Herpetology Notes, volume 8: 179-181 (2015) (published online on 10 April 2015)

Leucism in the Amazonian diurnal frog Anomaloglossus stepheni (Martins, 1989) (Anura: Aromobatidae)

Leandro João Carneiro de Lima Moraes1,* and Igor Luis Kaefer2

Phenotypic abnormalities in coloration patterns can and immunological abnormalities (e.g., Turkozan and occur in individuals of a certain species usually due to Durmus, 2001; Sanabria et al., 2010). genetic or environmental factors that cause an excess The genus Anomaloglossus comprises 29 species or deficit in the metabolism of dermal pigmentation, that inhabit tropical forests of northern Amazon restricted to a region or throughout the entire body region, with only four species recorded from Brazil: (Duellman and Trueb, 1994; Hayley-McCardle, 2012). A. baeobatrachus (Boistel and de Massary, 1999), A. Several divergent classifications for these events are roraima (La Marca, 1997), A. stepheni (Martins, 1989) based on extent of pigmentation loss, but among the and A. tamacuarensis (Myers and Donnelly, 1997) main recognized types we can cite the piebaldism, (Frost, 2015). Anomaloglossus stepheni is a small- leucism and albinism (Miller, 2005; Abreu et al., 2013). sized (14-18 mm) frog distributed along the French Piebaldism occurs when there are depigmented blotches Guiana, Suriname and Brazil and is one of the most along the animal’s body (Acevedo et al., 2009) and abundant amphibians in the forest litter from the region leucism when the animal’s body is partially or totally of Presidente Figueiredo and Manaus municipalities in depigmented, with remaining margins of the body and Amazonas State, Brazil (Deichmann et al., 2010; Lima eyes pigmented, as albinism occurs in animals with et al., 2012). complete absence of pigmentation, including the eyes, On 09 June 2014, we found an adult, unvouchered which becomes reddish or pink (Fertl and Rosel, 2002; male of A. stepheni with some level of depigmentation Miller, 2005). Although many cases of depigmentation but retention of eye color, configuring a case of for the major vertebrates lineages are documented, such leucism. The specimen was found active at 10:55 am as for fishes (e.g., Teixeira and Araújo, 2002), birds in the leaf litter of a primary dense forest area located (e.g., Nogueira and Alves, 2011), reptiles (e.g., Abegg in the municipality of Presidente Figueiredo (-1.9877, - et al., 2014; Erickson and Kaefer, in press), mammals 60.0591). This location is inside the limits of a protected (e.g., Abreu et al., 2013) and amphibians (e.g.,Toledo touristic complex settled around the Igarapé Santa Cruz, et al., 2011; Elgue et al., 2013), these events are rare a large tributary of the Negro River. The only other in natural populations (Bechtel, 1995), since the loss species of criptically colored aromobatid found in this of pigmentation makes individuals more susceptible region are Allobates sumtuosus (Morales, 2002), that to visually-oriented predators (Parsons and Bonderup- differs morphologically of A. stepheni principally by Nielsen, 1995) or is associated with morphological more slender appearance (robust in A. stepheni) the presence of a continuous dark band from rostrum to cloaca (interrupted in the middle of body in A. stepheni) and the different hind limb coloration compared with dorsum (similar in A. stepheni) (Martins, 1989; Lima et al., 2012). Despite the depigmentation on the registered 1 Instituto Nacional de Pesquisas da Amazônia - INPA. Av. individual of A. stepheni, these diagnostic characters Efigênio Sales 2239, 69060-020, Manaus, Amazonas, Brazil can be noted. The specimen showed a marked reduction 2 Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Av. Rodrigo Octávio 6200, 69077-000, Manaus, of dark pigment (melanin) in the whole body skin, as Amazonas, Brazil. compared to a normal coloration specimen (Fig. 1), * Corresponding author. E-mail: [email protected] thus lacking the large dark bands present in rostral 180 Leandro João Carneiro de Lima Moraes & Igor Luis Kaefer

Figure 1. Comparative dorsolateral, ventral and lateral views of leucistic (A, B, C) and normal (D, E, F) adults of Anomaloglossus stepheni (Martins, 1989) from Central Amazonia. Photos by L.J.C.L. Moraes (A, B, C, D, F) and Lima et al., 2012 (E).

and lateral regions, the transverse dark bars of limbs, Blouin, 2000; Vitt and Caldwell, 2013). Studying color and the dark spots present along the dorsal region. anomalies in snakes, Sazima and Di-Bernardo (1991) Nevertheless, the dorsal brownish coloration typical suggested that the survival rate is lower in depigmented of this species probably remained due to other types individuals of species with diurnal activity, as they are of chromatophores (Browder, 1968). We discarded the more subject to selective pressures related to visually- possibility of such depigmentation be caused by diseases oriented diurnal predators. This seems to be the reason due to the large amount of the body dominated by white why the loss of pigmentation is little documented color, since depigmentation caused by parasitic, fungal for adults of diurnal species of the frog superfamily or bacterial diseases in amphibians occurs in a punctual Dendrobatoidea (Dendrobatidae + Aromobatidae), and scattered manner along the body (Pessier, 2002). which shelters lineages that depend of their normal In addition, the animal had a healthy appearance and coloration pattern for both defense (aposematic moved normally under the leaf litter, showing no signs coloration) and camouflage (cryptic coloration), such of rash, itch, weight loss or fatigue. as the species recorded in this study. We hypothesized As coloration patterns play an important role in life that this depigmented individual of A. stepheni reached history of individuals, any phenotypic abnormality adulthood because the loss of dark pigmentation mainly can affect them positively or negatively (Hoffman and affected its ventrolateral region, with retention of Leucism in the Amazonian diurnal frog Anomaloglossus stepheni 181 most of its dorsal cryptic coloration, and consequently accessed on 06 January 2015. maintenance of its camouflage function. However, Hayley-McCardle, B.S. (2012): Albinism in wild vertebrates. – further development of this hypothesis depends on new Unpublished MSc Dissertation, Science Texas State University, San Marcos, USA, 71 pp. records of diurnal frogs with loss of pigmentation in Hoffman, E., Blouin M. 2000. A review of colour and pattern natural populations or experimental studies with these polymorphisms in anurans. Biological Journal of the Linnean species under controlled conditions, so that we can Society 70: 633–665. better understand this phenomenon and its physiological La Marca, E. (1997): Ranas Del gênero Colostethus (Amphibia: and ecological implications. Anura: Dendrobatidae) de la Guayana Venezolana con la descripción de siete especies nuevas. Publicaciones de la Acknowledgements We thank to M.F.A. Maximiano, F.B.R. Asociación de Amigos de Doñana. Sevilla 9: 1–64. Gomes and R.C.L. Gomes for the company in the day of this Lima, A.P., Magnusson, W.E., Menin, M., Erdtmann, L.K., record. We also thank P.I. Simões for confirming species Rodrigues, D.J., Keller, C., Hödl, W. (2012): Guia dos sapos da identification and T. Chiariello for discussions on the disease Reserva Adolpho Ducke - Amazônia Central/Guide to the frogs hypothesis. The Conselho Nacional de Desenvolvimento of Reserva Adolpho Ducke - Central Amazonia. 2nd edition. 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