Embryonic skull development in the neotropical viviparous skink Mabuya (Squamata: Scincidae)

Desarrollo embrionario del cráneo en la lagartija vivípara Mabuya (Squamata: Scincidae)

Adriana Jerez¹, Paola María Sánchez-Martínez² and Ricardo Arturo Guerra-Fuentes^2,3

¹ Departamento de Biología. Universidad Nacional de Colombia, Sede Bogotá, Bogotá, Colombia. Carrera 45 No 26-85, Bogotá, Cundinamarca, Colombia. <arjerezm@unal.edu.co>

² Museu de Zoologia da Universidade de São Paulo, São Paulo, Brasil. Av. Nazaré 481, Ipiranga, 04263-000, São Paulo (SP), Brasil. <paola.sanmart@gmail.com>;

Recibido: 01/03/2015.
Aceptado: 09/10/2015.

Abstract

The systematics of the Americans skinks of the genus Mabuya have been extensively studied, with new arrangements based on molecular analysis. However, the skeletal morphology, their development and ontogenetic variation have been poorly studied in this genus. We described the embryonic skull development of three species of Mabuya and compare it with the African species Trachylepis capensis. We observed that American genus Mabuya presents differences in the skull development, including the pila antotica, orbitosphenoid, vomer, and the basicranial fenestra closure. These morphological differences in Mabuya species may be interpreted as putative synapomorphic characters.

Key words: Skull development, chondrocranium, Mabuya, skin, Scincidae, Squamata.

Resumen

Palabras clave: Desarrollo craneal, condrocráneo, Mabuya, Scincidae, Squamata.

INTRODUCTION

The genus Mabuya constitutes a monophyletic unit with a recent diversification, and exhibits a unique combination of reproductive features in Squamata (Blackburn & Vitt 1992; Mausfeld et al. 2002; Carranza & Arnold 2003; Whiting et al. 2006; Miralles & Carranza 2010).

Until recently, the pantropical genus Mabuya included more than a hundred species distributed in America, Africa and Asia (Greer & Nussbaum 2000; Greer et al. 2000). However, on the basis of a molecular phylogenetic analysis this genus was divided into four clades (Mausfeld et al. 2002). In this way, the genus Mabuya actually includes about 53 species, distributed from Mexico to Argentina (Ávila-Pires 1995; Mausfeld et al. 2002; Miralles et al. 2005). The other three clades are Trachylepis (Fitzinger 1843) in Africa, Chioninia (Gray 1845) in Cape Verde, and Eutropis (Fitzinger 1843) in Asia (Mausfeld et al. 2002; Bauer 2003). We follow this taxonomic proposal and all species in this work are regarded to the genus Mabuya.

All Mabuya species present viviparous reproduction, smooth scales, lower eyelid with a semi-transparent disc, pterygoid teeth absent, and 25-31 presacral vertebrae (Mausfeld et al. 2002). This genus inhabits mainly lowland forests and evolved with a group of specializations related to viviparity, which are unique among reptiles and convergent only with placental mammals: a long period of gestation (9 to 12 months) and microlecithal eggs (0.92.2 mm) with a highly placentotrophic nutritional pattern (Blackburn & Vitt 1992; Blackburn 1993; Jerez & Ramírez 2001, 2003).

Despite the recent phylogenetic and taxonomic interest in the evolution of the genus Mabuya (Mausfeld et al. 2002; Carranza & Arnold 2003; Jesus et al. 2005; Miralles et al. 2005; Whiting et al. 2006; Miralles et al. 2009; Miralles & Carranza 2010; Hedges & Conn 2012), osteological and ontogenetic descriptions in comparative studies are scarce. Regarding African species, Skinner (1973) described the ontogenetic and adult morphology in Trachylepis capensis skull, whereas Rao & Ramaswami (1952) described the fully formed chondrocranium and the adult osteocranium of the Asian Eutropis carinata. Concerning American species, Jerez (2012) described the adult skull of Colombian Andean population of Mabuya sp., and Caicedo (2012) analyzed the adult skull in different species and populations in Colombia.

