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Home , Pseustes, Pseustes sulphureus, Spilotes, Spilotes pullatus

Herpetology Notes, volume 11: 441-444 (2018) (published online on 24 May 2018)

Eggs and hatchling morphometry of sulphureus (Wagler in Spix, 1824) (Serpentes: : : Colubroidea: Caenophidia) from northeastern Brazil

Mayara da Silva Ribeiro de Morais1,*, Rafaela Cândido de França2, Fagner Ribeiro Delfim³ and Frederico Gustavo Rodrigues França4

The Spilotes comprises two with Ortleb, 1969). It is oviparous and juveniles are known terrestrial and arboreal habits, S. pullatus and S. from February, March, April, August, November, and sulphureus (the latter formerly placed in the genus December in Brazil (Gos Santos-Costa et al., 2015; ; Jadin et al., 2014; Pereira-Filho et al., 2017). Martins and Oliveira, 1998). Boos (2001) stated that a Spilotes sulphureus is among the largest colubrid , female from Trinidad laid 12 eggs in June, and guarded reaching a maximum total length of 2495 mm (Rivas them “to some extent”. Goode (1989) reported two and Kane, 2003). This species is distributed throughout females with 1500 mm SVL and 1700 mm SVL with 7 northern South America. In Brazil, it is distributed in and 14 eggs, respectively. Atlantic Forest (França, et al., 2012; Andrade et al., On 23 August 2012, a gravid female Spilotes sulphureus 2017; Pereira-Filho et al., 2017) and Amazon Forest (Figure 1a) with a snout-vent-length (SVL) of 1100 mm biomes (together characterized as Brazilian rainforests; and tail length (measuring from the end of the cloaca Martins and Oliveira, 1998; Bernarde et al., 2012), as to the tip of the tail; TL) of 430 mm, was collected in well as in Cerrado (with the characteristic vegetation of the forest patch SEMA III in the Guaribas Biological savannah; Nogueira et al., 2010), and Caatinga biomes Reserve (REBIO; this reserve is fragmented into three (together characterized as dry tropical forest; Guedes et forest patches called SEMAs [Secretaria Especial do al., 2014). Meio Ambiente]; Arruda et al., 2014), located in Rio This is diurnally active and feeds mainly on Tinto municipality, state of Paraíba, northeast Brazil (- small and (Cunha and Nascimento, 6.806826°S, -35.087114°W; WGS84). This reserve is a 1993). When threatened, its defensive behaviour protected area representative of the Brazilian Atlantic involves puffing out the throat and vibrating the tail Forest biome and the patch SEMA III is characterized noisily (Rossman and Williams, 1966; Rand and by forested habitat formed by trees with fairly high canopy and rich shrub and herbaceous strata. The snake was kept in captivity at 22°C and was not fed. On 28 August 2012 it laid 15 eggs (Figure 1b) that averaged 53.68 ± 3.87 mm (mean ± standard error; range = 48.74 1 Programa de Pós-Graduação em Ecologia e Monitoramento to 64.32 mm) in length and 27.8 ± 1.25 mm (mean ± Ambiental, Universidade Federal da Paraíba, CEP 58297- standard error; range = 25.64 to 30.29 mm) in width. 000, Rio Tinto – PB, Brasil. 2 Programa de Pós-Graduação em Ecologia e Conservação After laying the eggs the snake was released at SEMA da Biodiversidade, Universidade Estadual de Santa Cruz, III. All eggs were measured at their longest and widest Salobrinho, CEP 45662-900, Ilhéus – BA, Brasil. point, using digital callipers (precision = 0.1 mm). 3 Laboratório e Coleção de Herpetologia do Departamento The eggs were incubated in a plastic box half-buried de Sistemática e Ecologia, Centro de Ciências Exatas e da in moistened vermiculite at a constant temperature of Natureza (CCEN), Universidade Federal da Paraíba, Cidade 25°C. On 20-22 November 2012, after 85-87 days of Universitária, CEP 58051-900, João Pessoa – PB, Brasil. incubation, 14 hatchlings emerged. One egg that did not 4 Departamento de Engenharia e Meio Ambiente, Centro de Ciências Aplicadas e Educação, Universidade Federal da hatch was dissected and contained a dead embryo. Paraíba, CEP 58297-000, Rio Tinto-PB, Brasil. The hatchlings snakes showed a juvenile colour * Corresponding author. Email: [email protected] pattern different from the mother (Figure 1c), with 442 Mayara da Silva Ribeiro de Morais et al.

