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Reproductive Biology of the Green Ground Snake Erythrolamprus Poecilogyrus Sublineatus (Serpentes: Dipsadidae) in Subtropical Brazil

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Reproductive Biology of the Green Ground Snake Erythrolamprus Poecilogyrus Sublineatus (Serpentes: Dipsadidae) in Subtropical Brazil Anais da Academia Brasileira de Ciências (2017) 89(3 Suppl.): 2189-2197 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201720160805 www.scielo.br/aabc | www.fb.com/aabcjournal Reproductive biology of the Green Ground Snake Erythrolamprus poecilogyrus sublineatus (Serpentes: Dipsadidae) in Subtropical Brazil FERNANDO M. QUINTELA¹, WILIAM C. MARQUES² and DANIEL LOEBMANN¹ ¹Laboratório de Vertebrados, Universidade Federal do Rio Grande, Av. Itália, Km 8, 96203-900 Rio Grande, RS, Brazil ²Instituto de Matemática, Estatística e Física, Universidade Federal do Rio Grande, Av. Itália, Km 8, 96203-900 Rio Grande, RS, Brazil Manuscript received on November 28, 2016; accepted for publication on February 20, 2017 ABSTRACT We investigated reproductive features of the dipsadid snake Erythrolamprus poecilogyrus sublineatus in the southernmost Brazilian coast, a subtropical region characterized by well-marked seasons. Females are significantly smaller than males, have a shorter tail, and reach sexual maturity at later times along their development. In contrast to tropical subspecies, E. p. sublineatus females presented a seasonal pattern, with secondary follicles occurring from late winter to early autumn and egg production restricted to the whole spring and early summer. Males presented seasonal variation in testes volume (increase in autumn and decrease in winter) while no significant seasonal variation was found in ductus deferens width. The number of oviductal eggs varied from two to nine, thus, real fecundity is also inferior than that observed in tropical E. poecilogyrus forms. Considering the thermal requirements for reproduction, it is possible that the colder climatic conditions of the southern Brazilian coast have shaped the seasonal reproductive pattern in E. p. sublineatus. The shorter body size of this subspecies may also represent a conditioning factor of low fecundity. Key words: Ecology, neotropics, Pampa Biome, reproduction, Squamata. INTRODUCTION reproductive cycles (Seigel and Ford 1987, Barros et al. 2012, 2014), investigations on species distributed Several studies on the reproductive biology of over more than one single morphoclimatic domain Neotropical snakes have demonstrated a great have revealed marked geographic divergences variety of spatial/temporal patterns, many of which on reproduction traits which were attributed to are strongly influenced by environmental factors climatic dissimilarities between the areas occupied (Vitt 1983, Pizzato and Marques 2006, Pizzato et by the examined populations (Pizzato and Marques al. 2007, 2008a, Marques et al. 2009, Siqueira et al. 2006, Leite et al. 2009, Siqueira et al. 2013). 2013, Loebens et al. 2016). Although phylogenetic Erythrolamprus poecilogyrus is a small-sized relationships are a recognized determinant of anurophagous dipsadid widely distributed in South Correspondence to: Fernando Marques Quintela America, from Venezuela and the Guyana to central E-mail: [email protected] Argentina (Dixon and Markezich 1992, Giraudo An Acad Bras Cienc (2017) 89 (3 Suppl.) 2190 FERNANDO M. QUINTELA et al. 2001). Currently, four subspecies are recognized: Rio Grande, Brazil (Appendix). All procedures the nominal E. p. poecilogyrus, restricted to adopted are in accordance with the institutional Atlantic Forest domains in the southeastern Brazil; committee on ethics in the use of animals for E. p. caesius, associated to Chaquean formations research. The study area is inserted in the Pampa in Bolivia, Paraguay and northern Argentina; E. p. biome (IBGE 2004) and comprises the climate types schotti, the most widespread subspecies, occurring “subtemperate humid” and “temperate humid” from Venezuela to Corrientes and Misiones according to the regional classification proposed provinces of Argentina; E. p. sublineatus, restricted by Maluf (2000). Seasons are well-defined and to the subtropical region of Rio Grande do Sul, in rainfall is concentrated mainly in the months of southernmost Brazil, up to Uruguay, Northeastern winter and spring (Vieira 1984). Monthly average and Central Argentina (Dixon and Markezich 1992, (grouped months) profiles of air temperatures and Giraudo 2001). fluvial discharge (spatial rainfall average estimates) Reproductive features are scarcely investigated measured throughout the sampling period (January in Erythrolamprus poecilogyrus. It is known that 2009-August 2016) in the study area are shown in Erythrolamprus p. poecilogyrus from the tropical Figure 1. Atlantic Forest shows a continuous pattern of Snout-vent length (SVL) and tail length (TL) vitellogenic development, which was attributed were measured in each specimen and a ventral to an abundance of anurans during the whole year incision was made from the middle of the body in the studied region (Pinto and Fernandes 2004). to around 5 mm above the cloaca. After sex A smaller sample of E. p. schotti from the semi- confirmation, the significance of differences in arid biome of Caatinga also revealed a continuous SVL values and in tail proportion in relation to pattern, likewise associated to anuran abundance body length (ratio TL/SVL) between adult males (Vitt 1983). Herein, we investigated the reproductive (n=125) and females (n=99) was examined with a biology of the southernmost distributed subspecies t test. The following data were obtained from E. p. sublineatus, restricted to humid subtemperate/ females: total number of ovarian follicles, number temperate domains (Dixon and Markezich 1992). of follicles in secondary vitellogenesis (secondary We examined the reproductive cycle, fecundity, follicles), diameter of the largest secondary follicle, sexual dimorphism and size at sexual maturity of total number of eggs, diameter of the largest egg. specimens from the southernmost Brazilian coast, The initial diameter of secondary follicles was and compared such data with the previous studies determined based on the scatterplot of the largest on the reproductive biology of E. poecilogyrus. follicles of all specimens (Almeida-Santos et al. MATERIALS AND METHODS 2014), which indicated a pronounced growth from 10 mm. In recently fixed specimens, follicles with We examined 283 specimens of Erythrolamprus diameters around 10 mm or greater differed from poecilogyrus sublineatus collected between smaller follicles due to the dark yellow coloration January 2009 and August 2016 along a stretch of (see Almeida-Santos et al. 2014). Thus, follicles approximately 450 km of coastal plain in the Rio with diameter equal or over 10 mm were considered Grande do Sul state (30º15’S, 50º29’W – 33º38’S, as in secondary vitellogenesis. Females were 53º17’W), in southernmost Brazil. All specimens considered mature when showing at least one of are deposited in the herpetological collection of the following characteristics: secondary follicles; Universidade Federal do Rio Grande (CHFURG), oviductal eggs; fold oviducts, an indicative of recent An Acad Bras Cienc (2017) 89 (3 Suppl.) Erythrolamprus p. sublineatus REPRODUCTION 2191 Figure 1 - Monthly average (grouped months) profiles of air temperatures (dashed line) and fluvial discharge (spatial rainfall average estimates; straight line) in the southernmost Brazilian coast throughout the sampling period of this study (January 2009-August 2016). oviposition (Mesquita et al. 2013). The female ellipsoid formula 4/3 π (a/2) x (b/2) x (c/2), where a reproductive cycle was characterized by analyses of = length, b = width and c = thickness (Pleguezuelos the distribution of females with secondary follicles and Feriche 1999, Rojas et al. 2013). Values of testes and/or oviductal eggs along the months of the year volume and distal ductus deferens of mature males and from analyses of the annual profile resultant (n=111) were submitted to statistical analysis. We from the plot of the largest follicules/eggs of each first examined the correlation between SVL and female (Mesquita et al. 2013, Almeida-Santos et al. the testes/ductus deferens variables. Since positive 2014). Fecundity was determined by the number of and moderate correlation was found between SVL eggs in the oviduct (real fecundity) and number of and both variables (SVL/testes volume: r= 0.412, secondary follicles (potential fecundity) (Mesquita p< 0.05; SVL/ductus deferens width: r= 0.414, p< et al. 2013). We examined the relationship between 0.05), we examined the occurrence of significant female SVL and fecundity parameters (real seasonal variation in the residuals generated by fecundity and potential fecundity) through a simple the linear regressions of testes volume and SVL linear regression analysis (Siqueira et al. 2013). and distal ductus deferens width and SVL through Males were considered mature when presenting an analysis of variance (ANOVA). This procedure coiled and opaque ductus deferens, indicating the aimed to remove the effect of the specimens’ body presence of sperm (Shine 1977, Almeida-Santos size on the seasonal variation of testes/ductus et al. 2014). The following measures were taken deferens dimensions (Pleguezuelos and Feriche from males: length, width and thickness of the right 1999). Samples were grouped by seasons as testis; width of the distal portion of the right ductus follows: summer (January-March), autumn (April- deferens (between the kidney and the cloaca). June), winter (July-September), spring (October- Volume of the right testis was calculated by the December). Next, aiming to identify the season(s)
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