Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-22T17:02:10.181Z Has data issue: false hasContentIssue false

Diversity of avian haemosporidians in arid zones of northern Venezuela

Published online by Cambridge University Press:  12 March 2012

NAYARA O. BELO*
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
ADRIANA RODRÍGUEZ-FERRARO
Affiliation:
Department of Biology, University of Missouri-St Louis, St Louis, Missouri, USA Departamento de Estudios Ambientales, Universidad Simón Bolívar, Sartenejas, Venezuela
ERIKA M. BRAGA
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
ROBERT E. RICKLEFS
Affiliation:
Department of Biology, University of Missouri-St Louis, St Louis, Missouri, USA
*
*Corresponding author: Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627. Instituto de Ciências Biológicas, Departamento de Parasitologia. 31270-910. Belo Horizonte, MG.Brazil. Tel: +5531 34992876. Fax: +5531 34992790. E-mail: [email protected]

Summary

Arid zones of northern Venezuela are represented by isolated areas, important from an ornithological and ecological perspective due to the occurrence of restricted-range species of birds. We analysed the prevalence and molecular diversity of haemosporidian parasites of wild birds in this region by screening 527 individuals (11 families and 20 species) for parasite mitochondrial DNA. The overall prevalence of parasites was 41%, representing 17 mitochondrial lineages: 7 of Plasmodium and 10 of Haemoproteus. Two parasite lineages occurred in both the eastern and western regions infecting a single host species, Mimus gilvus. These lineages are also present throughout northern and central Venezuela in a variety of arid and mesic habitats. Some lineages found in this study in northern Venezuela have also been observed in different localities in the Americas, including the West Indies. In spite of the widespread distributions of some of the parasite lineages found in northern Venezuela, several, including some that are relatively common (e.g. Ven05 and Ven06), have not been reported from elsewhere. Additional studies are needed to characterize the host and geographical distribution of avian malaria parasite lineages, which will provide a better understanding of the influence of landscape, vector abundance and diversity, and host identity on haemosporidian parasite diversity and prevalence.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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

