Haemosporidian parasites prevalence associated with physical conditioning of avian species from the Brazilian Cerrado
DOI:
https://doi.org/10.5902/2179460X40002Keywords:
Avian malaria, Wild birds, Host-parasite relationshipAbstract
Blood parasites can infect myriad avian species and thereby affect the fitness and survival of their hosts. There is wide interspecific variation in parasite prevalence related to biological, ecological, and evolutionary host factors. This study aimed to determine the blood parasite prevalence in avian species from the Brazilian Cerrado and to investigate the associations among biomass, body condition, and blood parasitism. A total of 1,098 blood smears from 549 individuals (56 species) collected in four forest fragments were analyzed. Of these, 109 (19.85%) individuals from 33 species were infected: 13 (2.36%) were positive for Haemoproteus and 103 (18.76%) for Plasmodium. There was co-infection between both genera of parasites in 7 individuals. Among bird species, prevalence ranged from zero to 100%. There were significant positive correlations between prevalence and biomass and the body condition index. Hemosporid vectors track their hosts by carbon dioxide detection. Since large organisms emit more carbon dioxide, our results suggest that larger birds may be more susceptible to hemosporid vectors. Additionally, species with higher body condition indices can be more tolerant to parasites, possibly because they have more energy reserves. This study showed that species with higher biomass and body condition indices were associated with higher blood parasite prevalence, a finding that suggests these factors are efficient predictors to explain the interspecific variations. This information could be important for the understanding parasite-host relationships and useful for bird conservation programs.
Downloads
References
Asghar M, Hasselquist D, Bensch S. Are chronic avian haemosporidian infections costly in wild birds?. Journal of Avian Biology. 2011;42:530-537.
Atkinson CT, La Pointe, DA. Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. Journal of Avian Medicine and Surgery. 2009;23:53-63.
Atkinson CT, Van Ripper III C. Pathogenicity and epizootilogy of avian haematozoa: Plasmodium, Leucocytozoon and Haemoproteus. In: LOYE JR, ZUK M, editors. Bird parasite interactions. Oxford: Oxford University Press; 1991. p. 19-48.
Ayres JS, Schneider DS. Tolerance of Infections. Annual Review of Immunology. 2012;30:271-294.
Baesse CQ. Aves como biomonitores de qualidade ambiental em fragmentos florestais do Cerrado. [dissertation]. Uberlândia: Instituto de Biologia/UFU; 2015. 114 p.
Balenger SL, Zuk M. Testing the Hamilton–Zuk hypothesis: past, present, and future. Integrative and Comparative Biology, 2014;54:601-613.
Braga EM, Belo NO, Pinheiro RT. Técnicas para estudo de hemoparasitos em aves. In: MATTER SV et al., editors. Ornitologia e Conservação: Ciência Aplicada, Técnicas de Pesquisa e Levantamento. Rio de Janeiro: Editora Technical Books; 2010. p. 395-412.
Belo NO, Pinheiro RT, Reis ES, Ricklefs RE, Braga EM. Prevalence and lineage diversity of avian haemosporidians from three distinct Cerrado habitats in Brazil. Plos One. 2011;6:1-8.
Brito JLS, Prudente TD. Mapeamento do uso da terra e cobertura vegetal do município de Uberlândia – MG, utilizando imagens CCD/CBERS 2. Caminhos de Geografia. 2005;13:144-153.
Clark NJ, Clegg SM, Lima MR. A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. International Journal for Parasitology. 2014;44:329-338.
Cornet S, Bichet C, Larcombe S, Faivre B, Sorci G. Impact of host nutritional status on infection dynamics and parasite virulence in a bird-malaria system. Journal of Animal Ecology. 2013;10:1-10.
Dinhopl N, Nedorost N, Mostegl MM, Weissenbacher-Lang C, Weissenböck H. In situ hybridization and sequence analysis reveal an association of Plasmodium spp. with mortalities in wild passerine birds in Austria. Parasitology Research. 2015;114:1455-62.
Fecchio A, Marini MÂ, Braga ÉM. Baixa prevalência de hemoparasitos em aves silvestres no Cerrado do Brasil Central. Neotropical Biology and Conservation. 2007;2:127-135.
Fecchio A, Lima MR, Silveira P, Braga ÉM, Marini MÂ. High prevalence of blood parasites in social birds from a neotropical savanna in Brazil. Emu. 2011;111:132-138.
