian infectious diseases. Journal of Experimental Biology 213, 955960.CrossRefGoogle ScholarPubMed
Silveira, P., Damatta, R. A. and D'Agosto, M. (2009 a). Hematological changes of chickens experimentally infected with Plasmodium (Bennettinia) juxtanucleare. Veterinary Parasitology 162, 257262.CrossRefGoogle ScholarPubMed
Silveira, P., Vashist, U., Cabral, A., Amaral, K. B., Soares, G. L. G. and D'Agosto, M. (2009 b). Effect of rutin and chloroquine on White Leghorn chickens infected with Plasmodium (Bennettinia) juxtanucleare. Tropical Animal Health and Production 41, 13191323.CrossRefGoogle ScholarPubMed
Simionatto, S., Lima-Rosa, C. A., Binneck, E., Ravazzolo, A. P. and Canal, C. W. (2006). Characterization and phylogenetic analysis of Brazilian chicken anaemia virus. Virus Genes 33, 510.CrossRefGoogle ScholarPubMed
Smyth, J. A., Moffett, D. A., McNulty, M. S., Todd, D. and Mackie, D. P. (1993). A sequential histopathologic and immunocytochemical study of chicken anemia virus infection at one day of age. Avian Diseases 37, 324338.CrossRefGoogle ScholarPubMed
Snoeck, C. J., Komoyo, G. F., Mbee, B. P., Nakouné, E., Le Faou, A., Okwen, M. P. and Muller, C. P. (2012). Epidemiology of chicken anemia virus in Central African Republic and Cameroon. Virology Journal 1, 189.CrossRefGoogle Scholar
Tan, Y., Zhu, R., Wang, H., Wang, X., Wei, K., Sun, Z. and Sheng, P. (2011). Establishment of multiple PCR detection for pathogens of chicken embryos. Chinese J Preventive Veterinary Medicine 33, 374377.Google Scholar
Todd, D., Mawhinney, K. A. and McNulty, M. S. (1992). Detection and differentiation of chicken anemia virus isolates by using the polymerase chain reaction. Journal of Clinical Microbiology 30, 16611666.CrossRefGoogle ScholarPubMed
Umesaki, Y., Setoyama, H., Matsumoto, S. and Okada, Y. (1993). Expansion of alpha beta T-cell receptor-bearing intestinal intraepithelial lymphocytes after microbial colonization in germ-free mice and its independence from thymus. Immunology 79, 3237.Google ScholarPubMed
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Vashist, U., Silveira, P., Cabral, A., Amaral, K. B., Soares, G. L. G. and D'Agosto, M. (2008). Atividade malaricida da quercetina em Gallus gallus L., 1758 imunossuprimidos infectados por Plasmodium (Bennettinia) juxtanucleare Versiani e Gomes, 1941. Revista Brasileira de Parasitologia Veterinária 17, 220223.Google Scholar
Vashist, U., Falqueto, A. D., Lustrino, D., Tunholi, V. M., Tunholi-Alves, V. M., dos Santos, M. A., D'Agosto, M., Massard, C. L. and Pinheiro, J. (2011). Hepatic profile of Gallus gallus Linnaeus, 1758 experimentally infected by Plasmodium juxtanucleare Versiani & Gomes, 1941. Veterinary Parasitology 175, 207211.CrossRefGoogle ScholarPubMed
Versiani, V. and Gomes, B. F. (1941). Sobre um novo hematozoário de galinha, Plasmodium juxtanucleare n. sp. (nota prévia). Revista Brasileira de Biologia 1, 231233.Google Scholar
Vogelstein, B. and Gillespie, D. (1979). Preparative and analytical purification of DNA from agarose. Proceedings of the National Academy of Sciences USA 76, 615619.CrossRefGoogle ScholarPubMed
Wright, E. J., Nayar, J. K. and Forrester, D. J. (2005). Interactive effects of turkeypox virus and Plasmodium hermani on turkey poults. Journal of Wildlife diseases 41, 141148.CrossRefGoogle ScholarPubMed
Zehtindjiev, P., Ilieva, M., Westerdahl, H., Hansson, B., Valkiūnas, 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.CrossRefGoogle Scholar
Supplementary material: Image

Silveira Supplementary Material

Image

Download Silveira Supplementary Material(Image)
Image 2.4 MB