Phymaturus fiambala, Kottarathil & Kappalli, 2019

Kottarathil, Helna Ameri & Kappalli, Sudha, 2019, Fig. 1. Norileca indica and its protandrous hermaphroditic reproductive system. A in Chloeia incerta de Quatrefages 1866, Zoological Studies (Zool. Stud.) 58 (20), pp. 1-14 : 4-14

Family Liolaemidae Frost and Etheridge, 1989 Genus Phymaturus Gravenhorst, 1838

Phymaturus fiambala sp. nov. Lobo, Hibbard, Quipildor and Valdecantos ( Figs. 1 , 3–6 ) urn:lsid:zoobank.org:act:04F90EF0-A70A-49C4-A91F-A1FDFCB7466

Synonymy: Phymaturus sp5 : Lobo et al. 2012: 21. Phymaturus sp. fia: Lobo et al. 2016: 650.

Deposition of types: Holotype: IBIGEO 5756. Male ( Fig. 1 ). Paratypes: IBIGEO 5757–59, 5765, 5774 (4 adult males); 5769–70 (2 juvenile males). 5760–61, 63–64, 5766, 68 (6 females) deposited at the Reptiles collection of the Instituto de Bio y Geociencias del Noa (IBIGEO), Salta, Argentina. Site: 27.25583 S 67.20980 W; altitude: 4533 m. Locality: Cerca del Puesto de la lagunilla, Fiambalá Department, Catamarca Province, Argentina. Dates: 6 December 2017. Collectors: Thomas Hibbard and Matías Quipildor. MACN 51034- 035 (ex IBIGEO 5762, 5767). Same data, deposited at the Herpetological collection of the Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina. MCNUNSa 2122, 2123 (2 females, MCN-UNSa 2123 is voucher of DNA sequences), deposited at Museo de Ciencias Naturales, Universidad Nacional de Salta, Salta, Argentina. Locality: Puesto la Lagunita, 35–38 km NE of Medanitos, climbing from Medanitos, Fiambalá Department, Catamarca Province, Argentina. Dates: 23 March 2006. Collectors: Sebastián Barrionuevo, Juan Manuel Díaz Gómez and Sebastián Quinteros. MCNUNSa 2125 juvenile. Same data, deposited at Museo de Ciencias Naturales, Universidad Nacional de Salta, Salta, Argentina.

Diagnosis: Phymaturus fiambala sp. nov. Doral pattern with very thin spray, throats and chests light gray, rostral scales always undivided. Males with enlarged postcloacal scales, females with slender white transversal lines over trunk, enlarged scales on posterior gular fold, a patch of enlarged scales between gular folds evident, vertebral stripe absent.

Deposition of types: Holotype: IBIGEO 5756. Male ( Fig. 1 ). Paratypes: IBIGEO 5757–59, 5765, 5774 (4 adult males); 5769–70 (2 juvenile males). 5760–61, 63–64, 5766, 68 (6 females) deposited at the Reptiles collection of the Instituto de Bio y Geociencias del Noa (IBIGEO), Salta, Argentina. Site: 27.25583 S 67.20980 W; altitude: 4533 m. Locality: Cerca del Puesto de la lagunilla, Fiambalá Department, Catamarca Province, Argentina. Dates: 6 December 2017. Collectors: Thomas Hibbard and Matías Quipildor. MACN 51034– 035 (ex IBIGEO 5762, 5767). Same data, deposited at the Herpetological collection of the Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina. MCNUNSa 2122, 2123 (2 females), deposited at Museo de Ciencias Naturales, Universidad Nacional de Salta, Salta, Argentina. Locality: Puesto la Lagunita, 35–38 km NE of Medanitos, climbing from Medanitos, Fiambalá Department, Catamarca Province, Argentina. Dates: 23 March 2006. Collectors: Sebastián Barrionuevo, Juan Manuel Díaz Gómez and Sebastián Quinteros. MCNUNSa 2125 juvenile. Same data, deposited at Museo de Ciencias Naturales, Universidad Nacional de Salta, Salta, Argentina.

