Skip to main content Accessibility help

Structure and organization of an avian haemosporidian assemblage in a Neotropical savanna in Brazil



Studies on avian haemosporidia are on the rise, but we still lack a basic understanding of how ecological and evolutionary factors mold the distributions of haemosporidia among species in the same bird community. We studied the structure and organization of a local avian haemosporidian assemblage (genera Plasmodium and Haemoproteus) in the Cerrado biome of Central Brazil for 5 years. We obtained 790 blood samples from 54 bird species of which 166 (21%) were infected with haemosporidians based on molecular diagnostics. Partial sequences of the parasite cytochrome b gene revealed 18 differentiated avian haemosporidian lineages. We also analysed the relationship of life-history traits (i.e., nesting height, migration status, nest type, sociality, body mass, and embryo development period) of the 14 most abundant bird species with the prevalence of avian haemosporidia. It was found that host species that bred socially presented a higher prevalence of Haemoproteus (Parahaemoproteus) than bird species that bred in pairs. Thus, aspects of host behaviour could be responsible for differential exposure to vectors. The assemblage of avian haemosporidia studied here also confirms a pattern that is emerging in recent studies using molecular markers to identify avian haemosporidians, namely that many lineages are host generalists.


Corresponding author

*Corresponding author: Universidade Federal do Amazonas, Departamento de Biologia, Laboratório de Evolução e Genética Animal, Manaus AM, 69077-000. Brazil. Tel: + 55 92 36474233. Fax: + 55 92 36474229. E-mail:


