Haemosporidian parasites in Antilophia galeata (Aves: Pipridae) in a Cerrado forest fragment
DOI:
https://doi.org/10.14393/BJ-v39n0a2023-53589Keywords:
Avian Malaria, Leukocytes, Parasite-host Relationship, Wild Birds.Abstract
Haemosporidian parasites can cause pathogenic infections, leading to death or a reduction in the physical and reproductive abilities of the host. Several studies have identified haemosporidian infections in neotropical bird communities, but few have been conducted in populations, relating the infection to the biological attributes of the species. To determine haemosporidian prevalence in a population of Antilophia galeata and to assess factors that may be associated with parasitaemia, we analysed blood smears of 62 individuals from a Cerrado forest fragment. For each individual, the body mass, length of tarsus, sex, presence/absence of brood patch and feather moult were recorded. In total, 33 (53.2%) individuals were infected with haemosporidian parasites, 32 (51.6%) were infected with Plasmodium spp. and one (1.61%) was infected with Haemoproteus sp. Parasitaemia was not related to seasons, sex, reproduction, moulting or body condition but correlated positively with total leucocyte count, suggesting that individuals may be effective in infection control. This population may be tolerant to haemosporidian parasites because, despite the high prevalence, parasitaemia was low and constant; this is a potentially chronic infection that showed no adverse effects on the parameters analysed in this population.
Downloads
References
ATKINSON, C.T., et al. Epizootiology of Haemoproteus meleagridis (Protozoa: Haemosporina) in Florida: seasonal transmission and vector abundance. Journal of Medical Entomology. 1998, 25(1), 45-51. https://doi.org/10.1093/jmedent/25.1.45
ATKINSON, C.T. and LA POINTE, D.A. Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. Journal of Avian Medicine and Surgery. 2009, 23(1), 53-63. https://doi.org/10.1647/2008-059.1
ATKINSON, C.T., et al. Parasitic Diseases of Wild Birds. Ames, Iowa: Wiley-Blackwell, 2009. https://doi.org/10.1002/9780813804620
ATKINSON, C.T. and VAN RIPPER III, C. 1991. Pathogenicity and epizootilogy of avian haematozoa: Plasmodium, Leucocytozoon and Haemoproteus. In: J.R. LOYE and M. ZUK, eds. Bird parasite interactions. Oxford University Press, pp. 19-48.
BARTON, K. and BARTON, M.K.. Package ‘mumin’. R package version. 2015 1(18), 439.
BATES, D., et al. Package ‘lme4’. Linear mixed-effects models using S4 classes. R package version. 2011, 1(6).
BELO, N.O., et al. Prevalence and lineage diversity of avian haemosporidians from three distinct Cerrado habitats in Brazil. Plos One. 2011, 6(3),1-8. https://doi.org/10.1371/journal.pone.0017654
BENSCH, S., et al. Temporal dynamics and diversity of avian malaria parasites in a single host species. Journal of Animal Ecology. 2007, 76(1), 112-122. https://doi.org/10.1111/j.1365-2656.2006.01176.x
BICHET, C., et al. Epidemiology of Plasmodium relictum infection in the house sparrow. Journal of Parasitology. 2014, 100(1), 59-65. https://doi.org/10.1645/12-24.1
BRAGA, E.M., et al. 2010. Técnicas para estudo de hemoparasitos em aves. In: S.V. MATTER et al., eds. Ornitologia e Conservação: Ciência Aplicada, Técnicas de Pesquisa e Levantamento. Rio de Janeiro: Editora Technical Books, pp. 395-412.
