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Blood parasites of passerines in the Brazilian Pampas and their implications for a potential population supplementation program for the endangered Yellow Cardinal (Gubernatrix cristata)

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Abstract

Espinilho savanna (“seasonal steppe savanna”) is a unique vegetation formation of the Pampas biome that is found near the tri-border of Brazil, Uruguay, and Argentina. The Yellow Cardinal (Gubernatrix cristata) is a flagship species of this ecosystem, but it is classified as “critically endangered” in Brazil due to habitat loss and poaching for the illegal trade. Population supplementation through the release of individuals that were captive-bred or apprehended by authorities from the illegal trade has been considered as a conservation strategy for this species; however, the risk of pathogen introduction is a critical concern. We used microscopy and molecular methods to investigate the occurrence of blood parasites in wild passerines (n = 64, including three Yellow Cardinals) at Espinilho State Park, Rio Grande do Sul, Brazil, and in captive Yellow Cardinals (n = 30) at three facilities in Brazil. Haemosporidian parasites were detected in the blood smears of 10.9% of the wild passerines, comprising the morphospecies Haemoproteus erythrogravidus in Rufous-collared Sparrow (Zonotrichia capensis), H. quiscalus in Grayish Baywing (Agelaioides badius), and H. tyranni in Great Kiskadee (Pitangus sulphuratus); these are the southernmost records for these morphospecies and their first record for the Pampas biome. No haemosporidian parasites were detected in the blood smears of the Yellow Cardinals, wild or captive. Microfilariae were detected in the blood smears of 14.1% of the wild passerines, including all wild Yellow Cardinals, and in 43.3% of captive Yellow Cardinals. Trypanosoma sp. was detected in the blood smear of one captive Yellow Cardinal. Nested PCR and gene sequencing of the cyt-b gene of Haemoproteus/Plasmodium was used to test a subset of wild passerines and captive Yellow Cardinals, allowing for the molecular barcoding of H. quiscalus lineage AGEBAD04 and H. tyranni lineage PITSUL01; additionally, DNA identical to that of lineage PITSUL01 was detected in the blood of one captive Yellow Cardinal. This study provides valuable data to support the conservation management of the Yellow Cardinal and other threatened passerines from the Pampas and highlights the need for further studies on the epidemiology and pathology of filarioid worms and trypanosomes in passerines from this biome.

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Data availability

Genetic sequences produced in this study were deposited at GenBank (accession codes ON703102–4) and MalAvi (lineages AGEBAD04 and PITSUL01).

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Acknowledgements

We wish to thank Secretaria Estadual do Meio Ambiente e Infraestrutura do Rio Grande do Sul (SEMA) and Espinilho State Park staff for permitting to research in a protected area and for all the support during fieldwork and Fazenda São Marcos owners for granting access to one of the study sites. We also thank Pai Passo farm Owners (especially Paulo, Pedro Bastos and Maria), Condomínio Agropecuário Ceolin, and Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for their huge support during field expeditions.

Funding

This study was supported by the ICMBio, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 422053/2016–3), and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG APQ-00645–18). FCF was supported by the National Science Foundation grant 1717498 as part of the joint NSF-NIH-USDA Ecology and Evolution of Infectious Diseases program. CSF was supported by CNPq grant 309438/2016–0 and 310608/2019–8. EMB was granted by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 304334/2019–7).

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Authors and Affiliations

  1. Programa de Pós-Graduação em Ciências Veterinárias, Setor de Ciências Agrárias, Universidade Federal do Paraná, Rua dos Funcionários 1540, Curitiba, PR, 80035-050, Brazil

    Bianca Ressetti da Silva & Rosangela Locatelli-Dittrich

  2. Instituto de Pesquisa e Reabilitação de Animais Marinhos, Rodovia BR 262 Km 0, Cariacica, ES, 29140-130, Brazil

    Ralph Eric Thijl Vanstreels

  3. Centro Nacional de Pesquisa e Conservação de Aves Silvestres, Instituto Chico Mendes de Conservação da Biodiversidade, Rodovia Jornalista Maurício Sirotski Sobrinho km 1, Florianópolis, SC, 88053-700, Brazil

    Patricia P. Serafini

  4. Laboratory of Biomarkers of Aquatic Contamination and Immunochemistry, Federal University of Santa Catarina, Servidão Caminho Do Porto S/N, Florianópolis, SC, 88034-257, Brazil

    Patricia P. Serafini

  5. Laboratório de Ornitologia, Museu de Ciências e Tecnologia, Programa de Pós-Graduação Em Ecologia E Evolução da Biodiversidade, Pontifícia Universidade Católica do Rio Grande do Sul, Avenida Ipiranga 6681, Porto Alegre, RS, 90619-900, Brazil

    Carla Suertegaray Fontana, Thaiane Weinert da Silva & Eduardo Chiarani

  6. Laboratório de Patologia Clínica Veterinária e Diagnóstico Molecular, Faculdade de Agronomia e Medicina Veterinária, Universidade de Brasília, Brasília, DF, 70910-900, Brazil

    Andréa M. Carvalho

  7. Center for Conservation Genomics, Smithsonian Conservation Biology Institute, Washington, DC, USA Center for Vector Biology, Rutgers University, New Brunswick, NJ, USA

    Francisco C. Ferreira Junior

  8. Departamento de Parasitologia, Universidade Federal de Minas Gerais, Avenida Presidente Antônio Carlos, 6627, Belo Horizonte, MG, 31270-901, Brazil

    Érika Martins Braga

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  1. Bianca Ressetti da Silva
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  2. Ralph Eric Thijl Vanstreels
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  10. Rosangela Locatelli-Dittrich
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Contributions

BRS, PPS, CSF, TWS, EC, and RLD conceived the project. BRS, PPS, CSF, TWS, and EC conducted field expeditions and collected and processed data and biological samples. BRS, RETV, FCF, and EMB examined blood smears and morphologically identified the parasites. AMC, FCF, RETV, and EMB conducted molecular and phylogenetic analyses. BRS, RETV, and RLD wrote the first manuscript draft and prepared the tables and figures. All authors reviewed and edited the manuscript and approved its final version.

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Correspondence to Rosangela Locatelli-Dittrich.

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The study was approved by the Animal Use Ethics Committee of the Agricultural Sciences Campus of the Universidade Federal do Paraná (CEUA 038/2018) and was conducted under permits issued by the Brazilian Ministry of Environment (SISBIO 53935–6).

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da Silva, B.R., Vanstreels, R.E.T., Serafini, P.P. et al. Blood parasites of passerines in the Brazilian Pampas and their implications for a potential population supplementation program for the endangered Yellow Cardinal (Gubernatrix cristata). Parasitol Res 121, 3203–3215 (2022). https://doi.org/10.1007/s00436-022-07638-w

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