Hence, the main purpose of this work is to describe the development of the embryonic skull in Mabuya sp., M. cassaira and M. macrorhyncha. In addition, the chondrocranium of Mabuya is compared with the species of the old world Trachylepis capensis and Eutropis carinata, therefore, these morphological studies could provide additional anatomical characters to support the taxonomic status of this American clade as monophyletic. This is particularly important, given that Hedges & Conn (2012) proposed sixteen genera for America. On the other hand, though many molecular phylogenetic analyses support the monophyly of American clade (Mausfeld et al. 2002; Carranza & Arnold 2003; Jesus et al. 2005; Whiting et al. 2006; Miralles & Carranza 2010), some herpetologists consider that the division of pantropical genus Mabuya in four genera has been premature (Jesus et al. 2005; Whiting et al. 2006).

We described the skull development in an Andean population of Mabuya sp. and compared it with the transandean species M. caissara and M. macrorhycha. Mabuya is widely distributed in Colombia (Sánchez et al. 1995) and their populations represent a complex of species (Ávila-Pires 1995; Miralles et al. 2005; Miralles 2006). According to Miralles (2005) neither M. mabouya nor M. nigropunctata, nominations for populations in Colombia, are present in the Andean Colombian regions. For this reason, in this work the studied population is referred as Mabuya sp. The embryos of Mabuya sp. were taken from females of a population collected at the Inspección de Policía Guadualito, in the Municipality of Yacopí, Cundinamarca, Colombia. They are housed in the Colección Herpetologica, Escuela de Biología, Universidad Industrial de Santander. A series of twelve embryos of Mabuya sp. was selected (UIS-R-289, 310, 311, 314, 319, 320, 321, 351, 355, 366, 404, and 415). Stages of development follow Defaure & Hubert (1961), this table starts at stage 1 with the cleavage and ends at stage 40 with the hatching. The series studied include embryos from limb bud stage (stage 32) to preparturition stage (stage 40). The chondrocranium of Mabuya sp. was compared with that of M. cassaira and M. macrorhyncha, two Brazilian species. We described a series of eight embryos of M. cassaira from Bertioga, SP Brazil (MZUSP-40720, MZUSP-40771, MZUSP-40777, MZUSP-40779, MZUSP-45703), and five of M. macrorhyncha from Guarujá, SP, Brazil (MZUSP-40695, MZUSP-40792, MZUSP 40800) and Ilha dos Búzios, SP, Brazil (MZUSP-11148, MZUSP 11176). In this comparison we described embryos of stages 32, 39 and 40 (D&H) for all species. The stage 34 (D&H) is described just for Mabuya sp. The skeletal embryonic development was described using cleared and double-stained specimens, prepared following Wassersug (1976). The description of the chondrocranium follows those of Bellairs & Kamal (1981). In Mabuya sp. the first stage is described, while in the subsequent stages only the registered variations are explained. In contrast, with M. caissara and M. macro-rhyncha only the differences relating to Mabuya sp. are reported.

RESULTS

Mabuya sp. Stage 32-33 (Fig. 1): In this stage, elements of three regions of the chondrocranium are observed: the anterior ethmoidal region, the intermediate orbitotemporal region, and the posterior occipital region (Table 1). In the ethmoidal region, the cartilages of the nasal capsule start being condensed. The interorbital septum is low and contacts the trabecula communis. In the posterior region, the skull consists of the basal plate and the occipital arch. The elements of splachnocranium, the quadrate, the ascending process and the Meckel's cartilage are observed (Table 1). The Meckel's cartilages are fused at the symphisis and caudally the retroarticular process is present. Regarding to the dermatocranium, the pterygoid starts to ossify (Table 2).

Differences with Mabuya macrorhyncha: in this stage the cartilages of ethmoidal and orbitotemporal regions are not clearly observed in the chondrocranium. However, the trabecula communis, the basal plate, the otic capsule and the occipital arch are totally visible (Table 1). In the dermatocranium, besides the pterygoid, the dentary starts to ossify in the anterior region of Meckel's cartilage.

Differences to Mabuya caissara: There are no differences with this species (Table 1).

Mabuya sp. Stage 34 (Fig. 2): In this stage the chondrocranium presents further development in orbitotemporal and occipital regions (Table 1). In the orbitotemporal region, the sphenethmoid commissures, a pair of arched slender cartilaginous rods, extends from the nasal capsule to the planum supraseptale. Then it forms a large fenestra olfactoria.

