Herpetology Notes, volume 14: 969-971 (2021) (published online on 07 July 2021)

Melanism in Leptodactylus aff. podicipinus (Anura: Leptodactylidae) from southern Amapá, Brazil

Jackson Cleiton Sousa1, Fillipe Pedroso-Santos2, Débora Regina dos Santos Arraes3, Janaina Freitas Calado3, Patrick de Castro Cantuária4, Vinícius A.M.B. de Figueiredo2, and Carlos Eduardo Costa-Campos2,*

The presence of dark-coloured body colouration characterised by presenting a white or yellowish anomalies (melanism) is a pervasive phenomenon in body colour and red eyes (albinism), white or pinkish the animal kingdom, particularly in amphibians (Alho body colour, with dark eyes (leucism), and colouring et al., 2010; Kolenda et al., 2017; Vásquez-Cruz et al., appearing dark blue or grey (axanthism) (Jablonski et 2020), lizards (Escudero et al., 2016; Recknagel et al., al., 2014; Chilote and Moreno, 2019). Melanism has 2018), and snakes (Costa-Campos et al., 2015; Barbosa previously been reported in salamanders (Lunghi et al., et al., 2019; Martins et al., 2019). Melanism is involved 2017; Vásquez-Cruz et al., 2020), however very few in a wide range of non-mutually exclusive vital adaptive information is available on anurans (Alho et al., 2010). functions that are associated with different aspects of life In the Amapá state, there is only one report of colour history, such as reproductive signaling (Griffith et al., anomaly in an anuran (leucism; see Tavares-Pinheiro et 2006) and thermal biology (Vences et al., 2002; Clusella al., 2020). Trullas et al., 2007), and is characterised as a chromatic Here we present the first case of melanism in anomaly caused by an excessive concentration of Leptodactylus aff. podicipinus (Cope, 1862). This frog melanin or black-brown pigment in the skin, melanistic is a small-moderate size species (snout-vent length = individuals exhibiting a darker phenotype (Gilhen and 24.5–54.0 mm), terrestrial and nocturnal frog belonging Scott, 2014). to the L. melanonotus group and distributed from central In anurans, the most frequent pigmentary abnormalities Brazil, extending along the Madeira and Amazonas are albinism, leucism and axanthism (e.g., Toledo Rivers within the Amazon basin (Frost, 2020). This et al., 2011; Moraes and Kaefer, 2015; Araújo et al., species is well adapted to anthropogenic disturbance 2020; Tavares-Pinheiro et al., 2020), with reports also and is found in open formations where males call amidst in tadpoles (in this case albinism; e.g., Rodrigues and the vegetation at the edge of temporary and permanent Oliveira, 2004; Johnston, 2006; Sanabria and Laspiur, water bodies (De Sá et al., 2014). Our identification of 2010; Elgue et al., 2013), in which individuals are such a specimen is based on a revalidation of its junior synonym still in progress. Our record occurred during the night on 2 December 2017 in a flooded area (0.0358º S, 51.1591º W, datum 1 Universidade Federal do Amapá, Programa de Pós-Graduação WGS84, 26 m a.s.l.), located in the municipality em Biodiversidade Tropical, 68.903-419, Macapá, Amapá, Brazil. of Santana, State of Amapá, Brazil. We observed a 2 Universidade Federal do Amapá, Departamento de Ciências melanistic individual of Leptodactylus aff. podicipinus Biológicas e da Saúde, Laboratório de Herpetologia, Campus with totally dark dorsum and maculated black pattern Marco Zero do Equador, 68.903-419, Macapá, AP, Brazil. with light spots scattered at the ventral part of the 3 Universidade do Estado do Amapá, Curso de Ciências body. Given the unusual appearance of the anuran, we Naturais, Avenida Presidente Vargas, 68.900-070, Macapá, captured it to see if its particular dark colour would AP, Brazil. 4 Instituto de Pesquisas Científicas e Tecnológicas do Estado do remain until the next day, in which we photographed Amapá, Avenida Juscelino Kubitschek, Fazendinha, 68.903- the individual exposed to daylight in the laboratory 970, Macapá, AP, Brazil. (Fig. 1A, B). We did not observe changes in its uniform * Corresponding author. E-mail: dark pigmentation and the animal maintained the [email protected] same characteristics observed in its natural habitat. We © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. deposited this melanistic species in the Herpetological 970 Jackson Cleiton Sousa et al.

