Tropical Zoology 23, 000-000, 2010

Morphological characterization of adults of Orbigny’s slider dorbignyi (Duméril & Bibron 1835) (Testudines ) in southern Brazil

A. Bager 1,1, T.R.O. Freitas 2 and L. Krause 3 1 Departamento de Biologia, Universidade Federal de Lavras, Campus Universitário, 37200-000 Lavras, Minas Gerais, Brazil 2 Departamento de Genética, Universidade Federal do Rio Grande do Sul, C.P. 15053, Porto Alegre-RS, Brazil, 91501 970 3 Departamento de Zoologia, I.B., Setor de Herpetologia, Prédio 43.435-S/105, Universidade Federal do Rio Grande do Sul, Avenida Bento Gonçalves 9.500, Porto Alegre-RS, Brazil, 91501 970

Received 11 March 2010, accepted, 11 June 2010

We characterized a population of the Southern Orbigny’s slider , Trachemys dorbignyi (Duméril & Bibron 1835), in its natural environment, focusing on the sex ratio, morphology and sexual dimor- phism. The male:female sex ratio was 1.02:1. The 16.8% difference in mean size between the sexes of T. dorbignyi is among the small- est in the family Emydidae. The female is larger than the male in all measurements except one (carapace and plastron terminal distance, CPD). CPD proved to be the most useful measurement to identify the gender of smaller individuals. The discriminant analysis was ca- pable of differentiating males and females with 100% accuracy. CPD was the most important variable in differentiating males, and the cara- pace height and width of the mouth were most important for females. key words: sexual dimorphism, morphometry, sexual maturity, population structure, Trachemys dorbignyi, Emydidae.

Introduction ...... 2 Material and methods ...... 3 Results ...... 6 Discussion ...... 9 Acknowledgements ...... 11 References ...... 11

1 Corresponding author: Dr Alex Bager, (E-mail: [email protected]). 2 A. Bager, T.R.O. Freitas and L. Krause

INTRODUCTION

According to Ernst (1990), the most frequently studied of fresh- water is probably Trachemys (Reptilia Testudines Emydidae), commonly known as sliders. Seidel et al. (1999) reported that the Trachemys scripta com- plex, including T. dorbignyi (Duméril & Bibron 1835), is an especially difficult group, with no clear taxonomic relationships among the species and because of a lack of sufficient genetic and morphological data. Phylogenetic anal- yses of the 26 taxa recognized in the genus Trachemys have suggested the existence of 15 species, 8 of them polytypic (Seidel 2002). Trachemys dorbignyi, the Southern Orbigny’s slider, is the southernmost species of the group, inhabiting Uruguay, northern Argentina and the state of Rio Grande do Sul in southernmost Brazil (Lema & Ferreira 1990). There is no explanation for the isolation of T. dorbignyi in southern South America. The geographically closest species is Trachemys adiutrix (Vanzolini 1995), which occurs 3000 km to the north in the Brazilian state of Maranhão (Vanzolini 1995). According to Seidel (2002), the relationships of T. adiutrix with T. dor- bignyi and the other South American species require further study. Freiberg (1969) described two subspecies: T. d. dorbignyi from Uruguay and Argentina, and the Brazilian T. d. brasiliensis. However, these subspecies have not been widely accepted by subsequent authors. Barco & Larriera (1991) repeated Freiberg’s analysis using larger samples and concluded that the suppos- edly diagnostic morphological characteristics separating the two subspecies were mainly a reflection of ontogenetic variation. Seidel (2002) continued to recog- nize T. d. brasiliensis as a subspecies of T. dorbignyi. Among the publications describing the biology of T. dorbignyi (Freiberg 1969; Krause et al. 1982; Silva et al. 1984; Cascone et al. 1991; Vanzolini 1997, Molina & Gomes 1998a, 1998b; Malvasio et al. 1999; Souza et al. 2000; Bager et al. 2007a, 2007b; Gonçalves et al. 2007), none has described the morphology of the species in detail. Biometric studies have been an impor- tant tool for the differentiation between species and subspecies (Lamb & Lovich 1990, Lovich & Lamb 1995, Seidel et al. 1999), geographical variation within a species (Iverson 1985, Lubcke & Wilson 2007), analysis of reproductive parameters (Congdon & Van Loben Sels 1991, Daza & Páez 2007) and evaluation of the impact of commercial exploitation (Close & Seigel 1997, Gamble & Simons 2004). Thus, a more detailed understanding of morphologi- cal variation in Trachemys dorbignyi will be critical to elucidating the systematic relationships of this species. For example, Stephens & Wiens (2003) excluded T. dorbignyi from a phylogenetic study of the Emydidae because of a lack of data on its morphology and diet. In the present study, we characterized a wild population of T. dorbignyi in southern Brazil in order to complement the available morphological data and make it possible to compare this population with other species of the Trachemys complex. We analyzed the sex ratio, morphological variables in both genders and sexual dimorphism. Trachemys dorbignyi morphology 3

