Abstract
The Hyacinth Macaw (Anodorhynchus hyacinthinus) is a threatened species of the family Psittacidae. Its classification as vulnerable by the International Union for Conservation of Nature is especially a result of habitat loss and intense illegal trade of this species. The total estimated number of wild individuals in Brazil is around 6500 birds, distributed in three regions: Pantanal, Pará State, and Northeast Brazil. Data on the biology, ecology, and genetic variability of this species are fundamental to the development of conservation strategies for its natural populations. Therefore, the present study aimed to analyze the genetic structure of different populations of A. hyacinthinus and examine the population dynamics throughout its distribution in four areas of Brazil. We analyzed 100 individuals by amplifying and sequencing the mitochondrial DNA control region (D-loop) and identified 17 polymorphic sites and 16 distinct haplotypes. Total nucleotide diversity was 0.0034 and haplotype diversity was 0.7832. The fixation index indicated significant levels of genetic differentiation among all sampled populations. Our results indicate that different populations of A. hyacinthinus should be considered as evolutionarily significant units and must be independently protected and managed to preserve the adaptive diversity and evolutionary processes of this species throughout its distribution.
Zusammenfassung
Eine genetische Analyse des bedrohten Hyazinth-Ara (Anodorhynchus hyacinthinus) anhand mitochondrialer Marker: die Bemühungen zum Schutz dieser Art müssen für alle ihre verschiedenen Populationen gelten.
Der Hyazinth-Ara (Anodorhynchus hyacinthinus) ist eine bedrohte Papageienart, die auf der Liste der IUCN als „gefährdet“ eingestuft ist, in erster Linie wegen des Verlusts von Lebensraum und des intensiven illegalen Handels. Die geschätzte Gesamtanzahl wildlebender Individuen liegt für Brasilien bei etwa 6.500 Tieren, verteilt auf drei Regionen: Pantanal, den Bundesstaat Pará und Nordost-Basilien. Mehr Informationen über die Biologie, Ökologie und genetische Vielfalt dieser Art sind grundlegend für die Unterstützung und die Ausarbeitung von Schutzmaßnahmen für ihre natürlichen Populationen. Deshalb hatte diese Studie zum Ziel, die Genetik der unterschiedlichen Populationen des Hyazinth-Ara zu analysieren und die Populationsdynamik über das Verbreitungsareal hinweg zu untersuchen. Wir analysierten 100 Einzeltiere aus vier verschiedenen Gebieten durch Amplifizierung und Sequenzierung der mitochiondrialen DNS-Kontroll-Region (D-loop). Wir identifizierten 17 polymorphe Loci und 16 eindeutigen Haplotypen. Die gesamte Nukleotid-Vielfalt lag bei 0,0034 und die der Haplotypen bei 0,7832. Der FST-Wert weist signifikante genetische Differenzierung der verschiedenen Populationen aus. Unsere Ergebnisse legen nahe, dass die verschiedenen Populationen des Hyazinth-Aras als eigenständige „Evolutionary Significant Units“ (ESUs) angesehen und unabhängig voneinander geschützt werden sollten, um so die Anpassungsvielfalt und die evolutionären Abläufe quer durch ihre geographische Verbreitung hindurch erhalten zu können.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Antas PTZ, Carrara LA, Yabe RS, Ubaid FK, Oliveira-Júnior SB, Vasques ER, Ferreira LP (2010) A arara-azul na Reserva Particular do Patrimônio Natural Sesc Pantanal. SESC, Departamento Nacional, Rio de Janeiro
Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Bruford MW, Hanotte O, Brookfield JFY, Burke T (1992) Single locus and multilocus DNA fingerprint. In: Hoezel AR (ed) Molecular genetics analysis of population. A pratical approach. Oxford University Press, New York, pp 225–269
Caparroz R, Miyaki C, Baker AJ (2009) Contrasting phylogeographic patterns in mitochondrial DNA and microsatellite: evidence of female philopatry and male-biased gene flow among regional populations of the Blue-and-yellow Macaw (Psittaciformes: Ara ararauna) in Brazil. Auk 126(2):359–370
Clarke AL, Saether B-E, Roskaft E (1997) Sex biases in avian dispersal: a reappraisal. Oikos 79:429–438
Collar NJ (1997) Family Psittacidae (Parrots). In: Hoyo J, Elliot AE, Sargatal J (eds) Handbook of the birds of the world, vol. 4. Sandgrouse to Cuckoos. Lynx, Barcelona, pp 280–477
Eberhard JR, Wright TF, Bermingham E (2001) Duplication and concerted evolution of the mitochondrial control region in the parrot genus Amazona. Mol Biol Evolut 18:1330–1342
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Eizirik E (1996) Ecologia molecular, genética da conservação e o conceito de unidades evolutivamente significativas. Braz J Genet (Supl.) 19:23–29