Figure 1. Adult of Leptodactylus aff. podicipinus observed in the flooded area at the municipality of Santana, State of Amapá, Brazil. (A) dorsal and (B) ventral melanistic colouration. (C) dorsal and (D) ventral typical colour patterns.

Collection of Universidade Federal do Amapá (under cause in the affected individuals, as well as to investigate voucher CECCAMPOS 1383). This colouration differs the frequency rate of this phenomenon within the studied from the off-white yellow pattern on the belly and population. sides, and light brown to yellowish back described from normal individuals (Fig. 1C, D). Acknowledgements. We are grateful to Thiago R. de Carvalho To our knowledge, this is the first report of melanism for insight the taxonomic identification of the Leptodactylus in the genus Leptodactylus Fitzinger, 1826, specifically melanonotus group, and Instituto Chico Mendes de Conservação in Leptodactylus aff. podicipinus. It should be noted that, da Biodiversidade (ICMBio) for the collection permit (#48102-2). during fieldwork in the last five years at the “flooded area”, no other individuals of this species have been References observed presenting any type of conspicuous pigmentary Araujo, K.C., Cavalcante, L.A., Oliveira, D.B., Andrade, E.B. abnormalities (Costa-Campos pers. comm.). Thus, we (2020): Axanthism in the treefrog Dendropsophus minutus encourage future work to investigate the possible causes (Anura: Hylidae) from a montane forest relict in Northeastern and consequences that this rare congenital condition can Brazil. Herpetology Notes 13: 257–259. Melanism in Leptodactylus aff. podicipinus from southern Amapá, Brazil 971

