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Home , Bothrops jararacussu

Herpetology Notes, volume 10: 177-179 (2017) (published online on 25 April 2017)

Albinism in jararacussu Lacerda, 1884 (Serpentes: ) from the state of Espírito Santo,

Flora Roncolatto Ortiz1, Arthur Diesel Abegg1,* and Lívia Marcia Corrêa1

Albinism is a congenital disorder characterised by the its diet, in which adults forage predominantly small partial or complete inability of an organism to produce mammals but also lizards, anurans and, occasionally, melanin, due to recessive homozygosity of the gene other (Marques and Sazima, 2004; Martins et responsible for the production of this pigment (Alberts al., 2002), while juveniles feed mainly on ectothermic et al., 2009; Griffiths et al., 2013). This condition may prey (Martins et al., 2002). The colouring also changes be observed in several classes of vertebrates, including throughout development, ranging from yellowish to (McCardle, 2012). Depending on the gene dark grey, with dark trapezium-shaped spots bordered expression and the phenotypic characteristics there by a light colour in adults (Marques and Sazima, 2004). may be different types of albinism, such as xantism, Juveniles (Figure 1B) show sexual dichromatism, with piebaldism, leucism, and partial or complete albinism males being darker than females (Marques and Sazima, (Krecsák, 2008; McCardle, 2012). According to 2004). Sazima and Di-Bernardo (1991), individuals with this This paper describes the first case of total albinism abnormality can be disadvantaged because of the loss of in three new-born females of B. jararacussu. The cryptic colouration and occur primarily in snakes with individuals are from the municipality of Domingos cryptozoic habits. On the other hand, they can also be Martins, with municipality headquarters at -20.366667ºS, selected due to adaptive advantages in the environment -40.666667ºW in the state of Espírito Santo, Brazil and in which the is found as, for example, were sent to the Instituto Butantan (São Paulo) in June thermoregulation (Gibson and Falls, 1979; Cloudsley- 1968. There was no reported information about the Thompson, 1994). natural history of the individuals observed in the field. Bothrops jararacussu Lacerda, 1884 is the second The specimens are deposited at the Richard Alphonse largest of venomous in Brazil, reaching up Hoge Herpetological Collection (IBSP 28729, 28786 to 2.20 m in length. It occur preferably in forested areas and 28873) and were rescued from a big fire that affected of Atlantic Forest in the states of Bahia, Espírito Santo, the collection in May 2010 (Franco, 2012). The verified Rio de Janeiro, Minas Gerais, São Paulo, Mato Grosso biometric data are the snout-vent length (SVL) and the do Sul, Paraná, Santa Catarina, and Rio Grande do Sul caudal length (CL), obtained with the aid of a millimetre (Marques, 1998; Campbell and Lamar, 2004; Bernarde, ruler with a precision of 0.5 mm. The mass has not 2014), even in and (Campbell and been verified in order to prevent changes in the results, Lamar, 2004). The species is viviparous, giving birth to considering that the specimens were already preserved. between 13 and 73 offspring per pregnancy at the end of The largest individual has SVL = 224 mm and CL = 33 summer (Marques and Sazima, 2004). The tip of the tail mm, and the two smaller ones are the same size, with in juveniles is lightly coloured in order to attract prey SVL = 220 mm and CL = 32 mm. The specimens have by caudal luring (Sazima, 1991; Marques and Sazima, slightly reddish eyes and pink tongues. Dorsum and 2004). This species presents an ontogenetic change in venter are yellowish (Figure 1A). One specimen shows a tenuous trace of the dorsal pattern, while the other two are devoid of spots. The phenotype of the characterized specimens 1 Instituto Butantan, Laboratório Especial de Coleções shows complete albinism, classified as tyrosinase Zoológicas. negative albinism (sensu Bérnils et al., 1990). Data * Corresponding author e-mail: [email protected] present in the literature suggest a greater capture of 178 Flora Roncolatto Ortiz et al.

