An Acad Bras Cienc (2021) 93(1): e20190206 DOI 10.1590/0001-3765202120190206 Anais da Academia Brasileira de Ciências | Annals of the Brazilian Academy of Sciences Printed ISSN 0001-3765 I Online ISSN 1678-2690 www.scielo.br/aabc | www.fb.com/aabcjournal ECOSYSTEMS Morphological and biological variations of Running title: POPULATION the glass snake Ophiodes striatus (Spix, 1825) AND SEXUAL VARIATION IN GLASS SNAKE (Squamata, Anguidae) from southeastern Brazil PAOLA R. DE OLIVEIRA, JULIANE FLORIANO LOPES SANTOS, JORGE ABDALA Academy Section: ECOSYSTEMS DERGAM DOS SANTOS & BERNADETE M. DE SOUSA Abstract: Lizards of the Ophiodes genus, popularly known as glass snakes, are e20190206 exclusively Neotropical. Despite their wide geographic distribution, glass snakes are poorly studied and there are many knowledge gaps in their biology and ecology to be filled. In this context, the objective of this study was to analyze possible sexual and 93 (1) population morphological differences of Ophiodes striatus specimens collected from 93(1) different municipalities in the state of Minas Gerais, Brazil. A total of 63 specimens belonging to the Herpetological Collection of the Federal University of Juiz de Fora DOI - Reptiles (CHUFJF-Reptiles), collected between 1995 and 2015 were analyzed. All the 10.1590/0001-3765202120190206 specimens were necropsied and morphometric measures related to body and head were measured. The males and females analyzed showed similar morphometric measures, and there was no size-related sexual dimorphism. Principal component analysis did not group the analyzed specimens by sex or locality. A positive correlation was observed between the snout-vent length and the vestigial limb length. The present study brings new information related to sexual dimorphism and population morphometric variation of O. striatus, adding information that will help in better understanding the ecology, biology and evolution of the genus in Brazil. Key words: Lizards, morphometric, population variation, sexual dimorphism. INTRODUCTION & Teixeira 2007, Montechiaro et al. 2011, Cacciali & Scott 2012, 2015). The lizards belonging to the Ophiodes The Ophiodes genus is currently composed Wagler, 1828 genus (Squamata, Anguidae, of six species: Ophiodes fragilis (Raddi, 1820); Diploglossinae), popularly known as glass Ophiodes striatus (Spix 1825); Ophiodes snakes, glass lizards or smash breaks, are vertebralis Bocourt 1881; Ophiodes intermedius exclusively Neotropical and distributed from Boulenger 1894; Ophiodes luciae Cacciali & Scott the east of the Andes to the southeast of South 2015; Ophiodes enso Entiauspe-Neto et al. 2017. America (Borges-Martins 1998, Pizzato 2005, In addition to the species described above, three Barros & Teixeira 2007, Montechiaro et al. 2011, are morphospecies: Ophiodes sp. 1, Ophiodes Cacciali & Scott 2012, 2015, Oliveira et al. 2016, sp. 2 and Ophiodes sp. 3 (Borges-Martins 1998, Ortiz et al. 2017, Entiauspe-Neto et al. 2017). Pizzato 2005, Montechiaro et al. 2011, Cacciali & Some morphological characteristics include a Scott 2012, 2015, Costa & Bérnils 2018, Oliveira small pointed head, elongated body and tail, et al. 2016, Entiauspe-Neto et al. 2017). However, and an absence of external vestiges of anterior taxonomic and phylogenetic review studies of limbs with rudimentary posterior limbs (Barros An Acad Bras Cienc (2021) 93(1) PAOLA R. OLIVEIRA et al. POPULATION AND SEXUAL VARIATION IN GLASS SNAKE this group are lacking (Bernardo & Pires 2006, Federal De Juiz De Fora - Reptiles (CHUFJF- Barros & Teixeira 2007), causing it to still have Répteis) (Appendix 1) were used in the present several gaps. study. The lizards were collected in fields surveys In Brazil, the O. striatus species is found between 1995 and 2015, in the cities of Juiz de from mountainous areas of the southeast and Fora, Santa Bárbara do Monte Verde, Chácara, center-west in the biomes Cerrado and Atlantic Lavras, Ingaí, Ijaci, Ribeirão Vermelho, Coronel Forest (Barros & Teixeira 2007, Trindade et al. Xavier Chaves, Ritápolis, São João del Rei and 2013). The morphological variations observed in Tiradentes, in the state of Minas Gerais (Brazil). O. striatus and its wide geographic distribution The sexual determination for adults and suggest the existence of a complex species sub-adults was performed through macroscopic (Borges-Martins 1998, Bernardo & Pires 2006, observation of gonadal traits by necropsy. Barros & Teixeira 2007, Montechiaro et al. Specimens which had body length between 47.24 2011). Studies with O. striatus in Brazil are mm and 63.19 mm were considered juveniles limited to local information mainly on its diet, and were not necropsied; therefore, sexual reproductive biology and herpetofauna surveys identification was not performed. (Pizzatto 2005, Bernardo & Pires 2006, Quintela The external morphometric measurements et al. 2006, Barros & Teixeira 2007, Barbo 2008, calculated were: snout-vent length (SVL), tail Salles & Silva-Soares 2010, Montechiaro et al. length (TL), length of the vestigial hind limbs (LVL 2011, Zaher et al. 2011, Novelli et al. 2011, 2012, – measured