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Herpetology Notes, volume 13: 393-395 (2020) (published online on 26 May 2020)

First report of xanthism in jararacussu Lacerda, 1884 (Serpentes: )

Lucas R. Mendonça¹,*, Leandro de A. Oliveira¹, Clodoaldo L. Assis¹, Jhonny J. M. Guedes¹,2, and Renato N. Feio¹

Chromatic anomalies are known to occur in all pigment called xanthine, being a rare anomaly in major terrestrial vertebrate groups, such as mammals, (Cardoso and Parpinelli, 2006). Chromatic anomaly was birds, amphibians and (e.g., De-Carvalho et well documented for a specimen of Epicatres cenchria al., 2015; Lucati and López-Baucells, 2017; García- (Linnaeus, 1758) (Hoge and Bulloumini, 1957), though Padrón and Bosch, 2019), including snakes (Sazima other cases are known in the literature, including reports and Di-Bernardo, 1991; Ortiz et al., 2017). It may be for Dipsas mikanii (Schlegel, 1837), Crotalus durissus related with adaptive advantages to the environment (Linnaeus, 1758), (Wied-Neuwied, when the individual has a darker colouration (Gibson 1824), B. alternatus Duméril et al., 1854, and B. cotiara and Falls, 1979), but, on the other hand, individuals with (Gomes, 1913) (see Sueiro et al., 2010). Regarding lighter colour patterns may have their fitness reduced Bothrops jararacussu Lacerda, 1884, there is one case (Krecsák, 2008). Among several known anomalies, of albinism reported in the literature for three newborn albinism refers to the total absence of melanin, however, females (Ortiz et al., 2017). This is the second it may also be expressed less intensely, being named as largest pitviper in , reaching up to 2.20 meters in xanthism, piebaldism or leucism (sensu Sazima and total length (Marques, 1998). It occurs in forested areas Di-Bernardo, 1991). These conditions are caused by of the Atlantic Forest, from the states of Bahia to Rio genetic mutations and may be related, for example, Grande do Sul, also reaching and with environmental factors during the embryological (Marques, 1998; Campbell and Lamar, 2004; Bernarde, development (Bechtel, 1978). In general, the cause of 2014; Nogueira et al., 2020). This also presents albinism is generally attributed to a mutation in the sexual dimorphism, where adult females have dark sequencing gene of tyrosinase enzyme, a key component brown or black adornments on a yellow background, in the formation of melanin (Bechtel, 1978; Griffiths et and adult males have less contrasting adornments, on a al., 1998; Alberts et al., 2004). Therefore, the xanthism brown or greyish background (Melgarejo, 2013). Herein, might occur through a mutation in the sequencing gene we report a specimen with a very distinct colour pattern, that depresses the presence of melanophores, but does which can be classified as xanthism, representing, by the not interfere with the expression of the xanthophores, best of our knowledge, the first case of this chromatic so the final result is a yellowish individual, as it occurs anomaly in B. jararacussu. in salmonid skin (Colihueque, 2010). Xanthism is, On April 2016, an adult male B. jararacussu was therefore, characterized by the presence of a yellow donated to the Museu de Zoologia João Moojen (MZUFV) at Universidade Federal de Viçosa. The specimen (Fig. 1) was collected in the municipality of Viçosa (-20.754600°S, -42.882500°W), Minas Gerais state, Brazil. It was euthanized, fixed in formalin 10%, ¹ Museu de Zoologia João Moojen, Departamento de Biologia stored in alcohol 70%, and housed in the herpetological , Universidade Federal de Viçosa, Vila Gianetti, nº32, collection of the MZUFV (voucher #2457). After 36570-977, Viçosa, Minas Gerais, Brazil. fixation, the specimen weighed 0.213 kilograms, and 2 Current address: Programa de Pós-Graduação em Ecologia e presented the following morphometric and meristic Evolução, Departamento de Ecologia, Universidade Federal de Goiás – Campus Samambaia, Goiânia, GO, 74690-900, characteristics: snout-vent length = 816 mm; tail length Brazil. = 136 mm, 180 ventral scales, 23/21/17 dorsal scale * Corresponding author. E-mail: [email protected] rows, 54 subcaudals, 6 intrasupraoculars, 8 supralabials, 394 Lucas R. Mendonça et al.

and the postorbital stripe were light brown (Fig. 1). Xanthism, among others chromatic anomalies recorded for snakes, are mainly observable in nocturnal or cryptic species (Sazima and Di-Bernardo, 1991) which is the case of the species reported here. In diurnal species, there would be selection against such anomalies due to the loss of protective (or cryptic) colouration that would favour visually-oriented predators (Sazima and Di-Bernardo, 1991). Therefore, xanthism and other anomalies that induce lighter colour patterns may reduce the fitness of the carrier specimen, as suggested by Krecsák (2008). Despite their rarity, reports of chromatic anomalies are important to improve our understanding about the distribution and frequency of such anomalies in natural populations. Finally, such record is a necessary first step towards developing systematic studies about the evolution of colour pattern variation among animal groups, as well as how such anomalies may affect survivorship and reproduction.

