Liolaemus crandalli, Avila, Luciano Javier, Medina, Cintia Debora, Perez, Cristian Hernan Fulvio, Sites, Jack W. & Morando, Mariana, 2015

Avila, Luciano Javier, Medina, Cintia Debora, Perez, Cristian Hernan Fulvio, Sites, Jack W. & Morando, Mariana, 2015, Molecular phylogenetic relationships of the lizard clade Liolaemus elongatus (Iguania: Liolaemini) with the description of a new species from an isolated volcanic peak in northern Patagonia, Zootaxa 3947 (1), pp. 67-84 : 72-80

Liolaemus crandalli sp. nov.

Holotype. MLP.S 2631 (ex-LJAMM-CNP 12219, Figs. 2 , 3 ), an adult male collected near Park Ranger Station, on rocky outcrops on the roadside of the main unpaved road to the Auca Mahuida volcano summit, 25.9 km SW junction Provincial Road 6, Area Natural Protegida Auca Mahuida, Pehuenches Department, Neuquén, Argentina (37º42’06.7” S, 68º51’28.8” W, 1560 m), by L. J. Avila, M. Kozykariski, F. Breitman, 14 November 2009.

Paratypes. LJAMM-CNP 10470-10471 (male) and 10472 (female) collected at Gravel Quarry 10, YPF petroleum company, Area Natural Protegida Auca Mahuida, Pehuenches Department, Neuquén, Argentina (37º44’07.0” S, 68º54’21.3” W, 1841 m), by C.H.F. Pérez, D. Pérez, C. Poblete, L. Moreira, 7 March 2008. LJAMM-CNP 12158, 12218, 12220-12221 (male) and 12159-12160, 12222-12226 (female), same locality as holotype. Collected by L. J. Avila, M. Kozykariski, F. Breitman, 14 November 2009. LJAMM-CNP 12295, 12299 (male) and 12296 (female) collected at an unnamed site, Area Natural Protegida Auca Mahuida, Pehuenches Department, Neuquén, Argentina (37º43’01.9” S, 68º55’50.9” W, 1851 m), by L. J. Avila, M. Kozykariski, F. Breitman, 15 November 2009. LJAMM-CNP 12302 (male) and 12303-12304 (female) collected on Cerro de las Antenas, Area Natural Protegida Auca Mahuida, Pehuenches Department, Neuquén, Argentina (37º44’25.5”S, 68º53’42.4”W, 1935 m). Collected by L. J. Avila, M. Kozykariski, F. Breitman, 15 November 2009.

Diagnosis. Liolaemus crandalli sp. nov. can be distinguished from other members of the L. elongatus clade by a combination of characters: large size, number of dorsal and ventral scales, general body coloration, as well as by its genetic distinctiveness. Liolaemus crandalli sp. nov. is larger than L. burmeisteri , L. chillanensis and L. smaug (93.4 vs 85.2, 70.3 and 68.3 mm) but smaller than L. antumalguen , (93.4 vs 107.7 mm), and similar in size to L. choique , L. elongatus and L. shitan . Average number of scales around midbody is lower in L. crandalli sp. nov. (84.5±4.9) than in L. chillanensis (87.45.0±8.49), but is higher than in L. antumalguen (77.0±1.9), L. burmeisteri (76.2±2.7), L. choique (78.9±5.0), L. elongatus (77.5±4.0), L. smaug (74.1±2.6) and L. shitan (78.1±3.9). Average number of dorsal scales (between occiput to rump) in L. crandalli sp. nov. is lower than L. burmeisteri (77.9±4.3 vs 81.1±2.8) but higher than in L. antumalguen (73.0±1.9), L. chillanensis (74.09±4.61), L. choique (72.6±6.2), L. elongatus (73.4±5.2), L. smaug (70.3±3.2) and L. shitan (70.6±3.9). Average number of ventral scales is higher in L. crandalli sp. nov. than in all other species of the clade: 131.9±4.9 vs 108.6± 4.3 in L. antumalguen , 104.7± 2.8 in L. burmeisteri , 117.1± 7.43 in L. chillanensis , 123.7± 5.2 in L. choique , 108.1± 5.6 in L. elongatus , 111.9± 4.1 in L. smaug and 120.6± 5.9 in L. shitan . General body coloration in L. crandalli sp. nov. is patternless, at full sun, with an ochre-dark green dorsum with scales borders slightly edged in yellow; dorsal coloration usually extending to the tail; dorsal head scales are almost all covered by black, surrounded by red-brown edges. In head and lateral body areas, coloration becomes more dark brown, ventral areas usually gray with scales in the cloacal apron, inferior femoral areas and lower belly yellow. This coloration is usually found in males and females of L. crandalli and this combination is not found in others members of the species group. Liolaemus crandalli has no evident sexual dichromatism as is observed in L. smaug , and as weakly present in L. shitan .

