Annual Reproductive Cycle in the Scincid Lizard Chalcides viridanus from Tenerife, Canary Islands

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1 Current Herpetology 32(2): , August by The Herpetological Society of Japan doi /hsj Annual Reproductive Cycle in the Scincid Lizard Chalcides viridanus from Tenerife, Canary Islands PAULA SÁNCHEZ-HERNÁNDEZ 1, MIGUEL MOLINA-BORJA 1 *, AND MARTHA P. RAMÍREZ-PINILLA 2 1 Grupo de Investigación Etología y Ecología del Comportamiento, Depto. Biología Animal, Universidad de La Laguna, Tenerife, Islas Canarias, ESPAÑA 2 Laboratorio de Biología Reproductiva de Vertebrados, Grupo de Estudios en Biodiversidad, Escuela de Biología, Universidad Industrial de Santander, Bucaramanga COLOMBIA Abstract: Chalcides viridanus is a small skink endemic to Tenerife, the Canary Islands. This paper describes its annual reproductive cycle and sexual dimorphism by use of data from external measurements, dissection, and histological observation of gonads from monthly samples. Males were significantly larger than females in head forelimb length, distance between forelimbs and hind limbs, tail width, and body mass. Male testes were largest in March, when most individuals showed active spermiogenesis, although no spermiation was observed. In April, the testes were somewhat smaller but showed seminiferous tubules and epididymis ducts with abundant sperm. In this month, female gonads and ovarian follicles were significantly enlarged, and vitellogenesis was evident. Oviductal embryos were found in May and June, and parturition took place at the beginning of August. Both testis mass in males and diameter of the largest oocyte in females were significantly correlated to abdominal fat body mass. We conclude that in C. viridanus both sexes exhibit seasonal changes in gonadal activity with synchronous development of both male and female gonads in the spring months. Key words: Scincidae; Chalcides viridanus; Canary Islands; Reproductive cycle; Viviparity INTRODUCTION Knowledge of reproductive cycles and lifehistory traits in lizards is important both from a comparative point of view to understand their evolutionary processes (Dunham and * Corresponding author. Tel: ; Fax: ; address: mmolina@ull.edu.es Miles, 1985; Bauwens and Díaz-Uriarte, 1997; Mouton et al., 2012) and from a proximal causal approach to elucidation, for example, of responsible environmental factors (Rubenstein and Wikelski, 2003; Carretero, 2006). Viviparity has supposedly originated on more than 108 separate occasions within the Squamata (Blackburn, 1999), and has often evolved relatively recently (Heulin and Guillaume, 1989; Camarillo, 1990).

2 SÁNCHEZ-HERNÁNDEZ ET AL. REPRODUCTIVE CYCLE IN SKINK 171 In several lizard clades of temperate regions, evolution of viviparity has been accompanied by a shift from spring to autumn gametogenesis (Ramírez-Pinilla, 1991; Guillette and Méndez-de la Cruz, 1993; Mouton et al., 2012). Irrespective of the reproductive mode (oviparous or viviparous), most lizards from temperate and subtropical zones worldwide reproduce seasonally with ovulation occurring in spring, and appearance of hatchlings or neonates in summer and autumn months (James and Shine, 1985; Zug et al., 2001). However, several other viviparous lizards (phrynosomatids, liolaemids, cordylids) ovulate in autumn and are gravid during winter months with parturition occurring during the next spring (Fitch, 1970; Ramírez-Pinilla, 1991; Guillette and Méndez-de la Cruz, 1993; Ramírez-Pinilla et al., 2009; Mouton et al., 2012). On the other hand, viviparous species in aseasonal environments (i.e., tropical regions) may be able to continually reproduce throughout the year (Fitch, 1970; Hernández-Gallegos et al., 2002; Ramírez-Pinilla et al., 2002), or may show a markedly discontinuous, seasonal pattern (Vitt and Blackburn, 1983; Méndez de la Cruz et al., 1999). The scincid lizards of the genus Chalcides Laurenti, 1768 include 25 viviparous species, differing mainly in the degree of body elongation and limb reduction (Caputo et al., 1995). They are mainly distributed in the North Temperate Zone in Southern Europe and North Africa (Pasteur, 1981; Caputo et al., 1995; Mateo et al., 1995). The reproductive phenology has been studied for some species, revealing that mating occurs from March to May after hibernation, and neonates appear from May to August (C. chalcides: Rugiero, 