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Excoffier LGL, Schneider S (2005) Arlequin version 3.0: an integrated software package for population genetics data analysis. Evolut Bioinform Online 1:47–50
Faria PJ, Guedes NMR, Yamashita C, Martuscelli P, Miyaki CY (2008) Genetic variation and population structure of the endangered Hyacinth Macaw (Anodorhynchus hyacinthinus): implications for conservation. Biodivers Conserv 17:765–779
Forster M, Forster P, Watson J (2007) Network version 4.2.0.1: a software for population genetics data analysis. Fluxus
Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics. Cambridge University Press, Cambridge
Fu XY (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Fu XY, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709
Guedes NMR, Seixas GHF (2002) Métodos para estudos de reprodução de Psitacídeos. In: Galetti M, Pizo MA (eds) Ecologia e conservação de Psitacídeo no Brasil. Melopsittacus, Belo Horizonte, pp 141–156
Guedes NMR (1993) Biologia reprodutiva da Arara Azul (Anodorhynchus hyacinthinus) no Pantanal-MS, Brasil. Master’s thesis, University of São Paulo, São Paulo
Guedes NMR, Bianchi CA, Barros Y (2008) Anodorhynchus hyacinthinus v(II). In: Machado ÂBM et al (eds) Livro vermelho da fauna Brasileira ameaçada de extinção, 1 edn. Fundação Biodiversitas, Belo Horizonte, MG, pp 467–468
Handbook of the Birds of the World and BirdLife International (2017) Handbook of the Birds of the World and BirdLife International digital checklist of the birds of the world, version 9.1. https://datazone.birdlife.org/species/taxonomy. Accessed 17 Jan 2019
IUCN (2019) Disponível em: https://www.iucn.org/. Accessed 21 Jan 2019
Librado P, Rozas J (2009) DnaSP version 5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 1451–1452
Munn CA, Thomsen JB, Yamashita C (1989) The Hyacinth Macaw. In: Chadler WJ (ed) Audubon wildlife report. Academic Press, New York, pp 404–419
Munn CA, Thomsen JB, Yamashita C (1987) The distribution and status of the Hyacinth Macaw (Anodorhynchus hyacinthinus) in Brazil, Bolívia and Paraguay. Report to the Secretaria of the Convention on International Trade in Endangered Species of Wild Fauna and Flora. Conservation International, New York, p 50
Nielsen R, Wakeley JM (2001) Distinguishing migration from isolation: an MCMC approach. Genetics 158:885–896
Oliveira-Marques AR (2006) Filogenia Molecular das Espécies do Gênero Ara (Psittaciformes, Aves). Dissertação de Mestrado, Instituto de Biociências, Universidade de são Paulo, São Paulo.
Presti FT, Guedes NMR, Antas PTZ, Miyaki CY (2015) Population genetic structure in Hyacinth Macaws (Anodorhynchus hyacinthinus) and identification of the probable origin of confiscated individuals. J Hered 106:491–502
Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evolut 19:2092–2100
Seixas GHF, Guedes NMR (2002) Uso de radiotelemetria no estudo de psitacídeos. In: Galleti M, Pizo MA (eds) Ecologia e conservação de psitacídeos no Brasil. Melopsittacus, Belo Horizonte, pp 141–156
Sick H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro, p 912
Storfer A (1996) Quantitative genetics: a promising approach for the assessment of genetic variation in endangered species. Trends Ecol Evol 11:343–348
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595
Wright S (1978) Variability within and among natural populations. Evolution and the genetics of populations. University of Chicago Press, Chicago
Yamashita C (1992) Comportamento de araraúna (Anodorhynchus hyacinthinus) Psittacidae, Aves. Anais Etol 10:158–162
Acknowledgements
The authors thank all of the collaborators who contributed samples to this study, particularly Cristina Y. Miyaki of the University of São Paulo and Neiva R. M. Guedes of the Arara-Azul Institute. This work was authorized by the Brazilian government through the Brazilian Institute of the Environment and Renewable Natural Resources and the Chico Mendes Institute for Biodiversity Conservation through the Biodiversity Authorization and Information System (License Nos. 12.312-2 and 14.79101).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Wink.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
de Almeida, T.R.A., Presti, F.T., Cruz, V.P. et al. Genetic analysis of the endangered Hyacinth Macaw (Anodorhynchus hyacinthinus) based on mitochondrial markers: different conservation efforts are required for different populations. J Ornithol 160, 711–720 (2019). https://doi.org/10.1007/s10336-019-01652-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-019-01652-z