The interorbital septum has increased in height and appears continuously with the trabecula communis and extends into the ethmoidal region of the chondrocranium shaping of the nasal septum. Furthermore, the interorbital septum begins to develop other cartilages from the orbitotemporal scaffolding. The taenia medialis, the pila metoptica and the pila antotica are continuous cartilaginous rods. Further behind, the pila accessoria extends between the taenia marginalis and the pila antotica. This last one cartilage doesn't contact the basal plate. The taenia marginalis extends between the pila accessoria and the dorsal surface of the otic capsule. In the occipital region, the otic capsule is very conspicuous and presents the crista parotica. In this posterior region, the skull roof is formed by growth of the occipital arch and the otic capsule, then the tectum synoticum is observed. In this stage, the basicranial fenestra is small and separated from the pituitary fossa by the crista sellaris.

In relation to the dermatocranium, other bony elements start to ossify; these include the prefrontal, the frontal, the parietal, the supratemporal, the palatine, the dentary and the surangular (Table 2).

Mabuya sp. Stage 39 (Figs. 3, 4): In this stage the chondrocranium shows the configuration observed in the neonate. The principal changes are observed in the ethmoidal region, since the nasal cartilages are completely developed. The nasal capsule exhibits the pariotectal and para-nasal cartilages (Table 1).

In the nasal region, the pariotectal cartilage presents de nasal cupola with the foramen apical and the narina. Posteriorly, the fenestra superior is very conspicuous dorsally. The paranasal cartilage exhibits the bifid maxillary process, and the planum antorbitale, which is perpendicular to nasal septum, but they are not in contact.

In the orbitotemporal region, the planum supraseptale is completely formed; rostraly is formed by a cartilaginous rod and caudally by a width cartilaginous shield with a short process in the anterior region. The interorbital septum presents the small anterior and ventral fenestra and the big posterior fenestra below the planum supraseptale. In this stage, the taenia marginalis extends from the planum supraseptale to the otic capsule. So the interobital scaffolding is completely formed with all present cartilages. The epiotic fenestra is closed by the taenia marginalis, the taenia medialis, the pila metoptica and the pila accessoria. On the other hand, the optic fenestra is closed by the pila metoptica and the interorbital septum. Finally, the fenestra prootica and metoptica are continuous because the pila antotica does not have contact with the basal plate.

In the occipital region, the otic capsule presents the fenestra ovalis, and the tectum synoticum exhibits the ascending process. Ventrally, the basipterygoid process is lengthy with the distal portion expanded and contacting the pterygoid. The crista sellaris is a cartilaginous bar that separates the pituitary fenestra and the basicranial fenestra. This last fenestra is small in this stage. Posteriorly, the fissura metotica is separating the basal plate and the otic capsule. The perilymphatic foramen is present.

In this stage, ossification is beginning in the chondrocranium. The basisphenoid begins to ossify in the proximal region of basipterygoid processes and the crista sellaris (Table 2). Moreover, the parasphenoid is beginning to be observed in the region of the pituitary fenestra.

Regarding splachnocranium, the quadrate is fully differentiated and appears ossified in the medial region. The ascending process has begun to ossify in the middle to form the epipterygoid bone. Meckel's cartilage has become covered by the membrane bone of the lower jaw.

Differences to Mabuya macrorhyncha (Figs. 5, 6): the two species are very similar in their chondrocranium, although there are slight differences between them (Table 1). The fenestra lateralis is present in paranasal cartilage of the nasal capsule, and the anterior process of the planum supraseptale is shorter and thicker. The ossification is observed in the medial and posterior regions of the basal plate, which correspond to basisphenoid, basioccipital and exoccipital.

Differences to Mabuya caissara: this species differs to the others species in the nasal capsule, exhibiting a short rostral process and lacking the anterior process of the planum supraseptale in this stage. However, this species is similar to Mabuya sp. in the other characteristics of the nasal and orbital region (Table 1). Regarding splachnocranium, the columella is beginning the ossification. In this stage, the ossification of otic capsule, occipital arch and basal plate is more advanced than Mabuya sp. and M. macrorhyncha.

