Mabuya zuliae, Miralles & Fuenmayor & Bonillo & Schargel & Barros & García-Perez & Barrio-Amorós, 2009

Miralles, Aurélien, Fuenmayor, Gilson Rivas, Bonillo, Céline, Schargel, Walter E., Barros, Tito, García-Perez, Juan E. & Barrio-Amorós, César 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 (3), pp. 598-616 : 605-608

MABUYA ZULIAE SP. NOV. ( FIGS 1C, D , 2B )

Holotype: MHNLS 16647 . An unsexed adult specimen from Rio Escalante (09°03′08″N, 71°55′23″W), southwest lake Maracaibo, sector el Cañon, Zulia state, Venezuela, collected in October 2003 by E. Arrieta.

Paratypes: 13 specimens. Venezuela. Mérida: MHNLS 16671 , Finca Onia, 10 km south-west of El Vigia, via San Cristobal. Táchira : UMMZ 55933 , río Labatorito San Felix. Trujillo : ULABG 5008 , Quebrada Carvajal , 30 min from Valera. Zulia: MBLUZ 190 , Aragtoba , Bari indigenous community, Serranía de Abusanki , Sierranía de Perijá , Municipio Machiques (09°34′32″N, 72°55′15″W; 175 m a.s.l.); MBLUZ 254 , Frontalia , Río de Oro, Municipio Catatumbo (09°08′17″N, 72°52′17″W; 75 m a.s.l.); MBLUZ 737 , Embalse Burro Negro , Municipio Lagunillas ; MHNLS 10048–11864 , Misión El Tukuko , Sierranía de Perijá , collected by C. Lasso in July 1986 and W. C. Villalobos in November 1983, respectively; MHNLS 11856 , carretera Williams, Consejo de Ziruma ; MNHN 2007.0273 , Fundo La Orchila , Río Maché , Cuenca del Río Cachirí , Serrania de Perijá , Municipio Mara (10°48′44″N, 72°21′13″W; 227 m a.s.l.), collected in November 2003 by G. Rivas and F. Rojas; MHNLS 16676–16677 , Cerro el Mirador, km 495 on the Machiques-Colón road, municipality of Jesús Maria Semprún, collected in May 2004 by G. Rivas and T. Barros .

Additional material: Six foetuses ( MHNLS 17035– 17040 ) extracted from the uterus of the female MHNLS 16671 , at final stage of development (pig- mented integument). A specimen ( MHNLS 9720 ) from Hacienda El Jaguar, Sierra de Bobare , Yaracuy state, has been excluded from the type series because of its outlying locality (outside of the Maracaibo Basin) and its poor state of preservation .

Diagnosis: A medium-sized Mabuya with an undivided lower eyelid, all scales smooth, auricular lobes absent, and with a slightly acute snout, paired prefrontals and frontoparietals, a single pair of nuchals, four supraoculars, four supraciliaries, with the second being longest, and no dark dorsal stripes. Mabuya zuliae sp. nov. differs from neighbouring species of Mabuya by the combined presence of the following characters: four longitudinal dark stripes along the body (versus six long dark stripes in M. carvalhoi , M. croizati , M. nebulosylvestris sp. nov. and M. sloanii ; six dark stripes, including a shorter pair of dorsals, in M. bistriata and M. macleani ; seven dark stripes in M. cochabambae and M. meridensis ; and ten dark stripes in M. lineolata ); palms and soles dark coloured (versus palms and soles light coloured in M. bistriata , M. berengerae , M. falconensis , M. mabouya , M. macleani , M. luciae , M. pergravis , M. sloanii , and the Central American M. unimarginata complex species); frontoparietals separated (versus frontoparietals fused in M. croizati , M. carvalhoi , and M. cochabambae ); no secondary nuchal scales (versus between one and five pairs in M. berengerae , M. carvalhoi , M. croizati , M. macleani , variable, M. pergravis , and M. sloanii ); and in having parietals in broad contact behind the interparietal and four supracilliaries, with the second being the longest (versus parietal most often separated by the interparietals, and five or six subequal supraciliaries in M. nigropunctata ). Moreover, the presence of small white and black spots on legs and tail, and the distribution pattern of black spots on the back and neck, constitute a characteristic peculiar to this species.