MATERIAL AND METHODS

The study area lies on the coastal plain of Rio Grande do Sul, with a subtropi- cal climate (Cfa) (Köeppen 1948) characterized by well-distributed rainfall through- out the year and mean annual precipitation of 1252 mm. The maximum temperature exceeds 22 °C in summer (December to March) and oscillates between 18 and – 3 °C in winter (June to September) (Moreno 1961). The area is called the Verde La- goon Complex (UTM 22H 385820mE 6445000mN) and includes the Verde La- goon itself, the Senandes and Bolacha streams, and associated swamps, palustrine forest and fields (Fig. 1). This complex of aquatic, terrestrial and transitional habitats is an area of estuarine swamps of about 3500 ha, with a maximum water depth of 80 cm, salinities up to 17‰ and extensive aquatic macrophytes. Adults of T. dorbignyi were captured by hand via snorkeling (Moll & Moll 2004, Lubcke & Wilson 2007). Males and females occupy the same habitat, mak-

Fig. 1. — Verde Lagoon Complex, state of Rio Grande do Sul, Brazil. Te nearest large town is Rio Grande; urban areas are in gray. Axes are in UTM grid units. 4 A. Bager, T.R.O. Freitas and L. Krause

ing it possible to collect an unbiased sample of individuals of all length classes larger than 130 mm CL. The greatest advantage of sampling by diving is the elimination of errors produced by the use of baited traps. Traps can select individuals for sex or size, and trap samples may be influenced by diet, differing mobility between the sexes and other unknown factors (Boundy & Kennedy 2006). All the turtles were marked by notching the marginal scutes using Cagle’s (1939) method. Only data taken the first time each was captured were used. We combined the principal morphometric measurements of the carapace and plastron described in previous studies of freshwater turtles (Legler 1990, Daza & Paéz 2007, Rivera 2008) and established others. Up to 29 measurements were taken on each individual. Fig. 2 shows how the measurements were made and their acronyms. Circular measurements such as circular carapace length (CCL) or circular carapace width (CiCW) were taken with a non-stretching tape. They were measured at the same points for carapace length and maximum carapace width, respectively. Cephalic and mouth width were measured over the tympanic mem- branes and the maximum width of the lower rhamphotheca, respectively. Males were sexed on the basis of secondary sexual characteristics: tail length (longer in males) and carapace melanization (males have darker carapaces) (Seidel 1990, Molina 2001). Only females over 180 mm in carapace length were included in the descriptive statistics, because this is the shortest length recorded for nesting females in the area (A. Bager pers. comm.). Another 16 non-reproductive females with carapace lengths between 154 and 179 mm were included in the regression analysis. This allowed comparisons between males and females of the same size, and also estimation of the carapace length at which the allometry between the sexes begins. Original, non-transformed data were used for the statistical analyses, except in the discriminant analysis which was executed using the values of each variable divided by the maximum length of the carapace. This approach was used to reduce the effect of size and to improve the analyses of allometry of shape between males and females. Some investigators have questioned the use of data obtained from the ratio between two variables in morphometric analyses (Peres-Neto et al. 1995), but Seidel et al. (1999) and Aresco & Dobie (2000) used this technique for chelonians, with some success. Sexual size dimorphisms (SSD) were quantified as recommended by Stephens & Wiens (2009), according to the equation: SSD = (Mean of Female CL / Mean of Male CL) – 1 The sex ratio of males and females was compared by χ² analysis, using the Yates correction and equal expected proportions. The fit to a normal distribution was tested (Shapiro-Wilk), as well as the homogeneity of variance (Levene test). Analysis of variance (ANOVA) was used to compare both sexes in univariate analysis. Linear regression analyses were carried out using carapace length (CL) as the independent variable and maximum carapace height (MHS), circular carapace width (CiCW), cephalic width (CW), and carapace and plastron terminal distance (CPD) as the de- pendent variables. Parallelism tests were used to compare the linear regression results for males and females. When the parallelism test indicated a non-significant differ- ence, we used covariance analyses (with carapace length as the covariable parameter) to compare the intercept. The discriminant analysis was conducted with six vari- ables (CPD; ALW; MCW; MPW; MHS; CW) and 66 specimens, 44 males and 22 females. We selected the normal variables and those that maximized the number of specimens in the analysis. Only 66 specimens were analyzed because we could not Trachemys dorbignyi morphology 5

