Herpetology Notes, volume 14: 859-861 (2021) (published online on 03 June 2021)

First record of leucism in a tadpole of the cane toad Rhinella marina (Anura: Bufonidae)

Mahima Hemnani1,*, Izabela Sabrina Campos Guimarães1, and Igor Luis Kaefer1

Albinism is a chromatic abnormality characterised 2018) and in tadpoles of Rhinella ornata (Brassaloti by partial or complete absence of integumentary and Bertoluci, 2009), and Rhinella arenarum (Barg and pigmentation giving an individual organism a whitish, Canepuccia, 2003). Our study reports the first record of yellowish to golden or pinkish-reddish appearance leucism in a tadpole of the cane toad Rhinella marina (Henle et al., 2017). There are different types of (Linnaeus, 1758). This species has a broad distribution , being leucism one of the variants. Leucistic in natural and invaded areas throughout the globe (Frost, individuals can be distinguished from albinos by having 2020), and constitutes one of the most extensively partial where margins of the body and studied anurans. However, we are not aware of any often remain pigmented (Miller, 2005; Henle et al., other report of leucism in R. marina, independently of 2017; Lunghi et al., 2017). Causes of leucism can be developmental stage. genetic, morphological, and immunological (Sanabria In May 2018, in the morning, we collected parts of et al., 2010; Hayley-McCardle, 2012). Leucism can several egg strings of Rhinella attached to emergent also be attributed to environmental factors (Jablonski vegetation in a fish farming pond of the Experimental et al., 2014; Miura, 2018) such as excessive use of Farm of the Universidade Federal do Amazonas, agrochemicals that causes and morphological Manaus, Brazilian Amazon. The eggs were housed at anomalies during development of the organism (Brown the Behavioural and Evolutionary Ecology Laboratory, et al., 2020; Ferrante and Fearnside, 2020). Regarding where they were kept it in an aquarium (15 x 10 x 10) anurans, albin or leucistic are hardly seen containing water with a controlled temperature of 25 °C in natural populations (Betchel, 1995). It can be due (average temperature of the sampled ponds), and aquatic to associated phenotypic abnormalities or because, macrophytes from the collection site. When the tadpoles depending on where they live, leucistic anurans can be hatched, were all identified as Rhinella marina by the much more visible to their visually oriented predators following morphological characteristics: dark venter, reducing their survival rates (Betchel, 1995; Brown et intestine barely visible, dorsal side black with scattered al., 2020). white , upper half of tail muscle black There are records of leucism in adult of coloured, lower half of tail muscle and fins transparent stepheni (Moraes et al., 2015), Allobates femoralis (Tavares-Pinheiro et al., 2020), Leptodactylus melanonotus (Brown et al., 2020) and tadpoles of Leptodactylus latrans (Rodrigues and Oliveira Filho, 2004) and Boana albomarginata (Salles et al., 2013). In the genus Rhinella, depigmentation was identified in an adult of Rhinella crucifer (Barros et al.,

1 Universidade Federal do Amazonas, Instituto de Ciências Biológicas, Programa de Pós-graduação em Zoologia, Av. General Rodrigo Otávio Jordão Ramos, 6200, 69077-000 Manaus, Amazonas, . Figure 1. Comparative view of leucistic (A) and normal * Corresponding author. E-mail: [email protected] coloured (B) Rhinella marina tadpoles collected in Central © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. Amazonia, Brazil. Photo by Mahima Hemnani. 860 Mahima Hemnani et al.

Figure 2. Dorsal (A) and ventral (B) views of the Rhinella marina’s leucistic tadpole collected in Central Amazonia, Brazil. Photos by Mahima Hemnani.

