Molecular sexing in the formation of pairs of blue-and-yellow macaw (Ara ararauna) in reintroduction programs

Authors

DOI:

https://doi.org/10.33448/rsd-v10i10.19330

Keywords:

Reintroduction programs; Illegal trade; Molecular markers; Psittacidae; Heterosexual and homosexual pairs.

Abstract

Blue and yellow macaw is a species which does not show sexual dimorphism and is threatened by animal traffic. The identification of heterosexual pairs is important for reintroduction programs. The aim of this work was select parameters for sexing and use them to determine the frequency of heterosexual pairs in a population of blue-and-yellow macaws allocated in a Wild Animal Screening Center. Blood samples from 23 macaws were collected and genomic DNA extracted by Tris/SDS washes. Allele-specific molecular markers for sexing were amplified by PCR, and identified on 2% agarose gel. Three pairs of primers were tested: Pair 1 (P2/P8), Pair 2 (1237L/1272H) and Pair 3 (2550F/2718R). For the determination of animal pairs, all individuals had their social behavioral acts observed. The results showed that the low complexity DNA extraction protocol used was adequate. Pairs 2 and 3 of primers were effective for sexing and the Pair 3 was the most efficient. The study also showed that in the sample studied, the composition of males and females was similar (0.4 males n=10 and 0.6 females n=13); 70% (n=16) of the individuals formed pairs and 75% (n=12) of the pairs were heterosexual and the others male-male or female-female pairs. These results were used in the management of the animals in the reintroduction program.

References

Ágh, N., Kovács, Sz., Nemesházi, E., & Szabó, K. (2018). Univerzális, ivarhatározáshoz használt CHD1 markerek alkalmazhatósága különböző madárrendekben. Magyar állatorvosok lapja, 140(1), 47-59.

Allgayer, M. C., & Cziulik, M. (2007). Reprodução de psitacídeos em cativeiro. Revista Brasileira de Reprodução Animal, 31(3), 344–350.

Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49, 227–267.

Bagemihl, B. (1999). Biological exuberance: Animal homosexuality and natural diversity. New York: St. Martin’s Press.

Breuner, C. W. (2011). Stress and reproduction in birds. In D. O. Norris, & K. H. Lopez (Eds.). Hormones and Reproduction of Vertebrates (Vol. 4, Chap. 5, pp. 129-151). Cambridge: Academic Press.

Buchanan, O. M. (1966). Homosexual Behavior in Wild Orange-Fronted Parakeets. The Condor, 68(4), 399–400.

Çakmak, E., Pekşen, Ç. A., & Bilgin, C. C. (2016). Comparison of three different primer sets for sexing birds. Journal of Veterinary Diagnostic Investigation, 29(1), 59-63.

Caparroz, R., Guedes, N. M. R., Bianchi, C. A., & Wajntal, A. (2001). Analysis of the genetic variability and breeding behaviour of wild populations of two Macaw species (Psittaciformes, Aves) by DNA fingerprinting. Ararajuba, 9(1), 43-49.

Dagg, A. I. (1984). Homosexual behaviour and female‐male mounting in mammals—a first survey. Mammal Review, 14(4), 155–185.

Dalfovo, M. S., Lana, R. A., & Silveira, A. (2008). Métodos quantitativos e qualitativos: um resgate teórico. Revista Interdisciplinar Científica Aplicada, 2(4), 01-13.

Dawson, D. A., Darby, S., Hunter, F. M., Krupa, A. P., Jones, I. L., & Burke, T. (2001). A critique of avian CHD-based molecular sexing protocols illustrated by a Z-chromosome polymorphism detected in auklets. Molecular Ecology Notes, 1(3), 201-204

Dubiec, A., & Zagalska-Neubauer, M. (2006). Molecular techniques for sex identification in birds. Biological Lett, 43(1), 3-12.