Description of holotype. Adult male. SVL 89.4 mm, total length 244.4 mm; tail complete (155 mm length). Axilla-groin distance 37.0 mm. Head 20.6 mm long (from anterior border of auditory meatus to tip of snout), 15.9 mm wide (at anterior border of auditory meatus), 9.7 mm high. Arm length 25.3 mm. Tibia length 18.1 mm. Foot length 25.1 mm (ankle to tip of claw on fourth toe). Dorsal head scales irregular, smooth and protruding. Scale organs more abundant in the anterior head region than in the parietal and temporal region, which have become scarce. Sixteen scales between rostral and occiput (at level of anterior border of auditory meatus). Rostral scale wider (3.5 mm) than high (1.7 mm). Two postrostrals. Four internasals of similar height but the two middle scales twice as wide. Six frontonasals, the two outer scales on each side higher than wide and smaller that the two central scales, these last almost square and larger than the most external. Five prefrontals, irregular. Frontal scale divided longitudinally, forming two scale rows between circumorbitals. Five scales between frontal and rostral. Interparietal pentagonal, similar size to parietals. Interparietal surrounded by nine scales, with a central, small, and obscure ‘‘parietal eye’’ in center of scale. Supraorbital semicircles complete. Five enlarged supraoculars.

Four scales between frontal and supercilliaries. Six supercilliaries, irregular flattened and elongated. Nineteen temporals on each side, most of them smooth with one scale organ.

Canthal scales separated from nasal by one scale. Loreal region concave. Six scales surrounding nasals on each side. Nasal not in contact with rostral. Orbit with 13 upper and 12 lower ciliaries. Orbit diameter 1.9 x 3.8 mm (measured between upper and lower ciliaries). Subocular scale elongate. Preocular unfragmented. Eight lorilabials, four in contact with subocular. Seven supralabials on the left side and six on right side. Fourth supralabial curved upward posteriorly but fourth not in contact with subocular. Infralabials four, first scale twice as high as posterior infralabials. Postrostrals, internasals, frontonasals, prefrontals, loreal, lorilabials, supra- and infralabials with conspicuous scale organs.

Four outwardly projecting scales along anterior border of auditory meatus. Auditory meatus about twice as high (3.7 mm) than wide (2.4 mm). Lateral scales of neck granular with skin below appearing slightly inflated. Antehumeral, longitudinal, oblique, and postauricular neck folds distinct, gular incomplete, rictal not present.

Twenty-eight scales between auditory meatus and antehumeral fold (counted along longitudinal fold). Scales of dorsal neck region similar to dorsals.

Mental wider (3.7 mm) than long (2.1 mm), followed posteriorly by two rows of chinshields with three scales on the left side and four on right side. Rows of chinshields not in contact with mental. Throat scales between chinshields slightly imbricate, strongly imbricate toward auditory meatus. Fourty-four gulars between auditory meatus.

Eighty-two dorsal scales between occiput and anterior surface of thighs. Thirty-nine longitudinal keeled scales rows. Scales increase in size and become less keeled through flanks. Flank scales with one scale organ at the tip. Scales small and granular around limb insertions. Eighty-six scales around midbody. Ventral scales of similar size to dorsals, but smooth and round, 139 between mental and cloacal aperture. Precloacal scales slightly larger than ventrals. Three precloacal pores.