Fecchio A, Lima MR, Svensson-Coelho M, Marini MÂ, Ricklefs RE. Structure and organization of an avian haemosporidian assemblage in a Neotropical savanna in Brazil. Parasitology. 2013;140:181-192.
Ferreira Junior FC, Rodrigues RA, Ellis VA, Leite LO, Borges MA, Braga EM. Habitat modification and seasonality influence avian haemosporidian parasite distributions in southeastern Brazil. Plos One. 2017;12:1-18.
Gethings OJ, Sage RB, Morgan ER, Leather SR. Body condition is negatively associated with infection with Syngamus trachea in the ring-necked pheasant (Phasianus colchicus). Veterinary Parasitology. 2016;228:1-5.
Godfrey RD, Fredynich, AM, Pence DB. Quantification of hematozoan in blood smears. Journal of Wildlife Disease. 1987;23:558-565.
Gwynne JA, Ridgely RS, Tudor G, Argel M. Aves do Brasil: Pantanal e Cerrado. Belo Horizonte: Editora Horizonte; 2010.
Hamilton WD, Zuk M. Heritable true fitness and bright birds: a role for parasites? Science. 1982;218:384-387.
Isaksson C, Sepil I, Baramidze V, Sheldon BC. Explaining variance of avian malaria infection in the wild: the importance of host density, habitat, individual life-history and oxidative stress. BMC Ecology. 2013;13:1-11.
Knowles SCL, Palinauskas V, Sheldon BC. Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. Journal of Evolution Biology. 2010;23:557-569.
Lacorte GA, Felix GMF, Pinheiro RRB, Chaves AV, Almeida-Neto G. Exploring the diversity and distribution of neotropical avian malaria parasites – a molecular survey from southeast Brazil. Plos one. 2013;8:1-9.
Lehane M. The Biology of Blood-Sucking in Insects. New York: Cambridge University Press, 2005.
Leite YFC, Pinheiro RT, Braga EM. Prevalência de hemosporídeos em três localidades do estado do Tocantins, Brasil. Ornithologia. 2013;6:1-13.
Lobato DNC. Efeitos das alterações ambientais sobre a saúde de aves silvestres utilizando hemoparasitos como indicadores. [thesis]. Belo Horizonte: Instituto de Ciências Biológicas/UFMG; 2012. 120p.
Maia JP, Harris DJ, Carranza S, Gómez-Díaz EA. Comparison of multiple methods for estimating parasitemia of haemogregarine hemoparasites (Apicomplexa: Adeleorina) and its applications for studying infection in natural populations. Plos One. 2014;9:1-13.
Marquardt WC. Biology of disease vectors. San Diego: Elsevier Academic Press; 2005.
Marzal A, Asghar M, Rodríguez L, Reviriego M, Hermosell IG, Balbontín J, Garcia-Longoria L, Lope F, Bensch S. Co-infections by malaria parasites decrease feather growth but not feather quality in house martin. Journal of Avian Biology. 2013;44:437-444.
Medzhitov R, Schneider DS, Soares MP. Disease tolerance as a defense strategy. Science. 2012; 335:936-941.
Megía-Palma R, Martínez X, Merino S. A structural colour ornament correlates positively with parasite load and body condition in an insular lizard species. The Science of Nature. 2016;103:1-10.
Molnár O, Bajer K, Mészáros B, Török J, Herczeg G. Negative correlation between nuptial throat colour and blood parasite load in male European green lizards supports the Hamilton-Zuk hypothesis. Naturwissenschaften. 2013;100:551-558.
Nunn CL, Altizer SM, Sechrest W, Cunningham A.A. Latitudinal gradients of parasite species richness in primates. Diversity and Distributions. 2005;11:249-256.
Piacentini VQ, Aleixo A, Agne CE, Mauricio GN, Pacheco JF, Bravo GA, et al. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. Revista Brasileira de Ornitologia. 2015;23:91-298.
Råberg L, Graham AL, Read AF. Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society: Biological Sciences. 2009364:37-49.
Read AF. Passerine Polygyny: A Role for Parasites?. The American Naturalist. 1991;138:434-459.
Rosa R, Lima SC, Assunção WL. Abordagem preliminar das condições climáticas de Uberlândia (MG). Sociedade ; Natureza. 1991;3:91-108.
Scheuerlein A, Ricklefs RE. Prevalence of blood parasites in European passerine birds. Proceedings of the Royal Society of London. 2004; 271: 1363–1370.
Schultede-Hostedde AI, Zinner B, Millar JS, Hickling GJ. Restitution of mass-size residuals: validating body condition indices. Ecology. 2005;86:155-163.