from left side), distance between Sousa et al. 2010, 2012, Trindade et al. 2013, Lucas nostrils (DN), face commissure (FC), head height et al. 2016). Studies that analyze the ecological (HH) and head width (HW), as shown in Figure and biological variations of this species appear 2. Due to the curvature of the animal’s body, as a tool which contributes to the knowledge on linear measurements of the body (SVL) and tail the taxonomy and conservation of this group. (TL) were measured with the line of a string. It The morphological similarity between O. was placed on the animal (Figure 1) and then striatus specimens makes sexual determination extended to determine the size in millimeters based on external characteristics difficult. However, studies such as Pizzato (2005) and Montechiaro et al. (2011) determined the sexual dimorphism from external morphometric analyzes. In this context, we investigated the existence of sexual dimorphism and variation related to external morphological measurements of O. striatus collected from different municipalities in the state of Minas Gerais (Brazil) using morphometric data. MATERIALS AND METHODS Figure 1. Relation of the morphometric variables measured in Ophiodes striatus belonging to the A total of 63 O. striatus specimens of the Coleção Coleção Herpetológica da Universidade Federal de Herpetológica de Répteis da Universidade Juiz de Fora - Reptiles (CHUFJF-Reptiles). An Acad Bras Cienc (2021) 93(1) e20190206 2 | 9 PAOLA R. OLIVEIRA et al. POPULATION AND SEXUAL VARIATION IN GLASS SNAKE using a digital caliper. Tail length was measured adult specimens, it was possible to identify the on all specimens, including those having sex in 50 specimens (31 males and 19 females). regenerated or fragmented tails (the portions From the 19 necropsied females, four were being measured and then summed to define the pregnant with embryos at some gestational stage, total value of the tail length). and the specimens were collected between June Some descriptive statistics were investigated and September. The morphometric measures such as the mean, standard deviation, and were only verified in the individuals that were amplitude (maximum = M and minimum = m) in an advanced gestational stage, with complete for each variable, which were calculated by formation (Table I). The mean litter size was 4.50 analyzing the measurements of males, females (± 1.26, n = 4). The specimen that had the largest and juveniles of the whole sample. The size litter (n = 6) had SVL of 196.18 mm, while the variation of the specimens belonging to most smallest litter (n = 3) had SVL of 192.03 mm. geographically distant (Juiz de Fora and Ritápolis) The mean SVL of males and females was was also analyzed, aiming to investigate the similar, and no apparent differences were population variation since these populations. observed between their sizes (Table I). A similar Principal Component Analysis (PCA) was result was observed when the analysis was performed in order to analyze whether the performed with the specimens belonging to the sample would be organized into groups. PCA two most geographically distant (Juiz de Fora was done to find out if the morphometric and Ritápolis) (Table II). data showed groupings of the sample by sex There was no sex grouping in either PCA (male x female) and by location (Juiz de Fora (Figure 2a, b). PC1 explained 51.1% of the variation x Ritápolis). Principal Component Analysis observed, and PC2 explained 31.8%, with the (PCA) was performed to determine if variables accumulated proportion of 82.82% when using influenced the formation of groups based on body measures (Figure 2a). When using head sex and location. PCA was performed separately measures, PC1 explained 57.1% and PC2 17.5% for body variables (SVL, TL and LVL; n = 50) and of the variation observed, with a cumulative head (DN, FC, HH and HW; n = 45). Both analyzes proportion of 89.35% (Figure 2b). were performed to determing whether these According to the PCA data, it was also not variables influenced grouping by sex or location. possible to separate the populations from Juiz The Pearson Correlation test was performed to de Fora (n = 10) and Ritápolis (n = 17), indicating verify the correlation between the morphometric that both populations have similar size variation data. Both statistical tests were performed in (Figure 3). PC1 explained 92.3% of the variation Statistical Program R, version 3.4.2 (Vincent 2011, found in the sample, while PC2 only explained Paradis & Schliep 2018, Makiyama 2018, Oksanen 5.5% (cumulative ratio = 97.8%) (Figure 3). et al. 2019, Wickham et al. 2019). As there was no grouping of males and females in PCA, Pearson’s correlation test was performed with the whole sample without RESULTS distinction by sex. The correlation indicated a Fifty-five (55) of the 63 O. striatus specimens positive and moderate relationship (r = 0.46) belonging to CHUFJF-Reptiles were young/adult, between SVL and LVL (Figure 4), meaning that while eight were juveniles. Among the young/ the higher the SVL, the higher the LVL. An Acad Bras Cienc (2021) 93(1) e20190206 3 | 9 PAOLA R.