Genetic diversity in captive Yellow Cardinals (Gubernatrix cristata) from Southern Brazil: implications for the management and conservation of an endangered species

Abstract

Yellow Cardinal is an Endangered Species. Its populations are in constant decline due to habitat reduction and loss and illegal capture. There are approximately 50 free-living animals in the south of Brazil (state of Rio Grande do Sul), but estimates indicate more than 1000 in captivity. Our goals were to investigate the genetic variability of captive animals in Brazil, compare it with the genetic variability found in free-living populations, estimate the kinship of captive individuals, and obtain updated data about the number of captive animals. We found only 13% of the registered captive Yellow Cardinals. Analysis of mitochondrial sequences of captive and free-living populations was performed. We obtained 14 haplotypes, one of them (H14) exclusive of captive individuals. Furthermore, we found a haplotype exclusive to the La Pampa population in a male born in captivity in 2013. The most frequent haplotype in captive animals was the same reported for northern Argentina and Uruguay populations, which border Brazil. We found a high number of alleles by locus (mean = 9.6) for microsatellite markers, with high average heterozygosity (HO = 0.605 and HE = 0.727). The global F was 0.168. Kinship analysis of captive birds indicates a degree of kinship means of 0.082. In addition, the probability of relationship indicates that 79.4% of them are unrelated. Our data demonstrated that the captive group retains a high degree of genetic diversity with a low level of kinship. Nevertheless, the presence of haplotype exclusive for Argentina’s population in captive birds, and the low level of parentage among captive animals may be representing cases of illegal wildlife trade.

Zusammenfassung

Genetische Diversität bei in Gefangenschaft gehaltenen Grüntangaren Gubernatrix cristata aus Südbrasilien: Konsequenzen für Management und Schutz einer stark gefährdeten Vogelart

Die Grüntangare ist eine stark gefährdete Vogelart, deren Populationen aufgrund von schrumpfenden Lebensräumen und Habitatverlust sowie illegalem Fang stetig abnehmen. In freier Wildbahn leben etwa 50 Vögel im Süden Brasiliens (Bundesstaat Rio Grande do Sul), Schätzungen zufolge allerdings mehr als 1.000 in Gefangenschaft. Unser Ziel war es, die genetische Variabilität der Volierenvögel in Brasilien zu untersuchen und diese mit der genetischen Variabilität der freilebenden Populationen zu vergleichen sowie den Verwandtschaftsgrad der Individuen in Volierenhaltung zu bestimmen und aktualisierte Daten zur Anzahl der Vögel in Gefangenschaft zu erhalten. Wir konnten nur 13% der registrierten Grüntangaren in Gefangenschaft ausfindig machen. Wir führten Analysen mitochondrialer Sequenzen der gefangenen und freilebenden Populationen durch. Wir entdeckten 14 Haplotypen, von denen einer (H14) ausschließlich bei Individuen aus Gefangenschaft vorkam. Des Weiteren konnten wir einen ausschließlich in der La Pampa-Population vertretenen Haplotyp bei einem 2013 in Gefangenschaft geschlüpften Männchen nachweisen. Der bei den Volierenvögeln häufigste Haplotyp war derjenige, welcher von den Populationen im Norden Argentiniens und Uruguays an der Grenze zu Brasilien bekannt ist. Wir stellten eine hohe Anzahl von Allelen pro Genlokus (Mittelwert = 9,6) bei den Mikrosatellitenmarkern fest, bei einer hohen Durchschnittsheterozygosität (HO = 0,605 und HE = 0,727). Der globale F-Wert betrug 0,168. Verwandtschaftsanalysen an Vögeln in Gefangenschaft deuten auf einen mittleren Verwandtschaftsgrad von 0,082 hin. Außerdem weist die Verwandtschaftswahrscheinlichkeit darauf hin, dass 79.4% der Individuen nicht verwandt sind. Unsere Daten zeigen, dass sich die Volierenpopulation ein hohes Maß an genetischer Diversität in Verbindung mit einem niedrigen Verwandtschaftsgrad bewahrt hat. Dennoch könnten das Vorhandensein eines für die argentinische Population typischen Haplotyps sowie der geringe Abstammungsgrad bei den Volierenvögeln Fälle illegalen Vogelhandels widerspiegeln.

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Fig. 1
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Availability of data and material (data transparency)

All DNA sequences from this study are available on GenBank, Accession Numbers MW029496 – MW029606.

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Acknowledgements

This research was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) through fellowship for Sandra Eloisa Bülau and Willian Thomaz Peçanha, Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). Thales Renato Ochotorena de Freitas received financial support from CAPES, CNPq, and FAPERGS. The authors are grateful to Centro Nacional de Pesquisa e Conservação de Aves Silvestres (CEMAVE) and Instituto Brasileiro do Meio Ambiente e recursos Naturais Renováveis (IBAMA) for all their support and assistance with this research. We also thank the Programa de Desenvolvimento Tecnológico em Ferramentas para a Saúde – PDTISFIOCRUZ for the use of nucleotide sequencing facilities at Instituto René Rachou – Fiocruz Minas.

Funding

This research was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

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Sandra Eloisa Bülau and Thales Renato Ochotorena de Freitas conceptualized. Sandra Eloisa Bülau and Willian Thomaz Peçanha analyzed the data. Sandra Eloisa Bülau and Claiton Martins-Ferreira performed the fieldwork. Thales Renato Ochotorena de Freitas supervised the study. All the authors discussed the results and wrote the article.

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Correspondence to Thales Renato Ochotorena de Freitas.

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Bülau, S.E., Peçanha, W.T., Martins-Ferreira, C. et al. Genetic diversity in captive Yellow Cardinals (Gubernatrix cristata) from Southern Brazil: implications for the management and conservation of an endangered species. J Ornithol (2021). https://doi.org/10.1007/s10336-021-01857-1

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Keywords

  • Passeriformes
  • Birds
  • South america
  • habitat reduction
  • mtDNA
  • Microsatellite