Fig. 2. — Morphological measurements of Trachemys dorbignyi (circular and cephalic measurements are excluded) (Modifed from Legler, 1990). Key: 1. carapace length (CL); 2. maximum carapace width (MCW); 3. central carapace width (CCW); 4. length of third central scute (LC3); 5. width of third central scute (WC3); 6. nuchal scute length (NL); 7. maximum carapace height (MHS); 8. carapace and plastron terminal distance (CPD); 9. maximum plastron length (MPL); 10. mid-ventral suture length (MVSL); 11. anterior lobe width (ALW); 12. maximum plastron width (MPW); 13. posterior lobe width (PLW); 14. central bridge length (CBL); 15. maximum bridge length (MBL); 16. width of left and right gular scutes (WGS); 17. left gular scute length (GSL); 18. left pectoral scute length (PEL); 19. left pectoral scute width (PSW); 20. left abdominal scute length (ASL); 21. left abdominal scute width (ASW); 22. left femoral scute length (FSL); 23. left anal scute length (ANSL); 24. left anal scute width (ASW). perform all measurements in each turtle. The χ² analysis was carried out with the program BioEstat 5.0 (Ayres et al. 2007) and the other analyses with Statistica 6.0 (Statsoft 2004). All analyses used a significance level of α = 0.05. 6 A. Bager, T.R.O. Freitas and L. Krause

RESULTS

In total, 210 individuals were collected, 106 males and 104 females (1.02:1). The sex ratio was not significantly different from 1:1 (χ² = 0.005, P = 0.945). The carapace of T. dorbignyi is oval, and in both sexes the maximum cara- pace width occurred at the seventh or, predominantly, the eighth marginal scute. Males and females showed a mean ratio of 0.76 between the width and length of the carapace. In adult females and non-melanistic males, the color of the carapace ranged from dark green to brown. Black stripes with orange streaks of variable shape and size appear at the carapace margin, above the vertebral line. A black-