Hide All
Alexander, R. D. (1974). The evolution of social behavior. Annual Review of Ecology and Systematics 5, 325383.
Arriero, E. and Møller, A. P. (2008). Host ecology and life-history traits associated with blood parasite species richness in birds. Journal of Evolutionary Biology 21, 15041513.
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.
Bates, D. and Maechler, M. (2010). lme4: Linearmixed-effects Models using S4 Classes. R package Version 0.999375–34.
Bennett, G. F. and Fallis, A. M. (1960). Blood parasites of birds in Algonquin Park, Canada, and a discussion of their transmission. Canadian Journal of Zoology 38, 261273.
Bensch, S., Pérez-Tris, J., Waldenström, J. and Hellgren, O. (2004). Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: Multiple cases of cryptic speciation? Evolution 58, 16171621.
Bensch, S., Stjernman, M., Hasselquist, D., Östman, Ö., 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 of the Royal Society of London, B 267, 15831589.
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach. Springer, New York, USA.
Burnham, K. P., Anderson, D. R. and Huyvaert, K. P. (2011). AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behavioral Ecology and Sociobiology 65, 2335.
Côté, I. M. and Poulin, R. (1995). Parasitism and group size in social animals: a meta-analysis. Behavioral Ecology 6, 159165.
Crawley, M. J. (2007). R Book. John Wiley and Sons Ltd, Chichester, UK.
Davies, C. R., Ayres, J. M., Dye, C. and Deane, L. M. (1991). Malaria infection rate of Amazonian primates increases with body weight and group size. Functional Ecology 5, 655662.
Derreik, J. G. B., Snell, A. E. and Slaney, D. (2005). Vertical distribution of adult mosquitoes in native forest in Auckland, New Zealand. Journal of Vector Ecology 30, 334336.
Escalante, A. A., Freeland, D. E., Collins, W. E. and Lal, A. A. (1998). The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proceedings of the National Academy of Sciences, US A 95, 81248129.
Fallon, S. M., Bermingham, E. and Ricklefs, R. E. (2005). Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. The American Naturalist 165, 466480.
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 85, 10441047.
Fecchio, A., Lima, M. R., Silveira, P., Braga, É. M. and Marini, M. Â. (2011). High prevalence of blood parasites in social birds from a neotropical savanna in Brazil. Emu 111, 132138.
Futuyma, D. J. and Moreno, G. (1988) The evolution of ecological specialization. Annual Review of Ecology and Systematics 19, 207233.
Garvin, M. C. and Remsen, J. V. Jr. (1997). An alternative hypothesis for heavier parasite loads of brightly colored birds: exposure at the nest. The Auk 114, 179191.
Gelman, A. (2008). Scaling regression inputs by dividing by two standard deviations. Statistics in Medicine 27, 28652873.
Hellgren, O., Pérez-Tris, J. and Bensch, S. (2009). A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90, 28402849.
Jovani, R. and Tella, J. L. (2006). Parasite prevalence and sample size: misconceptions and solutions. Trends in Parasitology 22, 214218.
Krasnov, B. R. (2008). Functional and Evolutionary Ecology of Fleas: A Model for Ecological Parasitology. Cambridge University Press, New York, USA.
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. and Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 29472948.
Latta, S. C. and Ricklefs, R. E. (2010). Prevalence patterns of avian haemosporida on Hispaniola. Journal of Avian Biology 41, 2533.
Lehane, M. (2005). The Biology of Blood-Sucking in Insects. Cambridge University Press, New York, USA.
Maia, J. M. F. and Baptista, G. M. M. (2008). Clima. In Águas Emendadas (ed. Fonseca, F. E.), pp. 101109. Athalaia Gráfica e Editora LTDA, Brasília.
Mazerolle, M. J. (2004). Making sense out of Akike's information criterion (AIC): its use and interpretation in model selection and inference from ecological data. Thesis, Appendix 1, Université Laval, Québec, Canada.
Mazerolle, M. J. (2010). AICcmodavg: Model Selection and Multimodel Inference Based on (Q)AIC(c). R package version 1.07.
Møller, A. P. (1998). Evidence of larger impact of parasites on hosts in the tropics: investment in immune function within and outside the tropics. Oikos 82, 265270.
Mooring, M. S. and Hart, B. L. (1992). Animal grouping for protection from parasites: selfish herd and encounter-dilution effects. Behaviour 123, 173193.
Olival, K. J., Stiner, E. O. and Perkins, S. L. (2007). Detection of Hepatocystis sp. in Southeast Asian flying foxes (Pteropodidae) using microscopic and molecular methods. Journal of Parasitology 93, 15381540.
Outlaw, D. C. and Ricklefs, R. E. (2009). On the phylogenetic relationships of haemosporidian parasites from raptorial birds (Falconiformes and Strigiformes). Journal of Parasitology 95, 11711176.
Outlaw, D. C. and Ricklefs, R. E. (2011). Rerooting the evolutionary tree of malaria parasites. Proceedings of the National Academy of Sciences, USA 108, 1318313187.
Palacios, M. G. and Martin, T. E. (2006). Incubation period and immune function: a comparative field study among coexisting birds. Oecologia 146, 505512.
Perkins, S. L. (2000). Species concepts and malaria parasites: detecting a cryptic species of Plasmodium. Proceedings of the Royal Society of London, B 267, 23452351.
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.
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ, USA.
Poulin, R. and Mouillot, D. (2005). Combining phylogenetic and ecological information into a new index of host specificity. Journal of Parasitology 91, 511514.
R Development Core Team (2008). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Read, A. F. (1991). Passerine polygyny: a role for parasites? The American Naturalist 138, 434459.
Remsen, J. V. Jr., Cadena, C. D., Jaramillo, A., Nores, M., Pacheco, J. F., Pérez-Emán, J., Robbins, M. B., Stiles, F. G., Stotz, D. F. and Zimmer, K. J. (2011). A Classification of the Bird Species of South America. American Ornithologists’ Union. ∼ Remsen/SACCBaseline.html.
Ricklefs, R. E. (1992). Embryonic development period and the prevalence of avian blood parasites. Proceedings of the National Academy of Sciences, USA 89, 47224725.
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.
Ricklefs, R. E., Fallon, S. M. and Bermingham, E. (2004). Evolutionary relationships, cospeciation and host switching in avian malaria parasites. Systematic Biology 53, 111119.
Ricklefs, R. E., Swanson, B. L., Fallon, S. M., Martinez-Abrain, A., Scheuerlein, A., Gray, J. and Latta, S. C. (2005). Community relationships of avian malaria parasites in southern Missouri. Ecological Monographs 75, 543559.
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.
Scheuerlein, A. and Ricklefs, R. E. (2004). Prevalence of blood parasites in European passerine birds. Proceedings of the Royal Society of London, B 271, 13631370.
Snow, W. F. and Wilkes, T. J. (1977). Age composition and vertical distribution of mosquito populations in the Gambia, West Africa. Journal of Medical Entomology 13, 507513.
Stamatakis, A., Hoover, P. and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758771.
Tella, J. L. (2002). The evolutionary transition to coloniality promotes higher blood parasitism in birds. Journal of Evolutionary Biology 15, 3241.
Tella, J. L., Blanco, G., Forero, M. G., Gajón, Á., Donázar, J. A. and Hiraldo, F. (1999). Habitat, world geographic range, and embryonic development of hosts explain the prevalence of avian hematozoa at small spatial and phylogenetic scales. Proceedings of the National Academy of Sciences, USA 96, 17851789.
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidian. CRC Press, Boca Raton, FL, USA.
Ventim, R., Morais, J., Pardal, S., Mendes, L., Ramos, J. A. and Pérez-Tris, J. (2012). Host-parasite associations and host-specificity in haemoparasites of reed bed passerines. Parasitology 139, 310316.
Veras, R. S. and Castellón, E. G. (1998). Culicoides Latreille (Diptera, Ceratopogonidae) in Brazilian Amazon. V. Efficiency of traps and baits and vertical stratification in the Forest Reserve Adolpho Ducke. Revista Brasileira de Zoologia 15, 145152.
Waldenström, J., Bensch, S., Kiboi, S., Hasselquist, D. and Ottoson, U. (2002). Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology 11, 15451554.
Yezerinac, S. M. and Weatherhead, P. J. (1995). Plumage coloration, differential attraction of vectors and haematozoa infections in birds. Journal of Animal Ecology 64, 528537.
Zurr, A. F., Ieno, E. N. and Elphick, C. S. (2010). A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 314.



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed