Herpetology Notes, volume 11: 553-555 (2018) (published online on 25 July 2018)

Anomalous colour pattern in Oxyrhopus rhombifer (Serpentes: Dipsadidae)

Weverton dos Santos Azevedo1,*, Fernando Marques Quintela2, Omar Machado Entiauspe-Neto2, Arthur Diesel Abegg1, Rafael Almeida Porciúncula² and Daniel Loebmann2

Colour patterns in reptiles perform an important role are small- to medium-sized, usually do not exceed 1 m in several aspects of their ecology, and colouration (������������������������������������������������� anomalies can have a direct effect on an individual’s angulated snout, and usually present a coral-mimicking fitness (Sazima and Di-Bernardo, 1991; Kolenda et. dorsal pattern (Bernardo, 2010). al., 2017). Amaral (1932a,b) described colour pattern Oxyrhopus rhombifer Duméril et al., 1854 is a anomalies in several snake species, highlighting cases medium-sized species (up to 1000 mm total length), in Oxyrhopus trigeminus Duméril et al., 1854 and O. presenting sexual dimorphism in which females are petolarius (Linnaeus, 1758), with the latter presenting larger than males (Borges-Martins et al., 2007). It has the first known case of erythrism in Brazilian snakes. terrestrial and nocturnal habits, and is usually found in Since then, few studies have reported or described open areas and forest edge habitats (Borges-Martins et chromatic anomalies in Brazilian snakes, and those al., 2007; Sawaya et al., 2008). According to Bernardo that exist usually present insufficient detail or describe (2010), the taxonomy of O. rhombifer is relatively stable, partial anomalies. For example, Pires (2011) identified while the species has notable geographic colour pattern a specimen of Micrurus lemniscatus (Linnaeus, 1758) polymorphism associated with its extensive geographic with reduced cephalic pigmentation, describing it as an distribution. Usually, specimens of O. rhombifer from abnormally-coloured individual, while other authors southern Brazil possess a colour pattern composed of recorded more delineated anomalies, such as albinism irregular bands of black, red, and yellow on the dorsum, (Sazima and Di-Bernardo, 1991; Abegg et al., 2015), with a yellow or white venter, with our without black partial albinism (Abegg et al., 2014), or leucism dots (Fig. 1A) (Borges-Martins et al., 2007; Sawaya (Noronha et al., 2013; Entiauspe-Neto et al., 2018). et al., 2008). We here report on a striking, atypically The dipsadid snake genus Oxyrhopus Wagler, 1830 is coloured individual of O. rhombifer. composed of 14 species widely distributed from central Mexico to southern Argentina, occurring in several Materials and Methods biomes (Bernardo, 2010; Bosque, 2012; Guedes et al., The predator-killed individual was fixed in a solution of 2017). In Brazil, 10 species of Oxyrhopus have been 10% formalin, after 48 hours shifted into a preservation recorded (Costa and Bérnils, 2016). Species in this genus solution of 75% ethanol, and then deposited in the Coleção Herpetológica Universidade Federal do Rio Grande (CHFURG). Measurements were taken with a flexible ruler to the nearest millimetre. Bilateral counts are indicated as left/right. Ventral scale counts following 1 Instituto Butantan, Laboratório Especial de Coleções Dowling (1951). The terminal spine is included after a Zoológicas, Avenida Vital Brasil, 1.500, Butantã, São Paulo – SP, 05503-900, Brazil plus sign in the subcaudal scale count. 2 Universidade Federal do Rio Grande, Instituto de Ciências Biológicas, Laboratório de Vertebrados, Avenida Itália, Km Results and Discussion 8, Vila Carreiros, Rio Grande – RS, 96203-900, Brazil * Corresponding author. E-mail: Collection.—On 2 November 2017 Rafael Almeida [email protected] Porciúncula encountered an anomalously coloured 554 Weverton dos Santos Azevedo et al.

