Research Article |
Corresponding author: Jaime Troncoso-Palacios ( jtroncosopalacios@gmail.com ) Academic editor: Johannes Penner
© 2016 Jaime Troncoso-Palacios, Alvaro A. Elorza, German I. Puas, Edmundo Alfaro-Pardo.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Troncoso-Palacios J, Elorza AA, Puas GI, Alfaro-Pardo E (2016) A new species of Liolaemus related to L. nigroviridis from the Andean highlands of Central Chile (Iguania, Liolaemidae). ZooKeys 555: 91-114. https://doi.org/10.3897/zookeys.555.6011
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The Liolaemus nigroviridis group is a clade of highland lizards endemic to Chile. These species are distributed from northern to central Chile, and currently there are no cases of sympatric distribution. This study describes a new species, Liolaemus uniformis sp. n., from this group, and provides a detailed morphological characterization and mitochondrial phylogeny using cytochrome-b. Liolaemus uniformis was found in sympatry with L. nigroviridis but noticeably differed in size, scalation, and markedly in the color pattern, without sexual dichromatism. This new species has probably been confused with L. monticola and L. bellii, both of which do not belong to the nigroviridis group. The taxonomic issues of this group that remain uncertain are also discussed.
Liolaemus nigroviridis , L. uniformis sp. n., lizard, Cyt-b , mtDNA
The Liolaemus nigroviridis group is a clade of highland lizards endemic to central and northern Chile, the species of which are allopatrically distributed (
Very few studies have used molecular data within this group.
In a field trip to the vicinity of Piuquenes (Valparaíso Region, Chile), we believe we found some populations probably previously assigned to Liolaemus monticola Müller & Hellmich, 1932 by
The current study describes this new species and provides a full diagnosis in regards to other species of the nigroviridis group. Although the color pattern of this new species resembles L. juanortizi and L. lorenzmuelleri, the scalation is markedly different and the distribution is allopatric (> 240 km of separation). Moreover, various taxonomical aspects of the nigroviridis group that require attention are discussed.
Specimens of all species currently considered within the nigroviridis group were examined. Morphological characteristics were examined according to
Samples from liver and thigh muscle were obtained from ethanol-fixed lizards which were subject to a rehydration process according to
The accession numbers of the Cyt-b mitochondrial loci sequences generated in this study and the sequences obtained from GenBank are indicated in Appendix II. Forty three nucleotide sequences involved in the analysis were aligned using MUSCLE (
The genetic tree constructed from mitochondrial DNA (mtDNA) (Fig.
Bayesian inference of phylogeny tree using Cyt-b showing phylogenetic relationships of Liolaemus uniformis sp. n. (red) and related species (HKY+G+I model). Liolaemus bellii and L. monticola, probably confused with the new species, are also in red. Posterior probability is indicated at each node. Scale shows the number of substitutions per site. Number between parentheses indicates the number of sequences for the collapsed nodes.
Liolaemus
altissimus
altissimus
(in part?),
Liolaemus
monticola
?,
SSUC Re 674. Adult male. Collected in the west shore of the Chepical Lagoon (32°15'S – 70°30'W), approximately 30 km NE Alicahue, San Felipe de Aconcagua Province, Valparaíso Region, Chile. Collectors: J. Troncoso-Palacios and E. Alfaro. December, 2012.
The species name “uniformis” (Latin) refers to the lack of dorsal pattern and uniform color found for both males and females.
Liolaemus uniformis is larger than L. constanzae (Mann–Whitney U = 0.5, P < 0.01, Table
Chilean species of the nigroviridis group (with the exception of Liolaemus nigroviridis), ordered from north to south. A Liolaemus constanzae, male from vicinity of San Pedro (picture by JTP) B L. melanopleurus, male from Atacama (picture by JTP) C L. isabelae, male from Montandón (picture by JTP) D L. juanortizi, unknown sex specimen from road to Negro Francisco (picture by F. de Grotee) E L. lorenzmuelleri, unknown sex specimen from Embalse La Laguna (picture by A. Labra) F L. maldonadae, male from vicinity of Alcohuaz (picture by JTP).