Acknowledgements. We would like to thank Daniela Pinto- Coelho and Rodrigo Castellari Gonzalez for their valuable contributions in a previous draft of this manuscript.

References

Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., Walter, P. (2004): Biologia molecular da célula. 4th Edition. Porto Alegre, Brazil, Artmed. Bechtel, H.B. (1978): Color and pattern in snakes (Reptilia, Snakes). Journal of Herpetology 12: 521–532. Bernarde, P.S. (2014): Serpentes peçonhentas e acidentes ofídicos no Brasil. São Paulo, Brazil, Anolis Books. Campbell, J.A., Lamar, W.W. (2004): The venomous reptiles of the western hemisphere. Second Edition. Ithaca, USA, Cornell University. Cardoso, S.R.T., Parpinelli, C. (2006): Crotallus durissus terrificus (Rattlesnake): a case of xanthism. Natural History Notes. Herpetological Bulletin 97: 38–39. Colihueque, N. (2010): Genetics of salmonid skin pigmentation: clues and prospects for improving the external appearance of farmed salmonids. Reviews in Fish Biology and Fisheries 20: 71–86. DOI: 10.1007/s11160-009-9121-6. Figure 1. Adult male of Bothrops jararacussu with xanthism De-Carvalho, C.B., Freitas, E.B., Pires, R.A.P., Limas, C.A., collected in the municipality of Viçosa, Minas Gerais state, Carvalho, R., Arruda, F.V. (2015): Chromatic aberration in the southeastern Brazil. (A) Dorsal view. (B) Ventral view. (C) plumage of Athene cunicularia (Strigiformes: Strigidae) for the Live specimen in dorsal view. Cerrado Biome, Central Brazil. Atualidades Ornitológicas 187: 21. García-Padrón, L.Y., Bosch, R.A. (2019): Anomalous colour in a Cuban cave-dwelling frog: first record of piebaldism in Eleutherodactylus zeus (Anura: Eleutherodactlylidae). The 10 infralabials – all within the known range of B. Herpetological Bulletin 147: 1–3. jararacussu (see Campbell and Lamar, 2004). Its Gibson A.R., Falls, J.B. (1979): Thermal biology of the common dorsum and belly were yellowish, including head and Garter Snake Thamnophis sirtalis (L.), II. The effects of tail, with dark yellow dorsal ornamentations; its eyes melanism. Oecologia 43: 99–109. First report of xanthism in Bothrops jararacussu in southeastern Brazil 395

Griffiths, A.J.F., Miller, J.H., Suzuki, D.T., Lewontin, R.C., Gelbart, W.M. (1998): Introdução à genética. Sixth Edition. Rio de Janeiro, Brazil, Guanabara-Koogan. Hoge, A.R., Belluomini, H.E. (1957/8): Aberrações cromáticas em serpentes brasileiras. Memórias do Instituto Butantã 28: 95–98. Krecsák, L. (2008): Albinism and leucism among European Viperinae: a review. Russian Journal of Herpetology 15: 97– 102. Lucati, F., López-Baucells, A. (2017): Chromatic disorders in bats: a review of pigmentation anomalies and the misuse of terms to describe them. Mammal Review 47: 112–123. Marques, O.A.V. (1998): Composição faunística, história natural e ecologia de serpentes da Mata Atlântica, na região da Estação Ecológica Juréia-Itatins, São Paulo, SP. Unpublished PhD thesis, Universidade de São Paulo, São Paulo, Brazil. Melgarejo, A.R. (2013): Criando serpentes salvando vidas. Rio de Janeiro, Brazil, Rio Books. Nogueira, C.C., Argôlo, A.J.S., Arzamendia, V., Aevedo, J.A., Barbo, F.E., et al. (2020): Atlas of Brazilian snakes: verified point-locality maps to mitigate the Wallacean Shortfall in a megadiverse snake fauna. South American Journal of Herpetology 14(Special Issue, 1): 1–274. Ortiz, F.R., Abegg, A.D., Corrêa, L.M. (2017): Albinism in Bothrops jararacussu Lacerda, 1884 (Serpentes: Viperidae) from the state of Espírito Santo, Brazil. Herpetology Notes 10: 177–179. Sazima, I., Di-Bernado, M. (1991): Albinismo em serpentes neotropicais. Memórias do Instituto Butantã 53: 167–173. Sueiro, L.R., Rojas, C.A., Risk, J.Y., França, F.O.S., Almeida- Santos, S.M. (2010): Anomalias cromáticas em Bothrops jararaca (Serpentes, Viperidae): xantismo interfere na sobrevivência? Biotemas 23: 155–160.

Accepted by Rodrigo Gonzalez