Tail quadrangular in cross section near cloacal area, becoming oval to round in the rest. Caudal scales in discernible annuli. Dorsal and upper lateral caudals scales keeled, imbricate and mucronate. Lower lateral scales moderately keeled, some mucronate, and ventral scales slightly keeled, not mucronate.

Suprabrachials, imbricate, slightly keeled; prebrachials rhombic, imbricate, smooth, grading into smaller subimbricate with a central strip granular infrabrachials. Supra-antebrachials imbricate, very weakly keeled; postantebrachials imbricate, moderately; pre-antebrachials imbricate, smooth; and infra-antebrachials imbricate, changing from smooth in the posterior region to moderately keeled at the anterior region. Suprametacarpals imbricate, smooth; inframetacarpals imbricate, keeled, not mucronate. Supradigitals of manus smooth, wider than long; subdigitals with three keels, each terminating in a short blunt mucron, numbering: I: 11, II: 16; III: 23; IV: 25; V: 14. Claws robust, moderately curved, opaque brown.

Suprafemorals imbricate, moderately keeled; prefemorals and infrafemorals imbricate, smooth. Postfemorals small, granular. Supra- and pretibials imbricate, moderately bluntly keeled; infratibials imbricate, smooth. Supratarsals imbricate moderately keeled and smooth toward the posterior region; infratarsals imbricate, 1-keeled, mucronate on the anterior region and smooth toward the posterior region. Supradigitals of foot smooth, rhombic; subdigital scales keeled, changing from 4-keeled in the posterior region of digit to 3-keeled in the tip, numbering: I: 12; II: 18; III: 25; IV: 30; V: 20. Claws robust, moderately curved, opaque brown.

Color of holotype in life. Dorsal and lateral head scales dark brown, with black smudges on parietals, interparietal, supraoculars, frontals, prefrontals and occipital scales in most of its surface giving the appearance of homogeneous black. Temporal clear with two to three rows of dark scales between these and the eye. Thin line of black on subocular upper border. Infralabials whitish, a few dark brown.

Dorsal pattern between nuchal and cloacal region dark brown without pattern well marked, with a diffused vertebral band formed up of thirteen series of black scales with clear anterior border. Dorso lateral region speckled with few white spots formed by one scale. Body lateral region dark brown, with central region between axilla and groin black, formed by dark scales. Tail light brown, weakly ringed with dark brown. Upper limb surfaces light brown with reticulated of dark brown. Ventral scales of throat, neck, chest, belly and forelimbs light gray with a black reticulated, most notably in the throat and belly. Femoral and lower belly region, yellow. Ventral scales of cloacal and postcloacal region light gray with a dark reticulated not well defined. Ventral region of tail light gray.

Color of holotype in preservative. After three years in preservative, the dorsal coloration of the head, dorsum, body flanks and tail darken and have become less noticeable. Ventral scales of throat, neck, chest, belly and forelimbs light gray, and the distinctive yellow ventral coloration of the femoral region and belly turned light gray.

Variation.— Adults range from 68.9–93.4 mm SVL. As in other members of this clade, no obvious body size dimorphism was observed (except tail expansion in males and smaller head width in females). In ten males ( Table 3 ): SVL: 70.5–93.4 mm. Head length: 16.7–20.6 mm. Head width: 13.2–16.5mm. Head high: 8.2–10.9 mm. Foot length: 21.2–25.1 mm. Tibial length: 15.2–18.1mm. Arm length: 21.6–25.3 mm. Midbody scales: 77–92. Dorsal scales (between occiput at the anterior margin of auditory meatus and anterior surface of thighs): 67–86. Ventral scales 125–139. Fourth toe lamellae: 27–33. Supralabial scales: 6–7. Infralabial scales: 4–5. Cloacal pores: 3–6. In eleven females ( Table 2 ): SVL: 68.9–90.6 mm. Head length: 16.2–18.8mm. Head width: 12.7–15.9 mm. Head height: 7.0– 10.6 mm. Foot length: 21.3–24.5 mm. Tibial length: 14.9–17.4 mm. Arm length: 20.8–25.5 mm. Midbody scales: 75–94. Dorsal scales: 72–85. Ventral scales: 120–137. Fourth toe lamellae: 25–31. Supralabial scales: 6–7. Infralabial scales: 4–5. For twenty-one individuals (males and females): dorsal scales: 77.95 ±4.30 (72–86). Supralabial scales 6–7. Infralabial scales 4–5. Third finger lamellae ranges 18–24. Fourth toe lamellae ranges 25–33.

