Herpetology Notes, volume 11: 161-165 (2018) (published online on 10 February 2018)

A remarkable specimen of the genus Anilius (Serpentes: Aniliidae): rare colour aberration or a new species?

Raiany Cristine Cruz-da-Silva1, Marco Antonio de Freitas2 and Arthur Diesel Abegg3,*

Traditionally, the clade Anilioidea Fitzinger, 1826 subspecies: Anilius scytale scytale (Linnaeus, 1758) and covers fossorial snakes that share singular cranial Anilius scytale phelpsorum Roze, 1958, distinguishing characteristics, with the palatine meeting palatal plate them based on the width and number of black body bands of the vomer to form a complete bony floor to the (wider and larger in average in the nominal subspecies). choanal passage, encompassing the monotypic genus In this study, we recorded a morphologically distinct Anilius Oken, 1816 (Aniliidae) besides Cylindrophis specimen from the two taxa currently recognizable Wagler, 1828 and Anomochilus Berg, 1901, in addition under the name A. scytale, without black dorsal bands, to Uropeltidae (McDowell, 1975; Hsiang et al., 2015). and discuss some possibilities about whether it is a new However, recent phylogenetic analyses have found species or specimen presenting an anomalous colour similarities between Anilius and Tropidophiidae and morphology. Brongersma, 1951, who share a morphological The specimen (Figure. 1A-B), was collected on apomorphism in the reproductive system, thus rejecting 07/26/2017, at 10:00 pm, in the municipality of Palmas the monophyletic Anilioidea (Siegel and Aldridge, (-10.2166, -48.3500, DATUM WGS84, 230 m ASL), in 2011; Pyron et al., 2013; Hsiang et al., 2015). the state of Tocantins, Brazil, by Raiany Cristine Cruz da Anilius scytale (Linnaeus, 1758) is widely distributed Silva and Marco Antonio de Freitas (Collecting permit along the Amazonian forest, also occurring in the SISBIO 52416-2). The meristic and morphometric data Brazilian Cerrado and in the humid enclaves of the were taken with a dial calliper to the nearest 1 mm. Caatinga (Beebe, 1946; Duellman, 1978; Cunha and Our terminology for Anilius cephalic shields follows Nascimento, 1993; Pérez-Santos and Moreno, 1988; Roze (1958) and ventral and subcaudal counts follow Starace, 1998, Silva-Jr. and Puorto, 2001; Catenazzi et Dowling (1951). The collection acronym according to al., 2013). It is a morphologically conspicuous species Sabaj-Perez (2016). (a mimic of venomous coral snakes, sensu Savage and During the capture, the specimen (IBSP 89520) Slowinski, 1992), presenting a reddish orange colour presented the defensive behavior of hiding the head dorsally, with several irregular black bands that, most of under its own body, as previously reported for A. scytale the time, extend to the belly, whose colour is yellowish (Sawaya, 2010). In life, the dorsal background colour cream, except in the gular region and tail, which are also is reddish orange, with black spots near the paraventral reddish orange (Figure 1). Roze (1958) recognizes two region, arranged longitudinally up to the cloaca; the belly is yellowish cream, with nearby transverse black bands, often connected to each other. The gular and caudal region is reddish orange. The meristic and morphometric 1 Instituto Natureza do Tocantins – NATURATINS 302 Norte, data (taken with a dial caliper to the nearest 1 mm) are Alameda 01, Lote 03 – Plano Diretor Norte, CEP 77006-336, the following: total length (TTL) 570 mm; tail length Palmas, TO, Brazil. 23 mm (4% TL); head length 16 mm (2.8% HL); 235 2 Instituto Chico Mendes de Conservação da Biodiversidade ventral scales; 12 subcaudal; a single anal plate; dorsal (ICMBio), ESEC Murici, Rua Marino Vieira de Araújo 32, plates as 21/21/21 rows; a small rostral plate, visible Cidade Alta, CEP 57820-000, Murici, AL, Brazil. from above; large prefrontals, being the largest cephalic 3 Instituto Butantan, Laboratório Especial de Coleções Zoológicas, Avenida Doutor Vital Brazil, 1.500, Butantã, scales; absent internals; small frontal, almost half the CEP 05503-900 São Paulo, SP, Brazil. size of the prefrontals; preocular, post-ocular and loreal * Corresponding author. E-mail: [email protected] absent; supraocular in contact with the prefrontals, 162 Raiany Cristine Cruz-da-Silva et al.

Figure 1. Anomalous A. scytale specimen (IBSP 89520), in dorsal (A) and ventral (B) views; A. scytale specimens showing normal coloration in dorsal (C) (unvouchered) and ventral (D) (IBSP 89518) views. Arrows (in A and C) indicate the parietal region.

separating the frontal from the oculars; a parietal region In contrast, from a taxonomically more splitter point with a single large scale, whose shape resembles a of view, the presence of a single character (one big scale “heart” (Figure 1A); supralabials 6/6; infralabials 6/6; in the parietal region), coupled with the very different symphysal separated from the anterior chin shields by marking pattern than that often observed for A. scytale, the second pair of supralabials. could be interpreted as sufficient characteristics for the In general, the meristic characters of the IBSP 89520 recognition of another taxon. Although this is plausible, specimen are inserted within the known variation for we opted for a more conservative posture, considering A. scytale (Table 1), except for the presence of a single specimen IBSP 89520 as anomalous, according to the large scale in the parietal region (vs. usually three small following arguments: (1) absence of other individuals scales in typical A. scytale specimens). No records are with similar characteristics: according to Oliveira et available demonstrating variations in the number of al. (2016) knowledge about the richness, composition scales from the parietal region in A. scytale (Cunha and and endemism of species of the Brazilian fauna is Nascimento, 1978). However, the examination of the strongly influenced by sampling bias, in a context in few remaining A. scytale specimens (n = 8) from the which the similarity of species composition decreases Butantan Institute Herpetological Collection, revealed a with increasing distance to access routes. Although specimen (IBSP 82228, from Palmas, state of Tocantins, exceptions to this panorama may exist, the municipality Brazil) with only two scales in the parietal region, with of Palmas, the capital of the state of Tocantins, with the central and left fused, indicating that the fusion of several terrestrial and fluvial access routes, is certainly these scales seems to occur eventually. not among the poorly sampled Brazilian areas regarding A remarkable specimen of the genus Anilius 163

Table 1. Comparison of meristic data between the anomalous A. scytale specimen and normal individuals (based on Roze, 1958 and Cunha and Nascimento, 1978).