Description of holotype ( Fig. 1 ): Male. SVL 98.4 mm. Head length: 18.1 mm. Head width: 18.7 mm. Head height (at parietal): 8.2 mm. Axilla-groin length: 50.1 mm (50.9% of SVL). Tail length (complete, not regenerated): 71.3 mm to the point of regeneration. Body moderately wide, trunk width: 36.5 mm (37.1% of SVL). Twenty smooth dorsal head scales. Three scale organs in three postrostrals. Nasal bordered by ten scales, not in contact with rostral. Canthal separated from nasal by two scales. Loreal region flat. Twelve enlarged supralabial scales, none contacting subocular. Ten enlarged infralabials. Auditory meatus oval shaped (height: 3.9 mm; width: 2.1 mm) with four enlarged, flat and keeled backwardly projecting scales on the anterior margin. Auricular scale absent. Twelve convex, juxtaposed temporals. Auditory meatusciliary scales posterior commissure distance: 6.3 mm. Rostral undivided. Mental scale sub-pentagonal, in contact with six scales. Interparietal scale bordered by eight scales, being of larger size than postparietals. Frontal region without an azygous scale. Supraorbital semicircles inconspicuous. No distinctly enlarged supraoculars. Eleven juxtaposed superciliaries, seventeen upper ciliaries and sixteen lower ciliaries. Subocular fragmented in two scales. Fifteen lorilabials, without contacting subocular. Preocular larger than canthal, separated by one scale. Preocular separated from lorilabial row by three scales. Scales of throat round, small, and juxtaposed. Eighty-eight gulars between auditory meata. Lateral nuchal folds well developed, with granular scales over longitudinal fold. Antehumeral pocket well developed. Sixty-four scales between auditory meatus and shoulder. Fortyone scales between antehumeral fold and shoulder. In ventral view, anterior and posterior gular folds present, their anterior margins with two to three enlarged scales on their borders. Dorsal scales round, smooth and juxtaposed. Thirty-six dorsal scales along midline of the trunk in a length equivalent to head length. Scales around midbody: 178. Ventral scales larger than dorsals. Ventral scales between mental and precloacal pores: 187. Ten precloacal pores in an undivided row with two supernumerary pores. Two slightly enlarged postcloacal scales. Brachial and antebrachial scales smooth, with round posterior margins. Supracarpals laminar, round and smooth. Subdigital lamellae of fingers have three keels. Subdigital lamellae of finger (left manus) IV: 21. Claws moderately long (fourth toe’s claw: 2.6 mm). Supradigital lamellae convex, imbricate. Infracarpals and infratarsals have round margins and 2–3 keels. Supracarpals and supratarsals smooth, with rounded posterior margins. Subdigital lamellae of toe (left pes) IV: 25.

Coloration of holotype: the holotype exhibits a homogeneous yellow dorsal background, with small light brown scales scattered irregularly over all its body. Dorsum of tail of the same yellow coloration as trunk (no ringed or variegated pattern). Head uniformly light brown, with this coloration extended over the lateral neck folds. Throat immaculate light gray with no variegation. It has almost inconspicuous, very small and disperse spots, slightly darker than the background. Immaculate chest and belly entirely yellow from the anterior gular fold to the cloacal opening, extended over fore and hindlimbs and ventral surfaces of thighs and tail. Ventral surface of tail does not have any pattern.

Color of a female ( Fig. 2 ): background dorsal coloration light brown all over head, trunk, tail and limbs. Light brown coloration speckled with darker brown scales, which become confluent on the sides of neck and shoulders. Scapular spot conspicuous. Flanks with yellow coloration that extends to the belly as symmetrical patches. Most of ventral surfaces immaculate, light gray to white. Dorsal pattern of tail ringed. Ventral surface of tail lacks any kind of pattern.

Etymology: The species inhabits Sierra de Fiambalá (Fiambalá mountains). The toponym Fiambalá comes from an ancient language (Cacán) of natives who lived in northwestern Argentina before Quechua (Inca) and Spanish became dominant. “Cacán” voice: fiambalao (fiambal = wind; ao = house, place), meaning “house of winds”.