Coloration in life is very variable, and depends in part on whether lizards are in full sun or shade, time of day (e.g. early morning or midday), and behavior ( Fig. 4 ). At full sun, usually have a very dark coloration, almost completely black (but usually a shiny black), with a dark green or green “moss shine”, with dorsal scales edged with yellow/light brown, sometimes with white spots randomly distributed along paravertebral bands. In full sun conditions, usually near midday, head scales are darker than body scales, giving an appearance of a black head, but usually only the dorsal head scales are completely black, coloration that occupies almost all the surface of the head scales with clear coloration only in the scales edges. Some individuals show a slightly reticulated pattern formed by anastomosed groupings of ochre and dark green scales. When individuals are not at full sun, they usually show a dorsal body pattern of a paravertebral band flanked by two clear dorsolateral bands, and darker lateral bands, but in some individuals this pattern is not shown, having the appearance of a uniform plain pattern of dark brown-green scales. Usually the paravertebral band is very evident or not, because scales in this area varies from entirely black to have only a small portion of its surface with melanism (usually the keel). This gives a very variable appearance to the vertebral band. Dorsolateral bands are usually more homogenous but their coloration varies from dark gray, light to dark brown or dark green but in some individuals black or white spots can be randomly distributed between occiput and rump or first portion of the tail. White coloration is usually in the distal edges of each scale; meanwhile the black coloration is limited to the insertion area of each scale. In medium-size specimens, white spots can merge and form irregular transverse bands. Lateral bands can be very good defined or not, usually lateral scales became darker than dorsolateral scales and a very dark band is marked between axilla and groin but in other individuals the coloration of the dorsolateral bands continues to reach the ventral scales. Some individuals exhibit brown scales very conspicuous in the areas pre, supra and postscapular and in the area around the insertion of the hindlimb.

Usually dorsal scales are completely black in the majority of the individuals but in some, dark coloration extends to the sides, almost reaching supralabial or gular scales. Clear coloration (almost white) is evident in supralabial and infralabial scales of some individuals but in general surface of the throat, chest, limbs, belly and tail varies from light to dark gray, with a conspicuous yellow coloration observed in lower belly, infrafemoral and usually cloacal apron of all individuals. Tail is usually ringed, with two dark gray scale rings separated by a white scales ring in almost all the tail length.

Etymology. The specific name is to honor our colleague Keith A. Crandall, an evolutionary biologist from George Washington University, Washington, D.C. As former professor at Brigham Young University, Provo, Utah, USA, he strongly supported MM and LJA in our studies of Patagonian herpetofauna with Dr. J.W. Sites Jr.

Geographic distribution. Liolaemus crandalli sp. nov. is only known from the Patagonian Steppe vegetation environments found between 1300–2100 m elevation in the Auca Mahuida Volcanic Field, Añelo and Pehuenches Departments, in Neuquén Province ( Fig. 5 ). The main physiographic feature in the Auca Mahuida Volcanic Field is the volcano of the same name that occupies the majority of the volcanic field, and harbors all the Patagonian Steppe environments. This environment is isolated from other similar Patagonian Steppe environments, and surrounded by dunes fields or sandy/rocky flatlands with extremely arid characteristics and vegetation typical of the Monte phytogeographic region. Liolaemus crandalli sp. nov. is not in contact with the geographic distributions of other members of the elongatus clade; the geographically closest related species are found in the Tromen volcanic field, 100 km west of Auca Mahuida and probably in the Chachahuen mountains, a small formation 70 km north. Both regions are separated from Auca Mahuida by sandy lowlands, riverbeds or smaller volcanic chains where no members of the Liolaemus elongatus clade have ever been found in several years of field surveys. The Chachahuen Mountains are separated from the Auca Mahuida Volcanic Field by the Colorado River valley, and the most closely-related species found in those environments were specimens of Liolaemus austromendocinus Cei, 1974 , a typical species of Monte rocky environments in Mendoza and Neuquén provinces. In some parts of the Auca Mahuida volcano between 1200–1300 m, Liolaemus austromendocinus is found in syntopy with L. crandalli sp. nov. sharing the same rocks.