(Hero, 1990). Amongst them, we observed one leucistic and DiBernardo, 1991). Infrequent documentation R. marina tadpole that was kept with its conspecifics in of anomalies might also stem from inconsistent the aquarium and was fed daily with commercial rabbit classification and recognition of those anomalies food. (Jablonski et al., 2014; Allain and Goodman, 2017; Regarding differences in relation to the other tadpoles, García Padrón and Bosch, 2019). The presence of the leucistic specimen had partial depigmentation albinistic or leucistic individuals can be considered in the entire body, except for the retention of dark as an indirect measure of the conservation status of a pigmentation in its eyes (Fig. 1). We did not observe population, since frequency of depigmented individuals any sign of anatomical abnormality, except that it was in vertebrates is rare, varying between 1:10.000 and notably larger than its sibling conspecifics throughout 1:30.000 (Villee and Dethier, 1971; Bechtel, 1995; its development (Fig. 2), even though we did not take Brassaloti and Bertoluci, 2009). A recent study any morphometric measurements. conducted in the same place where we collected Colouration patterns play an important role in the life the egg strings revealed morphological anomalies history of individuals (Price et al., 2019). Tadpoles of in several species probably due to exposure to Rhinella marina have dark skin colour and are visible agrochemicals, since the surroundings of the sampled against the bright coloured background where they pond are continuously used for agriculture (Ferrante and are usually found. This may provide predators with Fearnside, 2020). Additional studies involving leucistic information on their toxicity and unpalatability (Wells et tadpoles, especially from aposematic organisms, are al., 2007; Hayes et al., 2009). One of the main predators needed to assess the implications of such depigmentation of R. marina tadpoles are dragonfly larvae, also known on life history parameters such as development and as naiads (Magnusson et al., 1991). They are known survival. as ambush predators, slowly approaching the prey through visual and mechanical perception (Touchon Acknowledgments. We thank the Experimental Farm of the et al., 2014). Along with them, other predators such as Universidade Federal do Amazonas for the logistical support snakes (Kaefer and Montanarin, 2011) are also visually during tadpole collection; Dr. Marcelo Menin (in memorian) for the identification of the species; the Behavioural and Evolutionary oriented predators of R. marina tadpoles. Similar as Ecology Laboratory, especially Dr. Tiago S. Pires, for the suggested for albino Rhinella ornata, depigmented logistical support during tadpole rearing. We are also grateful to tadpoles may suffer higher predation pressure due to two reviewers for criticisms and suggestions. Collection permit the absence of aposematism, which is typical of bufonid was provided to ILK by SISBIO/ICMBio permanent licence larvae (Brassaloti and Bertoluci, 2009). # 46959-1 and Ethics committee on experimentation Leucistic individuals can be infrequent in populations (CEUA) Protocol # 011/2017 – CEUA/UFAM. because they tend to have less success in their protection and communication with other conspecifics due to their different colour (Sazima and Pombal, 1986; Sazima First record of leucism in a tadpole of the cane toad Rhinella marina 861