Mabuya sp. Stage 40 (Figs. 7, 8): In this stage the principal change is the advanced ossification of the whole skull. In the chondrocranium this is observed in the occipital and supraoccipital region; the prootic, otoccipital (opisthotic-exoccipital), basioccipital and basisphenoid are present. The parasphenoid is a triradial bone observed in the anterior region of the pituitary fenestra. The basicranial fenestra is smaller and it is limited by the basisphenoid and basioccipital. The paroccipital process is formed by ossification of the crista parotica. The prootic presents the alar process, which is projecting towards the epipterygoids, but does not contact this bone. Regarding dermatocranium, all bony elements are notably more developed than the stage before except of the frontal and parietal. Consequently, the frontoparietal fenestra is present. In the lower jaw, all bone elements are completely developed.

Embryos in preparturition stage present minimal changes (Fig. 8). In the orbitotemporal region of chondrocranium, the orbitosphenoid is observed (Table 1). This is a semilunar ossification developed on the pila metotica. In the occipital region, the parabasisphenoid is formed by the fusion of basisphenoid and parasphenoid elements. Finally, the basicranial and pituitary fenestrae are closed (Table 1).

In the dermatocranium, frontal bones are not fully differentiated in its posterior region yet. However, they are fused in the medial region. The parietal is completely differentiated except in the anterior region. Therefore, the frontoparietal suture is not formed and the frontoparietal fenestra is still present. This fenestra is smaller and extends as far out as the parietal foramen.

Differences to Mabuya macrorhyncha and M. caissara (Fig. 9): the only difference is observed in embryos in preparturition stage, where the basicranial fenestra is not completely closed (Table 1).

DISCUSSION

In general, Mabuya species included in this morphological study exhibit a complete chondrocranium, with the ethmoidal, orbitotemporal and occipital regions fully developed (Rao & Ramaswami 1952; Skinner 1973; Bellaris & Kamal 1981). In the ethmoidal region, the nasal capsule of the Mabuya is broad, very developed, and similar to others lizards such as the scincids Chalcides ocellatus, Eutropis carinata ( = Mabuya carinata), Plestiodon fasciauts ( = Eumeces quinquelineatus), Trachylepis capensis ( = Mabuya capensis), Lygosoma, the lacertids Lacerta vivipara, and Acanthodactylus boskiana, the anguid Anguis fragilis, and the gimnophthalmid Ptychoglossus bicolor (Rice 1920; Pearson 1921; Rao & Ramaswami 1952; El Toubi & Kamal 1961; Skinner 1973; Bellaris & Kamal 1981; Hernandez et al. 2012).

The scaffolding in orbitotemporal region changes with the body-plan, presenting reductions of some cartilages in serpentiform skinks like Lygosoma sp., Acontias meleagris and Chalcides sepsoides (Pearson 1921; Bellaris & Kamal 1981). In lacertiform skinks, the scaffolding is fully developed, like C. ocellatus, P. fasciauts and T. capensis (Rice 1920; El-Toubi & Kamal 1959; Skinner 1973); this last characteristic is observed in M. cassaira, M. macrorhyncha and Mabuya sp. On the other hand, the pila antotica is short and has no contact with the basal plate in Mabuya species (Table 1). This characteristic is observed in C. ocellatus, T. capensis and Lygosoma sp., while in P. fasciauts is absent (Pearson 1921; El-Toubi & Kamal 1959; Skinner 1973). In Mabuya species, the pila antotica is similar to that of T. capensis, which is short and only reaches the epipterigoyd position; however, during development Mabuya species present differences with African T. capensis, since Skinner (1973) observed that the pila antotica is contacting the basal plate in stages 32 to 35 (D&H), this contact being lost in later stages. In Mabuya species the pila antotica has not been seen in contact with the basal plate during embryonic development. While we do not have other skink species for further embryonic comparisons, it is nonetheless obvious that Mabuya species are different in the development of pila antotica in respect to T. capensis, thus indicating a difference between American and African clades in the development of this chondrocraneal characteristic.

On the other hand, the differentiation of the orbitosphenoid, a semi-lunar ossification in the pila metoptica of the orbitotemporal region, is observed in the stage 40 (D&H) in Mabuya species (Table 1). In T. capensis it is developed in postembryonic stages, appearing in adults (Skinner 1973). A similar characteristic is probably present in Lygosoma sp., since the orbitosphenoid is not present in the fully formed chondrocranium of the embryo, but it is present in the adult stage (Rao & Ramaswami 1952). Therefore, the development of the orbitosphenoid in Mabuya species shows differences in the rate of ossification in respect to African and Asiatic species.