Figure 1. (a) Gravid female Spilotes sulphureus from Rio Tinto, state of Paraíba, Qortheast Brazil; (b) clutch comprised of 15 eggs of S. sulphureus; (c) S. sulphureus neonate; (d) the five neonates housed in the Herpetological Collection of the Universidade Federal da Paraíba.

conspicuous bands all along the body. For each neonate 1d) in the Herpetological Collection of the Universidade we measured the snout-vent length (SVL), the tail Federal da Paraíba at one week post-hatching (vouchers: length (TL), the head length (distance of the tip of the CHUFPB 15846, 15847, 15850, 15851, 15852) and the snout to the posterior margin of the parietal scales; +L),RWher nine neonates were released at REBIO Guaribas head width (distance between the widest points of the (SEMA III) eight days after hatching. head;; HW), head height (distance between the highest Morphometric measurements of snakes at all life points of the head; HH), eye diameter (ED), length stages are important data both in taxonomic analyses between nostrils (distance between the two nostrils; and in population/community studies, because they BN), body height (measured in the middle of the body; allow comparisons among individuals and species, BH), and body width (measured in the middle of the help parameterize life history analyses, and can be a body; BW) using digital callipers (precision = 0.1 proxy for habitat use in studies of ecomorphological mm), and the body mass using a Pesola spring scale structure of communities (França et al., 2008; Passos (precision = 0.3 g). The average values were 394.07 and Prudente, 2012; França and Braz, 2013). These ± 27.31 mm (range = 323 to 424 mm) SVL, 141.35 ± are the first morphometric measurements of Spilotes 10.02 mm (range = 125 to 158 mm) TL, and 18.42 ± sulphureus eggs and hatchlings, and these records may 2.73 g (range = 14 to 25 g) mass (see Table 1). Five of be useful in future ecological and taxonomic studies of the 14 neonates were euthanised and deposited (Figure the species. Eggs and hatchling morphometry of Spilotes sulphureus from Brazil 443

Table 1. Morphometry (mm) and mass (g) of the hatchlings of Spilotes sulphureus from the municipality of Rio Tinto, state of Paraíba, northeast Brazil. Snout-vent length = SVL, Tail length = TL, Head length=HL, Head width= HW, Head height = HH, Eye Diameter = ED, Between nostrils = BN, Body width = BW, Body height = BH, F = female, M = male, and UNK = indeterminate sex. *Individuals released at Guaribas Biological Reserve; **Individuals deposited in the Herpetological Collection of the Universidade Federal da Paraíba.

SVL TL HL HW HH ED BN BW BH Mass Sex Indiv. 1* 412 149 19.10 10.37 8.2 4.77 4.98 8.61 11.77 18 F Indiv. 2* 424 143 21.24 10.79 8.58 4.39 4.98 13.22 8.75 20 F Indiv. 3* 390 148 20.02 9.72 7.55 4.59 4.91 8.68 9.94 16 M Indiv. 4* 385 132 19.54 10.01 8.02 4.74 4.7 8.35 8.91 16 M Indiv. 5* 392 134 20.26 19.08 7.71 4.37 5.04 9.44 12.58 17 F Indiv. 6* 419 156 20.26 9.76 8.23 4.96 4.86 7.35 9.68 17 M Indiv. 7* 414 137 20.07 9.74 8.1 4.79 5 7.96 10.49 18 F Indiv. 8* 398 133 20.31 7.34 7.7 4.53 4.54 9.05 12.35 18 F Indiv. 9* 410 144 21.21 9.85 8.21 5.09 4.94 8.73 11.37 19 F CHUFPB 15846** 351 130 20.54 10.94 8.35 5.03 4.62 8.34 8.00 14 UNK CHUFPB 15847** 392 140 19.86 11,00 8.61 4.62 4.63 7.78 9.02 18 UNK CHUFPB 15850** 403 158 19.77 11.57 8.75 4.87 5.31 7.28 9.46 22 UNK CHUFPB 15851** 323 125 18.01 10.88 9.63 3.97 4.66 8.87 9.16 20 UNK CHUFPB 15852** 404 150 21.75 11.92 8.77 4.64 5.15 8.88 10.55 25 UNK Mean 394.07 141.35 20.13 10.92 8.31 4.66 4.88 8.75 10.14 18.42 - Standard deviation 27.31 10.02 0.93 2.59 0.53 0.29 0.22 1.43 1.42 2.73 -

