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Co-infections of haemosporidian and trypanosome parasites in a North American songbird

Published online by Cambridge University Press:  20 September 2016

LETÍCIA SOARES*
Affiliation:
Department of Biology, University of Missouri-St. Louis, R223 Research Building, One University Boulevard, St. Louis, 63121 MO, USA
VINCENZO A. ELLIS
Affiliation:
Department of Biology, University of Missouri-St. Louis, R223 Research Building, One University Boulevard, St. Louis, 63121 MO, USA Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
ROBERT E. RICKLEFS
Affiliation:
Department of Biology, University of Missouri-St. Louis, R223 Research Building, One University Boulevard, St. Louis, 63121 MO, USA
*
*Corresponding author: Department of Biology, University of Missouri-St. Louis, R223 Research Building, One University Boulevard, St. Louis 63121 MO, USA. E-mail: [email protected]

Summary

Hosts frequently harbour multiple parasite infections, yet patterns of parasite co-occurrence are poorly documented in nature. In this study, we asked whether two common avian blood parasites, one haemosporidian and one trypanosome, affect each other's occurrence in individuals of a single host species. We used molecular genotyping to survey protozoan parasites in the peripheral blood of yellow-breasted chats (Aves: Passeriformes [Parulidae]: Icteria virens) from the Ozarks of Southern Missouri. We also determined whether single and co-infections differently influence white blood cell and polychromatic erythrocyte counts, the latter being a measure of regenerative anaemia. We found a positive association between the haemosporidian and trypanosome parasites, such that infection by one increases the probability that an individual host is infected by the other. Adult individuals were more likely than juveniles to exhibit haemosporidian infection, but co-infections and single trypanosome infections were not age-related. We found evidence of pathogenicity of trypanosomes in that infected individuals exhibited similar levels of regenerative anaemia as birds infected with haemosporidian parasites of the genus Plasmodium. Counts of white blood cells did not differ with respect to infection status.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Alizon, S., de Roode, J. C. and Michalakis, Y. (2013). Multiple infections and the evolution of virulence. Ecology Letters 16, 556567.CrossRefGoogle ScholarPubMed
Apanius, V. (1991). Avian trypanosomes as models of hemoflagellate evolution. Parasitology Today 7, 8790.Google 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.Google Scholar
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.Google Scholar
Atkinson, C. T., Saili, K. S., Utzurrum, R. B. and Jarvi, S. I. (2014). Experimental evidence for evolved tolerance to avian malaria in a wild population of low elevation Hawai'i ‘Amakihi (Hemignathus virens). EcoHealth 10, 366375.Google Scholar
Baker, J. R. (1956 a). Studies on Trypanosoma avium Danilewsky 1885. II. Transmission by Ornithomyia avicularia . Parasitology 46, 321334.Google Scholar
Baker, J. R. (1956 b). Studies on Trypanosoma avium Danilewsky 1885. I. Incidence in some birds of Hertfordshire. Parasitology 46, 308320.Google Scholar
Baker, J. R. (1956 c). Studies on Trypanosoma avium Danilewsky 1885. III. Life cycle in vertebrate and invertebrate hosts. Parasitology 46, 335352.Google Scholar
Balmer, O., Stearns, S. C., Schötzau, A. and Brun, R. (2009). Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology 90, 33673378.CrossRefGoogle ScholarPubMed
Bennett, G. F., Earle, R. A. and Squires-Parsons, D. (1994). Trypanosomes of some sub-Saharan birds. Onderstepoort Journal of Veterinary Research 61, 263271.Google Scholar
Budischak, S. A., Sakamoto, K., Megow, L. C., Cummings, K. R., Urban, J. F. Jr. and Ezenwa, V. O. (2015). Resource limitation alters the consequences of co-infection for both hosts and parasites. International Journal for Parasitology 45, 455463.Google Scholar