Scalation and morphological characteristics for the species of the nigroviridis group. Juvenile specimens examined are excluded. M = males; F = females. (*) Taken from
L. constanzae (M = 14, F = 13) | L. isabelae (M = 4) | L. juanortizi (M = 1) | L. lorenzmuelleri (M = 3, F = 5) | L. maldonadae (M = 3) | L. melanopleurus (M = 2) | L. nigroviridis (M = 9, F = 4) | L. uniformis sp. n. (M = 2, F = 3) | |
---|---|---|---|---|---|---|---|---|
Midbody scales | 54–64 | 54–60 | 54–59** | 50–62 | 58–64 | 42–56 | 55–64 | 58–62 |
Dorsal scales | 56–67 | 56–67 | 52 | 44–55 | 48–50 | 40–51 | 45–53 | 56–63 |
Vental scales | 86–96 | 86–97 | 88 | 86–96 | 83–91 | 91**** | 85–97 | 91–102 |
Nasal-rostral contact | 92.6% | 25% | 100% | 100% | 100% | 100% | 100% | 100% |
Sexual dichromatism | Present | Present* | Absent*** | Absent | ? | ? | Present | Absent |
Vertebral line (males) | Present | Present/ absent | Present/ absent | Present | Absent/ inconspicuous | Absent | Absent/ inconspicuous | Absent |
Maximum SVL (mm) | 75,3 | 82,8 | 94.4*** | 88.8 | 85.6 | 70.6 | 73,8 | 89.1 |
Liolaemus uniformis differs from L. isabelae (Fig.
Liolaemus uniformis resembles L. lorenzmuelleri (Fig.
Liolaemus uniformis differs from L. melanopleurus (a species with only three known specimens from an undetermined location, Fig.
Liolaemus uniformis differs from L. maldonadae (Fig.
Liolaemus uniformis is found in sympatry with L. nigroviridis (Fig.
Molecular data show that Liolaemus uniformis is not closely related to L. monticola (Fig.
Variation in species probably confused with Liolaemus uniformis sp. n. A L. monticola from Salto de Apoquindo (picture by JTP) B L. monticola from La Cruz Mountain (picture by J. Abarca-Díaz) C L. monticola from Provincia Mountain (picture by JTP) D L. bellii from La Parva (JR Martini) E L. bellii from Lagunillas (picture by JTP) F L. bellii from San Ramón Mountain (picture by JTP).
Molecular data show that Liolaemus uniformis is not closely related to L. bellii (Fig.
Adult male. SVL = 84.7 mm. Horizontal diameter of the eye: 4.3 mm. Subocular length: 4.5 mm. Length of the fourth supralabial: 4.1 mm. Head length (from the posterior border of the auditory meatus to the tip of the snout): 22.1 mm. Head height (distance between the two ear openings): 10.4 mm. Head width (at the level of ear openings): 15.8 mm. Neck width: 12.4 mm. Interorbital distance: 6.3 mm. Ear-eye distance: 7.5 mm. Internarine distance: 3.8 mm. Ear width: 2.5 mm. Ear height: 3.5 mm. Axillary-groin distance: 34.9 mm. Body width: 24.7 mm. Forelimb length: 25.7 mm. Hindlimb length: 46.1 mm. Length of the right hand: 10.4 mm. Length of the right foot: 22.4 mm. Tail length (not autotomized): 132.4 mm, with relation tail length/SVL = 1.56. Pentagonal rostral scale, wider (4.2 mm) than high (1.4 mm).
Two postrostrals. Four internasals. Heptagonal interparietal, with a central, small, and whitish central spot marking the position of the parietal eye. Interparietal smaller than the parietals, surrounded by seven scales. Seven scales between the interparietal and rostral. Thirteen scales between the occiput and the rostral. Orbital semicircle incomplete on the right side and complete on the left (formed by thirteen scales). Three supraoculars on the left side and four on the right. Six superciliary scales. Frontal area divided into three scales (1 posterior and 2 anterior). Preocular separated from the lorilabials by one loreal scale. Two scales between nasal and canthal. Nasal in contact with the rostral, surrounded by six scales. One row of lorilabials between the supralabials and subocular. Four lorilabials in contact with the subocular. Six supralabials, the fourth is curved upward without contacting the subocular. Four infralabials scales. Pentagonal mental scale, in contact with four scales. Four pairs of post-mental shields, the second is separated by two scales. Temporal scales smooth or slightly keeled, imbricated. Six temporal scales between the level of superciliary scales and the rictal level. Four scales on the anterior edge of the ear, which do not cover the auditory meatus. Poorly differentiated auricular scale, pentagonal and located at the upper part of the meatus. Thirty gulars between the auditory meatus. Lateral neck fold is “Y” shaped. Ventrolateral fold running from the neck to the groin. Dorsolateral fold slightly developed, running from the ear to the base of the tail. Midbody scales: 60. Dorsal scales are lanceolated, imbricated, keeled (without mucrons), with few interstitial granules. Dorsal smaller than the ventrals. Dorsal scales: 58. Ventrals scales are polymorphic (rounded, rhomboidal, pentagonal or hexagonal) smooth, imbricated, without interstitial granules. Ventrals: 91. Three precloacal pores. Supra-femoral scales lanceolate, imbricated, smooth or keeled. Infra-femoral scales lanceolate or rounded, smooth and imbricated. Supra-antebrachials scales are rounded or lanceolated, imbricated and smooth or keeled. Infra-antebrachials are rounded, imbricated and smooth. Dorsal scales of tail are pentagonal or rhomboidal, imbricated and keeled. Ventral tail scales are rounded or rhomboidal, smooth and imbricated. Lamellae of the fingers: I: 9, II: 13, III: 20, IV: 20 and V: 13. Lamellae of the toes: I: 11, II: 15, III: 21, VI: 27 and V: 17.