Alho, J.S., Herczeg, G., Söderman, F., Laurila, A., Jönsson, K.I., Laurenti, 1768 (Serpentes: Dipsadidae: Dipsadini) in northern Merilä, J. (2010): Increasing melanism along a latitudinal and northeastern Brazil. Herpetology Notes 12: 1197–1200. gradient in a widespread amphibian: local adaptation, ontogenic Moraes, L.J.C.L., Kaefer, I.L. (2015): Leucism in the Amazonian or environmental plasticity? BMC Evolutionary Biology 10: 317. diurnal frog Anomaloglossus stepheni (Martins, 1989) (Anura: Barbosa, V.N., Amaral, J.M.S., Lima, L.F.L., França, R.C., Aromobatidae). Herpetology Notes 8: 179–181. França, F.G.R., Santos, E.M. (2019): A case of melanism in Recknagel, H., Layton, M., Carey, R., Leitão, H., Sutherland, M., Dendrophidion atlantica Freire, Caramaschi & Gonçalves, 2010 Elmer, K.R. (2018): Melanism in common lizards (Squamata: (Colubridae) from Northeastern Brazil. Herpetology Notes 12: Lacertidae: Zootoca vivipara): new evidence for a rare but 109–111. widespread ancestral polymorphism. Herpetology Notes 11: Clusella Trullas, S., van Wyk, J.H., Spotila, J.R. (2007): Thermal 607–612. melanism in ectotherms. Journal of Thermal Biology 32: 235– Rodrigues, A.P., Oliveira, J.C. (2004): Leptodactylus ocellatus 245. (Rã-manteiga). Tadpole albinism. Herpetological Review 35 Costa-Campos, C.E., Sampaio, P.G.N., Corrêa, J.G., Silva e Silva, (4): 373. Y.B., Baía, R.R.J., Pamphilio-Júnior, et al. (2015): Oxyrhopus Sanabria, E.A., Laspiur, L.B.Q.A. (2010): First record of partial occipitalis. Melanism. Herpetological Review 46: 105. albinism and scoliosis in Odontophrynus occidentalis tadpoles Chilote, P.D., Moreno, L.E. (2019): First axantism record for the (Anura: Cycloramphidae). Brazilian Archives of Biology and genus Melanophryniscus (Anura: Bufonidae). Boletín de la Technology 53 (3): 641–642. Asociación Herpetológica Española 30: 60–61. Tavares-Pinheiro, R., Costa-Campos, C.E., Kaefer, I.L. (2020): De Sá, R.O., Grant, T., Camargo, A., Heyer, W.R., Ponssa, M.L., A leucistic brilliant-thighed poison frog Allobates femoralis Stanley, E. (2014): Systematics of the Neotropical Genus (Dendrobatoidea). Herpetology Notes 13: 321–323. Leptodactylus Fitzinger, 1826 (Anura: Leptodactylidae): Toledo, L.F., da Silva, N.G., Araújo, O.G.S. (2011): Albinism in Phylogeny, the Relevance of Non-molecular Evidence, and two Amazonian frogs: Elachistocleis carvalhoi (Microhylidae) Species Accounts. South American Journal of Herpetology 9: and Lithobates palmipes (Ranidae). Herpetology Notes 4: 145– 1–128. 146. Elgue, E., Cruces, S., Pereira, G., Achaval-Coppes, F., Maneyro, R. Vásquez-Cruz, V., Fuentes-Moreno, A., Campos-Cerón, M. (2013): Leptodactylus gracilis (Duméril’s Striped Frog). Albino (2020): First report of melanism in the salamander Bolitoglossa tadpole. Herpetological Review 44: 123–124. rufescens (Caudata: Plethodontidae) in Veracruz, México. Escudero, P.C., Minoli, I., González Marín, M.A., Morando, Cuadernos de Herpetología 34: 99–101. M., Avila, L.J. (2016): Melanism and ontogeny: a case study Vences, M., Galán, P., Vieites, D.R., Puente, M., Oetter, K., Wanke, in lizards of the Liolaemus fitzingerii group (Squamata: S. (2002): Field body temperatures and heating rates in a Liolaemini). Canadian Journal of Zoology 94: 199–206. montane frog population: the importance of black dorsal pattern Frost, D.R. (2020): Amphibian Species of the World: an Online for thermoregulation. Annales Zoologici Fennici 39: 209–220. Reference. Version 6.0. Accessed on 21 May 2020. Electronic Database accessible at http://research.amnh.org/herpetology/ amphibia/index.html Griffith, S.C., Parker, T.H., Olson, V.A. (2006): Melanin-versus carotenoid-based sexual signals: is the difference really so black and red? Animal Behaviour 71: 749–763. Gilhen, J., Scott, F.W. (2014): Melanistic diversity in the Maritime Gartersnake, Thamnophis sirtalis pallidulus, in Nova Scotia, Canada. Canadian Field-Naturalist 128: 63–71. Johnston, G.R. (2006): Scaphiopus holbrookii holbrookii, Albinism. Herpetological Review 37 (2): 211–212. Jablonski, D., Alena, A., Ylcek, P., Jandzik, D. (2014): Axanthism in amphibians: A review and the first record in the widespread toad of the Bufotes viridis complex (Anura: Bufonidae). Belgian Journal of Zoology 144: 93–101. Kolenda, K., Najbar, B., Najbar, A., Kaczmarek, P., Kaczmarski, M., Skawiński, T. (2017): Rare colour aberrations and anomalies of amphibians and reptiles recorded in Poland. Herpetology Notes 10: 103–109. Lunghi, E., Ficetola, G.F., Barzaghi, B., Vitillo, C., Mulargia, M., Manenti, R. (2017): Melanism in European plethodontid salamanders (Amphibia, Plethodontidae, Hydromantes). Spixiana 40: 157–160. Martins, R.A., Scheeffer, I., Turci, L.C.B., Machado, R.A., Accepted by Mirco Solé Bernarde, P.S. (2019): Cases of melanism in Dipsas indica indica