Chatterjee, D. K. and Ray, H. N. (1971). Some observations on the morphology and developmental stages of Trypanosoma avium bakeri ssp. nov. from the red-whiskered bulbul (Otocompsa jocosa Linn.). Parasitology 62, 331338.CrossRefGoogle ScholarPubMed
Cornet, S., Nicot, A., Rivero, A. and Gandon, S. (2014). Evolution of plastic transmission strategies in avian malaria. PLoS Pathogens 10, e1004308.Google Scholar
Cox, F. E. (2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl.), S23S38.Google Scholar
Černý, O., Votýpka, J. and Svobodová, M. (2011). Spatial feeding preferences of ornithophilic mosquitoes, blackflies and biting midges. Medical and Veterinary Entomology 25, 104108.Google Scholar
de Roode, J. C., Helinski, M. E. H., Anwar, M. A. and Read, A. F. (2005). Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. American Naturalist 166, 531542.Google Scholar
de Roode, J. C., Yates, A. J. and Altizer, S. (2008). Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proceedings of the National Academy of Sciences of the United States of America 105, 74897494.Google Scholar
Desser, S. S., McIver, S. B. and Jez, D. (1975). Observations on the role of simuliids and culicids in the transmission of avian and anuran trypanosomes. International Journal for Parasitology 5, 507509.Google Scholar
Dimitrov, D., Palinauskas, V., Iezhova, T. A., Bernotienė, R., Ilgūnas, M., Bukauskaitė, D., Zehtindjiev, P., Ilieva, M., Shapoval, A. P., Bolshakov, C. V., Markovets, M. Y., Bensch, S. and Valkiūnas, G. (2015). Plasmodium spp.: an experimental study on vertebrate host susceptibility to avian malaria. Experimental Parasitology 148, 116.Google Scholar
Ellis, V. A., Kunkel, M. R. and Ricklefs, R. E. (2014). The ecology of host immune responses to chronic avian haemosporidian infection. Oecologia 176, 729737.Google Scholar
Ellis, V. A., Collins, M. D., Medeiros, M. C. I., Sari, E. H. R., Coffey, E. D., Dickerson, R. C., Lugarini, C., Stratford, J. A., Henry, D. R., Merrill, L., Matthews, A. E., Hanson, A. A., Roberts, J. R., Joyce, M., Kunkel, M. R. and Ricklefs, R. E. (2015). Local host specialization, host-switching, and dispersal shape the regional distributions of avian haemosporidian parasites. Proceedings of the National Academy of Sciences of the United States of America 112, 1129411299.Google Scholar
Ferguson, H. M. and Read, A. F. (2002). Why is the effect of malaria parasites on mosquito survival still unresolved? Trends in Parasitology 18, 256261.Google Scholar
Fridolfsson, A. K. and Ellegren, H. (1999). A simple and universal method for molecular sexing of non-ratite birds. Journal of Avian Biology 30, 116121.Google Scholar
Gering, E. and Atkinson, C. T. (2004). A rapid method for counting nucleated erythrocytes on stained blood smears by digital image analysis. Journal of Parasitology 90, 879881.Google Scholar
Girish, V. and Vijayalakshmi, A. (2004). Affordable image analysis using NIH Image/ImageJ. Indian Journal of Cancer 41, 47.Google Scholar
Greiner, E. C., Bennett, G. F., White, E. M. and Coombs, R. F. (1975 a). Distribution of the avian hematozoa of North America. Canadian Journal of Zoology 53, 17621787.Google Scholar
Greiner, E. C., Bennett, G. F., White, E. M. and Coombs, R. F. (1975 b). Distribution of the avian hematozoa of North America. Canadian Journal of Zoology 53, 17621787.Google Scholar
Haag, J. (1998). The molecular phylogeny of trypanosomes: evidence for an early divergence of the Salivaria. Molecular and Biochemical Parasitology 91, 3749.Google Scholar
Ivkovic, M., Kesic, M., Mihaljevic, Z. and Kudela, M. (2013). Emergence patterns and ecological associations of some haematophagous blackfly species along an oligotrophic hydrosystem. Medical and Veterinary Entomology 28, 94102.Google Scholar
Kirkpatrick, C. E. and Lauer, D. M. (1985). Hematozoa of raptors from southern New Jersey and adjacent areas. Journal of Wildlife Diseases 21, 16.Google Scholar