Favoretto, G. R. (2016). Comportamento de arara-azul-de-lear (Anodorhynchus leari, Bonaparte, 1856) em cativeiro e a influência da técnica flocking na interação de pares. Dissertação de mestrado, Fundação Parque Zoológico de São Paulo, Universidade Federal de São Carlos, Sorocaba, SP, Brasil.

Franco-Gutiérrez, L. J., Álvarez-Cardona, J., & Soto-Calderón, I. D. (2017). Sex identification of neotropical macaws (Ara spp.) from invasive and non-invasive samples. Ornitología Colombiana, (16), eNB03, 01-07.

Fridolfsson, A-K., & Ellegren, H. (1999). A simple and universal method for molecular sexing of non-ratite birds. Journal of avian biology, 30(1), 116-121.

Gill, F., Donsker, D., & Rasmussen, R. (Eds.). (2020). IOC World Bird List. v. 10.1. http://www.worldbirdnames.org/DOI-10/master_ioc_list_v10.1.xlsx

Griffiths, R., Double, M. C., Orr, K., & Dawson, R. J. G. (1998). A DNA test to sex most birds. Molecular ecology, 7(8), 1071-1075.

Hardy, J. W. (1963). Epigamic and reproductive behavior of the orange-fronted parakeet. The Condor, 65(3), 169-199.

IBGE – Instituto Brasileiro de Geografia e Estatística. (2001). Fauna ameaçada de extinção. Rio de Janeiro: Centro de Documentação e Disseminação de Informações do IBGE.

BirdLife International. (2018). The IUCN Red List of Threatened Species: Ara ararauna. https://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22685539A131917270.en

Jankowiak, Ł., Tryjanowski, P., Hetmański, T., & Skórka, P. (2018). Experimentally evoked same-sex sexual behaviour in pigeons: better to be in a female-female pair than alone. Scientific Reports, 8(1654), 1-7.

Jensen, T., Pernasetti, F. M., & Durrant, B. (2003). Conditions for rapid sex determination in 47 avian species by PCR of genomic DNA from blood, shell-membrane blood vessels, and feathers. Zoo Biology, 22(6), 561-571.

Joseph, L., Toon, A., Schirtzinger, E. E., Wright, T. F., & Schodde, R. (2012). A revised nomenclature and classification for family-group taxa of parrots (Psittaciformes). Zootaxa, 3205, 26-40.

Kahn, N. W., St. John, J., & Quinn, T. W. (1998). Chromosome-specific intron size differences in the avian CHD gene provide an efficient method for sex identification in birds. The Auk, 115(4), 1074-1078.

Kotrschal, K., Hemetsberger, J., & Weiss, B. M. (2006). Making the best of a bad situation: homosociality in male greylag geese. In V. Sommer, & P. L. Vasey (Eds.) Homosexual behaviour in animals: an evolutionary perspective (Chap. 2, pp. 45-76). New York: Cambridge University Press.

MacFarlane, G. R., Blomberg, S. P., & Vasey, P. L. (2010). Homosexual behaviour in birds: frequency of expression is related to parental care disparity between the sexes. Animal Behaviour, 80(3), 375-390.

Mills, J. A. (1994). Extra-pair copulations in the red-billed gull: females with high-quality, attentive males resist. Behaviour, 128(1-2), 41-64.

Miyaki, C. Y., Duarte, J. M. B., Caparroz, R., Nunes, A. L. V., & Wajntal, A. (1997). Sex identification of south american parrots (Psittacidae, Aves) using the human minisatellite probe 33.15. The Auk, 114(3), 516-520.

Ong, A. H. K., & Vellayan, S. (2008). An evaluation of CHD-Specific primer sets for sex typing of birds from feathers. Zoo Biology, 27(1), 62-69.