BRUNO, D.L., et al. Breeding behavior of the Helmeted Manakin Antilophia galeata (Passeriformes: Pipridae) in a gallery forest from São Paulo state, Brazil. Zoologia. 2021, 38(1). https://doi.org/10.1590/S1984-4689.v38.e21011
CALERO-RIESTRA, M. and GARCÍA, J.T. Sex-dependent differences in avian malaria prevalence and consequences of infections on nestling growth and adult condition in the tawny pipit, Anthus campestris. Malaria Journal. 2016, 22(15), 178. https://doi.org/10.1186/s12936-016-1220-y
CAMPBELL, T.W. Exotic animal hematology and cytology. New Jersey: John Wiley & Sons, 2015. https://doi.org/10.1002/9781118993705
CHAGAS, C.R.F., et al. Diversity and distribution of avian malaria and related haemosporidian parasites in captive birds from a Brazilian megalopolis. Malaria Journal. 2017, 16(1), 1-20. https://doi.org/10.1186/s12936-017-1729-8
CLARK, N.J., et al. A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. International Journal for Parasitology. 2014, 44(5), 329-338. https://doi.org/10.1016/j.ijpara.2014.01.004
COSGROVE, C.L., et al. Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. Journal of Animal Ecology. 2008, 77(3), 540-548. https://doi.org/10.1111/j.1365-2656.2008.01370.x
CORNELIUS, J.M., et al. Assessing the role of reproduction and stress in the spring emergence of haematozoan parasites in birds. Journal of Experimental Biology. 2014, 217(6), 841-849. https://doi.org/10.1242/jeb.080697
DAVIS, A.K., et al. The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Functional Ecology. 2008, 22(5), 760-772. https://doi.org/10.1111/j.1365-2435.2008.01467.x
DAVIS, A.K. and MANEY, D.L. The use of glucocorticoid hormones or leucocyte profiles to measure stress in vertebrates: what’s the difference?. Methods in Ecology and Evolution. 9(6),1556-1568, 2018. https://doi.org/10.1111/2041-210X.13020
DEVICHE, P. and PARRIS, J. Testosterone treatment to free-ranging male dark-eyed juncos (Junco hyemalis) exacerbates hemoparasitic infection. The Auk. 2006, 123(2), 548-562. https://doi.org/10.1642/0004-8038(2006)123[548:TTTFMD]2.0.CO;2
DINHOPL, N., et al. In situ hybridization and sequence analysis reveal an association of Plasmodium spp. with mortalities in wild passerine birds in Austria. Parasitology Research. 2015, 114(4), 1455-62. https://doi.org/10.1007/s00436-015-4328-z
EDLER, R., et al. Experimentally elevated testosterone levels enhance courtship behaviour and territoriality but depress acquired immune response in red bishops Euplectes orix. Ibis. 2011, 153(1), 46-58. https://doi.org/10.1111/j.1474-919X.2010.01075.x
FALLON, S.M., et al. Temporal stability of insular avian malarial parasite communities. Proceedings of the Royal Society of London B: Biological Sciences. 2004, 271(1538), 493-500. https://doi.org/10.1098/rspb.2003.2621
FECCHIO, A., et al. Baixa prevalência de hemoparasitos em aves silvestres no Cerrado do Brasil central. Neotropical Biology and Conservation. 2007, 2(3), 127-135.
FECCHIO, A., et al. High prevalence of blood parasites in social birds from a neotropical savanna in Brazil. Emu. 2011, 111(2), 132-138. https://doi.org/10.1071/MU10063
FECCHIO, A., et al. Structure and organization of an avian haemosporidian assemblage in a Neotropical savanna in Brazil. Parasitology. 2013, 140(2), 181-192. https://doi.org/10.1017/S0031182012001412
FECCHIO, A., et al. Age, but not sex and seasonality, influence Haemosporida prevalence in white-banded tanagers (Neothraupis fasciata) from central Brazil. Canadian Journal of Zoology. 2015, 93(1), 71-77. https://doi.org/10.1139/cjz-2014-0119
FECCHIO, A., et al. Host associations and turnover of haemosporidian parasites in manakins (Aves: Pipridae). Parasitology. 2017, 144(7), 984-993. https://doi.org/10.1017/S0031182017000208
FERREIRA-JUNIOR, F.C., et al. Habitat modification and seasonality influence avian haemosporidian parasite distributions in southeastern Brazil. PLoS One. 2017, 12(6), e0178791.