Fig. 3. — Color variation in Trachemys dorbignyi adults. A. — Carapace melanization of a mature male; B.— Melanization of soft tissue of a mature male; C .— Carapace of a mature female (with supernumerary epidermal shields); D. — Soft tissue coloration of a mature female. bordered orange spot is normally aligned with the shield on each costal scute. On the first costal scute, this spot can sometimes resemble a three-pointed star. On the fourth costal scute, the markings form an ocellus. The softer parts of the ani- mal have orange spots, which may be yellow on the head. Melanization in males begins on the carapace and plastron, and subsequently reaches the soft parts of the animal, especially the head and limbs. During this process, the color pattern found in most females and immatures changes to a general ocher-black spotted pattern, which appears as a nearly black carapace in some males. The large black pattern on the plastron begins to dissolve in the center part of the scutes, eventu- ally remaining only in their seams. This change appears to be ontogenetic, and very old males usually have a uniformly light plastron (Fig. 3). Trachemys dorbignyi morphology 7

Table 1. Descriptive statistics for the 27 variables measured on individuals of Trachemys dorbignyi from the Verde Lagoon complex. Linear measurements in millimeters; body weight in grams.

Male Female n x Min. Max. 1 SD n x Min. Max. 1 SD Carapace length 105 181.6 138.0 231.0 17.08 104 212.1 180.0 250.0 14.82

Maximum carapace width 87 137.4 111.0 167.0 11.46 67 161.5 139.0 185.0 10.47 Central carapace width 104 132.9 105.0 157.0 11.28 97 157.3 135.0 184.0 10.98 Length of third central 82 33.7 24.6 44.0 3.95 60 42.0 33.0 53.4 3.95 scute Width of third central 47 41.8 33.0 51.9 4.20 34 48.2 42.4 52.9 3.44 scute Circular carapace length 104 202.3 154.0 262.0 20.65 101 237.9 199.0 285.0 17.74

Circular carapace width 105 179.4 139.0 223.0 16.79 104 219.3 178.0 268.0 17.26

Maximum plastron length 105 165.1 127.0 206.0 14.73 104 198.3 169.0 236.0 13.72

Mid-ventral suture length 103 160.2 120.3 199.0 14.81 102 194.8 163.0 234.0 14.36

Maximum plastron width 106 106.5 86.7 130.4 8.07 104 126.1 104.7 144.2 8.42 Anterior lobe width 104 88.6 68.2 107.7 7.67 103 105.3 89.4 123.4 7.77

Posterior lobe width 106 90.3 70.5 116.5 8.36 104 106.5 92.0 123.9 7.75

Maximum bridge length 106 77.4 58.4 100.8 8.00 103 92.3 69.0 117.0 9.06

Central bridge length 85 55.4 43.7 72.7 5.61 61 69.0 57.2 82.8 5.32

Left pectoral scute length 85 30.6 23.0 49.2 4.23 59 38.3 28.5 54.9 4.77

Left pectoral scute width 49 41.1 32.0 51.6 4.31 35 45.0 42.1 58.5 4.24 Left abdominal scute 49 35.0 22.6 44.2 4.64 35 44.2 33.1 53.1 4.74 length Left abdominal scute 49 41.7 32.0 53.7 4.62 35 50.2 41.1 63.9 4.84 width Left anal scute length 48 33.6 27.3 42.6 3.76 35 42.2 36.0 50.4 3.60 Left anal scute width 48 37.6 30.1 47.5 4.15 35 45.0 38.2 52.5 3.89 Left gular scute length 47 27.5 19.2 35.9 3.29 35 34.5 28.3 41.4 3.47 Width of left and right 48 43.6 35.6 54.0 4.50 35 54.1 45.5 69.3 4.94 gular scutes Carap. and plast. terminal 56 24.2 17.6 34.4 2.85 43 22.4 17.8 27.3 2.42 dist. Cephalic width 57 28.4 21.7 34.4 2.87 24 34.6 28.3 41.9 3.55

Mouth width 43 22.6 16.9 29.1 2.70 19 26.5 22.7 31.9 2.80 Maximum carapace 106 79.5 59.0 106.0 8.48 103 99.3 79.0 128.0 9.02 height Weight 100 840.3 350.0 1610.0 221.37 94 1459.7 800.0 2700.0 349.40 8 A. Bager, T.R.O. Freitas and L. Krause

The maximum carapace length was 231 mm for males and 250 mm for fe- males. Females had larger mean values than males in 28 of the 29 measurements; the carapace and plastron terminal distance (CPD) was the only measurement

Fig. 4. — Frequency distribution of carapace length (mm) for males (open bars) and females (flled bars) of Trachemys dorbignyi from the Verde Lagoon Complex.

