Review of chromatic disorder in the genus Artibeus (Chiroptera, Phyllostomidae), with new data for A. lituratus (Olfers, 1818)

Marcione Brito de Oliveira; Mariane de Almeida Gentil; Matheus A. Calvano Cosentino; Cibele Rodrigues Bonvicino

doi:10.31687/SaremNMS24.01.4

Autores/as

Marcione Brito de Oliveira Setor de Mastozoologia, Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
Mariane de Almeida Gentil Instituto de Biociências, Universidade Federal do Estado do Rio de Janeiro, Rio de Janeiro, Brazil.
Matheus A. Calvano Cosentino Laboratório de Diversidade e Doenças Virais, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
Cibele Rodrigues Bonvicino Laboratório de Biologia e Parasitologia de Mamíferos, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil.

DOI:

https://doi.org/10.31687/SaremNMS24.01.4

Palabras clave:

Chiroptera, depigmentation, piebaldism, restinga, Sternodematinae

Resumen

The known phenotypic variations in the coat of Artibeus lituratus include cases of albinism, piebaldism and leucism. We are reporting a case of piebaldism in A. lituratus from the Atlantic Forest of the Pau-Brasil Environmental Protection Area, located in the municipality of Armação dos Búzios. The predominant vegetation in the region is “restinga”, a coastal ecosystem on Quaternary marine sandy deposits found along the Brazilian Atlantic coast. This study documents the third case of piebaldism in Brazil, emphasizing the incorrect use of leucism in the literature. Additionally, we provide a review highlighting piebaldism as the most common chromatic anomaly in bats of the genus Artibeus.

Citas

Abreu, M. S., R. Machado, F. Barbieri, N. S. Freitas, & L. R. Oliveira. 2013. Anomalous colour in neotropical mammals: a review with new records for Didelphis sp. (Didelphidae, Didelphimorphia) and Arctocephalus australis (Otariidae, Carnivora). Brazilian Journal of Biology 73:185–94. https://doi.org/10.1590/S1519-69842013000100020.

Aguilar-López, M., P. A. Aguilar-Rodríguez, J. Cruzado-Cortés, M. C. MacSwiney, & J. Ortega. 2021. Noteworthy records of abnormal coloration in Mexican bats. Therya Notes 2:112–116. https://doi.org/10.12933/therya_notes-21-46.

Alves, R. J. V., L. Cardin, & M. S. Kropf. 2007. Disjunção de angiospermas Campos Rupestres–Restingas: uma reavaliação. Acta Botanica Brasilica 21:675–685. https://doi.org/10.1590/S0102-33062007000300014.

Araújo, P., & A. Langguth. 2010. Caracteres distintivos das quatro espécies de grandes Artibeus (Phyllostomidae) de Paraíba e Pernambuco, Brasil. Chiroptera Neotropical 16: 715–722.

Boada, C., & D. G. Tirira. 2010. First record of partial albinism (leucism) in Carollia perspicillata (Phyllostomidae) in Ecuador. Chiroptera Neotropical 16:755–757.

Bôlla, D. A. S., et al. 2017. Assembleia de morcegos (Mammalia: Chiroptera) em ambiente de Restinga alterada no sul do Brasil. Neotropical Biology & Conservation 12:135–142. https://doi.org/10.4013/nbc.2017.122.06.

Bravo-Salinas, R., & J. A. Salas. 2022. Chromatic disorder in Trachops cirrhosus (Spix, 1823) (Chiroptera: Phyllostomidae) on Ecuadorian Amazon. Revista Peruana de Biologia 29:1–6. https://doi.org/10.15381/rpb.v29i4.23598.

Brito, J., & K. Valdivieso-Bermeo. 2016. First records of leucism in eight species of small mammals (Mammalia: Rodentia). Therya 7:483–489. https://doi.org/10.12933/therya-16-408.

Caro, T. 2005. The adaptive significance of coloration in mammals. BioScience 55:125–136. https://doi.org/10.1641/0006-3568(2005)055[0125:TASOCI]2.0.CO;2.

Chacón, J. J., C. M. G. Charrasquiel, & J. B. Correa. 2015. Registro de leucismo en Artibeus planirostris (Chiroptera: Phyllostomidae) en Colombia. Acta Zoológica Mexicana 31:125–128.

Davis, J. N. 2007. Color abnormalities in birds: a proposed nomenclature for birders. Birding 39:36–46.

de Oliveira, M. B., M. L. Brandão, J. L. P. Cordeiro, L. F. B. Oliveira, & A. L. Peracchi. 2020. Composition and frequency of capture of bat assemblages in a landscape mosaic in northern Pantanal, Mato Grosso, Brazil. Mastozoología Neotropical 27:39–52. https://doi.org/10.31687/saremMN.20.27.1.0.25.

Díaz, M. M., S. Solari, R. Gregorin, L. F. Aguirre, & R. M. Barquez. 2021. Clave de identificación de los murciélagos neotropicales. Publicación Especial Nº 4 – PCMA (Programa de Conservación de los Murciélagos de Argentina), Tucumán.