https://doi.org/10.1371/journal.pone.0178791
FOO, Y. Z., et al. The effects of sex hormones on immune function: a meta-analysis. Biological Reviews. 2017, 92(1), 551-571. https://doi.org/10.1111/brv.12243
FRIGERIO, D., et al. Social and environmental factors modulate leucocyte profiles in free-living greylag geese (Anser anser). PeerJ. 5(1), e2792. https://doi.org/10.7717/peerj.2792
GETHINGS, O.J., et al. Body condition is negatively associated with infection with Syngamus trachea in the ring-necked pheasant (Phasianus colchicus). Veterinary Parasitology. 2016, 228(1), 1-5. https://doi.org/10.1016/j.vetpar.2016.08.007
GODFREY, R.D., et al. Quantification of hematozoan in blood smears. Journal of Wildlife Disease. 1987, 23(4)558-565. https://doi.org/10.7589/0090-3558-23.4.558
GRUEBER, C.E., et al. Multimodel inference in ecology and evolution: challenges and solutions. Journal of Evolutionary Biology. 2011, 24(4), 699-711. https://doi.org/10.1111/j.1420-9101.2010.02210.x
HANSSEN, S.A., et al. Reduced immunocompetence and cost of reproduction in common eiders. Oecologia. 2003, 136(1),457-464. https://doi.org/10.1007/s00442-003-1282-8
HANSSEN, S.A., et al. Cost of reproduction in a long-lived bird: incubation effort reduces immune function and future reproduction. Proceedings of the Royal Society of London B: Biological Sciences. 2005, 272(1), 1039-1046. https://doi.org/10.1098/rspb.2005.3057
HEMBORG, C. and LUNDBERG, A. Costs of overlapping reproduction and moult in passerine birds: an experiment with the Pied Flycatcher. Behavioral Ecology and Sociobiology. 1998, 43(1), 19-23. https://doi.org/10.1007/s002650050462
HERNÁNDEZ-LARA, C., et al. Spatial and seasonal variation of avian malaria infections in five different land use types within a Neotropical montane forest matrix. Landscape and Urban Planning. 2017, 157(1),151-160. https://doi.org/10.1016/j.landurbplan.2016.05.025
KNOWLES, S.C.L., et al. Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. Journal of Evolution Biology. 2010, 23(3), 557-569. https://doi.org/10.1111/j.1420-9101.2009.01920.x
LACORTE, G.A. et al. Exploring the diversity and distribution of neotropical avian malaria parasites – a molecular survey from southeast Brazil. Plos One. 2013, 8(3), 1-9. https://doi.org/10.1371/journal.pone.0057770
LANGSTON, N.E. and HILLGARTH, N. Moult varies with parasites in laysan albatrosses. Proceedings of the Royal Society of London B: Biological Sciences. 1995, 261(1361), 239-243. https://doi.org/10.1098/rspb.1995.0143
LEITE, Y.F.C., et al. Prevalência de Hemosporideos em três localidades do Estado do Tocantins, Brasil. Ornithologia. 2013, 6(1), 1-13.
LOBATO, D.N., et al. Hematological and parasitological health conditions of the pale-breasted thrush (Turdus leucomelas) (Passeriformes: Turdidae) in southeastern Brazil. Zoologia. 2011, 28(6), 771-776. https://doi.org/10.1590/S1984-46702011000600010
LÜDTKE, B., et al. Associations of forest type, parasitism and body condition of two European passerines, Fringilla coelebs and Sylvia atricapilla. Plos One. 2013, 8(12), e81395. https://doi.org/10.1371/journal.pone.0081395
MAIA, J.P., et al. A comparison of multiple methods for estimating parasitemia of haemogregarine hemoparasites (Apicomplexa: Adeleorina) and its applications for studying infection in natural populations. Plos One. 2014, 9(1), e95010. https://doi.org/10.1371/journal.pone.0095010
MAINWARING, M.C. and HARTLEY, I.R. The energetic costs of nest building in birds. Avian Biology Research, 2013, 6(1)12-17. https://doi.org/10.3184/175815512X13528994072997
MARÇAL, B.F. and LOPES, L.E. Breeding biology of the Helmeted Manakin Antilophia galeata in an ecotone between the Atlantic Forest and the Cerrado. Ornithology Research. 2019, 27(1), 1-9. https://doi.org/10.1007/BF03544440
MARINI, M.A. Notes on the breeding and reproductive biology of the helmeted manakin. The Wilson Bulletin. 1992, 104(1), 168-173.