Atkinson, C. T. (1988). Epizootiology of Haemoproteus meleagridis (Protozoa, Haemosporina) in Florida: potential vectors and prevalence in naturally infected Culicoides (Diptera: Ceratopogonidae). Journal of Medicine Entomology 25, 3944.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. Proceeding Biology Science 273, 29352944.Google Scholar
Belo, N. O., Passos, L. F., Junior, L. M. C., Goulart, C. E., Sherlock, T. M. and Braga, E. M. (2009). Avian malaria in captive psittacine birds: Detection by microscopy and 18S rRNA gene amplification. Preventive Veterinary Medicine 88, 220224.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
Bennett, G. F., Earle, R. A., Peirce, M. A., Huchzermeyer, F. W. and Squires-Parsons, D. (1991). Avian Leucocytozoidae: the leucocytozoids of the Phasianidae sensu latu. Journal of Natural History 25, 14071428.Google Scholar
Bennett, G. F. and Lopes, O. S. (1980). Blood parasites of some birds from São Paulo state, Brazil. Memórias do Instituto Oswaldo Cruz 75, 117134.CrossRefGoogle Scholar
Colwell, R. K. (2008). EstimateS: Statistical estimation of species richness and shared species from samples. Version 8.2, Department of Ecology and Evolutionary Biology University of Connecticut, Storrs, CT. http://purl.oclc.org/estimates.Google Scholar
Colwell, R. K., Mao, C. X. and Chang, J. (2004). Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85, 27172727.CrossRefGoogle Scholar
Durrant, K. L., Beadell, J. S., Ishtiaq, F., Graves, G. R., Olson, S. L., Gering, E., Peirce, M. A., Milensky, C. M., Schmidt, B. K., Gebhard, C. and Fleischer, R. C. (2006). Avian hematozoa in South America: a comparison of temperate and tropical zones. Ornithology Monograph 60, 98111.CrossRefGoogle Scholar
Fallon, S. M., Ricklefs, R. E., Swanson, B. L. and Bermingham, E. (2003). Detecting avian malaria: an improved PCR diagnostic. Journal of Parasitology 89, 10441047.CrossRefGoogle Scholar
Fallon, S., Ricklefs, R. E., Latta, S. and Bermingham, E. (2004). Temporal stability of insular avian malarial parasite communities. Proceedings of the Royal Society of London, B 271, 493500.CrossRefGoogle ScholarPubMed
Garnham, P. C. (1966). Malaria Parasites and other Haemosporidia. Blackwell Science, Oxford, UK.Google Scholar
Gaunt, A. and Oring, L. W. (1997). Guidelines to the Use of Wild Birds in Research. The Ornithological Council, Washington D. C., USA.Google Scholar
Greiner, E. C., Bennett, G. F., White, E. F. and Coombs, R. F. (1975). Distribution of the avian hematozoa of North America. Canadian Journal of Zoology 53, 17621787.CrossRefGoogle ScholarPubMed
Hatchwell, B. J., Wood, M. J., Anwar, M. and Perrins, C. M. (2000). The prevalence and ecology of the haematozoan parasites of European blackbirds, Tundrus merula. Canadian Journal of Zoology 78, 684687.CrossRefGoogle Scholar
Heinemann, S. J. and Belkin, J. N. (1978). Collection records of the project ‘Mosquitoes of Middle America.’ 11. Venezuela (VZ); Guianas: French Guiana (FG, FGC), Guyana (GUY), Surinam (SUR). Mosquito Systematics 10, 365459.Google Scholar
Hughes, V. L. and Randolph, S. E. (2001). Testosterone increases the transmission potential of tick-borne parasites. Parasitology 123, 365371.CrossRefGoogle ScholarPubMed
Ishak, H. D., Dumbacher, J. P., Anderson, N. L., Keane, J. J., Valkiūnas, G., Haig, S. M., Tell, L. A. and Sehgal, R. N. (2008). Blood parasites in owls with conservation implications for the Spotted Owl (Strix occidentalis). PLoSONE 3, e2304.CrossRefGoogle ScholarPubMed
Kirkpatrick, C. E. and Suthers, H. B. (1988). Epizootiology of blood parasite infections in passefine birds from central New Jersey. Canadian Journal of Zoology 66, 23742382.Google Scholar
Lachish, S., Knowles, S. C., Alves, R., Wood, M. J. and Sheldon, B. C. (2011). Infection dynamics of endemic malaria in a wild bird population: parasite species-dependent drivers of spatial and temporal variation in transmission rates. The Journal of Animal Ecology 80, 12071216.CrossRefGoogle Scholar
Levin, I. I., Outlaw, D. C., Hernan Vargas, F. and Parker, P. G. (2009). Plasmodium blood parasite found in endangered Galapagos penguins (Spheniscus mendiculus). Biological Conservation 142, 3193195.CrossRefGoogle Scholar
Linley, J. R. (1985). Biting midges (Diptera: Ceratopogonidae) as vectors of nonviral animal pathogens. Journal of Medical Entomology 22, 589599.CrossRefGoogle ScholarPubMed
Lyon, B. (2003). Enhanced seasonal rainfall in northern Venezuela and the extreme events of December 1999. Journal of Climate 16, 23022306.CrossRefGoogle Scholar
Matta, N. E., Basto, N., Gutierrez, R., Rodríguez, O. A. and Greiner, E. C. (2004). Prevalence of blood parasites in Tyrannidae (Flycatchers) in the eastern plains of Colombia. Memórias do Instituto Oswaldo Cruz 99, 271274.CrossRefGoogle ScholarPubMed
McCurdy, D. G., Shutler, D., Mullie, A. and Forbes, M. R. (1998). Sex-biased parasitism of avian hosts: relations to blood parasite taxon and mating system. Oikos 82, 303312.CrossRefGoogle Scholar
Møller, A. P. and Saino, N. (1994). Parasites, immunology of hosts, and host sexual selection. Journal of Parasitology 80, 850858.CrossRefGoogle ScholarPubMed