Kirkpatrick, C. E. and Suthers, H. B. (1988). Epizootiology of blood parasite infections in passerine birds from central New Jersey. Canadian Journal of zoology 66, 23742382.Google Scholar
Klemme, I., Louhi, K.-R. and Karvonen, A. (2016). Host infection history modifies co-infection success of multiple parasite genotypes. Journal of Animal Ecology 85, 591597.Google Scholar
Knowles, S. C. L., Nakagawa, S. and Sheldon, B. C. (2009). Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a meta-regression approach. Proceedings of the National Academy of Sciences of the United States of America 23, 405415.Google Scholar
Knowles, S. C. L., Wood, M. J. and Sheldon, B. C. (2010). Context-dependent effects of parental effort on malaria infection in a wild bird population, and their role in reproductive trade-offs. Oecologia 164, 8797.Google Scholar
Longmire, J. L., Maltbie, M. and Baker, R. J. (1997). Use of “lysis buffer” in DNA isolation and its implications for museum collections. Occasional Papers of the Museum of Texas Tech University 163, 13.Google Scholar
Lovette, I. J., Pérez-Emán, J. L., Sullivan, J. P., Banks, R. C., Fiorentino, I., Córdoba-Córdoba, S., Echeverry-Galvis, M., Barker, F. K., Burns, K. J., Klicka, J., Lanyon, S. M. and Bermingham, E. (2010). A comprehensive multilocus phylogeny for the wood-warblers and a revised classification of the Parulidae (Aves). Molecular Phylogenetics and Evolution 57, 753770.Google Scholar
Medeiros, M. C. I., Ellis, V. A. and Ricklefs, R. E. (2014). Specialized avian Haemosporida trade reduced host breadth for increased prevalence. Journal of Evolutionary Biology 27, 25202528.CrossRefGoogle ScholarPubMed
Mideo, N. (2009). Parasite adaptations to within-host competition. Trends in Parasitology 25, 261268.Google Scholar
Molyneux, D. H. and Robertson, E. (1974). Ultrastructure of the bloodstream forms of an avian trypanosome Trypanosoma bouffardi . Annals of Tropical Medicine and Parasitology 68, 369377.Google Scholar
Molyneux, D. H., Cooper, J. E. and Smith, W. J. (1983). Studies on the pathology of an avian trypanosome (T. bouffardi) infection in experimentally infected canaries. Parasitology 87(Pt 1), 4954.Google Scholar
Morris, D. L., Porneluzi, P. A., Haslerig, J., Clawson, R. L. and Faaborg, J. (2013). Results of 20 years of experimental forest management on breeding birds in Ozark forests of Missouri, USA. Forest Ecology and Management 310, 747760.Google Scholar
Oakgrove, K. S., Harrigan, R. J., Loiseau, C., Guers, S., Seppi, B. and Sehgal, R. N. M. (2014). Distribution, diversity and drivers of blood-borne parasite co-infections in Alaskan bird populations. International Journal for Parasitology 44, 717727.Google Scholar
Ots, I., MurumAgi, A. and HOrak, P. (1998). Haematological health state indices of reproducing Great Tits: methodology and sources of natural variation. Functional Ecology 12, 700707.Google 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.Google Scholar
Palinauskas, V., Valkiūnas, G., Kriћanauskienė, 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.Google Scholar
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.Google Scholar
Pérez-Rodríguez, A., de la Hera, I., Bensch, S. and Pérez-Tris, J. (2015). Evolution of seasonal transmission patterns in avian blood-borne parasites. International Journal for Parasitology 45, 605611.Google Scholar
Pérez-Tris, J. and Bensch, S. (2005). Diagnosing genetically diverse avian malarial infections using mixed-sequence analysis and TA-cloning. Parasitology 131, 1523.Google Scholar
R Core Team (2015). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ Google Scholar
Reidy, J. L., Thompson, F. R. III and Kendrick, S. W. (2014). Breeding bird response to habitat and landscape factors across a gradient of savanna, woodland, and forest in the Missouri Ozarks. Forest Ecology and Management 313, 3446.CrossRefGoogle Scholar