Variation: based on 16 adult specimens (7 males and 9 females). SVL 90.2–102.3 mm (x = 97.5; SD = 3.2) (two juveniles not included to avoid including ontogenetic variation). Head length 16.7–18.9% (x = 17.7%; SD = 0.7) of SVL. Tail length 0.80–1.08 (x = 0.96; SD = 0.08) times SVL. Scales around midbody 178–212 (x = 192.4; SD = 9.6). Dorsal head scales 15–22 (x = 18.6; SD = 1.9). Ventral scales 168–203 (x = 184.4; SD = 8.3). Scales surrounding interparietal 7–10 (x = 8.3; SD = 0.9). Scales surrounding nasal 7–10 (x = 8.4; SD = 0.9). Number of scale organs on postrostrals 1–3 (x = 1.1; SD = 0.5). Superciliaries 10–13 (x = 11.2; SD = 0.9). Subocular fragmented in half of the sample (ten specimens). Mental scale in contact with 6–7 (x = 6.1; SD = 0.3). Number of chinshields 2–7 (x = 4.5; SD = 1.8). All specimens exhibit enlarged scales on the border of the posterior gular fold (varying in number). Lorilabials 12–16 (x = 13.9; SD = 1.1). Enlarged scales on the anterior border of the auditory meatus 3–7 (x = 4.5; SD = 1.3) ( Fig. 3A ). Scales of neck along longitudinal fold from posterior border of auditory meatus to shoulder 60–76 (x = 68.4; SD = 4.6). Gulars 77–100 (x = 89.2; SD = 6.2). Scales between rostral and frontal 6–10 (x= 8.2; SD = 1.2). Subdigital lamellae on fourth finger 18–21 (x = 19.4; SD = 1.1). Subdigital lamellae on fourth toe 22–28 (x = 24.1; SD = 1.6). Males with 9–12 precloacal pores (x = 10.3; SD = 1.0). No females show precloacal pores. A small, newborn-sized individual was collected with 52.1 mm SVL (IBIGEO 5770). It shows two conspicuous enlarged postcloacal scales and a row of differentiated scales that will house later (at its maturity) precloacal pores ( Fig. 3B ). A juvenile male (IBIGEO 5769) with 78.2 mm SVL shows a row of differentiated scales but without pit or any signal of secretion. It has slightly conspicuous enlarged postcloacal scales and it exhibits a typical ringed tail as the smallest juvenile. Males ( Fig. 4 ) exhibit a yellow coloration all around their trunks. This color can be extended over tails, and in lesser degree over fore and hindlimbs. Dorsum and flanks speckled of dark brown/black scales that become more densely distributed in the neck and shoulders. Dorsal melanism of neck incomplete over the mid vertebral line (character 172). All males show a scapular yellow spot (character 139). Chest and abdomen immaculate yellow. Heads light brown, not a single specimen exhibits melanization common in the palluma group (character 124). Females ( Fig. 5 ) homogeneous brown (head, body, limbs and tail), their trunks speckled with black to dark brown scales. Lateral sides of neck, in several cases melanic, can be extended over the shoulders and the axilla. Scapular spot conspicuous in most females (character 140). Most females exhibit white slender transverse stripes across their backs (character 180). Ventral surfaces light gray almost white with a pair of yellow patches on the sides extended over flanks (character 183). Tails patterned (irregularly distributed darker spots) like in males but more conspicuous.

Distribution: At present, only known from its type locality.

Detailed comparisons to other members of the antofagastensis lineage

P h y m a t u r u s f i a m b a l a sp. nov. belongs to t h e a n t o f a g a s t e n s i s l i n e a g e b e c a u s e i t s h a r e s synapomorphies with all other members of the lineage: four discrete and three continuous characters (presence of flank color in females, loss of scale organ in mental, dark sides of neck speckled with small white spots among them) plus eight DNA changes (see below “Phylogenetic relationships”). Because of this, comparisons are restricted to all members of the lineage. Phymaturus fiambala sp. nov. males exhibit yellow tails continuing the same color of trunks, different from all other members of the mallimaccii subclade with males that exhibit brown tails (yellow tails are found in the vociferator clade, and the roigorum subclade).

