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Revista latinoamericana de herpetología

versão On-line ISSN 2594-2158

Rev. latinoam. herpetol. vol.6 no.1 Ciudad de México Jan./Mar. 2023  Epub 31-Ago-2023

https://doi.org/10.22201/fc.25942158e.2023.01.476 

Notas científicas

First Record of Complete Albinism in a Species of the Genus Pristimantis Jiménez de la Espada, 1870 (Anura: Strabomantidae) in the Ecuadorian Andes

Primer registro de albinismo completo en una especie del género Pristimantis Jiménez de la Espada, 1870 (Anura: Strabomantidae) en los Andes ecuatorianos

Culebras Jaime1  2  3  * 

Francesca Nicole Angiolani-Larrea4 

1 Photo Wildlife Tours, Isla Isabela 1021 y Río Coca, 170501, Quito, Ecuador.

2 Fundación Cóndor Andino, Tamayo N24-260 y Lizardo García, 170523, Quito, Ecuador.

3 The Biodiversity Group, Tucson, Arizona, United States.

4 Division of Behavioural Ecology, Institute of Ecology and Evolution, University of Bern, Bern 3012, Switzerland.


Abstract

We found an albino individual of the genus Pristimantis in the Ecuadorian Andes. This is the first case of complete albinism for direct-developing anurans in the Neotropics and the first record in amphibians for Ecuador.

Key words: chromatic anomalies; albinism; Pristimantis; coloration; direct development; Ecuador

Resumen

Encontramos un individuo albino del género Pristimantis en los Andes ecuatorianos. Este es el primer caso de albinismo completo para anuros de desarrollo directo en el Neotrópico y el primer registro en anfibios para el Ecuador.

Palabras clave: anomalías cromáticas; albinismo; Pristimantis; coloración; desarrollo directo; Ecuador

Although cases of albinism are rare in nature, it has been reported in several groups of vertebrates, e.g. reptiles (Valencia, 2009; Perrault & Coppenrath, 2019; García-Roa, 2020), mammals (Abreu et al., 2013; Lucati & López-Baucells, 2017), birds (Van Grouw, 2013), and fishes (Manoel et al., 2017). The terms “albinism” and “partial albinism” have been historically used by many authors indistinctively to describe different types of anomalies which encompass leucism (lack of melanin in the entire body, except for eyes which present normal coloration), piebaldism (certain patches or parts of the animal are lacking melanin), and true albinism, that can be recognized by the white phenotype in the body and reddish eyes (Lucati & López-Baucells, 2017). These colour anomalies are the most commonly reported for amphibians, with cases of partial or complete albinism reported in 86 anuran species and 64 urodeles (Henle et al., 2017). This phenomenon might be due to genetic mutations, chemical pollution, disease, UV radiation, temperature, parasites or injury (Henle et al., 2017; Lucati & López-Baucells, 2017; Lunghi et al., 2017).

Albinism in anurans has been reported in larvae (Brassaloti & Bertoluci, 2008; Martinuzzi et al., 2016; Fonseca et al., 2021), and in adults (Spadola & Insacco, 2010; Toledo et al., 2011). However, as mentioned before, there has been much confusion over the use of the term “albinism” to describe different chromatic anomalies (e.g., leucism, piebaldism and true albinism), especially under the term “partial albinism” (Henle et al., 2017; Lucati & López-Baucells, 2017).

On 6 October 2021 at 00:05h at Cloud Forest Organics, Baeza, Napo, Ecuador (-0.43642; -77.89583; 2,219 m a.s.l.) we found an albino adult individual of the genus Pristimantis. A photo voucher was deposited at Centro Jambatu, Quito, Ecuador (CJ12484; Fig. 1). We refer the mentioned individual as Pristimantis sp. because it is from a population that is between two newly described species (Bejarano-Muñoz et al., 2022), but due to their resemblance, we cannot confirm the correct identification of the species. The albino individual was found 150 cm from ground level on a leaf 10 m away from a stream in secondary forest. The individual was active similar to other individuals of the same species that we found less than 50 m away. The other individuals showed normal coloration ranging from dark to light brown (Fig 2).

Figure 1 A) dorsolateral and B) frontal views of the albino individual of Pristimantis sp. found in Baeza, Ecuador (Photo voucher CJ12484). Figura 1. A) vistas dorsolateral y B) frontal del ejemplar albino de Pristimantis sp. encontrado en Baeza, Ecuador (Foto voucher CJ12484). 

Figure 2 A) and B) dorsolateral view of normally coloured individuals of Pristimantis sp. found in the same locality as albino individual. Figura 2. A) y B) vista dorsolateral de individuos de Pristimantis sp. con coloración normal encontrados en la misma localidad que el individuo albino. 

This is the first case of true albinism in the genus Pristimantis Jiménez de la Espada, 1870, the first for New World direct-developing anurans (species in which there is no free-living larval stage), and also for Ecuadorian amphibians. The genus Pristimantis, from the Strabomantidae family, is the most diverse vertebrate groups in the world (Mendoza et al., 2015; Waddell et al., 2018), with more than 590 species distributed from eastern Honduras to northern Argentina and some Caribbean islands (Frost, 2021).

