High prevalence of blood parasites in social birds from a neotropical savanna in Brazil
Alan Fecchio A F , Marcos Robalinho Lima B , Patrícia Silveira C , Érika Martins Braga D and Miguel Ângelo Marini E
+ Author Affiliations
- Author Affiliations
A Programa de Pós-graduação em Biologia Animal, Universidade de Brasília, Brasília, DF 70919-970, Brazil.
B Programa de Pós-graduação em Ecologia, Universidade de Brasília, Brasília, DF 70910-900, Brazil.
C Programa de Pós-graduação em Parasitologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil.
D Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil.
E Departamento de Zoologia, ICB, Universidade de Brasília, Brasília, DF 70910-900, Brazil.
F Corresponding author. Email: alanfecchio@yahoo.com.br
Emu 111(2) 132-138 https://doi.org/10.1071/MU10063
Submitted: 23 July 2010 Accepted: 14 December 2010 Published: 3 May 2011
Abstract
Blood parasites play a fundamental role in the ecology and evolution of passerine birds because they are able to affect the fitness and survival of their hosts. The prevalence of avian malarial parasites among host species can vary from 0 to 100% but the ecological and evolutionary reasons for this variation are not clear. In this study we tested if height or type of nest, body mass or social system, which we believe are variables associated with exposure of hosts to vectors, could explain the variation in the prevalence of blood parasites in a bird community from the Cerrado biome of central Brazil. We found a significant positive correlation between nest-height and prevalence of Haemoproteus, which is consistent with the hypothesis linking prevalence of blood parasites with nesting stratum in North American birds. We also found evidence for increased levels of parasitism by Haemoproteus in neotropical birds that live in groups and breed cooperatively and increased levels of parasitism by Plasmodium in species that nest in cavities or closed cups. We suggest that reproductive and behavioural parameters of hosts may be responsible for their differential exposure to vectors and that these parameters may therefore be able to indicate interspecific variation in the prevalence of blood parasites in other bird communities.
Additional keywords: avian malaria, breeding biology, haemosporidian parasites.
References
Alexander, R. D. (1974). The evolution of social behavior. Annual Review of Ecology and Systematics 5, 325–383.| The evolution of social behavior.Crossref | GoogleScholarGoogle Scholar |
Atkinson, C. T., and van Riper, C. III (1991). Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In ‘Bird–Parasite Interactions: Ecology, Evolution and Behavior’. (Eds J. E. Loye and M. Zuk.) pp. 19–48. (Oxford University Press: Oxford, MA.)
Bennett, G. F. (1993). Phylogenetic distribution and possible evolution of the avian species of the Haemoproteidae. Systematic Parasitology 26, 39–44.
| Phylogenetic distribution and possible evolution of the avian species of the Haemoproteidae.Crossref | GoogleScholarGoogle Scholar |
Bennett, G. F., and Coombs, R. F. (1975). Ornithophilic vectors of avian hematozoa in insular Newfoundland. Canadian Journal of Zoology 53, 1241–1246.
| Ornithophilic vectors of avian hematozoa in insular Newfoundland.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE28%2FptVSqtQ%3D%3D&md5=f160eefbd6c3db571339554a67acfc81CAS | 1203812PubMed |
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, 261–273.
| Blood parasites of birds in Algonquin Park, Canada, and a discussion of their transmission.Crossref | GoogleScholarGoogle Scholar |
Bennett, G. F., Blancou, J., White, E. M., and Williams, N. A. (1978). Blood parasites of some birds from Senegal. Journal of Wildlife Diseases 14, 67–73.
| 1:STN:280:DyaE1c7jtlWrug%3D%3D&md5=c81712c62ae20a4afb04249209ee0b98CAS | 633519PubMed |
Bennett, G. F., Bishop, M. A., and Peirce, M. A. (1993). Checklist of the avian species of Plasmodium Marchiafava & Celli, 1885 (Apicomplexa) and their distribution by avian family and Wallacean life zones. Systematic Parasitology 26, 171–179.