1997; C. bedriagai: Galán, 2003; C. lanzai: Bogaerts, 2006). Similar patterns have also been reported for a few other species within the genus (Salvador, 1985; Schleich et al., 1996; Spawls et al., 2004), but their comprehensive reproductive cycles have not been described. In the Canary Islands, a subtropical volcanic archipelago, this genus has four endemic species: C. sexlineatus (Gran Canaria), C. simonyi (Fuerteventura and Lanzarote), C. coeruleopunctatus (La Gomera and El Hierro), and C. viridanus (Tenerife and La Palma) (Báez, 1998; Carranza et al., 2008). Chalcides viridanus, originally described by Gravenhorst (1851), is at the base of a western clade of the genus (Carranza et al., 2008) and their biological data were revised by Báez (1998), and is distributed throughout the two islands, including high altitudes such as the peak area of Teide volcano (3718 m asl: Klemmer, 1976). Chalcides viridanus is a small, diurnal secretive skink that lives under bushes and stones or inside stone walls. Individuals are not easily observed in exposed areas except at midday from March to May (the authors unpublished observations). The species is viviparous as are other congeners, and shows morphological variation between sexes, and within and between islands (Báez and Thorpe, 1990; Brown et al., 1993). Adult females may have two to four neonates per season, and parturition occurs in July and August. In the present study, we performed a morphometric comparison and histological examination of the gonads of male and female C. viridanus. This is the first description of complete year-round changes of the gonads in this species. MATERIAL AND METHODS Environment data and specimen collection We collected skinks in two field sites with similar habitats and weather characteristics close to La Laguna city (Geneto, 28 28'476'' N 16 18'976'' W and Los Baldíos, 28 27'52''N 16 19'29''W). Figure 1 shows the monthly variation of mean temperature and precipitation during 2009 at Los Baldíos meteorological station (La Laguna, Tenerife, 28 28'16''N 16 19'43''W), situated at 638 m asl, next to the catch zone; maximum air temperature occurred between July and September, and highest monthly precipitation occurred between November and March. Drought occurred between May and October. Photoperiod in

3 172 Current Herpetol. 32(2) 2013 than four days after capture. Euthanized skinks were deposited in the Herpetological Collection of the Department of Zoology (Universidad de La Laguna) with the accession numbers DZUL-1064 to DZUL FIG. 1. Annual variation of rains (left axis) and temperature (right axis) from the study area. Data correspond to our study year. the Canary Islands changes between 10 to 14 hours of light from the beginning of winter in December up to the beginning of summer in June. The habitats were characterized by small shrubs and herbs (Lavatera cretica, Oxalis pes-caprae, Spartium junceum, Rubus ulmifolius) together with stone walls and rock piles. Skinks were captured by hand while they were basking or by checking under stones. We sampled individuals between December 2008 and December 2009, one to two days per week of each month with the aim of collecting at least ten individuals per month. Despite high capture efforts in each month, we could only capture eight skinks during July and August. We included in our study only male and female skinks with a minimum body size of 60 mm because smaller individuals never had differentiated gonads. We released juvenile skinks and only used adult animals for our study. Captured specimens were transported inside cloth bags to the laboratory where they were kept in individual terraria. These, in turn, were placed inside small rooms where the light-dark cycle and temperature were changed gradually each month so as to simulate values in the natural environment. Temperatures inside the rooms ranged from 15 C in December to 24 C in August and humidity from 30% in August to 85% in December. Most specimens were euthanized on the first or second day after capture, but never more Analysis of sexual dimorphism For each individual, the following measurements were taken with digital calipers (precision 0.01 mm): snout-to-vent length (SVL), head depth and width (HD, HW), pileus length (PL), distance between forelimbs and hind limbs (DFH), distance between left and right forelimbs (DFL), distance between right and left hind limbs (DHL), forelimb length (FLL) hind limb length (HLL), and tail depth and width (TD, TW). Body mass (BM) was weighed with a digital balance (0.1 g precision). External morphometric variables provided normality and homoscedasticity requirements, and after confirming that they were linearly and significantly related to SVL, multivariate analyses of variance (MANOVA with sex as factor and SVL as covariate) were applied to these data to test degree of sexual dimorphism. Between sex and among month comparisons of SVL were performed with twoway ANOVA with sex and months as fixed factors. Alpha level was always set at 0.05 and Bonferroni correction for multiple comparisons was applied (Chandler, 1995). Gonad morphometrics and reproductive stages After taking all biometric traits, and in order to analyse histological aspects of gonadal changes among months, specimens were euthanized by intra peritoneal anesthesia (1 ml of sodium pentobarbital at 20 mg/kg). Afterwards, a ventral incision was made and several internal parameters were taken for each specimen: length of the largest ovarian follicle, and length, width and mass of the gonad and abdominal fat tissue (fat body volume-fbv, mm 3 - was calculated using the ellipsoid formula: (4/3)πa 2 b, where a and b are the shortest and largest diameter, respectively). To statistically analyse the data, we

4 SÁNCHEZ-HERNÁNDEZ ET AL. REPRODUCTIVE CYCLE IN SKINK 173 initially confirmed normality, homoscedasticity and linearity requirements. After proving that male testis and ovarian follicle sizes were significantly related to SVL, ANCOVA was applied within each sex to each parameter, using the month as factor and SVL as covariate. Female gonad mass was not used because the linearity requirement was not fulfilled. To explore the relationship of gonad parameters and fat body volume with environmental variables (precipitation and temperature), partial correlations were calculated separately for males and females taking into account the variation in SVL. Male and female whole gonads were then extracted and weighed, fixed in Bouin s solution for 12 hours, washed in running water, and stored in 70% ethanol. Subsequently, the specimens were dehydrated, embedded in paraplast, sectioned at 6 μm, and stained with hematoxylin-eosin. In males, the reproductive stage was determined according to the classification of Ballinger and Nietfeldt (1989) as follows: Stage 1: growing testes; stage 2: early spermatogenesis, primary spermatocytes, no lumen; stage 3: spermatogenesis, abundant spermatocytes, some tubules with lumen; stage 4: spermiogenesis, undifferentiated spermatids at luminal margin; stage 5: metamorphosing spermatids at luminal margin; stage 6: reproductive testis, mature sperm in seminiferous tubules and epididymes; stage 7: postreproductive testes, early regression, mature sperm at luminal margin and cellular debris in the lumen, epididymes with abundant sperm; stage 8: postreproductive testis, later regression. In females the reproductive stages were categorized as stage 1: previtellogenic, oocytes <2 mm in diameter; stage 2: vitellogenic, oocytes >2.0 mm in diameter, yellowish; stage 3: pregnancy, oviductal eggs or embryos; stage 4: postparturition, wide flaccid oviducts. Reproductive stage data for each animal permitted establishing the percentage of males and females in each reproductive stage for each month throughout the year. To detect intra and inter sex variation by month (synchrony) and over time (seasonality), we employed a G-test of independence. RESULTS Number and SVL of specimens captured We captured 116 specimens, 53 males and 63 females during the whole year and the number of collected individuals of each sex did not change significantly from month to month (G 12 =4.85, P=0.96). SVL of males and females did not differ significantly (F 1,92 =2.31, P=0.13) nor did they change significantly in any month (F 11,92 =1.82, P=0.062, Fig. 2); the interaction of sex and month was not significant (F 11,92 =0.51, P=0.89). Figure 2 also shows the gonad stages at which adult male and female skinks were collected. Sexual size dimorphism Table 1 shows the statistical data for biomet- FIG. 2. Monthly distribution of body sizes (SVL) from 47 males (a) and 63 females (b) of Chalcides viridanus during the sampling year, showing gonad stages. A larger symbol for vitellogenic females corresponds to more than one skink with similar SVL.