MARTIN, R.E. and KIRK, K. Transport of the essential nutrient isoleucine in human erythrocytes infected with the malaria parasite Plasmodium falciparum. Blood. 2007, 109(5), 2217-2224. https://doi.org/10.1371/journal.pone.0095010
MARZAL, A., et al. Co-infections by malaria parasites decrease feather growth but not feather quality in house martin. Journal of Avian Biology. 2013a, 44(5), 437-444. https://doi.org/10.1111/j.1600-048X.2013.00178.x
MARZAL, A., et al. Malaria infection and feather growth rate predict reproductive success in house martins. Oecologia. 2013b, 171(4), 853-861. https://doi.org/10.1007/s00442-012-2444-3
MEGÍA-PALMA, R., et al. Structural colour ornament correlates positively with parasite load and body condition in an insular lizard species. The Science of Nature. 2016, 103(7), 52-62. https://doi.org/10.1007/s00114-016-1378-8
MOLNÁR, O., et al. Negative correlation between nuptial throat colour and blood parasite load in male European green lizards supports the Hamilton-Zuk hypothesis. Naturwissenschaften. 2013, 100(6), 551-558. https://doi.org/10.1007/s00114-013-1051-4
MURPHY, M.E. 1996. Energetics and Nutrition of Molt. In: C. CAREY, ed. Avian Energetics and Nutritional Ecology. New York: Plenum, pp. 158-198. https://doi.org/10.1007/978-1-4613-0425-8_6
NORRIS, K. and EVANS, M. Ecological immunology: life history tradeoffs and immune defense in birds. Behavioral Ecology. 2000, 11(1), 19-26. https://doi.org/10.1093/beheco/11.1.19
NORTE, A.C., et al. Haematozoa infections in a great tit Parus major population in central Portugal: relationships with breeding effort and health. Ibis. 2009, 151(4), 677-688. https://doi.org/10.1111/j.1474-919X.2009.00960.x
PALINAUSKAS, V., et al. Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Experimental Parasitology. 2008, 120 (4), 372-380. https://doi.org/10.1016/j.exppara.2008.09.001
PANIAGO, L.P.M. Aspectos ecológicos de Antilophia galeata (Passeriformes: Pipridae) e seu potencial em biomonitoramento e conservação. Dissertação (Mestrado em Ecologia e Conservação de Recursos Naturais). Universidade Federal de Uberlândia, 89f. 2016. http://doi.org/10.14393/ufu.di.2016.135
PEIG, J., GREEN, A.J. New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos. 2009, 118(12),1883-1891. https://doi.org/10.1111/j.1600-0706.2009.17643.x
PIRES, L.P.; MELO, C. Individual–resource networks reveal distinct fruit preferences of selective individuals from a generalist population of the Helmeted Manakin. Ibis. 2020, 162(3),713-722. https://doi.org/10.1111/ibi.12794
PIRES, L.P., et al. Seasonality drives variation in the use of forest strata by adult males of a dimorphic frugivorous bird species. Austral Ecology. 2022, 47(2), 392-399.