The specimen is notable for its lack of pattern and uniform color. The head is brown and darker than the body. There are several white dots dispersed over the head and cheeks. The dorsum is coppery brown and has a few white-spotted scales that did not form a pattern. The subocular is brown and crossed by three white, vertical lines. The dorsal surface of the tail is light brown and without a pattern. The limbs are a dorsal-brown, similar to the dorsal surface, with white dots dispersed on the forelimbs and white transversal lines on the hindlimbs. The flanks are whitish with abundant dark brown scales. Ventrally, the hands, feet, thighs, vent, and tail are yellowish. The belly is whitish with dark dispersed spots and a dark ventral stripe. The throat is whitish with a dark thick reticulation. The precloacal pores are orange.
Males are larger and more corpulent than females. In two males: SVL: 84.7–89.1 mm. Axilla-groin distance: 34.9–37.8 mm. Head length: 21.9–22.1 mm. Head width: 15.8–16.3 mm. Head height: 10.4–11.2 mm. Leg length: 45.4–46.1 mm. Arm length: 25.0–25.8 mm. Tail length: 132.4 mm in one specimen, with relation tail length/SVL = 1.56 (autotomized in the other). In three females: SVL: 67.7–73.1 mm. Axilla-groin distance: 33.1–35.7 mm. Head length: 17.8–20.0 mm. Head width: 11.8–13.3 mm. Head height: 7.5–8.3 mm. Leg length: 32.0–34.8 mm. Arm length: 19.2–21.3 mm. Tail length: 98.1 mm in one specimen, with relation tail length/SVL = 1.45 (autotomized in other).
The variation of the scalation in Liolaemus uniformis is as follows. Midbody scales: 58–62 (60.4 ±1.7). Dorsal scales: 56–63 (60.0 ±2.9). Ventral scales 91–102 (96.2 ±4.8). Fourth finger lamellae: 17–20 (19.0 ±1.4). Fourth toe lamellae: 25–27 (26.4 ±0.9). Supralabial scales: 6. Infralabial scales: 4–5 (4.4 ±0.6). Interparietal scale pentagonal, hexagonal or heptagonal, bordered by 5–7 scales (6.0 ±0.7). Nasal and rostral always in contact. Precloacal pores in males: 3. Precloacal pores are absent in females.
In general, all specimens have the pattern and color described for the holotype, with slight variations in shade. The male paratype has a dark brown throat. Two females have inconspicuous dark rings and an inconspicuous vertebral stripe on the dorsal surface of the tail. Also, two females have an olive hue on the snout. One female has a very inconspicuous series of dark crossbars on the paravertebral fields, which, while difficult to count, approximated eight. The juvenile has a similar pattern and color as the holotype, but it has an inconspicuous and fragmented dark vertebral line and inconspicuous dark spots on the paravertebral fields.
This species is currently only known from the type locality in the surroundings of the Chepical Lagoon, approximately 30 km NE of Alicahue, in the San Felipe de Aconcagua Province, Valparaíso Region, Chile (Fig.
Distributional map for Liolaemus uniformis sp. n. along with geographically proximate species of the nigroviridis group. Red star: L. uniformis sp. n., Chepical Lagoon, type locality. Green circles: L. nigroviridis (1 = Manque, 2 = El Arpa, 3 = Juncal, 4 = Riecillo, 5 = La Campana, 6 = El Roble, without number = near Chepical Lagoon). Pink squares: L. maldonadae (1 = near Alcohuaz, 2 = Los Molles). Yellow triangles: L. lorenzmuelleri (1 = Baños del Toro, 2 = Embalse La Laguna).