| Checklist of the avian species of Plasmodium Marchiafava & Celli, 1885 (Apicomplexa) and their distribution by avian family and Wallacean life zones.Crossref | GoogleScholarGoogle Scholar |
Bennett, G. F., Peirce, M. A., and Earlé, R. A. (1994). An annotated checklist of the valid avian species of Haemoproteus, Leucocytozoon (Apicomplexa : Haemosporida) and Hepatozoon (Apicomplexa : Haemogregarinidae). Systematic Parasitology 29, 61–73.
Bensch, S., Stjernman, M., Hasselquist, D., Örjan, 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. Series B. Biological Sciences 267, 1583–1589.
| Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1Oiurw%3D&md5=3e15e034c86d852be54e63607b6d34eaCAS |
Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H., and White, J. S. S. (2009). Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127–135.
| Generalized linear mixed models: a practical guide for ecology and evolution.Crossref | GoogleScholarGoogle Scholar |
Brown, C. R., and Brown, M. B. (1986). Ectoparasitism as a cost of colonialitv in Cliff Swallows (Hirundo pyrrhonota). Ecology 67, 1206–1218.
| Ectoparasitism as a cost of colonialitv in Cliff Swallows (Hirundo pyrrhonota).Crossref | GoogleScholarGoogle Scholar |
Eiten, G. (1993). Vegetação do Cerrado. In ‘Cerrado: Caracterização, Ocupação e Perspectivas’. (Ed. M. N. Pinto.) pp. 17–73. (Editora Universidade de Brasília: Brasília.)
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, 1044–1047.
| Detecting avian malaria: an improved polymerase chain reaction diagnostic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVWjsrg%3D&md5=e9d64eaf7d9a0251a76497daccc56835CAS | 14627154PubMed |
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. American Naturalist 165, 466–480.
| Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles.Crossref | GoogleScholarGoogle Scholar | 15791538PubMed |
Fecchio, A., Marini, M. Â., and Braga, É. M. (2007). Baixa prevalência de hemoparasitos em aves silvestres no Cerrado do Brasil. Neotropical Biology and Conservation 2, 127–135.
Garvin, M. C., and Greiner, E. C. (2003). Ecology of Culicoides (Diptera : Ceratopogonidae) in southcentral Florida and experimental Culicoides vectors of the avian hematozoan Haemoproteus danilewskyiruse. Journal of Wildlife Diseases 39, 170–178.
| 12685081PubMed |
Garvin, M. C., and Remsen, J. V. (1997). An alternative hypothesis for heavier parasite loads of brightly colored birds: exposure at the nest. Auk 114, 179–191.
Gibson, G., and Torr, S. J. (1999). Visual and olfactory responses of haematophagous Diptera to host stimuli. Medical and Veterinary Entomology 13, 2–23.
| Visual and olfactory responses of haematophagous Diptera to host stimuli.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M3htVKnuw%3D%3D&md5=8a9fe75d0c1e62fe6296bb551b1ce98aCAS | 10194745PubMed |
Greiner, E. C., Bennett, G. F., White, E. M., and Coombs, R. F. (1975). Distribution of the avian hematozoa of North America. Canadian Journal of Zoology 53, 1762–1787.
| Distribution of the avian hematozoa of North America.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE287hsF2rtA%3D%3D&md5=b2a2c9a12abe3431544972c094997b72CAS | 1212636PubMed |
Hakkarainen, H., Ilmonen, P., Koivunen, V., and Korpimäki, E. (1998). Blood parasites and nest defense behaviour of Tengmalm’s Owls. Oecologia 114, 574–577.
| Blood parasites and nest defense behaviour of Tengmalm’s Owls.Crossref | GoogleScholarGoogle Scholar |
Hamilton, W. D., and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387.
| Heritable true fitness and bright birds: a role for parasites?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3s%2Fhs1Kgsw%3D%3D&md5=940c6404ffc33d7ce2db7a4b1af170dbCAS | 7123238PubMed |
Henry, L. G., and Adkins, T. R. J. (1975). Vertical distribution of biting midges in coastal South Carolina. Annals of the Entomological Society of America 68, 321–324.