Pereira, A. S., Shitsuka, D. M., Parreira, F. J., & Shitsuka R. (2018). Metodologia da pesquisa científica (1a ed.). [free e-book]. Santa Maria: Núcleo de Tecnologia Educacional da Universidade Federal de Santa Maria. https://repositorio.ufsm.br/handle/1/15824

Breuner, C. W. (2011). Stress and reproduction in birds. In D. O. Norris, & K. H. Lopez (Eds.). Hormones and Reproduction of Vertebrates (Vol. 4, Chap. 5, pp. 129-151). Cambridge: Academic Press.

Piacentini, V. Q., Aleixo, A., Agne, C. E., Maurício, G. N., Pacheco, J. F., Bravo, G. A., Brito, G. R. R., Naka, L. N., Olmos, F., Posso, S., Silveira, L. F., Betini, G.S., Carrano, E., Franz, I., Lees, A. C., Lima, L. M., Pioli, D., Schunck, F., Amaral, F. R., Bencke, G. A., Cohn-Haft, M., Figueiredo, L. F. A., Straube, F. C., & Cesari, E. (2015). Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. Revista Brasileira de Ornitologia, 23(2), 91-298.

Rodríguez-Mahecha, J. V. R., Suárez, F. R., Arzuza, D. E., & Hernández, A. G. (2005). Loros, Pericos & Guacamayas Neotropicales. Bogotá: Conservación Internacional.

Rudbeck, L., & Dissing, J. (1998). Rapid, simple alkaline extraction of human genomic DNA from whole blood, buccal epithelial cells, semen and forensic stains for PCR. BioTechniques, 25(4), 588-592.

Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning: a laboratory manual (Vol. 3, 2a ed.). New York: Cold Spring Harbor Laboratory Press.

Sanz, V., & Rodriguez-Ferraro, A. (2006). Reproductive parameters and productivity of the yellow-shouldered parrot on Margarita Island, Venezuela: a long-term study. The Condor, 108(1), 178-192.

Sick, H. (1997). Ornitologia brasileira. Rio de Janeiro: Nova Fronteira.

Smith, L. M., & Burgoyne, L. A. (2004). Collecting, archiving and processing DNA from wildlife samples using FTA® databasing paper. BMC ecology, 4, 1-11.

Souza, G. M., & Soares-Filho, A. O. (2005). O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia. Enciclopédia Biosfera, 1(1), 1-11.

Sulandari, S., & Zein, M. S. A. (2012). Application of two molecular sexing methods for indonesian bird species: Implication for captive breeding programs in indonesia. HAYATI Journal of Biosciences, 19(4), 183-190.

Thanou, E., Giokas, S., Goutner, V., Liordos, V., & Fraguedakis-Tsolis, S. (2013). Efficiency and accuracy of PCR-based sex determination methods in the European Phalacrocoracidae. Annales Zoologici Fennici, 50(1-2), 52-63.

Vieira, J. N., Coelho, E. G. A., & Oliveira, D. A. A. (2009). Sexagem molecular em aves silvestres. Revista Brasileira de Reprodução Animal, 33(2), 66-70.

Vucicevic, M., Stevanov‐Pavlovic, M., Stevanovic, J., Bosnjak, J., Gajic, B., Aleksic, N., & Stanimirovic, Z. (2012). Sex determination in 58 bird species and evaluation of CHD gene as a universal molecular marker in bird sexing. Zoo biology, 32(3), 269-276.

Young, L. C., Zaun, B. J., & VanderWerf, E. A. (2008). Successful same-sex pairing in Laysan albatross. Biology Letters, 4(4), 323-325.

Downloads

Published

19/08/2021

How to Cite

PEREIRA, D. C.; MIRABAL, B. .; FRANÇA, A. M. M. de; ANTONIO, E. S. de; FRAGA, R. E.; TOMAZI, L. Molecular sexing in the formation of pairs of blue-and-yellow macaw (Ara ararauna) in reintroduction programs. Research, Society and Development, [S. l.], v. 10, n. 10, p. 570101019330, 2021. DOI: 10.33448/rsd-v10i10.19330. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/19330. Acesso em: 25 oct. 2021.

Issue

Section

Agrarian and Biological Sciences