Description of the holotype: MHNLS 16647 ( Fig. 1C, D ). Good state of preservation. Snout–vent length 83.5 mm; tail length 102.4 mm (partly regenerated); head length 15.0 mm. Fore- and hindlimbs easily touching each other when adpressed against body.

Rostral wider than high, contacting first supralabials, nasals, and supranasals. Paired supranasals in median contact, contacting anteriormost loreal. Frontonasal approximately rhomboid, wider than long, laterally contacting anterior loreal. Paired prefrontals roughly quadrilateral, wider than long, separated medially, contacting frontonasal, both anterior and posterior loreals, first supraciliaries, first supraoculars, and tip of second supraoculars, and frontal. Frontal lanceolate, approximately one and a half times longer than wide, wider anteriorly, in contact with frontonasal, prefrontal, second supraoculars, and frontoparietals. Four supraoculars: the first being the smallest, and the second being the longest and widest. The posteriormost supraocular in contact with the frontal is the second. Four supraciliaries, with the second being the longest. Paired frontoparietals, longer than wide, in broad contact at midline, in contact with frontal, all supraoculars, except the first, the parietal, and the interparietal. Interparietal rhomboid, longer than wide, wider anteriorly, posterior part rounded and separated from nuchals by parietals. Parietal eye hardly distinct. Parietals larger than interparietal, wider than long, overlapping the upper temporal scale. Single pair of transversely enlarged nuchals, each as wide as three rows of dorsals. Nasal trapezoidal. Nostril located posteriorly. Postnasal small, in contact with supranasal, anterior loreal, and first supralabial. Two subrectangular loreals behind nasal: subequal in size, with the second being slightly longer. First loreal in contact with first and second supralabials; second loreal in contact with second and third supralabials. One small presubocular in contact with fifth and sixth supralabials. Two preoculars in contact, with the anteriormost behind the second loreal, and in contact with the third and fourth supralabials, and with the posteriormost in front of presubocular, and in contact with the fourth and fifth supralabials. Lower eyelid undivided, with a transparent disc, and one row of small scales across its dorsal edge. Eight supralabials, with the sixth being the enlarged subocular. Eight infralabials. Temporals imbricate, smooth, cycloid, and not distinctly delimited from scales on the nape or sides of the neck. Two pretemporals. One primary temporal, two secondary temporals in contact, and three tertiary temporals. Ear opening relatively small, oval, and with inferior and posterior margin bordered by small scales. Auricular lobules absent. Mental wider than long, posterior margin straight. Postmental wider than long, adjacent to the first infralabial, and to two-thirds of the second infralabial. Two pairs of chin shields, in contact with postmental, and second, third, and fourth infralabials. Gulars similar in size and outline to ventrals. Palms and soles covered with small tubercles, subequal in size. Both regions delimited by a row of larger and flatter scales. Subdigital lamellae smooth, single, with 12 under fourth finger (on each side), 17 under left fourth toe, and 18 under right fourth toe. Finger and toes clawed. Relative length of toes in the following order: I <II <III = V <IV. All scales, except head shields and scales on palms, soles, and digits, cycloid, smooth, and imbricate. Thirty scale rows around midbody, 52 transverse rows of dorsal scales, 35 transverse rows of ventral scales. Four preanals larger than adjacent ventral scales. Median supra- and subcaudal series of scales twice as wide as long on the posterior third of the tail.