Figure 1. Colour pattern in Oxyrhopus rhombifer. (A–C) Common pattern of individuals found in southern Brazil. (A) Dorsal view showing the regular black and red banding pattern. (B) Ventral view showing a uniformly cream-colored venter. (C) Lateral view with detail of the banding, showing that the black colour diminishes closer to the venter. (D–F) Anomalous pattern of CHFURG 5966 from Rio Grande do Sul (D) Dorsal view showing a beginning pattern including one red band and one black band anteriorly, with a switch to longitudinal banding without a transition zone. (E) Ventral view showing a yellowish colouration. (F) Lateral view, showing the sequential banding pattern with black along the vertebral line, bordered by yellow and red.

individual of what appeard to be O. rhombifer (Fig. Identification.—The specimen possesses 8/8 1D–F) in the Bosque neighbourhood, urban area of Rio supralabials (4th and 5th in contact with the orbit), 9/9 Grande Municipality, Rio Grande do Sul State, Brazil. infralabials, a single preocular, loreal scale present, two The individual was an adult male with 411 mm snout– postoculars, 2+3 temporals, single cloacal plate, with vent length and 107 mm tail length, that had been killed medial fissure, 179 ventrals, 62+1 subcaudals, and 19 by a domestic cat. The individual was accessioned under smooth middorsal scale rows, without posterior scale the specimen number CHFURG 5966. row reduction. These data fall within the known variation Anomalous colour pattern in Oxyrhopus rhombifer 555 for O. rhombifer (Carreira et al., 2005). However, the Grande do Sul. Brasília, Distrito Federal, Brazil, Ministério do specimen has a venter with a yellowish coloration (Fig. Meio Ambiente. 385 pp. 1E). Dorsally, it lacks the normal irregular bands but Bosque, R.J. (2012): Mimetismo, padrões de coloração e distribuição geográfica de serpentes Oxyrhopus Wagler, 1830 instead possesses longitudinal stripes along its body (Colubridae) e Micrurus Wagler, 1824 (Elapidae). Unpublished (Fig. 1D, F), including a black vertebral stripe bordered M.Sc. Thesis, Universidade de Brasília, Brasília, Distrito laterally by two yellow stripes, and wider, lateral red Federal, Brazil. 42 pp. stripes below the yellow stripes. Brodie, E.D., III. (1993): Differential avoidance of coral snake banded patterns by free-ranging avian predators in Costa Rica. Chromatic anomaly.—Malformation of transverse Evolution 47 (1): 227–235. body bands or their fusion into longitudinal stripes, Carreira, S., Meneghel, M., Achaval, F. (2005): Reptiles de has been previously recorded in other Brazilian snakes Uruguay. Montevideo, Uruguay, Faculdad de Ciencias. 639 pp. (Amaral, 1977; Lema, 2002; Cruz-da-Silva et al., Cruz-da-Silva, R.C., Freitas, M.A., Abegg, A.D. (2018): A 2018). However, CHFURG 5966 represents the first remarkable specimen of the genus Anilius (Serpentes: Aniliidae): record of this anomaly in O. rhombifer. It is remarkable Rare colour aberration or a new species?. Herpetology Notes 11, 161–165. that, although O. rhombifer is a common species, no Dowling, H.G. (1951): A proposed standard system of counting similar anomalies have been encountered across a ventrals in snakes. British Journal of Herpetology 1: 97–99. large sample of individuals collected over an extended Entiauspe-Neto, O.M., Abegg, A.D., Quintela, F.M., Mario-da- timespan (Quintela et al., 2006; ADA, OMEN, FMQ, Rosa, C., Malta-Borges, L., Loebmann, D. (2017): First