Ishtiaq, F., Gering, E., Rappole, J. H., Rahmani, A. R., Jhala, Y. V., Dove, C. J., Milensky, C., Olson, S. L., Peirce, M. A., and Fleischer, R. C. (2007). Prevalence and diversity of avian hematozoan. Journal of Wildlife Diseases 43, 382–398.
| 17699077PubMed |
Jovani, R., and Tella, J. L. (2006). Parasite prevalence and sample size: misconceptions and solutions. Trends in Parasitology 22, 214–218.
| Parasite prevalence and sample size: misconceptions and solutions.Crossref | GoogleScholarGoogle Scholar | 16531119PubMed |
Korpimäki, E., Hakkarainen, H., and Bennett, G. F. (1993). Blood parasites and success of Tengmalm’s Owls: detrimental effects on females but not on males? Functional Ecology 7, 420–426.
| Blood parasites and success of Tengmalm’s Owls: detrimental effects on females but not on males?Crossref | GoogleScholarGoogle Scholar |
Latta, S. C., and Ricklefs, R. E. (2010). Prevalence patterns of avian haemosporida on Hispaniola. Journal of Avian Biology 41, 25–33.
| Prevalence patterns of avian haemosporida on Hispaniola.Crossref | GoogleScholarGoogle Scholar |
Lehane, M. J. (2005). ‘The Biology of Blood-sucking in Insects.’ (Cambridge University Press: New York.)
Loye, J. E., and Carroll, S. P. (1991). Nest ectoparasite abundance and Cliff Swallow colony site selection, nestling development, and departure time. In ‘Bird–Parasite Interactions: Ecology, Evolution and Behavior’. (Eds J. E. Loye and M. Zuk.) pp. 69–92. (Oxford University Press: Oxford, MA.)
Martínez-de la Puente, J., Merino, S., Lobato, E., Aguilar, J. R., Cerro, S., Castañeda, R. R., and Moreno, J. (2009). Does weather affect biting fly abundance in avian nests? Journal of Avian Biology 40, 653–657.
| Does weather affect biting fly abundance in avian nests?Crossref | GoogleScholarGoogle Scholar |
Martínez-de la Puente, J., Merino, S., Tomás, G., Moreno, J., Morales, J., Lobato, E., Fraile, S. G., and Belda, E. B. (2010). The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment. Biology Letters 6, 663–665.
| The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment.Crossref | GoogleScholarGoogle Scholar | 20181556PubMed |
Martinsen, E. S., Perkins, S. L., and Schal, J. J. (2008). A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Molecular Phylogenetics and Evolution 47, 261–273.
| A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktV2jtrs%3D&md5=ca4debeb017c846770b99efab80d6c3cCAS | 18248741PubMed |
Marzal, A., de Lope, F., Navarro, C., and Møller, A. P. (2005). Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142, 541–545.
| Malarial parasites decrease reproductive success: an experimental study in a passerine bird.Crossref | GoogleScholarGoogle Scholar | 15688214PubMed |
Mellor, P. S., Boorman, J., and Baylis, M. (2000). Culicoides biting midges: their role as arbovirus vectors. Annual Review of Entomology 45, 307–340.
| Culicoides biting midges: their role as arbovirus vectors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVequ7k%3D&md5=7ca40aaffe1715ea03dd244abac4673cCAS | 10761580PubMed |
Merino, S., Moreno, J., Sanz, J. J., and Arriero, E. (2000). Are avian blood parasites pathogenic in the wild? A medication experiment in Blue Tits (Parus caeruleus). Proceedings of the Royal Society of London. Series B. Biological Sciences 267, 2507–2510.
