Herpetology Notes, volume 12: 205-209 (2019) (published online on 16 January 2019)

Offspring morphology and early growth of pallidus (Linnaeus, 1758) in the Brazilian Atlantic Forest (Serpentes; Thachymenini)

William M. da Silva¹, Paula F. de Araújo2, Rafaela C. de França3,4, Isabella M. M. C. Pedrosa2, and Frederico G. R. França2,5,*

The Thamnodynastes comprises 19 Information about the reproduction of T. pallidus is in , all presenting an opisthoglyphous scarce. Marques et al. (2014) found two reproductive dentition and viviparous reproductive mode (Nóbrega females in the Atlantic Forest in the State of Bahia, et al., 2016; Pereira-Filho et al., 2017). Thamnodynastes presenting two oviductal eggs in September 2008 and pallidus (Linnaeus, 1758) is a small (reaching six ovarian follicles in July 2013. Santana et al. (2017) 580 mm of total length), presents nocturnal and semi reported the birth of five offspring from Sergipe in arboreal habits in forest environments, and feeds mainly February 2015 and presented their morphometry. on amphibians (Diaz et al., 2004; Hamdan and Lira- Herein we report fetal size, offspring morphology and DaSilva, 2012). The species’ poison may present a mild early growth of T. pallidus based on the fetuses and or high toxicity (Araújo et al., 2018). Thamnodynastes newborns of two adult females collected during active pallidus occurs in , , Ecuador, , searches in the Reserva Biológica (REBIO) Guaribas , , , and (Nóbrega et (6.8068°S, 35.0871°W, 46 m elevation; Datum al., 2016). In Brazil, it presents a disjoint distribution WGS84), an Atlantic Forest fragment located in the including the Amazonian Forest in the States of Pará, Rio Tinto municipality, Paraíba State, northeast Brazil Rondônia, Acre, and Mato Grosso do Sul, and the (Mesquita et al., 2018). Atlantic Forest in the States of Paraíba, Pernambuco, Alagoas, Sergipe, and Bahia (Franco and Ferreira, 2002; Material and Methods Nóbrega et al., 2016; Santana et al., 2017). The two adult females of T. pallidus found in the field were initially kept in a translucent plastic box (300 x 200 x 400 mm) with holes in its cover, sawdust in the bottom and a water container. The first female was collected (under SISBIO license nº59536-1), fixed on formalin 10%, and housed in the Coleção Herpetológica ¹ Universidade Federal da Paraíba, Av. Santa Elizabete s/n, da Universidade Federal da Paraíba (CHUFPB) under Centro, 58297-000, Rio Tinto, Paraíba, Brazil. the collection number RF 309. Two fetuses were found 2 Núcleo de Ecologia de Serpentes, Laboratório de Ecologia in its oviduct and were measured before being fixed. , Universidade Federal da Paraíba, Av. Santa Elizabete s/n, Centro, 58297-000, Rio Tinto, Paraíba, Brazil. The second female and its offspring Zere measured on th ³ Universidade Estadual de Santa Cruz, Rodovia Jorge Amado the day of the birth (6 of January 2018) and one month Km 16, 45662-900, Ilhéus, Bahia, Brazil. later (Tables 1–2). In the meanwhile, we offered them 4 Herpetology Section, Zoologisches Forschungsmuseum live anurans as small as possible, so they could feed Alexander Koenig, Adenauerallee 160, 53113 Bonn, twice. The newborns were offered anurans three and Germany. 10 days after hatchling, while the mother was offered 5 Departamento de Engenharia e Meio Ambiente, Centro de prey five and 10 days after giving birth (Table 3). The Ciências Aplicadas e Educação, Universidade Federal da Paraíba, Av. Santa Elizabete s/n, Centro, 58297-000, Rio anurans were captured in a riparian forest close to an Tinto, Paraíba, Brazil. urban area of Rio Tinto city, about 5 km from REBIO * Corresponding author. E-mail: [email protected] Guaribas. 206 William M. da Silva et al.