Natural history. Liolaemus crandalli sp. nov. is found in rocky environments between 1300–2100 m ( Fig. 6 ), with vegetation characteristic of the Payunia District, Patagonica Province, Andino Patagonico Domain ( Roig 1998), and dominated by shrubs such as Senna annorttiana , S. kurtzi , Mulinum spinosum , and several species of grass ( Poa ligularis and Stipa spp). Lizards were found by active search along transects established along the main roads, trails or open field on the slopes of the Auca Mahuida volcano. They were most frequently found basking in exposed rocky areas, small canyons, small volcanic craters, rocky cliffs or outcrops, and when observers approached, they dropped off the perch gently, either remained near the perch or run to hid under rocks, crevices or bushes. They were often collected by flipping rocks where they usually hid immediately after a short chase. They have also been seen climbing the low vegetation but never burying in sand, despite early in the morning juveniles were commonly observed in the sand drifts found at the edges of shrubby vegetation ( Prosopis denudans , Senna kurtzii , S. arnottiana ). Some behavioral observations were recorded by M. Kozykariski and P. Escudero in 2009– 2011 (Escudero & Kozykariski unpublished data). Individuals were observed active between 09:00 to 20:00 on sunny days of the austral summer, but showed a bimodal activity pattern on the hottest days (in December) and a unimodal pattern on cloudy or cold days or in November and March. More active lizards were observed in November, usually running between refuges or perch sites, probably related with reproductive behavior, while in December the majority of the lizards were observed basking on perches. Air temperatures varied between 21–25°C when the majority of the lizards were observed. Males were more frequently observed when the substrate temperature was 26–30°C, and females were more often seen at temperature between 31–35°C. Several individuals were observed sharing basking areas on rocky surfaces. They seem to be territorial at some point because aggressive encounters between males or females were observed. Juvenile activity was more frequent in early hours of the morning or late hours of the afternoon.

Based on analyses of stomach contents, L. crandalli sp. nov. feeds on a variety of insects and plants. In four digestive tracts, we found Orthoptera, Coleoptera, Formicidae , sand grains, Asteraceas tubular flowers, Stipa sp. caryopsis, and indeterminate parts of other arthropods. These contents are very similar to those found by Videla (1983) in L. elongatus from Mendoza Province. No data on reproduction or other natural history characteristics are available, but detailed biological information has been published only for a few of the other Liolaemus species related to L. crandalli ( Ibargüengoytıa & Cussac 1998, 1999, 2002; Quatrini et al. 2001; Videla 1983), with observations in Acosta et al. (1996), Cei (1986), Espinoza and Lobo (2003), Espinoza et al. (2000), Hulse (1979), and Schulte et al. (2000). This species shares its habitat with other Liolaemus species ( Liolaemus cyaneinotatus , L. austromendocinus , L. sitesi ), as well as Diplolaemus leopardinus , Leiosaurus belli , Phymaturus sitesi and P. roigorum . In the lower limit of altitudinal distribution, L. crandalli was observed in syntopy with L. austromendocinus , a similar looking lizard. This area seems to be restricted to the northeast corner of Auca Mahuida volcano were both species are found sharing the same rocky areas, but the elevation range of syntopy between these species is no greater than 200– 300 m. Several snakes were observed by Park Rangers in the area, including Bothrops ammodytoides , Philodryas trilineata , Pseudotomodon trigonatus and Micrurus pyrrocryptus , all potential predators of this species but none were observed by us during our field surveys.