For direct-developing frogs (Brachycephaloidea) there are two previous records of chromatic anomalies, both in species from the family Eleutherodactylidae: Eleutherodactylus planirostris (Petrovic, 1973) and E. zeus (García-Padrón & Bosch, 2019), however, the two cases correspond to piebaldism. In the report for E. planirostris (Petrovic, 1973), although the author refers to it as albino, describes the specific dark coloration in the head of the individual.

Some authors hypothesize that, due to predation, albinism might increase selective pressure against these individuals (Childs, 1953; Petrovic, 1973: Toledo et al., 2011; Silva-Caballero et al., 2014). Nevertheless, Stephenson et al. (2022) did not find differences on the attack rate of birds among albino and normal phenotypes of the eastern garter snakes. On the other hand, Sazima & Di-Bernardo (1991) suggest that survival of albino individuals is greater in species with nocturnal habits, since selective pressure is higher on diurnal animals as their predators are more visually oriented. Fonseca et al. (2021) found only tadpoles and newly methamorphosed albino individuals in a population of Leptodactylus macrosternum, suggesting that this could be evidence of higher risk of predation on these individuals. However, also suggest that due to the nocturnal and fossorial habits of adults of L. macrosternum, albino individuals could increase their chances of survival. Other authors proposed that animals with an uncommon phenotype (e.g., albinism) could be less predated because some predators may reject them as a prey (Tinbergen, 1960) due to some sort of neophobia. It is clear that further studies are required to understand better the implication of predation in frogs -and other animal groups- with abnormal colorations (Childs, 1953) thus, we suggest caution when drawing conclusions based on casual observations.

Finally, when albino recessive gene is present in a population, the frequency of albinism may increase in consequence of high levels of deforestation and fragmentation that drive the populations into isolation enhancing inbreeding (Chetnicki et al., 2007; Russell et al., 2011; Gilhen et al., 2012; Prado-Martinez et al., 2013; Espinal et al., 2016).

Acknowledgements

This work was done under collection permit number N°MAE-ARSFC-2019-0163. We thank Craig Leon and the staff of Cloud Forest Organics for the logistic, financing and help in the field, and Anyelet Valencia-Aguilar for her valuable revision and comments of this manuscript.

Cited literature

Abreu, M.S.L., 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 73:185-194. [ Links ]

Bejarano-Muñoz, P., S.S. Ron, M.J. Navarrete & M.H. Yánez-Muñoz. 2022. Dos nuevas especies del grupo Pristimantis boulengeri (Anura: Strabomantidae) de la cuenca alta del río Napo, Ecuador. Cuadernos de Herpetología 36:125-154. [ Links ]

Brassaloti, R. & J. Bertoluci. 2008. Albinism in tadpoles of Rhinella ornata (Anura, Bufonidae) from southeastern Brazil. Herpetological Bulletin 106:31-33. [ Links ]

Chetnicki, W., S. Fedyk & U. Bajkowska. 2007. Cases of coat colour anomalies in the common shrew, Sorex araneus L. Folia Biologica 55:73-76. [ Links ]

Childs, H.E. 1953. Selection by predation on albino and normal spadefoot toads. Evolution 7:228-233. [ Links ]

Espinal, M., J.M Mora, L.A Ruedas, L.I López & L. Marineros. 2016. A case of albinism in the central American spider monkey, Ateles geoffroyi, in Honduras. Mastozoología Neotropical 23:63-69. [ Links ]

Fonseca, M.G., K.O.R. Picheli & M.V. Garey. 2021. Albinism in Leptodactylus macrosternumMiranda-Ribeiro, 1926 (Anura: Leptodactylidae) in south Piauí, northeastern Brazil. Herpetology Notes 14:731-733. [ Links ]

Frost, D.R. 2021. Amphibian Species of the World: an Online Reference. Version 6.1. https://amphibiansoftheworld.amnh.org/ . American Museum of Natural History, New York, USA. [Accessed on May 2022]. [ Links ]

García-Padrón, L.Y. & R.A. Bosch. 2019. Anomalous colour in a Cuban cave-dwelling frog: first record of piebaldism in Eleutherodactylus zeus (Anura: Eleutherodactylidae). Herpetological Bulletin 157:1-3. [ Links ]

García-Roa, R. 2020. An albino ladder snake (Zamenis scalaris) found dead with a partially swallowed rabbit. Boletín de la Asociación Herpetológica Española 31:54-56. [ Links ]

Gilhen, J., G. Caswell, C. Drake, M. MacDonald & H. McKinnonramshaw. 2012. A partial albino hatchling Northern Ring-necked Snake, Diadophis punctatus edwardsii, from Big Tancook Island, Mahone Bay, Lunenburg County, Nova Scotia, Canada. The Canadian Field-Naturalist 126:336-339. [ Links ]

Henle, K., A. Dubois & V. Vershinin. 2017. A review of anomalies in natural populations of amphibians and their potential causes. Mertensiella 25:57-164. [ Links ]

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. [ Links ]