Table 1. Measurements of the five offspring (Tp 1–5) and mother (Adult) of in the day of birth (6th of January 2018) and one month later (* – 6th of February 2018). Abbreviations: SVL – Snout-vent length; TL – Tail length; HH – Head height; HL – Head length; HW – Head width; BH – Body height; BW – Body width; OD – Ocular diameter; DBN – Distance between nostrils; OCD – Ocular-Nasal Distance; DBE – Distance between eyes; TW – Tail Width; SLD – Snout-labial distance; VSD – Ventral-Symphysial Distance; MA – Mass. All measures are in mm except mass in g.

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After the second round of measurements, the adult width; OD – Ocular diameter; DBN – Distance between female was fixed on formalin 10%, (SISBIO licensenostrils; OCD – Ocular-Nasal Distance; DBE – Distance nº59536-1) and housed at CHUFPB under the collection between eyes; TW – Tail Width; SLD – Snout-labial number RF 337. Two of the five newborns were also distance; VSD – Ventral-Symphysial Distance; MA housed at CHUFPB (Tp 2 = RF 359 and Tp 5 = RF 375) – Mass. For newborns and adults, ToL, SVL, and TL and the other three (Tp 1, Tp 3, Tp 4) were released at were taken with a stainless-steel ruler (1 mm precision), REBIO Guaribas. while HH, HL, HW, BH, BW, OD, DBN, OCD, DBE, For each individual of T. pallidus we took the following TW, SLD, and VSD were taken with a Mitutoyo® measures: ToL – Total length; SVL – Snout-vent length; digital caliper (0.1 mm precision). The body masses of TL – Tail length; HH – Head height; HL – Head length; newborns and both adults were measured, respectively, HW – Head width; BH – Body height; BW – Body with 10 g and 50 g Pesola® scales (0.1 g precision). The

Table 2. Mean (M) and standard deviation (SD) of the dimensions of five offspring of Thamnodynastes pallidus in the day of birth (6th of January 2018) and one month later (6th of February 2018) and the growth rates (GR in %) of all dimensions. Abbreviations: SVL – Snout-vent length; TL – Tail length; HH – Head height; HL – Head length; HW – Head width; BH – Body height; BW – Body width; OD – Ocular diameter; DBN – Distance between nostrils; OCD – Ocular-Nasal Distance; DBE – Distance between eyes; TW – Tail Width; SLD – Snout-labial distance; VSD – Ventral-Symphysial Distance; MA – Mass. All measures are in mm except mass in g.

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SVL of each frog was taken with a stainless-steel ruler Results and Discussion (1 mm precision) and the mass with a 10 g Pesola® (0.1 The first adult female of T. pallidus (RF 309; SVL = g precision). 320 mm, TL = 99 mm, HL = 11.5 mm, mass = 11 g) was captured on 9 December 2017 at 1403 h inside bushes on the border of the trail and died one day after. When examined, the specimen presented no dietary content in stomach or gut, but two fetuses partially formed in the Table 3. Measurements of frogs offered to the offspring (Tp oviduct (ToL = 91 mm and 89 mm). 1–5) on the 9th of January 2018 (without an asterisk) and on The second adult female of T. pallidus (Fig. 1A) was th the 16 of January 2018 (with an asterisk) and to the mother captured on the 18th of December 2017 at 1939 h, on a th (Adult) on the 11 of January 2018 (without an asterisk) and bush in the border of the trail. On 6 January 2018 the on the 16th of January 2018 (with an asterisk). Frog mass animal gave birth to five offspring (measurements and (F-mass) in g; Frog length (F-length) in mm. Behavioural observation (OBS): E – eat; N – Not eat nor kill; K – Kill but masses in Table 1). did not eat. The smallest and biggest offspring had, respectively, 175 mm and 192 mm of ToL, equivalent to respectively 31% and 35% of the mother’s ToL (548 mm). These            measures are similar to those found by Santana et al.         (2017), where the smallest and biggest snake offspring         had 35% and 39% of the mother’s ToL, respectively.         Comparing the ToL average for all newborns from         each State, the offspring of T. pallidus from Sergipe         (Santana et al., 2017) are approximately 15% bigger         than those from Paraíba (Table 2), whereas the snake        mother from Sergipe was 5% bigger than the one from         Paraíba, suggesting a correlation between the lengths of       the mother and offspring.         The adult and three offspring ate all the anurans offered            to them (Table 3). One snake (Tp 2) rejected both frogs            offered and did not even attack the prey. Another one

Figure 1. (A) The mother Thamnodynastes pallidus from Reserva Biológica Guaribas, Rio Tinto Municipality, Paraíba State, northeast Brazil; (B) A T. pallidus offspring (Tp 3) eating a Rhinella crucifer. 208 William M. da Silva et al.