Fernández de Córdova, J., C. Nivelo-Villavicencio, & P. X. A. Webster. 2017. Primer reporte de leucismo para Artibeus fraterculus (Chiroptera: Phyllostomidae) en Ecuador. Revista Biodiversidad Neotropical 7:114–118. https://doi.org/10.18636/bioneotropical.v7i1.555.

Fertl, D., & P. E. Rosel. 2009. Albinism. Encyclopedia of marine mammals (W. F. Perrin, B. Würsig, & J. G. M. Thewissen, eds.). Academic Press. https://doi.org/10.1016/B978-0-12-373553-9.X0001-6.

Flores Salazar, S. A. 2021. Registros de leucismo en cuatro especies de murciélagos (orden: Chiroptera) en la estación de biodiversidad Tiputini (EBT) en Ecuador: Vampyressa thyone, Uroderma bilobatum, Artibeus obscurus y Noctilio albiventris. Tesis de Doctorado. Universidad San Francisco de Quito, Ecuador.

García, F. J., M. Machado, G. Flórez, P. Soriano, & H. Cabrera. 2020. Anomalous coloration in Neotropical mammals: new cases of pigmentation disorders in Venezuelan mammals revealed by review of natural history museums. Memoria de la Fundación La Salle de Ciencias Naturales 78:5–20.

García-Morales, R., A. E. Rojas-Martínez, E. S. Ávila Gómez, & C. E. Moreno. 2013. Leucism in the giant fruit-eating bat (Artibeus lituratus Olfers, 1818) in the state of Hidalgo, Mexico. Chiroptera Neotropical 19:1212–1215.

García-Morales, R., D. T. Duran, E. S. A. Gómez, C. E. Moreno, & M. S. Akmentis. 2012. Registro de leucismo en Sturnira ludovici y Artibeus jamaicensis (Phyllostomidae) en México. Chiroptera Neotropical 18:1101–1105.

García-Restrepo, S., M. J. Andrade-Erazo, P. J. Castiblanco-Camacho, Y. Escobar-Aguirre, P. D. Herreño-Rodríguez, & J. E. Carrero-Herrera. 2023. New reports of morphological anomalies in leaf-nosed bats (Chiroptera: Phyllostomidae) from Colombia. Mammalia 87:292–300. https://doi.org/10.1515/mammalia-2022-0067.

Hoekstra, H. E. 2006. Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 97:222–234. https://doi.org/10.1038/sj.hdy.6800861.

Hofreiter, M., & T. Schöneberg. 2010. The genetic and evolutionary basis of colour variation in vertebrates. Cellular and Molecular Life Sciences 67:2591–2603. https://doi.org/10.1007/s00018-010-0333-7.

INEA. 2023. Instituto Estadual do Ambiente. Estado do Rio de Janeiro. <http://www.inea.rj.gov.br/>.

Jehl, J. R. 1985. Leucism in eared grebes in western North America. The Condor 87:439–441.

Leal, E. S., T. C. Lira, A. C. Garcia, & M. A. Montes. 2021. Albinism in Artibeus planirostris (Chiroptera, Phyllostomidae) in the Caatinga biome and updated list of albino bats in Brazil. Anais da Academia Brasileira de Ciências 93:e20200582. https://doi.org/10.1590/0001-3765202120200582.

López-Wilchis, R., & Y. León. 2012. A noteworthy case of leucism in Artibeus lituratus (Chiroptera: Phyllostomidae) from Oaxaca, Mexico. Chiroptera Neotropical 18:1111–1114.

Lucati, F., & A. López-Baucells. 2017. Chromatic disorders in bats: a review of pigmentation anomalies and the misuse of terms to describe them. Mammal Review 47:112–123. https://doi.org/10.1111/mam.12083.

Luz, J. L., R. Mangolin, C. E. L. Esbérard, & H. D. G. Bergallo. 2011. Morcegos (Chiroptera) capturados em lagoas do Parque Nacional da Restinga de Jurubatiba, Rio de Janeiro, Brasil. Biota Neotropica 11:161–168.

Marin-Vasquez, A., M. Ortega-Rincón, & H. E. Ramírez-Chaves. 2010. Records of leucism in three species of Colombian bats: Carollia brevicauda, Artibeus jamaicensis and Lophostoma silvicolum (Phyllostomidae). Chiroptera Neotropical 16:706–709.

Møller, A. P., & T. A. Mousseau. 2001. Albinism and phenotype of barn swallows (Hirundo rustica) from Chernobyl. Evolution 55:2097–104. https://doi.org/10.1111/j.0014-3820.2001.tb01324.x. PMID: 11761068.

Moreno, C. R., T. Pollock, L. Sánchez, & E. C. Mora. 2020. Acoustical and morphological comparisons between albino and normally-pigmented Jamaican fruit bats (Artibeus jamaicensis). Caribbean Journal of Science 50:1–8. https://doi.org/10.18475/cjos.v50i1.a1.

Muñoz-Romo, M., D. Ruiz-Ramoni, & P. Ramoni-Perazzi. 2014. First record of leucism in the giant fruit-eating bat, Artibeus amplus (Chiroptera: Phyllostomidae). Chiroptera Neotropical 20:1301–1304.