One of the collected specimens had a yellow flower inside of its mouth. An analysis of intestinal contents showed that L. uniformis is omnivorous; plant and Hymenoptera remains were found. A large quantity of nematodes from an unidentified species was found in the intestines. While the reproductive mode is yet unknown, at the time of sampling (December) no evidence of embryos was found but one female had several small oocytes. Comparisons with the reproductive modes of other species in the nigroviridis group would not be helpful as there is little available data. It is known that L. nigroviridis is viviparous (
Almost no molecular data are currently available for the nigroviridis group, probably due to the great difficulties of obtaining samples since all of these species inhabit high altitude mountainous areas (
We recognize that one limitation to our work is that it is based in a phylogenetic analysis of only one mtDNA gene and that a wider phylogenetic DNA analysis (including nuclear genes) should be conducted in the future. This is also true for most of the 21 species of Liolaemus (sensu stricto) described in the last five years, which have been classified through different methodologies in regards to DNA comparisons. For example, three species (L. chavin, L. pachacutec and L. wari) include data from two mtDNA genes and shared data in GenBank (
Although L. uniformis is strongly supported as a sister species of L. nigroviridis (pp = 1), a comprehensive phylogenetic study with more species of this group is needed. For example, L. isabelae was not placed within the nigroviridis group in a mitochondrial phylogenetic study that included one specimen (
Liolaemus uniformis resembles L. lorenzmuelleri and L. juanortizi in that the three species share a similar background dorsal coloration. Although no molecular data exists to compare L. uniformis with these two species, we propose that the marked differences in scalation and the strongly allopatric distribution (> 240 km of separation), which is quiet considerable for lizards, support classifying L. uniformis as a new taxon. Liolaemus uniformis has probably been misidentified as L. monticola by
Several aspects of the nigroviridis group remain uncertain. For example, L. nigroviridis possibly contains at least two species, the nominal species from the Andean highlands and populations from Coastal highlands, formerly L. n. campanae (
The present work contributes to the existing taxonomical knowledge, but the nigroviridis group of Liolaemus lizards remains poorly studied, and new samples are required to better investigate its challenging taxonomy.
We thank P. Zabala (Pontificia Universidad de Católica de Chile) for allowing us to review and deposit material in the collection under his care. We are grateful to H. Núñez (Museo Nacional de Historia Natural) and J. Artigas (Museo de Zoología de la Universidad de Concepción) for allowing us to review specimens; K. Kelly (Field Museum of Natural History) for providing photographs of one syntype of Liolaemus melanoplaurus; A. Labra, F. Lobo, R. Díaz and C. Garín for sending literature; and A. VanCott (BioPub Ltda.) for improving the English. H. Díaz for the distribution map. J. Troncoso-Palacios thanks M. Penna and A. Labra for their support. We also thank the three anonymous reviewers that contributed to improving the manuscript. Thanks to the Servicio Agrícola y Ganadero (SAG) for the collecting permit (N°4468). Red de Observadores de
Specimens examined. Acronyms are: Field Museum of Natural History (
Liolaemus bellii. MNHNCL 1599. Sewell, O`Higgins Region, Chile. Elgueta M. coll. December 1982. SSUC 201–05. Casa de Piedra, Farellones, Metropolitan Region, Chile. Ferri F. coll. 12/10/2010. SSUC Re 206–09. El Colorado, Farellones, Metropolitan Region, Chile. Ferri F. coll. 13/11/2011. SSUC Re 398–404, 543. El Olivares, Metropolitan Region, Chile. Garín C. coll. SSUC Re 562–66. La Parva, Metropolitan Region, Chile. Opazo J. coll. December, 2003. SSUC Re 654, 656. Lagunillas, Metropolitan Region, Chile. Esquerré D. 15/02/2015.
Liolaemus constanzae.
Liolaemus isabelae. SSUC Re 157, 159, 160. El Cerrito, Salar de Pedernales, Atacama Region. F. Ferri & J. Troncoso-Palacios colls. 22/02/2012. SSUC Re 158. Montandón, Salar de Pedernales, Atacama Region. F. Ferri & J. Troncoso-Palacios colls. 22/02/2012.
Liolaemus juanortizi.
Liolaemus lorenzmuelleri. MNHNCL 2401, 2403, 2404, 2406–08. El Indio, Baños del Toro, Coquimbo Region. H. Núñez & J.C. Torres-Mura colls. 18-22/12/1992. MNHNCL 1708. La Laguna, Valle del Elqui, 3300 m, Coquimbo Region. L. Contreras coll. December, 1982.
Liolaemus maldonadae. SSUC Re 304, 305, 560. Quebrada Los Piuquenes, Interior de Alcohuaz, Paihuano, Río Claro, Coquimbo Region. Troncoso-Palacios, J., F. Lobo, A. Laspiur & J.C. Acosta Colls. 10/02/2011.