(Tp 3) did not eat a Scinax x-signatus (Spix, 1824) current master’s degree scholarship, PFA thanks CNPq for the regardless of attacking and killing it but, one week later, PIBIC undergraduate grant, RCF thanks FAPESB for her current it ate a Pristimantis ramagii (Boulenger, 1888). PhD scholarship (BOL0353/2016), and CNPq for Doutorado Sanduíche no Exterior (SWE) scholarship (208442/2017-0), and Variations in ’ growth rates are consistently FGRF thanks the financial support from CNPq (Universal Grant linked to food abundance, suggesting correlation with Nº 404671/2016-0) food supply, principally in the first year of life, called ‘silver spoon’ effect (Seigel and Ford, 1991; Madsen and References Shine, 2000). Therefore, it is common that newborns attempt to predate and eat in early stages of life (Greene, Araújo, P.F., Silva, W.M., França, R.C., França, F.G.R. (2018): A case of envenomation by neotropical opisthoglyphous 1983). All snakes that attacked the frogs in the body area snake Thamnodynastes pallidus (Linnaeus, 1758) (: remained with it in the mouth for approximately one to : Tachymenini) in Brazil. Revista do Instituto de two minutes (Fig. 1B). After this, they began to ingest Medicina Tropical de São Paulo 60 (38): 1–. the prey by its head and took from five to eight minutes Diaz, F., Navarrete, L.F., Pefaur, J., Rodrigues-Acosta, A. until total ingestion. (2004): Envenomation by neotropical opistoglyphous Almost all morphometric measures showed a quick colubrid Thamnodynastes cf. pallidus Linné, 1758 (Serpentes: growth in the newborns. During the first month, SVL Colubridae) in Venezuela. Revista do Instituto de Medicina Tropical de São Paulo 46 (5): 287–20. and TL grew by averages of 4% and 3%, respectively Franco, F.L., Ferreira, T.G. (2002): Descrição de uma nova espécie (Table 2). The dimensions did not change significantly de Thamnodynastes Wagler, 1830 (Serpentes, Colubridae) in the adult female. Young snakes grow rapidly during do Nordeste Brasileiro, com comentários sobre o gênero. the first few years of life, before attaining asymptotic Phyllomedusa 1(2): 57–74. sizes when reaching adulthood (Madsen and Shine, França, F.G.R., Mesquita, D.O., Nogueira, C.C., Araújo, A.F.B. 2000). (2008): Phylogeny and ecology determine morphological The first skin shedding of all newborn snakes took structure in a snake assemblage in the Central Brazilian Cerrado. Copeia 2008 (1): 20–36. place between 8–10 days after birth. Snake ecdysis or Greene, H.W. (1983): Dietary correlates of the origin and radiation skin shedding is an essential part of the growth for all of Snakes. American Zoologist 23 (2): 431–44. snake species, and newborns can shed their skin as of Hamdan, B., Lira-da-Silva, R.M. (2012): The Snakes of Bahia 24–36 h after birth or hatching (Lillywhite, 2014). 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While adults’ morphologies (e.g. maximum site variation in tropical pythons. Ecology 80 (3): 987–997. SVL) are generally used in ecomorphological studies Madsen, T., Shine, R. (2000): Silver spoons and snake body sizes: prey availability early in life influences long-term growth rates on populations and communities (Hedges, 2002; França of free-ranging pythons. Journal of Animal Ecology 69 (6): et al., 2008), the newborn morphometry is less explored 952–958. (Norval et al., 2007; Santana et al., 2017; Morais et Maderson, P.F.A. (1984): The Squamate epidermis: new light has al., 2018), but not less important. The knowledge of been shed. Symposium of the Zoological Society of London 52: morphometric variation of a snake, since its birth until 111–126. it reaches adult sizes, can be important to elucidate Marques, R., Fonseca, E., Tinôco, M.S. (2014): Thamnodynastes taxonomic and systematic questions, to understand pallidus (Amazon coastal house snake). Reproduction. 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Accepted by Pedro Pinna