5 174 Current Herpetol. 32(2) 2013 TABLE 1. Sample sizes (N), and mean, standard error (SE), minimum (Min) and maximum values (Max) of biometric traits (in mm and g) in male and female Chalcides viridanus examined, and the results of statistical comparison of each trait between sexes. See text for further details. Trait abbreviations are as follows: snout-to-vent length (SVL), head depth and width (HD, HW), pileus length (PL), distance between forelimb and hind limb (DFH), distance between left and right forelimbs (DFL), distance between right and left hind limbs (DHL), forelimb length (FLL), hind limb length (HLL), tail depth and width (TD, TW), body mass (BM), and fat body volume (FBV, in mm 3 ). Statistically significant P values are highlighted in bold. Sex Males (N=53) Females (N=63) Intersex variation Biometric trait Mean SE Min Max Mean SE Min Max F P SVL BM HD HW PL DFH DFL DHL FLL HLL TD TW FBV ric traits measured in both sexes. MANOVA analysis showed that, taking into account all morphological variables, males and females differed significantly (F 11,96 =6.79, P<0.001) in relation to SVL (F 11,96 =15.01, P<0.001). This difference was due to males having significantly larger BM, HD, HW, PL, DHL, HLL, TW and FBV than females (univariate analyses within MANOVA, Table 1). Reproductive data and monthly variation Male and female gonads were reproductively active in early spring (March and April); they showed signs of regression during the summer through early autumn (July and August to October) and recrudescence beginning in winter (December to January). Fat body volume followed a similar pattern in both sexes (Figs. 3b and 4b). There was a significant association between the reproductive stage of each sex and the month (G 33 =65.59, P<0.001 females, G 66 =114.02, P<0.001 in males), females in stage 2 (vitellogenic) only appeared during April and in stage 3 (pregnancy) mainly during June; parturitions must occur in August, because in that month we found females with hypertrophic and very convoluted oviducts, signs of having given birth recently (stage 4). In males, reproductive stage 5 was found in March and April and reproductive stages 6 and 7 from May to June. In our sample the smallest pregnant female measured 70 mm and the smallest potentially reproductive male had an SVL of 75 mm (Fig. 2). Individuals males or females smaller than 60 mm SVL did not have differentiated gonads. Three of the females captured in May were bigger than 70 mm, but they did not show evidence of being vitellogenic or pregnant. All females captured in June and July were pregnant (Fig. 2). There were significant regressions between female or male SVL (or body mass) and gonad

6 SÁNCHEZ-HERNÁNDEZ ET AL. REPRODUCTIVE CYCLE IN SKINK 175 FIG. 3. Means (±2SD) of follicular diameter (a) and female fat body volume (b), in Chalcides viridanus during the sampling months. Asterisks indicate significant differences between the marked and the other months. FIG. 4. Means (±2SD) of testis mass (a) and male fat body volume (b), in Chalcides viridanus during the sampling months. Asterisks indicate significant differences between the marked and the other months (see text). parameters and fat body volume (Table 2). Thus, there was a positive and significant relationship of body mass and testis mass, and of female SVL and largest follicle diameter. Therefore, to analyse the monthly variation in these parameters, ANCOVA was applied to adjust for the effect of SVL (or BM). ANCOVA showed that there were significant differences among months in the largest follicle diameter (F 11,51 =7.83 P<0.001) and in female fat body volume (F 11,48 =8.73, P<0.001), their values being significantly larger in April than in all the other months (Figs. 3a and b). ANCOVA analysis also showed that there was a significant difference among months in testis mass (F 11,38 =3.19, P=0.005), values being larger in March and April than in the other months (Fig. 4a); male fat body volume also had higher mean values in March and April (ANCOVA, F 10,35 =2.69, P=0.014) but post-hoc comparisons among months did not show any significant difference between them and the other months (Fig. 4b). DISCUSSION Sexual dimorphism Taking into account that we intentionally sampled a minimum number of skinks per month, it is understandable that there was no significant difference in the proportion of males and females captured throughout the year; however, adult males and females could be captured each month and SVL did not significantly change between months for any sex. Mean SVL of females was slightly larger