Regarding the ossification of chondrocranium (Table 2), in Mabuya species, it starts in stage 39 (D&H); after that, all elements of chondrocranium are ossified and joined by synchondrosis (stage 40 D&H). This condition is observed in general in lizards, e.g. Trachylepis capensis, Elgaria coerulea, Liolaemus scapularis and Ptychoglossus bicolor (Skinner 1973; Good 1995; Lobo et al. 1995, Hernandez et al. 2012). In Mabuya species the basicranial fenestra and pituitary fossa are still present in stage 40 D&H. However, in the preparturition stage, the pituitary fossa is closed and the basicranial fenestra are closed or almost closed (similar to a slit). This is different from T. capensis where the pituitary fossa is closed in the preparturition stage, but the basicranial fenestra is still present in the juvenile stage.

In relation to the dermatocranium, the development of bony elements starts in stage 33 with the differentiation of the pterigoyd in Mabuya sp. and M. caissara, and the pterigoyd and dentary in M. macrorhyncha (Table 2). Posteriorly, in stage 34, other bony elements start to ossify (frontal, prefrontal, parietal, supratemporal, palatine, dentary and surangular). Finally, in stage 40 (D&H), all elements are almost completely developed, except for the frontal and the parietal ones, which only show the margins. In the pre-parturition stage, the frontal and parietal bones are almost fully differentiated; therefore, the frontoparietal fenestra is small and remains open. Dermatocranium development in Mabuya species is similar to the other lizards and the pterygoids appear early, as in Elgaria coerulea (Good 1995), Trachylepis capensis (Skinner 1973), and Liolaemus scapularis (Lobo et al. 1995). The other bony elements ossify early and correspond to the palatine, orbital and jaw region; this characteristic is observed in Trachylepis capensis (Skinner 1973), Lacerta vivipara (Rieppel 1992), L. agilis (Rieppel 1994) and Elgaria coerulea (Good 1995). We found that the entire ossification of parietal and frontal is observed in preparturing stages of Mabuya species, while in T. capensis it occurs in postnatal development (juvenile stage) (Skinner 1973). On the other hand, the vomer is a paired bony element in Mabuya embryos, but in post-embrionary stage a distinctive bony element is formed by fusion, this is a characteristic of adult stages of Mabuya sp. (Jerez 2012), while in African and Asiatic species the vomer remains a paired bony element through their entire ontogeny.

Therefore, the skull development of the American Mabuya presents differences with Trachylepis capensis in the development of pila antotica, the differentiation of the orbitosphenoid, the closure of pituitary and basicranial fenestrae, the ossification of parietal, and the development of vomer. Our evidences suggest that these characteristics should be regarded as diagnostic for Mabuya. Therefore, these unique developmental patterns of Mabuya sp., Mabuya caissara and M. macrorhyncha add weight to the systematic hypothesis (Mausfeld et al. 2002), splitting the American genus Mabuya from the African genera Trachylepis and Chioninia, and the Asian genus Chioninia.

ACKNOWLEDGMENTS

We would like to thank the Colección Herpetologica, Laboratorio de Biologia Reproductiva de Vertebrados, Universidad Industrial de Santander (Bucaramanga, Colombia) and the Museu de Zoología da Universidade de São Paulo (São Paulo, Brazil) for allowing us to prepare the material examined. The first author would like to thank Marissa Fabrezi (IBIOGEO, CONICET, Salta, Argentina) and Virginia Abdala (Universidad Nacional de Tucumán, CONICET, Argentina) for her support and collaboration without which the realization of this work would not have been possible. PMSM and RAGF are grateful to H. Zaher for the use of the facilities at Colecao de Herpetologia do Museu de Zoologia da Universidade de Sao Paulo. This research was funded by FONCIT (Argentina), contract number 1102-05-13556.

