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Offspring Morphology and Early Growth of Thamnodynastes Pallidus (Linnaeus, 1758) in the Brazilian Atlantic Forest (Serpentes; Thachymenini)

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Offspring Morphology and Early Growth of Thamnodynastes Pallidus (Linnaeus, 1758) in the Brazilian Atlantic Forest (Serpentes; Thachymenini) Herpetology Notes, volume 12: 205-209 (2019) (published online on 16 January 2019) Offspring morphology and early growth of Thamnodynastes 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 genus Thamnodynastes comprises 19 species Information about the reproduction of T. pallidus is in South America, 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 snake (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 Bolivia, Colombia, Ecuador, Guyana, searches in the Reserva Biológica (REBIO) Guaribas Peru, Suriname, Venezuela, and Brazil (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. Animal, 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 Thamnodynastes pallidus 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. ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! 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. ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! Offspring morphology and early growth of Thamnodynastes pallidus 207 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 snakes’ 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) (Colubridae: remained with it in the mouth for approximately one to Dipsadinae: Tachymenini) in Brazil. Revista do Instituto de two minutes (Fig.
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