| Are avian blood parasites pathogenic in the wild? A medication experiment in Blue Tits (Parus caeruleus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzjslSqtg%3D%3D&md5=e254b8b4a0fe834468522cc7f29925b6CAS |
Møller, A. P. (1987). Advantages and disadvantages of coloniality in the swallow, Hirundo rustica. Animal Behaviour 35, 819–832.
| Advantages and disadvantages of coloniality in the swallow, Hirundo rustica.Crossref | GoogleScholarGoogle Scholar |
Møller, A. P., and Nielsen, J. T. (2007). Malaria and risk of predation: a comparative study of birds. Ecology 88, 871–881.
| Malaria and risk of predation: a comparative study of birds.Crossref | GoogleScholarGoogle Scholar | 17536704PubMed |
Oliveira-Filho, A. T., and Ratter, J. A. (2002). Vegetation physiognomies and woody flora of the Cerrado biome. In ‘The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna’. (Eds P. S. Oliveira and R. J. Marquis.) pp. 91–120. (Columbia University Press: New York.)
Paterson, S., and Lello, J. (2003). Mixed models: getting the best use of parasitological data. Trends in Parasitology 19, 370–375.
| Mixed models: getting the best use of parasitological data.Crossref | GoogleScholarGoogle Scholar | 12901939PubMed |
Peirce, M. A. (1981). Distribution and host-parasite check-list of the haematozoa of birds in western Europe. Journal of Natural History 15, 419–458.
| Distribution and host-parasite check-list of the haematozoa of birds in western Europe.Crossref | GoogleScholarGoogle Scholar |
Poulin, R. (1991). Group-living and infestation by ectoparasites in passerines. Condor 93, 418–423.
| Group-living and infestation by ectoparasites in passerines.Crossref | GoogleScholarGoogle Scholar |
R Development Core Team (2008). ‘R: A Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna, Austria.) Available at http://www.R-project.org [Verified 10 March 2011].
Rätti, O., Dufva, R., and Alatalo, R. V. (1993). Blood parasites and male fitness in Pied Flycatcher. Oecologia 96, 410–414.
| Blood parasites and male fitness in Pied Flycatcher.Crossref | GoogleScholarGoogle Scholar |
Read, A. F. (1991). Passerine polygyny: a role for parasites? American Naturalist 138, 434–459.
| Passerine polygyny: a role for parasites?Crossref | GoogleScholarGoogle Scholar |
Ricklefs, R. E. (1992). Embryonic development period and the prevalence of avian blood parasites. Proceedings of the National Academy of Sciences of the United States of America 89, 4722–4725.
| Embryonic development period and the prevalence of avian blood parasites.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383mt1Gisw%3D%3D&md5=76685c3b056bd179abe7ff754140671aCAS | 1584808PubMed |
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, 1254–1266.
| Malaria prevalence and white-blood-cell response to infection in a tropical and in a temperate thrush.Crossref | GoogleScholarGoogle Scholar |
Ricklefs, R. E., Fallon, S. M., and Bermingham, E. (2004). Evolutionary relationships, cospeciation and host switching in avian malaria parasites. Systematic Biology 53, 111–119.
| Evolutionary relationships, cospeciation and host switching in avian malaria parasites.Crossref | GoogleScholarGoogle Scholar | 14965906PubMed |
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, 543–559.
| Community relationships of avian malaria parasites in southern Missouri.Crossref | GoogleScholarGoogle Scholar |
Scheuerlein, A., and Ricklefs, R. E. (2004). Prevalence of blood parasites in European passerine birds. Proceedings of the Royal Society of London. Series B. Biological Sciences 271, 1363–1370.
| Prevalence of blood parasites in European passerine birds.Crossref | GoogleScholarGoogle Scholar |
Siikamäki, P., Rätti, O., Hovi, M., and Bennett, G. F. (1997). Association between haematozoan infections and reproduction in the Pied Flycatcher. Functional Ecology 11, 176–183.