Phymaturus fiambala sp. nov. differs from P. antofagastensis in that has a pattern of very thin spray, while P. antofagastensis exhibits a typical aggregated pattern ( Lobo and Quinteros 2005, fig. 12D) formed by larger brown spots irregularly distributed over its body. Males exhibit a yellow coloration covering head, trunk, limbs and tail ( Fig. 1 ) while in P. antofagastensis , yellow is more restricted to flanks, shoulders and neck, never shown in tails ( Fig. 6 ). Throats and chests in P. fiambala sp. nov. are light gray, being dark, almost completely melanic in P. antofagastensis . In P. fiambala sp. nov., granular scales among dorsal tibial scales are absent, while they are present in P. antofagastensis . In P. fiambala sp. nov. the rostral scale is always undivided, while 63% of studied individuals of P. antofagastensis show a divided rostral scale. In P. fiambala sp. nov., all males exhibit enlarged poscloacal scales (like in P. laurenti see Lobo et al. 2012c, fig. 3D) while only 37.5% of males of P. antofagastensis do. White transversal stripes are quite evident and wide in females of P. antofagastensis , but slender and almost inconspicuous in P. fiambala sp. nov. Also, P. fiambala sp. nov. shows significant differences in other five continuous characters ( Table 2): P. fiambala sp. nov. shows a larger SVL than P. antofagastensis , more lorilabials, superciliaries and gular scales, fewer scales between rostral and frontal, and fewer scales along midline of head (Hellmich’s index).

Phymaturus fiambala sp. nov. differs from P. mallimaccii in that males of the second species exhibit melanic throats, and several a very dark pattern formed by a dense distribution of small dark spots over dorsum. Also, in P. mallimaccii , a vertebral stripe is conspicuous, i.e., a vertebral stripe of a lighter coloration similar to the one shown by species of the punae lineage but absent in P. fiambala sp. nov. In P. mallimaccii , lateral neck folding is dark and speckled with small white spots even in males ( Fig. 6D ) but in certain individuals it is not so evident while in P. fiambala sp. nov. this character is absent. In P. fiambala sp. nov., enlarged scales on posterior gular fold and a patch of enlarged scales between gular folds are evident, while in P. mallimaccii they are inconspicuous or absent. Flank coloration in females of P. fiambala sp. nov. is yellow but orange in females of P. mallimaccii . According to statistical tests, P. fiambala sp. nov. have significantly larger SVL than P. mallimaccii , lower Hellmich’s index, fewer scales contacting interparietal, scales contacting mental ( Lobo and Quinteros 2005, fig. 9C & D), scales projecting on the anterior margin of the auditory meatus ( Fig. 3A ), scales between rostral and frontal but more lorilabial scales, gular scales and precloacal pores.

Phymaturus fiambala sp. nov. is different from P. laurenti in that the scapular spot is absent in P. laurenti , present in P. fiambala sp. nov. Flank coloration of females is orange in P. laurenti ( Fig. 3C ) but yellow in P. fiambala sp. nov. Tarsal scales in P. fiambala sp. nov. are strongly keeled but slightly keeled in P. laurenti . Enlarged poscloacal scales in males are larger in P. laurenti . Phymaturus fiambala sp. nov. lacks granular scales among dorsal tibial scales that are present in P. laurenti (see this character in Lobo et al. 2016, fig. 8F). Also, there are eight continuous characters that exhibit significant differences: P. fiambala sp. nov. has a larger SVL, lower Hellmich’s index, fewer subocular scales ( Lobo and Quinteros 2005, fig. 9A & B), scales contacting nasal, scales between frontal-rostral and more lorilabial scales, temporal scales and superciliaries scales, scales projecting over the auditory meatus and precloacal pores.