Acknowledgements. We are grateful to Dr. Daniel Oliveira França, F.G.R., Braz, V.D.S. (2013): Diversity, activity patterns, Santana for reviewing and confirming the species in this paper. and habitat use of the snake fauna of Chapada dos Veadeiros We thank the Herpetological Collection of the Universidade National Park in Central Brazil. Biota Neotropica 13: 74-84. Federal da Paraíba for support and the ICMBio for permits in França, F.G.R., Mesquita, D.O., Nogueira, C.C. , Araújo, A.F.B. REBIO Guaribas (SISBIO license 22940-2). MSRM thanks (2008): Phylogeny and ecology determine morphological CAPES for her master’s fellowship. RCF thanks FAPESB for her structure in a snake assemblage in the Central Brazilian Cerrado. current PhD scholarships. FGRF thanks financial support from Copeia 2008: 23-38. CNPq (Universal grant 404671/2016-0). Goode, M. (1989): . Reproduction. Herpetological Review 20: 73. Guedes, T.B., Nogueira, C., Marques, O.A. (2014): Diversity, References natural history, and geographic distribution of snakes in the Andrade, H., Almeida, R.P.S., Dias, E.J.R. (2017): Spilotes Caatinga, Northeastern Brazil. Zootaxa 3863: 1-93. sulphureus Wagler, 1824 (: Colubridae): review of Jadin, R.C., Burbrink, F.T., Rivas, G.A., Vitt, L. J., Barrio-Amorós, distribution and first record in the state of Sergipe, northeastern C.L., Guralnick, R.P. (2014): Finding arboreal snakes in an Brazil. &heck List 13: 2055. evolutionary tree: phylogenetic placement and systematic Arruda, D. B., Cunha, B. P., Rêgo, K. M. C. (2014): Conflitos entre revision of the Neotropical birdsnakes. Journal of Zoological REBIO Guaribas e comunidades locais: (in) justiça ambiental Systematics and Evolutionary Research 52: 257-264. e ecologia política. Revista Direitos Emergentes na Sociedade Martins, M., Oliveira, M. (1998): Natural History of snakes Global 2: 280-304. in forests of the Manaus region, Central Amazonia, Brazil. Bernarde, P.S., Albuquerque, S., Barros, T. O., Turci, L. C. Herpetological Natural History 2: 78-150. B. (2012): Serpentes do estado de Rondônia, Brasil. Biota Nogueira, C., Colli, G.R., Costa, G., Machado, R.B. (2010): Neotropica 12: 154-182. Diversidade de répteis Squamata e evolução do conhecimento Boos, H.E. (2001): The snakes of Trinidad and Tobago. College faunístico no Cerrado. In: Cerrado: conhecimento científico Station, Texas A&M University Press. quantitativo como subsídio para ações de conservação, p. 329- Cunha, O., Nascimento, F.P. (1993): Ofídios da Amazônia: As 371. Diniz, I.R., Marinho-Filho, J., Machado, R.B., Cavalcanti, cobras da região leste do Pará, Belém. Museu Paraense Emílio R.B., Ed., Brasília, UNB Press. Goeldi série Zoologia 9: 1−191. Passos, P., Prudente, A.L. (2012): Morphological variation, dos Santos-Costa, M. C., Maschio, G. F., da Costa Prudente, A. polymorphism and of the Atractus torquatus complex L. (2015): Natural history of snakes from Floresta Nacional de (Serpentes: Dipsadidae). =ootaxa 3407: 2-21. Caxiuanã, eastern Amazonia, Brazil. Herpetology Notes 8: 69- Pereira-Filho, G.A., Vieira, W.L.S., Alves, R.R.N., França, F.G.R. 98. (2017): Serpentes da Paraíba: Diversidade e Conservação, 1st 444 Mayara da Silva Ribeiro de Morais et al.

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Accepted by Andrew Durso