7 176 Current Herpetol. 32(2) 2013 TABLE 2. Regressions of gonadal traits to snout-vent length (for diameter of the largest follicle in female) or body mass (for the other traits) in male and female Chalcides viridanus. Degrees of freedom are given in parentheses below F values. Sex Male Female Variable R 2 F P R 2 F P Gonad volume (mm 3 ) Gonad mass (g) Diameter of the largest follicle (mm) Fat volume (mm 3 ) Body mass (g) (1, 45) (1, 49) (1, 46) (1, 50) (1,61) (1, 60) (1, 61) (1, 61) than mean SVL of males, but the difference did not reach statistical significance. In Chalcides, the larger species of the C. chalcides group (SVL>100 mm in adults, litter size up to 19; grass swimming clade of Carranza et al. 2008), females are considerably larger than males, whereas the small species (e.g. C. polylepis, C. ocellatus, and C. mionecton) are not dimorphic in body length (Caputo et al., 2000) as in C. viridanus. Two hypotheses explain sexual dimorphism in body size in skinks, the intrasexual selection hypothesis (in which females select for large males), and fecundity advantage hypothesis (natural selection leading to larger body size in females) (Thompson and Withers, 2005). Similarly, female to male comparison of distance between forelimb and hind limb lengths did not reach significance in our sample of C. viridanus; within Chalcides, large snake-like species (C. chalcides and C. striatus) are dimorphic in abdomen length (larger in females) whereas short snake-like and stout skinks are not dimorphic (C. mionecton, C. ocellatus, and C. polylepis: Caputo et al., 2000). Longer bodies in female lizards probably reflect selection pressure leading to more space available for embryos inside the female body (Fitch, 1981; Vitt and Blackburn, 1991). Several selective pressures for each sex, and even non-adaptive processes, have been suggested as long term causes of the differing pattern of sexual size dimorphism in different species (Olsson et al., 2002; Cox et al., 2003, 2007); however, different growth rates for males and females should also be considered as short-term causes (Badayev, 2002). Sexual dimorphism was more clearly manifested in several head and body traits, males having larger relative values than females as in other skink species (e.g., Mabuya heathi and M. frenata: Vitt and Blackburn, 1983; Vrcibradic and Rocha, 1998; Niveoscincus coventryi: Olsson et al., 2002; Clemann et al., 2004). These differences can be interpreted in terms of selection pressures acting on male traits suitable for intrasexual interactions; head sizes are commonly larger in winners than in losers of male encounters in different lizard species (Hews, 1990; Molina-Borja et al., 1998; Gvozdik and Van Damme, 2003; Dubey et al., 2011). Moreover, a larger head size in males could have been selected in an intersexual context as they usually continue biting the female s neck for a long time during mating (Sánchez-Hernández et al., 2012). Nevertheless, female skinks also compete with other females and may show agonistic interactions as intense as among males (Sánchez- Hernández et al., 2012). As there are no other behavioural studies for species of Chalcides, it

8 SÁNCHEZ-HERNÁNDEZ ET AL. REPRODUCTIVE CYCLE IN SKINK 177 is still difficult to interpret these dimorphic traits in terms of intersexual and intrasexual conflicts. Size at sexual maturity The individuals collected had differentiated gonads from 60 mm SVL on, and the smallest pregnant female and the smallest potentially reproductive male had an SVL of 70 and 75 mm, respectively. Therefore, this means either that individuals smaller than mm SVL were immature or that they could not reproduce that year. As we do not currently have data on growth rates, we cannot specify ages at which sexual maturity occurs. In other Chalcides of similar body sizes, females may ovulate at a mean SVL of 82.7 mm (Chalcides bedriagai: Galán, 2003), and Chalcides lanzai in captivity have their first clutch at four years of age. In southeast populations of C. bedriagai, sexual maturity is attained at mm SVL (López-Jurado et al., 1978) while in northwest populations of this species sexual maturity is reached at about mm SVL (Galán, 2003). Therefore, if we consider a SVL of 70 mm as the potential size of sexual maturity for females, C. viridanus would be placed between the two Iberian populations just mentioned. We cannot currently ascertain how long they will take after birth to arrive at the size of sexual maturity. As three adult females were not vitellogenic nor pregnant in the first appropriate month (May), some individuals may delay ovulation or do not reproduce every year. Newborns were only obtained from two females (before being euthanized), but our unpublished data showed that they (1 to 3 per female) had mean SVL of mm (±1 SE, ranging mm). This means that to attain the size of sexual maturity skinks should, at least, double their size at birth. We cannot currently ascertain if there is a relationship between female SVL and number of offspring because of the small sample size. Other Chalcides skinks with similar SVL have clutches of 1 6 (C. bedriagai: Pollo, 2003) or 2 3 offspring (C. sexlineatus: Harbig, 2000) and have newborn sizes similar to those of C. viridanus. Furthermore, C. sexlineatus may begin to reproduce at an age of 24 months (Harbig, 2000). Taking into account the close phylogenetic vicinity to the latter species, we can expect a similar time for first reproduction in C. viridanus. Annual reproductive cycle We have shown that the highest gonadal development in male and female C. viridanus occurred during March and April (moderate temperature increase in springtime) (Figs. 1 and 4). The lowest gonadal size appeared in the summer months for both sexes. Therefore, reproductive activity is markedly seasonal in