Phymaturus fiambala sp. nov. is different from P. denotatus in that this last species lacks enlarged postcloacal scales in males; it lacks a patch of enlarged scales in the center of chest between posterior gular folds (present in P. fiambala sp. nov.); throats of males are dark or completely melanic in P. denotatus males (light gray in P. fiambala sp. nov.); females of P. denotatus exhibit a well-differentiated pattern of dark neck folds speckled with small white spots ( Lobo et al. 2012c, fig. 2), almost absent in P. fiambala sp. nov. Phymaturus fiambala sp. nov. lacks granular scales among dorsal tibial scales that are present in P. denotatus ( Lobo et al. 2016, fig. 8F). Pattern of trunks in P. denotatus is formed by irregularly distributed small brown markings that are almost absent in P. fiambala sp. nov. (see figs. 1 and 2 of Lobo et al. 2012c) rostral scale can be divided in P. denotatus (36%) while this never happens in P. fiambala sp. nov., and also there are six continuous characters that exhibit significant differences: P. fiambala sp. nov. has fewer scales around midbody, subocular scales, scales contacting nasal, scales contacting mental, scales between frontal-rostral and a lower Hellmich’s index, but more gular scales, scales projected over auditory meatus and precloacal pores.

Phylogenetic relationships

The molecular analysis (all evidence available in GenBank, see supplementary file) with TNT recovered one most parsimonious tree of 2816 steps for the entire palluma group. The mallimaccii subclade is strongly supported (96% of jackknife). Phymaturus fiambala sp. nov. (sequences of the paratype MCNUNSa 2123) is found as sister to all other members of the antofagastensis lineage ( Fig. 7A ), P. mallimaccii is sister to the group formed by P. antofagastensis , P. laurenti and P. denotatus . Most of the nodes are well supported, with the exception of the one linking P. mallimaccii to the other species, the relationship between P. williamsi and P. bibroni and a basal node to these species plus P. williamsi , P. extrilidus and P. bibroni .

The reanalysis of the original matrix updated from Lobo et al. (2016), combining all DNA sequences available at GenBank and morphology, recovered four optimal trees of 3830,516 steps for the entire palluma group ( Fig. 7B ). In the present analysis, Phymaturus fiambala sp. nov. is recovered nested within the mallimaccii subclade, within the antofagastensis lineage , being sister to P. mallimaccii , basal to the node formed by P. antofagastensis and the sister species P. laurenti and P. denotatus . The antofagastensis lineage is supported (60% of jackknife) by three discrete characters: flank color in females (character 182 0 AE 1), acquisition of yellow flank color in females (character 183 0 AE 2), dark sides of neck speckled with small white spots (character 268 0 AE 1) (secondary loss in P. laurenti and P. antofagastensis ). Four continuous characters: decrease in the number of scales counted around midbody (character 3), decrease of the number of lateral scales on neck (character 5), increase of the number of scales in contact to interparietal (character 7), the supralabial scale upturned situated more posteriorly in the row (character 12), plus six nucleotide changes.

Phymaturus fiambala sp. nov. and P. mallimaccii as sister taxa are supported by four morphological discrete characters: rostral scale undivided (character 106 1 AE 0), scapular yellow to grey spot in males (character 139 0 AE 1), anterior projection of dorsal fascia melanism reaching the level over nuchal musculature (character 217 0 AE 1), dorsal tibial scales larger than anterior ones (character 221 0 AE 2). Four continuous characters: decrease in the number of scales counted around midbody (character 3), decrease in the number of scales contacting mental (character 14), decrease in the interorbit distance/head length ratio in females (character 26) decrease of the abdominal width/snout-vent length ratio (character 30). No DNA apomorphies.

Phymaturus antofagastensis is related to P. laurenti and P. denotatus supported by two discrete characters: lorilabial-subocular contact lost (character107 1 AE 2), 3-7 scales enlarged scales on the anterior border of the auditory meatus (character 165 1 AE 2), one continuous character: increase lateral rami / medial rami of interclavicle ratio (character 42). Five nucleotide changes.

Phymaturus laurenti and P. denotatus are closely related because they share nine synapomorphies: three discrete morphological characters, presence of enlarged scales on posterior gular fold (character 108 1 AE 2), sexual presence of sexual dimorphism in dorsal pattern (character 125 0 AE 1), parietal eye without opaque coloration conspicuous under corneal surface (character 175 1 AE 0). Three continuous characters, increase of subocular scales (character 13), increase of scales in contact to mental (character 14), increase number of scales separating the preocular from lorilabial row (character 17). Three nucleotide changes.