References Miller, J.D. (2005): All about albinism. Missouri Conservationist 66: 5–7. Allain, S.J., Goodman, M.J. (2017): A case of xanthochromism in Miura, I. (2018): Anomalies in the coloration of Japanese the common frog (Rana temporaria). Herpetological Bulletin and their applications in genetic research. KnE Life 139: 39–40. Sciences 4: 97–107. Barg, M., Canepuccia, A.D. (2003): Albinismo en una larva de Bufo Moraes, L.J.C.L., Kaefer, I.L. (2015): Leucism in the Amazonian arenarum. Boletin de la Asociacíon Herpetológica Española 14: diurnal frog Anomaloglossus stepheni (Martins, 1989) (Anura: 29–30. ). Herpetology Notes 8: 179–181. Barros, L.D.P.V., Muniz, R.F., Kloss-Degen, J.P., de Castro, T.M., Price, N., Green, S., Troscianko, J., Tregenza, T., Stevens, M. Oliveira, J.C., Rocha, C.F.D. (2018): Albinism in a juvenile (2019): Background matching and disruptive coloration of Rhinella crucifer Wied-Neuwied, 1821 (Anura: Bufonidae) as habitat-specific strategies for camouflage. Scientific from southeastern Brazil. Herpetology Notes 11: 599–600. Reports 9(1): 1–10. Bechtel, H.B. (1995): Reptile and variants: colors, Rodrigues, A.P., Oliveira Filho, J.C.D. (2004): Leptodactylus patterns and scales. Malabar, F.L., Krieger Publishing. ocellatus (Ra-manteiga). Tadpole albinism. Herpetological Brassaloti, R.A., Bertoluci, J. (2009): Albinism in tadpoles of Review 35: 373. Rhinella ornata (Anura, Bufonidae) from southeastern Brazil. Salles, R.O.L., Xisto, T., Ferreira, T., Nascimento, B. (2013): Herpetological Bulletin 106: 31–33. Albinism in a tadpole of Hypsiboas albomarginatus (Spix, Brown, T.W., Papini, F., Clayson, S.M. (2020): Leucism in a Sabinal 1824) (Anura: Hylidae) from Southeastern Brazil. Herpetology Frog, Leptodactylus melanonotus (Anura; Leptodactylidae), Notes 6: 577–578. from Utila Island, Honduras. Reptiles & Amphibians 27(3): Sanabria, E.A., Quiroga, L.B., Laspiur, A. (2010): First record of 432–433. partial albinism and scoliosis in Odontophrynus occidentalis Ferrante, L., Fearnside, P.M. (2020): Evidence of mutagenic and tadpoles (Anura: Cycloramphidae). Brazilian Archives of lethal effects of herbicides on Amazonian frogs. Acta Amazonica Biology and Technology 53: 641–642. 50: 363–366. Sazima, I., Di-Bernardo M. (1991): Albinismo em serpentes Frost, D.R. (2020): Amphibian Species of the World: an Online neotropicais. Memórias do Instituto Butantan 53: 167–73. Reference. Version 6.0. American Museum of Natural History, New York. Available at: http://research.amnh.org/herpetology/ Sazima, I., Pombal-Jr., J.P. (1986): Um albino de Rhamdella minuta, amphibia/index.html. Accessed on 12 November 2020. com notas sobre comportamento (Osteichthyes, Pimelodidae). García Padrón, L.Y., Bosch, R.A. (2019): Anomalous colour Revista Brasileira de Biologia 40: 377–381. in a Cuban cavedwelling frog: First record of Tavares-Pinheiro, R., Costa-Campos, C.E., Kaefer, I.L. (2020): in zeus (Anura: ). A leucistic brilliant-thighed poison frog Allobates femoralis Herpetological Bulletin 157: 1–3. (Dendrobatoidea). Herpetology Notes 13: 321–323. Hayes, R.A., Crossland, M.R., Hagman, M., Capon, R.J., Shine, R. Touchon, J.C., Wojda, J.M. (2014): Plastic hatching timing by red- (2009): Ontogenetic variation in the chemical defenses of cane eyed treefrog embryos interacts with larval predator identity toads (Bufo marinus): toxin profiles and effects on predators. and sublethal predation to affect prey morphology but not Journal of Chemical Ecology 35: 391–399. performance. PLoS ONE 9(6): e100623. Hayley-McCardle, B.S. (2012): Albinism in wild vertebrates. – Villee, C.A., Dethier, V.G., Harner, W.H. (1971): Biological Unpublished MSc Dissertation, Science Texas State University, Principles and Processes. Philadelphia, London, Toronto, San Marcos, USA, 71 pp. Saunders. Henle, K., Dubois, A., Vershinin, V. (2017): Commented glossary, Wells, K.D. (2007): The Ecology and Behavior of Amphibians. terminology, and synonymies of anomalies in natural populations The University of Chicago Press, London. of amphibians. Mertensiella 25: 9–48. Hero, J. M. (1990): An illustrated key to tadpoles occurring in the Central Amazon rainforest, Manaus, Amazonas, Brasil. Amazoniana: Limnologia et Oecologia Regionalis Systematis Fluminis Amazonas 11(2): 201–262. Jablonski, D., Alena, A., Vlček, 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(2): 93–101. Kaefer, I.L., Montanarin, A. (2011): Helicops angulatus (South american watersnake). Herpetological Review 42(2): 291. Lunghi, E., Monti, A., Binda, A., Piazzi, I., Salvadori, M., Cogoni, R., et al. (2017): Cases of albinism and leucism in amphibians in Italy: new reports. Natural History Sciences 4(1): 73–80. Magnusson, W.E., Hero. J. (1991): Predation and the evolution Accepted by Anyelet Valencia-Aguilar of complex oviposition behaviour in Amazon rainforest frogs. Oecologia 86: 310–318.