Coloration in preservative: background colour of upper side of the head, neck, back, limbs, and tail olive-greyish. Venter, lower side of head, throat, lower side of limbs, and tail immaculate cream/light-grey, lighter medially than laterally. Lower half of rostral and each supralabial white; each infralabial grey with a black posterior edge. A dark spot on the posterior edge of each fourth supraocular. Lateral and upper sides of limbs spotted with small black and white spots, often in contact together. Supradigital lamellae white, most of them with a black dot on each lateral side. Palms and soles dark grey. White and black triangular dots on the tail. Preanals pale cream. No dorsal stripes. Two dark upper lateral stripes, with irregular margins on each side; margins darker and better defined on the anterior part; about three scales wide at midbody; from nostrils, loreals, dorsal halves of supralabials, around eyes and temporals, along upper half of ear openings, on neck, above arms, and on sides extending to insertion of hindlimbs. Two lower lateral dark stripes formed by a succession of more or less aligned dark dots; extending from below ear opening, above forelimb, to insertion of hindlimbs. Four white stripes run along the body. Two white dorsolateral stripes nearly imperceptible, very short, and only present on the neck (from the parietal to the 15th dorsal). Two white lateral stripes clearly defined from supralabials to forelimbs, continuing in a succession of aligned spots to the hindlimbs. Numerous dark triangular dots on the dorsum, each one of them in the middle of a dorsal scale, and in contact with its posterior edge; on the neck, only present in two longitudinal scale rows, edging the dorsolateral white stripe dorsally, but present in all of the dorsal scale rows.

Variation: Dorsal scale rows, 47–53 (51.53 ± 1.50; 19); midbody scale rows, 28–30 (29.24 ± 0.97; 17); ventral scale rows, 29–36 (31.72 ± 1.84; 18); lamellae under fourth finger, 13–16 (15.38 ± 0.66; 40); lamellae under fourth toe, 16–19 (18.22 ± 0.85; 37); head length, 10.4–16.9 (14.89 ± 1.77; 12); snout–vent length, 65.7– 100.9 (81.04 ± 12.04; 12); tail length, 118.3–155.3 (136.31 ± 13.91; 7). Internasals: 95.0% in broad contact and 5.0% separated. Prefrontals: all separated. Parietals: 95.0% in broad contact and 5.0% separated (N = 20). Number of supraciliaries (n sides = 40): four, with the second being the longest (87.5%); five, with the second being the longest (10.0%); five, subequal in size (2.5%). Number of supralabials (n sides = 40): eight, with the sixth being the enlarged subocular (97.5%); nine, with the seventh being enlarged subocular (2.5%).

Etymology: The name of this species is given in reference to the state of Zulia, where this species is relatively common.

Distribution ( Fig. 3B ): Mabuya zuliae sp. nov. is widespread in Zulia state, and also marginally in the neighbouring states of Mérida and Trujillo. It is distributed around the Lake Maracaibo Basin, including the lowlands, foothills, and mountainous areas of the eastern slope of the Serranía de Périjá (under 1500 m a.s.l.).

Natural history: Mabuya zuliae sp. nov. is a diurnal species that can be found associated with rural houses, ranches, and farms with moderate intervention of the surrounding habitat. This species is a good climber, and is frequently observed higher than 1 m above ground, basking on tree trunks or shrubs, and also in debris associated with agricultural areas. Many specimens have been found foraging in mangrove areas, close to water (lakes, lagoons, or rivers). At Cerro Mirador, a young specimen was observed, apparently active (or just escaping) at night. Given the extensive distribution of this species in the Maracaibo Basin, and the high diversity of habitat spanning its distribution, a great diversity of lizards are to be found in sympatry with M. zuliae sp. nov., such as Norops annectens (Williams, 1974) , Norops auratus ( Daudin, 1802) , Norops biporcatus (Wiegmann, 1834) , Norops tropidogaster (Hallowell, 1856) , Basiliscus basiliscus (Linnaeus, 1758) , Iguana iguana (Linnaeus, 1758) , Polychrus marmoratus (Linnaeus, 1758) , Gonatodes petersi Donoso-Barros, 1967 , Gonatodes vittatus (Lichtenstein, 1856) , Thecadactylus rapicauda (Houttuyn, 1782) , and Phyllodactylus ventralis O’Shaughnessy, 1875 .