Genetic distances

Divergence among cyt b sequences are shown in table 1 among members of the mallimaccii subclade, three species of other palluma group species and P. indistinctus and P. somuncurensis ( patagonicus group). Phymaturus fiambala sp. nov. shows 1.4% distance from P. antofagastensis , 1.1% from P. denotatus (the shortest distances recorded). The shortest distance within the mallimaccii subclade is 0.6% between P. denotatus and P. antofagastensis , and 0.7% between P. extrilidus and P. bibroni . We found between P. denotatus and P. laurenti 0.0% of distance. Sequence used for P. laurenti is the one used by Morando et al. (2013), which belongs to a specimen collected at Cuesta de Randolfo that was considered P. laurenti in Lobo et al. (2010) before the discovery of P. denotatus (Lobo et al. 2012) . This population deserves to be re-evaluated, as it probably corresponds to P. denotatus . In a future contribution we will provide sequences from the type locality of P. laurenti . The average distance among members of the mallimaccii subclade is 1.9%, while that for the antofagastensis lineage is 1.1%. Average distance of P. dorsimaculatus and P. palluma from members of the mallimaccii subclade is 5.1%.

Figures

Fig. 1. (A) Dorsal view of the holotype of Phymaturus fiambala sp. nov. IBIGEO 5756. (B) Ventral view of the same specimen (Photos: M. Quipildor).

Fig. 3. (A) Details of the head in a female of Phymaturus fiambala sp. nov. (MCN-UNSa 2123); (B) newborn P. fiambala sp. nov. (IBIGEO 5770); (C) ventral view of females of P. laurenti; (D) females of P. denotatus. Character 35 (number of precloacal pores in males) 112 (row of precloacal pores); character 138 (1) presence of enlarged postcloacal scales in males; character 156 (1) preocular scale small separated from canthal by another scale; character 165 (1) three to seven enlarged scales on the anterior border of the auditory meatus; character 166 (0) enlarged scales on the anterior border of auditory meatus projected posteriorly over the ear opening (Photos: M. Quipildor).

Fig. 4. Homogeneous pattern and color of males of Phymaturus fiambala sp. nov. Character 124 (0): sides and dorsum of head melanism of mature males absent; character 111 (0): anterior gular fold absent; character 108 (1): presence of enlarged scales on posterior gular fold; character 113 (1): presence of supernumerary precloacal pores; character 139 (1): presence of a scapular yellow to grey spot in males; character 172 (1): dorsal melanism of neck incomplete over the mid vertebral line (Photos: M. Quipildor); character 116 (0): Throat of males immaculate; character 138 (1): Presence of enlarged postcloacal scales in males.

Fig. 5. Female variation of Phymaturus fiambala sp. nov. Character 140 (1): presence of a scapular yellow to grey spot (females); character 180 (1): females or/and juvenile with transversal lighter stripes (whitish) over their backs; character 183 (2): flank color in females yellow (Photos: M. Quipildor).

Fig. 6. Color in life of species of the Phymaturus antofagastensis lineage (males). (A) Phymaturus antofagastensis (Photo: S. Nenda); (B) Phymaturus laurenti (Photo: F. Lobo); (C) Phymaturus denotatus (Photo: D. Slodki); (D) Phymaturus mallimaccii (Photo: C. Abdala).

Fig. 2. (A) Dorsal view of a female of Phymaturus fiambala sp. nov. IBIGEO 5763. (B) Ventral view of the same specimen (Photos: M. Quipildor).

Fig. 7. Phylogenetic relationships recovered for the mallimaccii subclade of the Phymaturus palluma group. (A) based on all available DNA sequences of the genbank (P. aguanegra and P. sp. lar not included because the lack of data). (B) based on a combined data set of DNA sequences and morphology. We updated morphological information on the new species and other nine species and added 15 new characters to Lobo et al. (2016) and Hibbard et al. (2019) original data sets. Values under branches are Jackknife support calculated TNT v1.5. Running the analysis with only DNA sequences P. fiambala sp. nov. is basal to the remaining species of the antofagastensis lineage.