Avila-Pires, T. C. 1995. Lizards of Brazilian Amazonia (Reptilia: Squamata). Zoologische Verhandelingen, 299: 1-706.         [ Links ]

Bauer, A. M. 2003. On the identity of Lacerta punctata Linnaeus 1758, the type species of the genus Euprepis Wagler 1830, and the generic assignment of Afro-Malagasy skinks. African Journal of Herpetology, 52: 1-7.         [ Links ]

Bellairs, A. & Kamal, M. A. 1981. The chondrocranium and the development of the skull in recent reptiles. pp 1-263. In: Gans, C. & Parson, T. S. (Eds.). Biology of Reptilia, Vol 11. Academic Press, London.         [ Links ]

Blackburn, D. G. 1993. Choriallantoic placentation in squamate reptiles: structure, function, development, and evolution. Journal of Experimental Zoology, 266: 414-430.         [ Links ]

Blackburn, D. G. & Vitt, L. J. 1992. Reproduction in viviparous South American lizards of the genus Mabuya, pp. 150-154. In: Hamlett, W. (Ed.). Reproductive Biology of South American Vertebrates: Aquatic and Terrestrial. Springer-Verlag, New York.         [ Links ]

Caicedo-Portilla, J. R. 2012. Búsqueda y evaluación de caracteres morfológicos de posible utilidad filogenética y taxonómica del género Mabuya (Squamata: Scincidae) con base en especies presentes en Colombia. Tesis de Maestría. Universidad Nacional de Colombia, Bogotá D.C.         [ Links ]

Carranza, S. &. Arnold, E. N. 2003. Investigating the origin of transoceanic distributions: mtDNA shows Mabuya lizards (Reptilia, Scincidae) crossed the Atlantic twice. Systematics and Biodiversity, 1: 275-282.         [ Links ]

Dufaure, J. P. & Hubert, J. 1961. Table de developpment de lezard vivipare: Lacerta (Zootoca) vivípara. Jacquin. Archives Anatomie Microscopie Morphologie Expérimental, 50: 309-328.         [ Links ]

El-Toubi M. R. & Kamal, A. M. 1959. The development of the skull of Chalcides ocellatus. I. The development of the chondrocranium. Journal of Morphology, 104:269-306.         [ Links ]

El-Toubi M. R. & Kamal, A. M. 1961. The development of the skull of Ptyodactylus hasselquistii. I. The development of the chondrocranium. Journal of Morphology, 108: 63-93.         [ Links ]

Fitzinger, L. J. 1843. Systema Reptilium. Fasciculus Primus. Amblyglossae. Vienna: Braumuller et Seidel Biblipolas, Vindobonae.         [ Links ]

Good D. A. 1995. Cranial ossification in the northern alligator Elgaria coerulea (Squamata, Anguidae). Amphibia-Reptilia, 16: 157-166.         [ Links ]

Gray, J. E. 1845. Catalogue of the specimens of lizards in the collection of the British Museum. London: The Trustees of the British Museum (Natural History).         [ Links ]

Greer, A. E., Arnold, C. & Arnold, E. N. 2000. The systematic significance of the number of presacral vertebrae in the scincid lizard genus Mabuya. Amphibia-Reptilia, 21: 121-126.         [ Links ]

Greer, A. E. & Nussbaum, R. A. 2000. A new character useful in the systematics of the scincid lizard genus Mabuya. Copeia, 2000: 615-618.         [ Links ]

Hedges, S. B. & Conn, C. E. 2012. A new skink fauna from Caribbean islands (Squamata, Mabuyidae, Mabuyinae). Zootaxa, 3288: 1-244.         [ Links ]

Hernández-Jaimes, C., Jerez, A. & Ramírez, M. P. 2012. Embryonic development of the skull of the Andean lizard Ptychoglossus bicolor (Squamata, Gymnophthalmidae). Journal of Anatomy, 221: 285-302.         [ Links ]

Jerez, A. 2012. Características estructurales del esqueleto en Mabuya sp. (Squamata: Scincidae): una comparación con escíncidos africanos. Actualidades Biológicas, 34 (97): 207-224.         [ Links ]

Jerez, A. & Ramírez-Pinilla, M. P. 2001. The allantoplacenta of Mabuya mabouya (Sauria, Scincidae). Journal of Morphology, 249: 132-146.         [ Links ]

Jerez, A. & Ramírez-Pinilla, M. P. 2003. Morphogenesis of extraembryonic membranes and placentation in Mabuya mabouya (Squamata; Scincidae). Journal of Morphology, 258: 158-178.         [ Links ]

Jesus, J., Brehm, A. & Harris, D. J. 2005. Relationships of scincid lizards (Mabuya spp.) from the islands of the Gulf of Guinea based on mtDNA sequence data. Amphibia-Reptilia 26, 467-473.         [ Links ]