https://doi.org/10.1111/aec.13129
RIBEIRO, P.V.A., et al. Leukocyte profile of the helmeted manakin, Antilophia galeata (Passeriformes: Pipridae) in a Cerrado forest fragment. Zoologia. 2020a, 37(1). https://doi.org/10.3897/zoologia.37.e46441
RIBEIRO, P.V.A., et al. Haemosporidian parasites prevalence associated with physical conditioning of avian species from the Brazilian Cerrado. Ciência e Natura. 2020b, 42(1), e50. https://doi.org/10.5902/2179460X40002
RIBEIRO, P.V.A., et al. First record of microfilariae in Antilophia galeata (Aves: Pipridae). Acta Brasiliensis. 2020c, 4(2), 106-109. https://doi.org/10.22571/2526-4338302
RIBEIRO, P.V.A., et al. Effects of urbanisation and pollution on the heterophil/lymphocyte ratio in birds from Brazilian Cerrado. Environmental Science and Pollution Research. 2022, 29(1),40204–40212. https://doi.org/10.1007/s11356-022-19037-w
RODRIGUEZ, M.D., et al. Sex and nest type influence avian blood parasite prevalence in a high-elevation bird community. Parasites & vectors. 2021, 14(1), 1-12. https://doi.org/10.1186/s13071-021-04612-w
ROVED, J., et al. Sex differences in immune responses: hormonal effects, antagonistic selection, and evolutionary consequences. Hormones and Behavior. 2017, 88 (1), 95-105. https://doi.org/10.1016/j.yhbeh.2016.11.017
ROSA, R., et al. Abordagem preliminar das condições climáticas de Uberlândia (MG). Sociedade & Natureza. 1991, 3(5), 91-108.
SAINO, N., et al. Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation. Behavior Ecology. 2002, 13(2), 169-174. https://doi.org/10.1093/beheco/13.2.169
SCHULTE-HOSTEDDE, A.I., et al. Restitution of mass-size residuals: validating body condition indices. Ecology. 2005, 86(1), 155-163. https://doi.org/10.1890/04-0232
SEBAIO, F., et al. Blood parasites in passerine birds from the Brazilian Atlantic Forest. Revista Brasileira de Parasitologia Veterinária. 2012, 21(1),7-15. https://doi.org/10.1590/S1984-29612012000100003
SICK, H. Ornitologia brasileira: uma introdução. Rio de Janeiro: Editora Nova Fronteira. 2001.
SILVA, A.M. and MELO, C. 2011. Frugivory and seed dispersal by the helmeted manakin (Antilophia galeata) in forests of Brazilian Cerrado. Ornitología Neotropical. 2011, 22(1), 69-77.
TARELLO, W. Clinical signs and response to primaquine in falcons with Haemoproteus tinnunculi infection. Veterinary Record. 2007, 61(6), 204-205. https://doi.org/10.1136/vr.161.6.204
VALKIUNAS, G. Avian malaria parasites and other haemosporidians. Boca Raton: CRC Press, 2005.
VAN OERS, K., et al. Reduced blood parasite prevalence with age in the Seychelles Warbler: selective mortality or suppression of infection?. Journal of Ornithology. 2010, 151(1), 69-77. https://doi.org/10.1007/s10336-009-0427-x
VANSTREELS, R.E.T., et al. Outbreak of avian malaria associated to multiple species of Plasmodium in magellanic penguins undergoing rehabilitation in Southern Brazil. Plos One. 2014, 9(1), p. e94994. https://doi.org/10.1371/journal.pone.0094994
WALDENSTRÖM, J., et al. Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology. 2002, 11(8), 1545-1554. https://doi.org/10.1046/j.1365-294X.2002.01523.x
WILLIAMS, T.D. Mechanisms underlying the costs of egg production. Bioscience. 2005, 55(1), 39-48. https://doi.org/10.1641/0006-3568(2005)055[0039:MUTCOE]2.0.CO;2
ZUK, M. and MCKEAN, K.A. Sex differences in parasite infections: patterns and processes. International Journal of Parasitology. 1996, 26(10), 1009-1023. https://doi.org/10.1016/S0020-7519(96)80001-4
ZUK, M. and STOEHR, A.M. 2010. Sex Differences in Susceptibility to Infection: An Evolutionary Perspective. In: S.L. KLEIN and C.W. ROBERTS, eds. Sex Hormones and Immunity to Infection. Springer: New York, pp. 1-18. https://doi.org/10.1007/978-3-642-02155-8_1
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Paulo Vitor Alves Ribeiro, Luís Paulo Pires, Márcia Cristina Cury, Celine de Melo
This work is licensed under a Creative Commons Attribution 4.0 International License.