Liolaemus melanopleurus. MNHNCL 1646 (2 specimens). Atacama. R.A. Philippi col.
Liolaemus monticola. SSUC Re 372–79. Camino a Farellones, Curva 20, Metropolitan Region, Chile. Ferri F. coll. 15/03/2012.
Liolaemus nigroviridis. MNHNCL 214–215. San Ramón, 3000 m, Metropolitan Region. H. Núñez coll. February, 1979. SSUC Re 016. El Yeso, Metropolitan Region. C. Garín coll. 01/04/2004. SSUC Re 190–200. Farellones, Casa de Piedra, Camino a Valle Nevado, Metropolitan Region. F. Ferri coll. 12/10/2010.
Liolaemus uniformis. SSUC Re 674–79. West shore of the Chepical Lagoon, approximately 30 km NE Alicahue, San Felipe de Aconcagua Province, Valparaíso Region, Chile. J. Troncoso-Palacios & E. Alfaro. December, 2012.
Specimens used for phylogenetic analysis.
mtDNA sequences obtained in this study. Liolaemus uniformis sp. n.: SSUC Re 674, KU095836. SSUC Re 677 KU095837. L. nitidus: SSUC Re 298, Dunas de Ritoqui, Valparaíso Region, Chile. KU095835. L. confusus: SSUC Re 356, Cerro Robles Riscos de Jote, O`Higgins Region, Chile. KU095832. L. curicensis: SSUC Re 253, Termas del Flaco, O`Higgins, Chile. KU095833. L. kuhlmanni: SSUC Re 285, Termas del Flaco, O`Higgins, Chile. KU095834. L. bellii: SSUC Re 208, El Colorado, Farellones, Metropolitan Region. KU095830. L. bellii: SSUC Re 209, El Colorado, Farellones, Metropolitan Region. KU095831.
mtDNA sequences obtained from GenBank. Liolaemus nigroviridis: Farellones. KC313199, KC313202, KC313203, KC313204, KC313205, KC313206, KC313208, KC313211, KC313207, KC313210, KC313209. L. monticola: Yerba Loca AY850619, Alfalfal AY850616, Maipú AY851724, Cuesta Chacabuco AY851718, Quebrada Alvarado AY851726, Colorado Norte AY851713, Cabrería AY851708, Rocín AY851710. L. tenuis: Termas de Chillán DQ989790. L. abdalai: Valle Chimehuin JN410525. L. alticolor: Huancarani KF923660. Santa Ana KF923659. L. austromendocinus: Nihuil AY173838. L. buergeri: El Planchón KJ494079, KJ494070, KJ494080. L. capillitas: Ruta Provincial AY173844. L. chiliensis: Termas de Chillan DQ989785, Las Trancas EU649245. L. cyanogaster: Tucapel DQ989786. L. dicktracy: Alto del Carrizal AY367816. L. elongatus: Esquel AY173801, Gobernador Costa AY173818, Los Manantiales AY173826, Laguna Blanca AY173855, Pampa de Lonco Luan AY173827, Las Ardillas AY173852. L. gununakuna: La Amarga AY367807, AY173859. L. incaicus: Urco KF923658, Lucre KF923657. L. kriegi: all from Río Negro Province AY173802, KJ494012, KJ494150, KJ494190, AY173814, KJ494155, KJ494191, KJ494188. L. neuquensis: Primeros Pinos AY173828. L. parvus: Quebrada Honda AY173836. L. petrophilus: El Cuy AY173796, Los Menucos JN847211, Ingeniero Jacobacci JN847103. L. pictus: San Carlos de Bariloche AY173795. L. punmahuida: Volcán Tromen AY173824. L. ramirezae: E Amaicha del Valle JN410520. L. robertmertensi: Tinogasta DQ989769. L. saxatilis: Achiras JN410553, Río Cuarto JN410527. L. smaug: Las Leñas AY173832, Mallines Colgados AY173830. L. talampaya: Las Yeguas River AY173797. L. tregenzai: all from Termas de Copahue AY367817, KJ494036, KJ494230, KJ494040, KJ494039, KJ494037, KJ494038. L. tulkas: Quebrada Las Angosturas AY367813. L. umbrifer: Quebrada de Randolfo AY367814. L. villaricensis: Volcán Villarrica AY850629, AY730671. L. zabalai: all from Biobío Region KJ494059, KJ494056, KJ494057, KJ494086, KJ494074, KJ494085. Phymaturus vociferator: Laguna del Laja JX969016. Phymaturus felixi: Paso de Indios JX969044.