Figure 1. (A) Individual of Bothrops jararacussu with complete albinism. The detail shows the colour of the venter. (B) Young specimen of B. jararacussu with normal colour. Photos by Arthur D. Abegg (specimen with albinism), Edélcio Muscat (normal individual) and Bruno Rocha (venter of normal individual). Albinism in Bothrops jararacussu from the state of Espírito Santo, Brazil 179 females with chromatic anomalies, possibly due to Duarte, M.R., Franco, F.L., Oliveira, A.L. (2005): New records of higher thermoregulatory activity by females (Sueiro albinism in neotropical snakes. 0emórias do Instituto Butantan et al., 2010). Sazima and Di-Bernardo (1991) related 61: 66. Esqueda, L.F., Marca, E. and Soriano, P. (2005): Partial albinism in the frequency of albinism to the habits of snakes in a Venezuelan specimen of false coral snake, Oxyrhopus petola the Neotropics. The cases, including two species of petola (Linnaeus, 1758). Herpetotropicos: Tropical Amphibians the Bothrops, show that albinism is observed & Reptiles 2: 114-115. more frequently in cryptic or nocturnal snakes, due to Franco, F.L. (2012): A Coleção Herpetológica do Instituto Butantan: selective pressure caused by visually oriented predators. da sua origem ao incêndio ocorrido em 15 de maio de 2010. It is likely that pressure on albino’s specimens of diurnal Herpetologia Brasileira 1(1): 22-31. habits is exerted mainly by birds, (visually oriented and Gibson, A.R., Falls, J.B. (1979): Thermal biology of the common garter snake Thamnophis sirtalis. The effects of melanism. predominantly diurnal), recognized a group of important Oecologia 43: 99-109. predators of reptiles (Martín and López, 1990; Sazima Griffiths, A.J.F., Miller, J.H., Suzuki, D.T., Lewontin, R.C., and Di-Bernardo, 1991). This albinism record in B. Gelbart, W.M. (2013): Introdução à genética, 10th Edition.Rio jararacussu, as for other snake species (Duarte et al. de Janeiro, Brazil, Guanabara-Koogan.736 p. 2005; Esqueda et al., 2005; Sueiro et al. 2010; Noronha Krecsák, L. Albinism and leucism among european Viperinae: a et al. 2013; Abegg et al., 2014; Abegg et al. 2015) review. (2008): Russian Journal of Herpetology 15(2): 97-102. support the idea proposed by Sazima and Di-Bernardo Marques, O.A.V. (1998): Composição faunística, história natural e ecologia de serpentes da Mata Atlântica, na região da Estação (1991) that this anomaly is most easily observable in Ecológica Juréia-Itatins, São Paulo, SP. Unpublished doctoral nocturnal snakes. thesis, Universidade de São Paulo, São Paulo, Brazil. Marques, O.A.V., Sazima, I. (2004): História natural dos répteis da Acknowledgements. We thank Valdir José Germano for Estação Ecológica Juréia-Itatins. In: Estação Ecológica Juréia- identifying the specimens; Giuseppe Puorto for access to the IBSP Itatins: ambiente físico, flora e fauna, p. 257-277. Marques, collection; Francisco Luís Franco and Renato Silveira Bérnils for O.A.V., Duleba, V., Ed, Ribeirão Preto, Brazil, Holos. a prior review of the manuscript; Edélcio Muscat for providing a Martín, J., López, P. (1990): Amphibians and reptiles as prey of photograph of a normal B. jararacussu found on the trail of the birds in southwestern Europe. Smithsonian Herpetological Project Dacnis (Ubatuba, state of São Paulo), and Bruno Rocha Information Service 8(2):1-43. for the photograph of the venter of another normal individual. Martins, M., Marques, O.A.V., Sazima, I. (2002): Ecological and phylogenetics correlates of feeding habits in Neotropical References pitvipers of the Genus Bothrops. In: Biology of the vipers, p. 1-22. Schuett, G., Höggren, M., Douglas, M.E., Greene, H.W. Abegg, A.D., Mario-Da-Rosa, C., Cavalheiro, C.P., Ortiz, F.R. Carmel: Biological Sciences. and Malta-Borges, L., 2014. Partial albinism in Sibynomorphus McCardle, H. B.S. (2012): Albinism in wild vertebrates. ventrimaculatus (Boulenger, 1885) (Serpentes: Dipsadidae) in Unpublished master dissertation, Texas State University-San Rio Grande do Sul state, Brazil. Herpetology Notes 7: 475-476. Marcos, Texas, USA. Abegg, A.D., Entiauspe-Neto, O.M. and Lema, T., 2015. )irst Noronha, J.C., Barros, A.B., Miranda, R.M., Almeida, E.J. and record of albinism in the Elapomorphini tribe (Serpentes: Rodrigues, D.J. (2013): Record of leucism in Pseudoboa Dipsadidae). Herpetology Notes 8:503-505. nigra (Serpentes: Dipsadidae) in southern Amazon, Brazil. Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., Walter, P. Herpetology Notes 6:81–82. (2009): Biologia molecular da célula 5th Edition.Porto Alegre, Sazima, I. (1991): Caudal luring in two Neotropical pitvipers, Brazil, Artmed. 1396 p. and B. jararacussu. Copeia 1: 245-248. Amaral, A. D. (1927). Albinismo em” cobra coral. Revista do Sa]ima, I., Di-Bernardo, M. (1991): Albinismo em serpentes Museu Paulista 15:3-9. neotropicais. Memórias do Instituto Butantan 53: 167–173. Bernarde, P.S. (2014): Serpentes peçonhentas e acidentes ofídicos Sueiro, L.R., Rojas, C.A., Risk, J.Y., França, F.O.S., Almeida- no Brasil. São Paulo, Brazil, Anolis Books. 223 p. Santos, S.M. (2011): Anomalias cromáticas em Bothrops Bérnils, R.S., Moura-Leite, J.C., Ajuz, R.G. (1990): Albinismo em jararaca (Serpentes, Viperidae): xantismo interfere na Crotalus durissus (Serpentes: Viperidae) do estado do Paraná sobrevivência? Biotemas 23(1): 155-160. – Brasil. %iotemas 3: 129-132. Campbell, J.A., Lamar, W.W. (2004): The Venomous Reptiles of the Western Hemisphere, 2th Edition. Ithaca, USA, Cornell University. 476 p. Cloudsley-Thompson, J.L. (1994): Predation and defense amongst reptiles, 3th Edition. 6omerset, UK, R & A Publishing Limited. 138 p. Accepted by Robson Ávila