Oetting, W. S., et al. 2009. The R402Q tyrosinase variant does not cause autosomal recessive ocular albinism. American Journal of Medical Genetics Part A 149:466–469. https://doi.org/10.1002/ajmg.a.32654.

Olarte-González, G., I. M. Vela-Vargas, & Á. Jiménez. 2014. Primer Reporte de leucismo en Artibeus lituratus (Olfers, 1818)(Phyllostomidae: Stenodermatinae) en el Caribe colombiano. Mammalogy Notes 1:7–8. https://doi.org/10.47603/manovol1n1.7-8.

Oliveira, H. F., & L. M. Aguiar. 2008. A new case of complete albinism in a bat from Brazil. Chiroptera Neotropical 14:421–423.

Pereira, A. D., M. O. Bordignon, & V. C. Tavares. 2017. Subfamília Stenodermatinae. História natural dos morcegos Brasileiros: chave de identificação de espécies (N. R. Reis, A. L. Peracchi, C. B. Batista, I. P. Lima, & A. D. Pereira, eds.). Technical Books Editora, Rio de Janeiro.

Reis, N. R., A. L. Peracchi, C. B. Batista, I. P. Lima, & A. D. Pereira (eds.). 2017. História natural dos morcegos Brasileiros: chave de identificação de espécies. Technical Books Editora, Rio de Janeiro.

Ruelas, D., M. Ramos, M. Molina, & V. Pacheco . 2016. Primer registro de leucismo en Glossophaga soricina valens (Phyllostomidae: Chiroptera) en Perú. Therya 7:343–352. https://doi.org/10.12933/therya-16-381 ISSN 2007-3364.

Rui, A. M., M. E. Fabián, & J. O. Menegheti. 1999. Distribuição geográfica e análise morfológica de Artibeus lituratus Olfers e de Artibeus fimbriatus Gray (Chiroptera, Phyllostomidae) no Rio Grande do Sul, Brasil. Revista Brasileira de Zoologia 16:447–460. https://doi.org/10.1590/S0101-81751999000200011.

Sánchez-Hernández, C., et al. 2012. Leucism in five species of bats from Mexico. Chiroptera Neotropical 18:1123–1127.

Sánchez-Hernández, C., M. L. Romero-Almaraz, A. Taboada-Salgado, J. A. Almazán-Catalán, G. D. Schnell, & L. Sánchez-Vazquez. 2010. Five albino bats from Guerrero and Colima, Mexico. Chiroptera Neotropical 16:522–527.

Souza, R. D. F., et al. 2013. First record of leucism in Artibeus lituratus (Olfers, 1818) (Phyllostomidae) in Brazil. Chiroptera Neotropical 19:1216–1219.

Talamoni, S., P. I. M. Viana, C. G. Costa, L. Palú, R. B. Oliveira, & L. M. Pessôa. 2017. Occurrence of leucism in Eira barbara (Carnivora, Mustelidae) in Brazil. Biota Neotropica 17:e20170328. https://doi.org/10.1590/1676-0611-BN-2017-0328.

Tello, C., D. G. Streicker, J. Gómez, & P. M. Velazco. 2013. New records of pigmentation disorders in molossid and phyllostomid (Chiroptera) bats from Peru. Mammalia 78:191–197. http://doi.org/0.1515/mammalia-2013–0019.

Trujillo, L. A., & R. Barahona. 2014. First record of leucism in Artibeus phaeotis (Miller, 1902) (Chiroptera:Phyllostomidae) from Guatemala. Chiroptera Neotropical 20:1252–1254.

Uieda, W. 2000. A review of complete albinism in bats with five new cases from Brazil. Acta Chiropterologica 2:97–105.

Uieda, W. 2001. Behavior of an albino vampire bat, Desmodus rotundus (E. Geoffroy) (Chiroptera, Phyllostomidae), in captivity. Revista Brasileira de Zoologia 18. https://doi.org/10.1590/S0101-81752001000200031.

Velandia-Perilla, J. H., A. P. Yusti-Muñoz, M. A. Sánchez-Martínez, & A. Giraldo. 2013. Leucismo en murciélagos de hoja nasal (Chiroptera, Phyllostomidae) de Colombia. Boletín Científico. Centro de Museos. Museo de Historia Natural 17:87–94.

Ventorin, M. L., B. M. Dell'Antonio, J. P. M. Hoppe, & A. D. Ditchfield. 2021. First record of albinism in Artibeus obscurus (Chiroptera: Phyllostomidae) in an Atlantic Forest area. Notas sobre Mamíferos Sudamericanos 3:e21.1.2. https://doi.org/10.31687/saremNMS.21.1.2.

Zalapa, S. S., S. Guerrero, R. A. M. de Lourdes, & C. Sánchez-Hernández. 2016. Coloración atípica en murciélagos: frecuencia y fenotipos en Norte y Centroamérica e islas del Caribe y nuevos casos para México y Costa Rica. Revista Mexicana de Biodiversidad 87:474–482. https://doi.org/10.1016/j.rmb.2016.04.007.