| Association between haematozoan infections and reproduction in the Pied Flycatcher.Crossref | GoogleScholarGoogle Scholar |
Sodhi, N. S., Koh, L. P., Peh, K. S. H., Tan, H. T. W., Chazdon, R. L., Corlett, R. T., Lee, T. M., Colwell, R. K., Brook, B. W., Sekercioglu, C. H., and Bradshaw, C. J. A. (2008). Correlates of extinction proneness in tropical angiosperms. Diversity & Distributions 14, 1–10.
| Correlates of extinction proneness in tropical angiosperms.Crossref | GoogleScholarGoogle Scholar |
Sol, D., Jovani, R., and Torres, J. (2000). Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23, 307–314.
| Geographical variation in blood parasites in feral pigeons: the role of vectors.Crossref | GoogleScholarGoogle Scholar |
Sundberg, J. (1995). Parasites, plumage coloration and reproductive success in the Yellowhammer, Emberiza citrinella. Oikos 74, 331–339.
| Parasites, plumage coloration and reproductive success in the Yellowhammer, Emberiza citrinella.Crossref | GoogleScholarGoogle Scholar |
Sutcliffe, J. F. (1986). Black fly host location: a review. Canadian Journal of Zoology 64, 1041–1053.
| Black fly host location: a review.Crossref | GoogleScholarGoogle Scholar |
Takken, W., and Knols, B. G. J. (1999). Odor-mediated behavior of Afrotropical malaria mosquitoes. Annual Review of Entomology 44, 131–157.
| Odor-mediated behavior of Afrotropical malaria mosquitoes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXpvFKhtA%3D%3D&md5=d5e3959b10af4ff0cbe8f6121dfa3125CAS | 9990718PubMed |
Tella, J. L. (2002). The evolutionary transition to coloniality promotes higher blood parasitism in birds. Journal of Evolutionary Biology 15, 32–41.
| The evolutionary transition to coloniality promotes higher blood parasitism in birds.Crossref | GoogleScholarGoogle Scholar |
Tomás, G., Merino, S., Martínez-de la Puente, J., Moreno, J., Morales, J., and Lobato, E. (2008). Determinants of abundance and effects of blood-sucking flying insects in the nest of a hole-nesting bird. Oecologia 156, 305–312.
| Determinants of abundance and effects of blood-sucking flying insects in the nest of a hole-nesting bird.Crossref | GoogleScholarGoogle Scholar | 18317817PubMed |
Valkiūnas, G. (2005). ‘Avian Malaria Parasites and Other Haemosporidia.’ (CRC Press: Boca Raton, FL.)
Valkiūnas, G., Iezhova, T. A., Križanauskienė, A., Palinauskas, V., Sehgal, R. N. M., and Bensch, S. (2008). A comparative analysis of microscopy and PCR based detection methods for blood parasites. Journal of Parasitology 94, 1395–1401.
| A comparative analysis of microscopy and PCR based detection methods for blood parasites.Crossref | GoogleScholarGoogle Scholar | 18576856PubMed |
van Riper, C., van Riper, S. G., Goff, M. L., and Laird, M. (1986). The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 327–344.
| The epizootiology and ecological significance of malaria in Hawaiian land birds.Crossref | GoogleScholarGoogle Scholar |
Warner, R. E. (1968). The role of introduced diseases in the extinction of the endemic Hawaiian aviafauna. Condor 70, 101–120.
| The role of introduced diseases in the extinction of the endemic Hawaiian aviafauna.Crossref | GoogleScholarGoogle Scholar |
White, E. M., Greiner, E. C., Bennet, G. F., and Herman, C. M. (1978). Distribution of the hematozoa of Neotropical birds. Revista de Biologia Tropical 26, 43–102.
| 108771PubMed |