Lobo, F., Abdala, F. & Scrocchi, G. 1995. Desarrollo del esqueleto de Liolaemus scapularis (Iguania: Tropiduridae). Bolletino del Museo Regionale di Scienze Naturali (Torino), 13: 77-104.         [ Links ]

Mausfeld, P., Schmitz, A., BShme, W., Misof, B., Vrcibradic, D. & Rocha, C. F. D. 2002. Phylogenetic affinities of Mabuya atlantica Schmidt, 1945, endemic to the Atlantic Ocean archipelago of Fernando de Noronha (Brazil): necessity of partitioning the genus Mabuya Fitzinger, 1826 (Scincidae: Lygosominae). Zoologischer Anzeiger, 241: 281-293.         [ Links ]

Miralles, A. 2005. The identity of Lacerta mabouya Lacepède, 1788, with description of a Neotype: an approach toward the taxonomy of new world Mabuya. Herpetologica, 61: 46-53.         [ Links ]

Miralles, A. 2006. A new species of Mabuya (Reptilia, Squamata, Scincidae) from the Caribbean island of San Andres, with a new interpretation of nuchal scales: a character of taxonomic importance. Herpetological Journal, 16: 1-7.         [ Links ]

Miralles, A. & Carranza, S. 2010. Systematics and biogeography of the neotropical genus Mabuya, with special emphasis on the Amazonian skink Mabuya nigropunctata (Reptilia, Scincidae). Molecular Phylogenetics & Evolution, 54: 857-869.         [ Links ]

Miralles, A., Rivas-Fuenmayor, G. & Barrio-Amorós, C. L. 2005. Taxonomy of the genus Mabuya (Reptilia, Squamata, Scincidae) in Venezuela. Zoosystema, 27: 825-837.         [ Links ]

Miralles, A., Rivas Fuenmayor, G., Bonillo, C., Schargel, W. E., Barros, T., García-Pérez, J. E. & Barrio-Amorós, C. L. 2009. Molecular systematics of Caribbean skinks of the genus Mabuya (Reptilia, Scincidae), with descriptions of two new species from Venezuela. Zoological Journal of the Linnean Society, 156: 598-616.         [ Links ]

Pearson, H. S. 1921. The skull and some related structures of a late embryo of Lygosoma. Journal of Anatomy, 56: 20-43.         [ Links ]

Rao, M. K M. & Ramaswami, L. S. 1952. The fully formed chondrocranium of Mabuya with an account of the adult osteocranium. Acta Zoologica, 33: 209-275.         [ Links ]

Rice, E. L. 1920. The development of the skull in the skink Eumeces quinquelineatus. Journal of Morphology, 34: 120-243.         [ Links ]

Rieppel, O. 1992. Studies on skeleton formation in reptiles III. Patterns of ossification in the skeleton of Lacerta vivipara Jacquin (Reptilia: Squamata). Fieldiana Zoology, 68: 1-25.         [ Links ]

Rieppel, O. 1994. Studies on skeleton formation in reptiles. Patterns of ossification in the skeleton of Lacerta agilis exigua Eichwald (Reptilia, Squamata). Journal of Herpetology, 28: 145-153.         [ Links ]

Sánchez, H., Castaño, O. V. & Cárdenas, A. G. 1995. Diversidad de los Reptiles en Colombia. pp. 277-324. In: Rangel, J. O. (Ed.). Colombia Diversidad Biotica I. Convenio Inderena, Universidad Nacional de Colombia, Bogotá         [ Links ].

Skinner, M. M. 1973. Ontogeny and adult morphology of the skull of the south African skink, Mabuya capensis (Gray). Annals of the University of Stellenbosch, 48: 1-116.         [ Links ]

Wassersug, R. J. 1976. A procedure for differential staining of cartilage and bone in whole formalin fixed vertebrates. Stain Technology, 51: 131-134.         [ Links ]

Whiting, A. S., Sites, J.W., Jr., Pellegrino, K. C. M. & Rodrigues, M. T. 2006. Comparing alignment methods for inferring the history of the new world lizard genus Mabuya (Squamata: Scincidae). Molecular Phylogenetics and Evolution, 38: 719-730.         [ Links ]