Murata, K. (2002). Prevalence of blood parasites in Japanese wild birds. Journal of Veterinary Medical Science 64, 785790.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, 972978.CrossRefGoogle ScholarPubMed
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle ScholarPubMed
Ramírez-Albores, J. E. (2010). Bird biodiversity in natural and modified habitats in a landscape of the Central Depression of Chiapas, Mexico. Revista Biología Tropical 58, 511528.Google Scholar
Reiter, M. E. and Lapointe, D. A. (2009). Larval habitat for the avian malaria vector Culex quinquefasciatus (Diptera: Culicidae) in altered mid-elevation mesic-dry forests in Hawaii. Journal Vector Ecology 34, 208216.CrossRefGoogle Scholar
Reullier, J., Pérez-Tris, J., Bensch, S. and Secondi, J. (2006). Diversity, distribution and exchange of blood parasites meeting at an avian moving contact zone. Molecular Ecology 15, 753763.CrossRefGoogle ScholarPubMed
Ribeiro, S. F., Sebaio, F., Branquinho, F. C. S., Marini, M. A., Vago, A. R. and Braga, E. M. (2005). Avian malaria in Brazilian passerine birds: parasitism detected by nested PCR using DNA from stained blood smears. Parasitology 130, 261267.Google Scholar
Ricklefs, R. E. and Fallon, S. M. (2002). Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London, B 269, 885892.CrossRefGoogle ScholarPubMed
Ricklefs, R. E. and Outlaw, D. C. (2010). A molecular clock for malaria parasites. Science 329, 226229.CrossRefGoogle ScholarPubMed
Ricklefs, R. E., Swanson, B., Fallon, S. M., Martinez, A., Scheuerlein, A. and Latta, S. (2005). Community relationships of avian malaria parasites in southern Missouri. Ecological Monographs 75, 543559.Google Scholar
Rodríguez, O. A. and Matta, N. E. (2001). Blood parasites in some birds from eastern plains of Colombia. Memórias do Instituto Oswaldo Cruz 96, 11731176.CrossRefGoogle ScholarPubMed
Rodríguez-Ferraro, A. and Blake, J. (2008). Diversity patterns of bird assemblages in arid zones of northern Venezuela. Condor 110, 405420.CrossRefGoogle 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, 463470.Google Scholar
Sarmiento, G. (1972). Ecological and floristic convergences between seasonal plant formations of tropical and subtropical South America. Journal of Ecology 60, 367410.Google Scholar
Sarmiento, G. (1976). Evolution of arid vegetation in tropical America. In Evolution of Desert Biota (ed. Goodall, D. W.), pp. 6599. University of Texas Press, Austin, TX, USA.CrossRefGoogle Scholar
Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 26882690.CrossRefGoogle ScholarPubMed
Stattersfield, A., Crosby, M. J., Long, A. J. and Wege, D. C. (1998). Endemic Bird Areas of the World: Priorities for Biodiversity Conservation. BirdLife International, Cambridge, UK.Google Scholar
Szöllosi, E., Cichoń, M., Eens, M., Hasselquist, D., Kempenaers, B., Merino, S., Nilsson, J. Å., Rosivall, B., Rytkönen, S., Török, J., Wood, M. J. and Garamszegi, L. Z. (2011). Determinants of distribution and prevalence of avian malaria in blue tit populations across Europe: separating host and parasite effects. Journal of Evolutionary Biology 24, 20142024.CrossRefGoogle ScholarPubMed
Thompson, J. D., Gibson, T. J. and Plewniak, F. (1997). Clustal_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic acids Research 24, 48764882.CrossRefGoogle Scholar
Thomson, M. C., Mason, S. J. and Phindela, T. (2005). Use of rainfall and sea surface temperature monitoring for malaria early warning in Botswana. American Society of Tropical Medicine and Hygiene 73, 214221.CrossRefGoogle ScholarPubMed
Valkiūnas, G. (1997). Bird Haemosporida. Acta Zoologica Lituanica 3–5, 1607.Google Scholar
Valkiūnas, G., Salaman, P. and Iezhova, T. A. (2003). Paucity of Hematozoa in Colombian Birds. Journal of Wildlife Diseases 39, 445448.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Iezhova, T. A., Brooks, D. R., Hanelt, B., Brant, S. V., Sutherlin, M. E. and Causey, D. (2004). Additional observations on blood parasites of birds in Costa Rica. Journal of Wildlife Diseases 40, 555561.Google Scholar
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Zuk, M., (1996). Disease, endocrine-immune interactions, and sexual selection. Ecology 77, 10371042.CrossRefGoogle Scholar
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 10091024.Google Scholar
Weatherhead, P. J. and Bennett, G. F. (1992). Ecology of parasitism of brown headed cowbirds by haematozoa. Canadian Journal of Zoology 70, 17.Google Scholar
Weatherhead, P. J., Metz, K., Bennett, G. F. and Irwin, R. E. (1993). Parasite faunas, testosterone and secondary sexual traits in male red-winged blackbirds Agelaius phoeniceus. Behavioral Ecology and Sociobiology 33, 1223.Google Scholar
Winchell, E. J. (1978). Hematozoa of some birds of El Salvador. Journal of Parasitology 64, 558559.Google Scholar
White, E. M., Greiner, E. C., Bennett, G. F. and Herman, C. M. (1978). Distribution of the haematozoa of Neotropical birds. Revista de Biología Tropical 26, 43102.Google ScholarPubMed
Woodworth-Lynas, C. B., Caines, J. R. and Bennet, G. F. (1989). Prevalence of avian haematozoa in São Paulo, Brazil. Memorias Instituto Oswaldo Cruz 84, 515526.Google Scholar
Young, B. E., Garvin, M. C. and McDonald, D. B. (1993). Blood parasites in birds from Monteverde, Costa Rica. Journal of Wildlife Diseases 29, 555560.Google Scholar