Sebaio F, Braga EM, Branquinho F, Naninca LT, Marini MA. Blood parasites in Brazilian Atlantic Forest birds: effects of fragment size and habitat dependency. Bird Conservation International. 2010;20:432-439.
Sebaio F, Braga ÉM, Branquinho F, Fecchio A, Marini MÂ. Blood parasites in passerine birds from the Brazilian Atlantic Forest. Revista Brasileira de Parasitologia Veterinária. 2012;21:7-15.
Sick H. Ornitologia brasileira: uma introdução. Rio de Janeiro: Editora Nova Fronteira; 1997.
Sigrist T. Aves do Brasil: uma visão artística. São Paulo: Editora Leitura Dinâmica; 2009.
Sorci G, Faivre B. Inflammation and oxidative stress in vertebrate host-parasite systems. Philosophical Transactions of the Royal Society B: Biological Sciences. 2009;364:71-83.
Sorci G. Immunity, resistance and tolerance in bird-parasite interactions. Parasite Immunology. 2013;35:350-361.
Spencer KA, Buchanan KL, Leitner S. Parasites affect song complexity and neural development in a songbird. Proceedings of the Royal Society of London B: Biological Sciences. 2005;272:2037-2043.
Valkiunas G. Avian malaria parasites and other haemosporidians. Boca Raton: CRC Press; 2005.
Van Riper III C, Van Riper SG, Goff ML. The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs. 1986;56:327-344.
Vanstreels RET, Kolesnikovas CKM, Sandri S, Silveira P, Belo NO, Ferreira Junior, FC, et al. Outbreak of avian malaria associated to multiple species of Plasmodium in magellanic penguins undergoing rehabilitation in southern Brazil. Plos One. 2014;9:1-11.
Watson MJ. What drives population-level effects of parasites? Meta-analysis meets life-history. International Journal for Parasitology: Parasites and Wildlife. 2013;2:190-196.
Wilkinson L. SYSTAT: The System for Statistics. Chicago: SYSTAT Inc.; 2002.
Zar JH. Biostatistical Analysis. Rio de Janeiro: Prentice-Hall; 1999.
Žiegytė R, Valkiūnas G. Recent advances in vector studies of avian haemosporidian parasites. Ekologija. 2014;60:73-83.
Downloads
Published
Versions
- 2022-01-11 (2)
- 2020-05-14 (1)
How to Cite
Issue
Section
License
To access the DECLARATION AND TRANSFER OF COPYRIGHT AUTHOR’S DECLARATION AND COPYRIGHT LICENSE click here.
Ethical Guidelines for Journal Publication
The Ciência e Natura journal is committed to ensuring ethics in publication and quality of articles.
Conformance to standards of ethical behavior is therefore expected of all parties involved: Authors, Editors, Reviewers, and the Publisher.
In particular,
Authors: Authors should present an objective discussion of the significance of research work as well as sufficient detail and references to permit others to replicate the experiments. Fraudulent or knowingly inaccurate statements constitute unethical behavior and are unacceptable. Review Articles should also be objective, comprehensive, and accurate accounts of the state of the art. The Authors should ensure that their work is entirely original works, and if the work and/or words of others have been used, this has been appropriately acknowledged. Plagiarism in all its forms constitutes unethical publishing behavior and is unacceptable. Submitting the same manuscript to more than one journal concurrently constitutes unethical publishing behavior and is unacceptable. Authors should not submit articles describing essentially the same research to more than one journal. The corresponding Author should ensure that there is a full consensus of all Co-authors in approving the final version of the paper and its submission for publication.
Editors: Editors should evaluate manuscripts exclusively on the basis of their academic merit. An Editor must not use unpublished information in the editor's own research without the express written consent of the Author. Editors should take reasonable responsive measures when ethical complaints have been presented concerning a submitted manuscript or published paper.
Reviewers: Any manuscripts received for review must be treated as confidential documents. Privileged information or ideas obtained through peer review must be kept confidential and not used for personal advantage. Reviewers should be conducted objectively, and observations should be formulated clearly with supporting arguments, so that Authors can use them for improving the paper. Any selected Reviewer who feels unqualified to review the research reported in a manuscript or knows that its prompt review will be impossible should notify the Editor and excuse himself from the review process. Reviewers should not consider manuscripts in which they have conflicts of interest resulting from competitive, collaborative, or other relationships or connections with any of the authors, companies, or institutions connected to the papers.