Table 2. Linear regression, covariance, and parallelism for males and females of Trachemys dorbignyi. CL is the independent variable.

Regression parameters Covariance Parallelism

n a b r2 F P F P F P

Female 119 – 14.97 1.10 0.90 1071.6 < 0.01 CiCW — — 12.10 < 0.01 Male 105 9.52 0.94 0.90 986.3 < 0.01

Female 118 – 18.62 0.55 0.88 887.9 < 0.01 MHS — — 10.94 < 0.01 Male 105 – 5.17 0.47 0.87 713.7 < 0.01

Female 27 – 2.25 0.17 0.93 318.4 < 0.01 CW — — 7.94 < 0.01 Male 56 2.40 0.14 0.91 564.6 < 0.01

Female 45 3.01 0.09 0.51 4.1 < 0.01 CPD 135.60 < 0.01 0.75 0.39 Male 55 5.12 0.11 0.66 100.6 < 0.01 Trachemys dorbignyi morphology 9

Table 3. Canonical coefcients for the ratios between the maximum carapace length and the variables used in the discriminant analysis.

CAN I

CPD/CL – 0.892 ALW/CL – 0.512 MCW/CL 0.117 MPW/CL 0.119 MHS/CL 0.382 CW/CL 0.522

for which females showed significantly lower values (F1,97 = 11.3, P < 0.001). The variable that differed most between the genders was total body weight (F 1,192 = 220.24, P < 0.01). Excluding body weight, the four variables that varied most between the sexes referred to the plastral scutes: left abdominal scute length, left gular scute length, left pectoral scute length and left anal scute length. The de- scriptive statistics for all measurements are presented in Table 1. The SSD was 0.168. The frequency distribution of carapace length (CL) (Fig. 4) was normal for both males (Shapiro-Wilk W = 0.989, P = 0.516) and females (Shapiro-Wilk W = 0.988, P = 0.447). The mode of carapace length was 220 mm for females and 190 mm for males. All the regression equations had high coefficients of determination (Table 2). The highest was found between CL and CW for both genders, and the lowest for CL and CPD (Table 2). Parallelism analyses showed no parallelism between females and males for the variables CiCW, CW and MHS. CPD was parallel between the sexes, but the analysis of covariance was significant, confirming the independence of the equations for males and females (Fig. 5)Please eliminate all references to fig. 5 as you said you eliminated it. All female regression lines (ex- cept CPD) differed from those of the males between 150 and 160 mm carapace length. The discriminant function (Table 3) defined a classification matrix with a 100% success rate for both sexes, with a degree of explanation of 89% (Wilks’ lambda = 0.205; χ2 = 96.567; df = 6; P < 0.001).

Discussion The importance of the sex ratio in vertebrates has been widely reported (Gibbons 1970, 1990; Barbour & Litvaitis 1993; Girondot & Pieau 1993; Marcovaldi et al. 1997; Kruuk et al. 1999). Sex ratios in freshwater turtles are highly variable, although many of the reports of unbalanced ratios reflect inad- 10 A. Bager, T.R.O. Freitas and L. Krause