record and DL, pers. obs.). The specimen is in relatively good of leucism for Atractus reticulatus (Serpentes: Dipsadidae). condition, without apparent scars or missing body parts, Brazilian Journal of Biology 78 (1): 174–175. which suggests that this anomaly did not significantly Guedes, T.B., Sawaya, R.J., Zizka, A., Laffan, S., Faurby, S., Pyron, R.A., et al., Cisneros-Heredia, D.F. (2017): Patterns, biases and impact the fitness of this individual during its lifetime. prospects in the distribution and diversity of Neotropical snakes. Maintenance of a tricolored pattern, a mimetic pattern Global Ecology and Biogeography 27 (1): 14–21. to coral snakes, might actually have been useful to this Kolenda, K., Najbar, B., Najbar, A., Kaczmarek, P., Kaczmarski, individual against native visually oriented predators M., Skawiński, T. (2017): Rare colour aberrations and anomalies (Brodie, 1993); the domestic cat, likely unfamiliar with of amphibians and reptiles recorded in Poland. Herpetology coral snake patterns, probably was not deterred by its Notes 10: 103–109. mimetic pattern. Lema, T. (2002): Os répteis do Rio Grande do Sul: atuais e fósseis, biogeografia, ofidismo. Porto Alegre, Rio Grande do Sul, Brazil, Edipucrs. 264 pp. References Mosmann, M.N. (2001): Guia das Principais Serpentes do Mundo. Abegg, A.D., Entiauspe-Neto, O.M., Lema, T. (2015): First record Canoas, Brazil, Editora da Ulbra. 392 pp. of albinism in the Elapomorphini tribe (Serpentes: Dipsadidae). Noronha, J.C., Barros, A.B., Miranda, R.M., Almeida, E.J., Herpetology Notes 8: 503–505. Rodrigues, D.J. (2013): Record of leucism in Pseudoboa Abegg, A.D., Mario-da-Rosa, C., Cavalheiro, C.P., Ortiz, F.R., nigra (Serpentes: Dipsadidae) in southern Amazon, Brazil. Malta-Borges, L. (2014): Partial albinism in Sibynomorphus Herpetology Notes 6: 81–82. ventrimaculatus (Boulenger, 1885) (Serpentes: Dipsadidae) in Pires, M.G. (2011). Revisão taxonômica do complexo Micrurus Rio Grande do Sul State, Brazil. Herpetology Notes 7: 475– lemniscatus (Linnaeus, 1758) (Serpentes: Elapidae). 476. Unpublished Ph.D. Thesis, Universidade de São Paulo, São Amaral, A.D. (1932a): Notas sobre chromatismo de ophidios. I. Paulo, Brazil. 218 pp. Primeiro caso de erythrismo serpente, observado no Brasil. Quintela, F.M., Loebmann, D., Gianuca, N.M. (2006): Répteis Memórias do Instituto Butantan 7: 77–79. continentais do município de Rio Grande, Rio Grande do Sul, Amaral, A.D. (1932b): Notas sobre chromatismo de ophidios. II. Brasil. Biociências 14 (2): 180–188. Casos de variação de colorido de certas serpentes. Memórias do Sawaya, R.J., Marques, O.A.V., Martins, M. (2008): Composição e Instituto Butantan 7: 81–87. história natural das serpentes de Cerrado de Itirapina, São Paulo, Bernardo, P.H. (2010): Revisão taxonômica e sistemática de sudeste do Brasil. Biota Neotropica 8 (2): 127–149. Oxyrhopus clathratus Duméril, Bibron & Duméril, 1854 Sazima, I., Di-Bernardo, M. (1991): Albinismo em serpentes (Serpentes, Dispsadidade; Pseudoboini). Unpublished M.Sc. neotropicais. Memórias do Instituto Butantan 53 (2): 167–173. Thesis, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Rio Claro, São Paulo, Brazil. 92 pp. Borges-Martins, M., Alves, M.L.M., Araujo, M.L., Oliveira, R.B., Anés, A.C. (2007): Répteis, p. 292–315. In: Becker, F.G., Ramos R.A., Moura, L.A., Eds., Biodiversidade: Regiões da Lagoa do Accepted by Hinrich Kaiser Casamento e dos Butiazais de Tapes, Planície Costeira do Rio