Ricklefs, R. E. and Sheldon, K. S. (2007). Malaria prevalence and white-blood-cell response to infection in a tropical and in a temperate thrush. Auk 124, 12541266.Google Scholar
Ricklefs, R. E., Swanson, B. L., Fallon, S. M., MartÍnez-AbraÍn, A., Scheuerlein, A., Gray, J. and Latta, S. C. (2005). Community relationships of avian malaria parasites in southern Missouri. Ecological Monographs 75, 543559.Google Scholar
Samour, J. (2006). Diagnostic value of hematology. In Clinical Avian Medicine (ed. Harrison, G. and Lightfoot, T.), pp. 587610. Spix Publishing, Palm Beach, FL.Google Scholar
Sehgal, R. N. M., Jones, H. I. and Smith, T. B. (2001). Host specificity and incidence of Trypanosoma in some African rainforest birds: a molecular approach. Molecular Ecology 10, 23192327.Google Scholar
Stabler, R. M., Holt, P. A. and Kitzmiller, N. J. (1966). Trypanosoma avium in the blood and bone marrow from 677 Colorado birds. Journal of Parasitology 52, 11411144.Google Scholar
Svensson-Coelho, M., Blake, J. G., Loiselle, B. A., Penrose, A. S., Parker, P. G. and Ricklefs, R. E. (2013). Diversity, prevalence, and host specificity of avian Plasmodium and Haemoproteus in a western Amazon assemblage. Ornithological Monographs 76, 147.CrossRefGoogle Scholar
Svobodová, M., Weidinger, K., Peške, L., Volf, P., Votýpka, J. and Voříšek, P. (2015). Trypanosomes and haemosporidia in the buzzard (Buteo buteo) and sparrowhawk (Accipiter nisus): factors affecting the prevalence of parasites. Parasitology Research 114, 551560.Google Scholar
Telfer, S., Lambin, X., Birtles, R., Beldomenico, P., Burthe, S., Paterson, S. and Begon, M. (2010). Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243246.Google Scholar
Valkiūnas, G. (2004). Avian Malarial Parasites and other Haemosporidia. Taylor and Francis Publishing, London.Google Scholar
Valkiūnas, G., Bairlein, F., Iezhova, T. and Dolnik, O. V. (2004). Factors affecting the relapse of haemoproteus belopolskyi infections and the parasitaemia of Trypanosoma spp. in a naturally infected European songbird, the blackcap, Sylvia atricapilla . Parasitology Research 93, 218222.Google Scholar
Valkiūnas, G., Anwar, A. M., Atkinson, C. T., Greiner, E. C., Paperna, I. and Peirce, M. A. (2005). What distinguishes malaria parasites from other pigmented haemosporidians? Trends in Parasitology 21, 357358.Google Scholar
Valkiūnas, G., Iezhova, T. A., Carlson, J. S. and Sehgal, R. N. M. (2011). Two new Trypanosoma species from African birds, with notes on the taxonomy of avian trypanosomes. Journal of Parasitology 97, 924930.Google Scholar
Valkiūnas, G., Kazlauskienė, R., Bernotienė, R., Bukauskaitė, D., Palinauskas, V. and Iezhova, T. A. (2014). Haemoproteus infections (Haemosporida, Haemoproteidae) kill bird-biting mosquitoes. Parasitology Research 113, 10111018.Google Scholar
Van Dyken, M., Bolling, B., Moore, J. L., Blair, C., Beaty, B., Black, W. C. and Foy, B. (2006). Molecular evidence for trypanosomatids in Culex mosquitoes collected during a West Nile virus survey. International Journal for Parasitology 36, 10151023.Google Scholar
Votýpka, J. and Svobodová, M. (2004). Trypanosoma avium: experimental transmission from black flies to canaries. Parasitology Research 92, 147151.CrossRefGoogle ScholarPubMed
Votýpka, J., Lukeš, J. and Oborník, M. (2004). Phylogenetic relationship of Trypanosoma corvi with other avian trypanosomes. Acta Protozoologica 43, 225231.Google Scholar
Votýpka, J., Szabova, J., Radrova, J., Zidkova, L. and Svobodová, M. (2012). Trypanosoma culicavium sp. nov., an avian trypanosome transmitted by Culex mosquitoes. International Journal of Systematic and Evolutionary Microbiology 62, 745754.Google Scholar
Zídková, L., Cepicka, I., Szabová, J. and Svobodová, M. (2012). Biodiversity of avian trypanosomes. Infection, Genetics and Evolution 12, 102112.Google Scholar
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