Remarks. —With the description of Liolaemus crandalli sp. nov., four species of endemic lizards have now been described from Auca Mahuida region, L. cyaneinotatu s Martinez et al., 2011, L. sitesi Avila et al., 2013 and Phymaturus sitesi Avila et al., 2013 . Liolaemus cuyumhu e Avila et al., 2009 was described from the live dunes of nearby southern lowlands, the Bajo de Añelo. This new species, as well these other endemic mountain lizard species, are completely confined to the boundaries of a provincial nature reserve area (Area Natural Protegida Auca Mahuida) intended originally to mainly protect surviving populations of Lama guanicoe of northern Neuquén Province. However, in recent decades the region has become one of the most important oil and gas fields of northwestern Patagonia, and in the last few years it has become a ¨proving ground¨ for the new oil/gas ¨hydraulic fracturing¨ extraction technique or ¨fracking¨. This methodology can seriously affect biodiversity ( Kiviat 2013) but no study has been made on the impact of fracking on the endemic terrestrial vertebrates of this region. As Auca Mahuida harbors a very interesting and endemic vertebrate fauna, it is important for conservation authorities to strength control over fracking and to implement effective conservation and monitoring efforts for this biogeographic island.

Figures

FIGURE 2. Liolaemus crandalli (MLP. S 2631) adult male in dorsal and ventral view, from Auca Mahuida volcano type locality, Pehuenches Department, Neuquén province, Argentina.

FIGURE 3. Liolaemus crandalli, holotype adult male in dorsal and ventral view (MLP. S 2631), from Auca Mahuida volcano type locality, Pehuenches Department, Neuquén, Argentina.

FIGURE 4. Variation in dorsal coloration of several individuals observed at type locality; all in natural conditions. Bottom photograph, an adult male of Liolaemus elongatus showing the typical dorsal pattern in western Chubut (region were the species was originally described).

FIGURE 5. Map of northern Neuquén and southern Mendoza region showing the complex landscape of northwestern Patagonia. Arrow marks Liolaemus crandalli type locality. Small red circles mark L. crandalli collection / observed localities. Orange dotted line marks distributional limits of species related to the Liolaemus elongatus clade; question mark in Chachahuen Mountains are populations of uncertain phylogenetic placement. Yellow dotted line marks Auca Mahuida Volcanic Field boundaries. Main mountains ranges, cities, and roads are marked. Colorado River drainage is marked in blue. Inset: Region in South America.

FIGURE 6. Type locality of Liolaemus crandalli. Upper: general view of the region around Park Ranger Station on Area Natural Protegida Auca Mahuida. Below: close view of the common outcrops where lizards were collected or observed basking or hiding in crevices.

Tables

TABLE 3. Morphometric and meristic variation in Liolaemus crandalli type series. Means and standard deviations (SD) of the main morphometric and meristic characters. Measures in mm and scale in numbers. AGD = axilla – groin distance, HL = head length, HW = head width, HH = head high, FL = foot length, TL = tibial length, AM = arm length, SAM = scales around midbody, DS = dorsal scales, VS = ventral scales, 4 TL = fourth toe lamellae, SL = supralabial scales, IL = infralabial scales, PC = cloacal pores, SVL = snouth-vent length.

	Males (N= 10)		Females (N= 11)
	Mean SD	Range	Mean SD	Range
SVL	83.21 7.23	70.5–93.4	80.49 6.25	68.9–90.6
AGD	32.95 5.79	22.1–42.1	36.44 4.94	28.1–46.0
HL	18.77 1.16	16.7–20.6	17.49 0.76	16.2–18.8
HW	15.08 1.11	13.2–16.5	14.38 1.10	12.7–15.9
HH	9.67 0.86	8.2–10.9	9.06 1.15	7.0–10.6
FL	23.51 1.15	21.2–25.1	23.17 1.02	21.3–24.5
TL	17.24 1.01	15.2–18.1	16.27 0.83	14.9–17.4
AL	23.29 1.33	21.6–25.3	22.56 1.44	20.8–25.5
SAM	84.6 4.24	77–92	84.45 5.75	75–94
DS	78.5 5.31	67–86	77.45 3.32	72–85
VS	132.8 5.18	125–139	131 4.49	120–137
4TL	29.1 1.91	27–33	27.90 2.02	25–31
SL	6.5 0.52	6–7	6.36 0.50	6–7
IL	4.4 0.51	4–5	4.18 0.40	4–5
PC	3.9 1.19	3–6	– –	–