MOLECULAR RESULTS

The combined analysis of the mitochondrial 12S rRNA and cytochrome b genes constitutes a matrix of 1539 characters: 670 sites were variable, and 534 of them were parsimony informative. The heuristic search using MP analysis produced 20 equally mostparsimonious trees (n taxa = 47; tree length = 2791; consistency index, CI = 0.363; retention index, RI = 0.594; rescaled consistency index, RC = 0.216). The monophyly of the genus Mabuya is strongly supported, but most of the basal relationships are poorly resolved when examining the strict consensus tree ( Fig. 4A ). Mabuya carvalhoi and M. croizati are resolved as sister species, and are placed at the base of the genus. Most species around the Caribbean Sea constitute a strongly supported clade (referred to as the Carribean clade in the present study, and composed of M. falconensis , M. mabouya , M. meridensis , M. unimarginata , and the two new species), with the notable exceptions of M. sloanii (an Antillean species) and M. croizati (a species endemic to the Turumiquire massif in north-eastern Venezuela). The Central American Mabuya ( M. unimarginata complex) also represents a strongly supported monophyletic unit. The Bayesian tree topology is very similar to the MP tree ( Fig. 4B ), but with a higher support for the monophyly of the neotropical lineage, the Caribbean clade (with the exclusion of M. sloanii ), and the basal position of the clade ( M. carvalhoi + M. croizati ).

HYPOTHETICAL PHYLOGENETIC POSITION OF RARE

CARIBBEAN SPECIES

Most of the insular Antillean species of Mabuya appear to be extremely rare, if not extinct (e.g. M. berengerae , M. luciae , or M. pergravis ). Consequently, it was not possible to obtain tissue samples of five of the seven insular Mabuya so as to include those species in the molecular analyses. The genus Mabuya is morphologically too conserved to obtain sufficient phylogenetically informative characters to generate a phylogenetic tree including those species for which genetic data is not available. However, some hypothetical phylogenetic groupings of these species, based on a qualitative analysis of their morphology (including notions of overall similarity and some putative synapomorphies) and geographical distribution are proposed as follows: (1) M. luciae is placed as a sister species of M. mabouya ; (2) M. berengerae and M. pergravis are regarded as sister species (San Andrès clade), and are grouped with M. unimarginata and M. falconensis in a trifurcate consensus; (3) M. macleani is placed as a sister species of M. sloanii ; and (4) M. lineolata is placed as a sister species of the M. sloanii group ( M. sloanii + M. macleani ). These hypothetical groupings, combined with our molecular results, are presented in a hypothetical consensus tree ( Fig. 5).

Figures

Figure 1. A, B, holotype of Mabuya nebulosylvestris sp. nov. (MHNLS 17093). C, D, holotype of Mabuya zuliae sp. nov. (MHNLS 16647). The drawing (A) is symmetrically reversed, and represents the right side of the head. Scale bar: 2 mm. Illustrations by AM.

Figure 2. Uncollected specimens of (A) Mabuya nebulosylvestris sp. nov. (from the type locality, Colonia Tovar, Aragua, Venezuela), (B) Mabuya zuliae sp. nov (from Cerro El Mirador, km 495 on the Machiques–Colón road, Zulia, Venezuela), and (C) Mabuya meridensis (in the vicinity of Mérida city, Mérida, Venezuela). Photographs by AM, TB, and CLB-A, respectively.

Figure 3. Distribution of (A) Mabuya croizati, Mabuya falconensis, Mabuya nigropunctata (in part; the only locality, based on the bibliography of Lotzkat, 2007, is represented by a white circle with a black dot), and (B) distribution of Mabuya meridensis, Mabuya nebulosylvestris sp. nov., and Mabuya zuliae sp. nov.

Figure 4. Phylogenetic trees of the genus Mabuya obtained from 12S and cytochrome b sequences. A, cladogram of the strict consensus maximum parsimony (MP) tree with bootstrap values (1000 replicates; bootstrap proportions less than 50% are not shown). B, Bayesian analysis, with 50% majority rule consensus (posterior probabilities below 0.90 are unmarked). The most remarkable nodes are: (1) the genus Mabuya s.s. (exclusively neotropical clade) and (2) the Caribbean clade. Grey rectangles represent clades endemic to the Carribean region. Mountain species are marked with triangles so as to be distinguishable from lowland species. Abbreviations: Mex., Mexico; Venez., Venezuela.