equate sampling (Gibbons 1970, 1990). For T. dorbignyi, we found a sex ratio of 1.02 males per female and no evidence of asymmetry. Others authors have reported smaller individuals of T. dorbignyi than those encountered in our study ♀ x = 212.1 mm; ♂ x = 181.6 mm ). Freiberg (1969) reported a female with 234 mm CL and a male with 225 mm CL, and Vanzolini (1997) described a female with a carapace length of 234 mm. However, Bager et al. (2007a) reported females between 214 and 278 mm carapace length ( x = 235 mm; n = 50), and Bujes & Verrastro (2007) described a female with a carapace 252.1 mm long. The wide variation in weight between the sexes (♀ x =1459.7 mm; ♂ x = 840.3 mm ) may be related to the presence of eggs or retention of liquid by females, principally because the sampling was concentrated during the breeding season. The estimated SSD is among the lowest values reported by Stephens & Wiens (2009) for different genera of the family Emydidae, but it is very close to that for Trachemys scripta elegans (Wied-Neuwied 1839) (18.3%). According to Stephens & Wiens (2009), this result is congruent with the behavior of the males, which do not engage in combat or forcible insemination, allowing the females to grow larger and increasing the reproductive potential of the species. The morphological characteristics of T. dorbignyi agree with the general pattern of the genus. Gibbons & Lovich (1990) showed that females are larger than males in most genera of the family Emydidae, except for Clemmys. Other genera such as Emydoidea and Terrapene are also mentioned, but we feel that too few specimens have been sampled to permit generalizations with respect to these genera. Stephens & Wiens (2009) showed that males are larger than females in emydine emydids (i.e. Clemmys, , Emydoidea, , Terrapene), but the presence or absence of male combat and forced insemination explained little of the overall variance of SSD in emydids. All the males in our sample showed ontogenetic melanization, and we did not find melanistic females such as those described by McCoy (1968) and Moll & Legler (1971). Samples from five other geographical regions have given the same result (A. Bager pers. comm.). Lovich et al. (1990) noted that melaniza- tion of males occurs in many species of Trachemys, but within a specific popula- tion some males may not show melanization. Lovich et al. (1990) suggested that ontogenetic melanism is the most common pattern observed in turtles. According to Freiberg (1969), melanization starts in males at 150 mm carapace length; from our sample, we could not determine the start of melanization. Regression analyses identified carapace and plastron terminal distance (CPD) as the most important sexually dimorphic character. The only measure- ment where it was not possible to identify the intersection between the regression lines for females and males was CPD, suggesting that the intersection occurs at a CL of less than 130 mm. Parallelism analysis of CPD indicated no significant differences in the slope coefficients between males and females, indicating that the growth rate of T. dorbignyi males begins to increase with sexual maturation and later slows to the same rate as in females. Despite its significance, the correlation coefficient for CL and CPD was lower than in the other variables analyzed. This is explained by the correlations among the carapace and plastron terminal distance, variability in scute position and size of carapace and plastron. For the remaining Trachemys dorbignyi morphology 11

variables analyzed by regression, the line for the females crossed that for the males between 150 and 160 mm carapace length. Considering the lack of informa- tion about the size at maturation of the female, we propose that this interval be adopted as the CL of sexual maturity until studies of the internal anatomy of the species can better elucidate this question. The discriminant analysis also identified the importance of CPD in the differentiation of males. For the females, the variables with greatest influence were cephalic width and height of the carapace. The height (MHS) was predicted to be important, considering its importance in the increase of body volume, which increases the reproductive potential (Horne et al. 2003). Future studies will be necessary to assess the importance of cephalic width. Our results show that T. dorbignyi is a small Emydidae species, with females larger than males. Sexual dimorphism occurs in both carapace and plastron mor- phology, as well as in color patterns of mature specimens. The most evident sexually dimorphic measurements are carapace and plastron terminal distance (CPD) and male melanization. CPD is particularly useful in small specimens (CL < 130 mm), when melanization is not present.

ACKNOWLEDGMENTS

The first author is grateful to the Brazilian agency CNPq for a PhD schol- arship, which allowed this study to be carried out, and to the many students who helped by gathering data in the field or by processing the data in the Laboratory of Management and Environmental Conservation (LAMCA). The authors thank Drs Flávio de B. Molina, Márcio B. Martins, Andreas Kindel, Gilson R.P. Moreira and Helena P. Romanowski for their suggestions and helpful criticism.

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