Lunghi, E., A. Monti, A. Binda, I. Piazzi, M. Salvadori, R. Cogoni, L.A. Riefolo, C. Biancardi, S. Mezzadri, D. Avitabile, G.F. Ficetola, M. Mulargia, S. Manca, P. Blaimont, A.R DiCerbo & R. Manenti. 2017. Cases of albinism and leucism in amphibians in Italy: new reports. Natural History Sciences. Atti della Società italiana di scienze naturali e del Museo civico di storia naturale di Milano 4:73-80. [ Links ]

Manoel, P.S., E.R. Ono & M.I.B. Alves. 2017. First report of albinism in the South American catfish Imparfinis mirini (Siluriformes: Heptapteridae). Enfermería Universitaria 88:471-473. [ Links ]

Martinuzzi, C., P.M. Peltzer, A.M. Attademo, C.M. Junges & R.C. Lajmanovich. 2016. Albinism in larvae of the Chacoan frog Leptodactylus chaquensis (Anura, Leptodactylidae) from an urban lake from Argentina. Cuadernos de Herpetología 30:69-73. [ Links ]

Mendoza, Á.M., O.E. Ospina, H. Cárdenas-Henao & J.C García-R.. 2015. A likelihood inference of historical biogeography in the world’s most diverse terrestrial vertebrate genus: Diversification of direct-developing frogs (Craugastoridae: Pristimantis) across the Neotropics. Molecular Phylogenetics and Evolution 85:50-58. [ Links ]

Perrault, J.R. & C.M. Coppenrath. 2019. Albinism in Florida Green Turtle (Chelonia mydas) Hatchlings: Ratio-Based Evidence Of Basic Mendelian Recessiveness. Marine Turtle Newsletter 156:3840. [ Links ]

Petrovic, C.A. 1973. An “Albino” Frog. Eleutherodactylus planirostris Cope. Journal of Herpetology 7:49-51. [ Links ]

Prado-Martinez, J., I. Hernando-Herraez, B. Lorente-Galdos, M. Dabad, O. Ramirez, C. Baeza-Delgado, C. Morcillo-Suarez, C. Alkan, F. Hormozdiari, E. Raineri, J. Estellé, M. Fernandez-Callejo, M. Valles, L. Ritscher, T. Schöneberg, E. De la Calle-Mustienes, S. Casillas, R. Rubio-Acero, M. Melé, J. Engelken, M. Caceres, J.L. Gomez-Skarmeta, M. Gut, J. Bertranpetit, I.G. Gut, T. Abello, E.E. Eichler, I. Mingarro, C. Lalueza-Fox, A. Navarro & T. Marques-Bonet. 2013. The genome sequencing of an albino Western lowland gorilla reveals inbreeding in the wild. BMC Genomics 14:1-8. [ Links ]

Russell, R.W., W. Beslin, M. Hudak, A. Ogunbiyi, A. Withrow & J. Gilhen. 2011. A second amelanistic Eastern Red-backed Salamander, Plethodon cinereus, from Nova Scotia, Canada. The Canadian Field-Naturalist 125:359-362. [ Links ]

Sazima, I. & M. Di-Bernardo. 1991. Albinismo em serpentes neotropicais. Memórias do Instituto Butantan 53:167-173. [ Links ]

Silva-Caballero, A., F. Montiel-Reyes, E. Sánchez-Garibay & J. Ortega. 2014. Leucismo en el coatí de nariz blanca Nasua narica (Mammalia: Carnivora), en Quintana Roo, México. Therya 5:839-843. [ Links ]

Spadola, F. & G. Insacco. 2010. Incomplete albinism in Discoglossus pictus (Otth, 1837). Acta Herpetologica 5:245-253. [ Links ]

Stephenson, B.P., Z. Velani & N. Ihász. 2022. The effect of albinism on avian predator attack rates in eastern garter snakes. Zoology 150:125987. [ Links ]

Tinbergen, L. 1960. The natural control of insects in pinewoods. Archives Néerlandaises de Zoologie 13:265-343. [ Links ]

Toledo, L.F., N.R. da Silva & O.G.D.S. Araújo. 2011. Albinism in two Amazonian frogs: Elachistocleis carvalhoi (Microhylidae) and Lithobates palmipes (Ranidae). Herpetology Notes 4:145-146. [ Links ]

Valencia, J.H. 2009. Albinism in Ninia hudsoni Parker, 1940 from Ecuador. Herpetozoa 21:190-192. [ Links ]

Van Grouw, H. 2013. What colour is that bird? British Birds 106:17-29. [ Links ]

Waddell, E.H., M. Crotti, S.C. Lougheed, D.C. Cannatella & K.R. Elmer. 2018. Hierarchies of evolutionary radiation in the world’s most species rich vertebrate group, the Neotropical Pristimantis leaf litter frogs. Systematics and Biodiversity 16:807-819. [ Links ]

Received: May 25, 2022; Accepted: December 26, 2022; Published: February 15, 2023

* Correspondence: jaimebio85@gmail.com.

Editor: Francisco Brusquetti, Paraguay.

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