this species, both sexes are synchronic in their gonadal development, and mating and fertilization should occur in April; in fact, behavioural observations in the laboratory showed mating during that month (Sánchez- Hernández et al., 2012). However, males in stages 7 and 8 during June still might be able to fertilize females, as they have abundant sperm in their ducts. Both sexes of C. viridanus emerge from winter hibernation during March when temperatures begin to rise and they can be observed basking in sunny patches on the ground or on stones, sometimes in pairs. The onset of testicular activity and follicular growth is related with increasing ambient temperatures during March. As shown in Figs. 3 and 4, ovulation and mating must occur in April, pregnancy during the hottest summer months, and parturition in August at the end of summer. Consequently, reproductive activity in both sexes (final gametogenesis, mating, and ovulation) is synchronized to the time when environmental conditions (warm temperatures and available food) provide maximum energy for reproductive effort. Males and females were especially difficult to detect and capture during July and August, the hottest summer months in Tenerife. As burrows were commonly detected under stones where skinks were usually found, we suspect that animals can retire into the deepest part of

9 178 Current Herpetol. 32(2) 2013 their burrow to avoid high surface temperatures at those times. The high temperatures and absence of rain during those months, probably restrict skink activity to under the ground. The months when skinks were hidden coincided with the time of female pregnancy, when they have the lowest fat body values. From September on, fat body masses and gonad sizes begin to increase, reaching the highest values in March and April. Within the genus Chalcides a similar annual reproductive cycle has been described for C. chalcides in central Italy (Rugiero, 1997) and C. bedriagai from mainland Spain (Galán, 2003); however, in these two species, emergence and mating dates are somewhat delayed in comparison with those of C. viridanus. This seasonal pattern with ovulation occurring in the early spring is typical of many other Iberian lizard species (Carretero, 2006; Galán, 2009) and of some scincids from temperate (northern and southern) climates (e.g. Sphenomorphus indicus from China: Huang, 1997; Oligosoma maccanni from South New Zealand: Holmes and Cree, 2006), and therefore follow the generalized pattern known for temperate lizards. Other temperate skinks are fall breeders (ovulation and mating occurring in fall and pregnancy during winter ending with births in spring) in the cold climates of high mountains in Mexico (e.g. Plestiodon copei: Guillette, 1983; P. lynxe: Ramírez- Bautista et al., 1998). The differences in reproductive time among scincid species have been explained in relation to local ecological conditions. In the case of C. viridanus there is no indication that males may produce sperm in late summer or early autumn or that females could store sperm during the autumn and winter. The reproductive cycle reported for C. viridanus should allow females to access environmental food resources for vitellogenesis at the end of the rainy season and warm temperatures during the end of spring and mid-summer that would be beneficial for their developing embryos. In turn, offspring born in August should be able to obtain adequate temperatures for development and enough food (insects and arachnids) before the beginning of autumn. At present there are no reproductive data on any Chalcides species from other Canarian islands. The reproductive cycle of C. viridanus occurs earlier than that of other Canarian lizards such as Gallotia (Family Lacertidae) and Tarentola (Family Gekkonidae) in which mating occurs during May-June and offspring appear at the end of August or beginning of September (Molina-Borja and Rodríguez- Domínguez, 2004). This probably reflects a need for higher environmental temperatures for the developing embryos inside eggs of these species laid underground. ACKNOWLEDGEMENTS We thank Axia Rodríguez for her help with histological analysis, and two anonymous referees for their useful comments. M a del Mar González, María de Fuentes, and Martha L. Bohórquez helped us to capture the skinks during field trips. Also, we thank Airan Brito for allowing us to use the data of his meteorological station. We are also grateful to Cabildo Insular de Tenerife for permission to capture the skinks. LITERATURE CITED BADAYEV, A. V Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecology and Evolution 17: BÁEZ, M Chalcides viridanus (Gravenhorst, 1851) Kanarenskink. p In: W. Bischoff (ed.), Handbuch der Reptilien und Amphibien Europas. Band 6. Die Reptilien der Kanarischen Inseln, der Selvagens-Inseln und des Madeira- Archipels. Aula-Verlag, Wiebelsheim. BÁEZ, M. AND TORPE, R. S Análisis preliminar de las divergencias entre las poblaciones de Chalcides viridanus en las Islas Canarias. Vieraea 19: BALLINGER, R. AND NIETFELDT, J Ontogenetic stages of reproductive maturity in the viviparous lizard Sceloporus jarrovi (Iguanidae).

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