Meristic data IBSP 89520 A. scytale Dorsal scale rows 21/21/21 Usually 21/21/21 Ventrals 235 215 to 254 Subcaudals 12 11 to 14 Anal plate Single Single Supralabials 6/6 6/6 Infralabials 6/6 6/6 Parietal region With one big scale Usually with three small scales Sinfisal Separated from the anterior chin Usually separated from the anterior shields by the second pair of chin shields by the second pair of supralabials supralabials Preoculars Absent Absent Prefrontals Present, separating the frontal Present, separating the frontal from from the ocular the ocular Loreal Absent Absent Internasals Absent Absent

herpetofauna. In addition, in the early 2000s, the work in the area, collecting several A. scytale specimens, Tocantins River was dammed for the construction of the and none were similar in colour to specimen IBSP 89520 Luís Eduardo Magalhães Hydroelectric Power Plant. at (Valdir Germano pers. comm.); (2) the problem of the time, the Butantan Institute carried out regular field species description based on only one specimen: some snake species have been described in Brazil from only one specimen, through morphological comparisons (e. g. Lema, 2004a, b, c; Lema and Renner, 2006), which, by itself, is not a problem. However, this practice allows for the description of possibly anomalous specimens as new species, which tend to later be synonymized in taxonomic revisions (analyzing more specimens belonging to related taxa), and which generally clarify intraspecific morphological variations with greater robustness (e.g. Silveira, 2006, Costa and Bérnils, 2015; Mata-Silva and Wilson, 2016); (3) Chromatic and morphological anomalies may occur together in some cases: a high volume of scientific literature is available reporting cases of vertebrate specimens with aberrant colorations (e. g. Amaral, 1932, 1934; Sazima and Di-Bernardo, 1991; Van Grouw, 2006; Krecsák, 2008; Kolenda et al., 2017); at the same time, anomalies in the pattern of cephalic snake scutellation have also been observed, especially in fossorial species (Lema and Renner, 2005). In some cases, these anomalies (of both colour and morphology) occur together. While examining a large series of Apostolepis assimilis (Reinhardt, 1861) specimens, one of the authors (ADA) Figure 2. A) Apostolepis assimilis specimen (IBSP 83840) found a specimen (IBSP 62362, from Osasco, state with normal cephalic staining and scutellation; B) Anomalous of São Paulo, Brazil.) with aberrant marking pattern A. assimilis specimen (IBSP 62362). Both come from the (Figure 2B), whose cephalic scales (prefrontals, frontal municipality of Osasco, state of São Paulo, Brazil. and supraoculars) were all fused, forming a single large 164 Raiany Cristine Cruz-da-Silva et al. scale on the back of the head, a characteristic that is not early snakes using genomics, phenomics, and the fossil record. observable in any neotropical snake (Peters and Orejas- BMC Evolutionary Biology, 15(1):87. Miranda, 1970). In our opinion, both cases reported Kolenda, K., Najbar, B., Najbar, A., Kaczmarek, P., Kaczmarski, M., and Skawiński, T. (2017): Rare colour aberrations and herein (A. scytale and A. assimilis) resemble each other anomalies of amphibians and reptiles recorded in Poland. and the specimens should be considered anomalous. Herpetology Notes, 10:103-109. We chose to adopt a conservative stance and report Krecsák, L. (2008): Albinism and leucism among European it as an anomalous specimen, rather than describing it Viperinae: a review. Russian Journal of Herpetology, 15(2): 97- as a new taxon. Although A. scytale is under taxonomic 102. revision (Francisco Luís Franco pers. comm.) and the Lema, T. (2004a): Description of a new species of Apostolepis Cope, possibility of new taxa being revealed is pertinent, we 1861 (Serpentes, Elapomorphinae) from brazilian Cerrado. Acta Biológica Leopoldensia, 26(1): 155–160. believe that it is appropriate to await the appearance Lema, T. (2004b): New species of Tantilla Baird & Girard from of other specimens with similar characteristics to the northeastern Brazil (Serpentes, Colubrinae). Acta Biologica specimen described herein, that could better support a Leopoldensia, 26(2): 267–284. potential description in order to avoid future taxonomic Lema, T. (2004c): Nova espécie de Apostolepis Cope do estado de problems. Rondônia, Brasil (Serpentes: Elapomorphinae). Comunicações do Museu de Ciências e Tecnologia da PUCRS, Série Zoologia, Acknowledgements: To the Instituto Chico Mendes de 17: 81-89. Conservação da Biodiversidade (ICMBio) for issuing the research Lema, T. and Renner, M.F. (2005): Contribuição ao conhecimento license SISBio 52416-1; to Renato Gaiga, for the photograph of taxonômico de Apostolepis flavotorquata (Serpentes, the live specimen with normal coloration; (IBSP), Francisco Luís Elapomorphinae). 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Accepted by Robson Ávila