Liolaemus qalaywa, Chaparro & Quiroz & Mamani & Gutiérrez & Condori & De & Herrera-Juárez & Cerdeña & Arapa & Abdala, 2020

Chaparro, Juan C., Quiroz, Aarón J., Mamani, Luis, Gutiérrez, Roberto C., Condori, Peter, De, Ignacio, Herrera-Juárez, Gabriela, Cerdeña, José, Arapa, Luis P. & Abdala, Cristian S., 2020, An endemic new species of Andean lizard of the genus Liolaemus from southern Peru (Iguania: Liolaemidae) and its phylogenetic position, Amphibian & Reptile Conservation (e 238) 14 (2), pp. 47-63 : 52-57

Liolaemus qalaywa sp. nov.

( Figs. 2–3 )

urn:lsid:zoobank.org:act:047FCD4E-8717-4378-B130-0B1BB633D187

Holotype. MUBI 13286 , an adult male ( Figs. 2–3 ) from Choaquere , District of Challhuahuacho , Province of Cotabambas, Department of Apurimac, Peru, (14°7’20.32”S, 72°13’29.27”W) at 3,740 m above sea level (m asl), collected on 15 December 2011, by L. Mamani and J.C. Chaparro.

Paratypes. Four adult males: MUBI 13265, from Ñahuinlla, District of Chorrillos, Province of Cotabambas, Department of Apurimac, Peru (13°57’20.64”S, 72°23’59.12”W) at 4,010 m asl, collected on 25 April 2016 by F.P. Condori; MUBI 12981, from Progreso, District of Progreso, Province of Grau, Department of Apurimac, Peru (14°5’16.07”S, 72°27’32.23”W) at 4,180 m asl, collected on 25 April 2016 by A.J. Quiroz; MUBI 17621, from Punchayoc Ccasa, District of Cotabambas, Province of Cotabambas, Department of Apurimac, Peru (13°47’23.55”S, 72°18’15.19”W) at 4,290 m asl, collected on 15 October 2019 by L. Mamani; MUBI 17622, from Ccosana, District of Haquira, Province of Cotabambas, Department of Apurimac, Peru (14°21’58.53”S, 72°20’40.10”W) at 4,615 m asl, collected on 16 October 2019, by L. Mamani. One subadult male: MUSA 5600, from Pumamarca, District of Challhuahuacho, Province of Cotabambas, Department of Apurimac, Peru (14°2’56.27”S, 72°19’46.10”W) at 4,615 m asl, collected on 10 December 2011 by A.J. Quiroz. Nine adult females: MUSA 5601 ( MUBI 12080), MUBI 12081, and MUBI 12084, from Chila, District of Challhuahuacho, Province of Cotabambas, Department of Apurimac, Peru (14°7’5.65”S, 72°13’48.97”W) at 3,750 m asl, collected on 24 May 2012 by J.C. Chaparro; MUBI 12100, from Choaquere, District of Challhuahuacho, Province of Cotabambas, Department of Apurimac, Peru (14°7’20.32”S, 72°13’29.27”W) at 3,740 m asl, collected between 30 May and 6 June 2012 by J.C. Chaparro; MUBI 13260 ( Fig. 3B,D,F,H ) and MUBI 13264, from Ñahuinlla, District of Chorrillos, Province of Cotabambas, Department of Apurimac, Peru (13°57’20.64”S, 72°23’59.12”W) at 4,010 m asl, collected on 25 April 2016 by F.P. Condori; MUBI 13287 from Pumamarca, District of Challhuahuacho, Province of Cotabambas, Department of Apurimac, Peru (14°2’56.27”S, 72°19’46.10”W) at 4,615 m asl, collected on 10 December 2011 by L. Mamani; MUBI 15900 and MUBI 15903, from Ccomerococha, District of Coyurqui, Province of Cotabambas, Department of Apurimac, Peru (13°50’44.99”S, 72°21’24.14”W) at 4,310 m asl, collected on 13 July 2016 by A. Quiroz. Thirteen immatures: MUBI 12982–83, from Progreso, District of Progreso, Province of Grau, Department of Apurimac, Peru (14°5’16.07”S, 72°27’32.23”W) at 4,180 m asl, collected on 25 April 2016 by A.J. Quiroz; MUBI 12096– 99 and MUBI 12101–04, from Choaquere, District of Challhuahuacho, Province of Cotabambas, Department of Apurimac, Peru (14°7’20.32”S, 72°13’29.27”W) at 3,740 m asl, collected on 30 May 2012 by J.C. Chaparro; MUBI 15901–02, from Ccomerococha, District of Coyurqui, Province of Cotabambas, Department of Apurimac, Peru (13°50’44.99”S, 72°21’24.14”W) at 4,310 m asl, collected on 13 July 2016 by A.J. Quiroz; MUBI 17623, from Ccosana, District of Haquira, Province of Cotabambas, Department of Apurimac, Peru (14°21’58.53”S, 72°20’40.10”W) at 4,615 m asl, collected on 16 October 2019 by L. Mamani.

Diagnosis. We assign L. qalaywa sp. nov. to the L. montanus group because it presents a blade-like process on the tibia, associated with the hypertrophy of the tibial muscle tibialis anterior ( Abdala et al. 2019b; Etheridge 1995) and based on molecular phylogeny ( Fig. 1 ). The species of the L. montanus group differ from those of the L. boulengeri group by the complete absence of patches of enlarged scales in the posterior part of the thigh ( Abdala 2007). Compared to the species of the L. montanus group, L. qalaywa sp. nov. is a robust lizard differing by its larger size (max SVL = 96.06 mm) from L. andinus , L. audituvelatus , L. balagueri , L. cazianiae , L. chiribaya , L. duellmani , L. eleodori , L. erguetae , L. erroneus , L. etheridgei , L. evaristoi , L. fabiani , L. famatinae , L. fittkaui , L. foxi , L. gracielae , L. griseus , L. hajeki , L. halonastes , L. huacahuasicus , L. insolitus , L. islugensis , L. molinai , L. montanus , L. multicolor , L. nazca , L. omorfi , L. orko , L. ortizi , L. pantherinus , L. poconchilensis , L. poecilochromus , L. porosus , L. pulcherrimus , L. reichei , L. robertoi , L. rosenmanni , L. ruibali , L. schmidti , L. stolzmanni , L. tajzara , L. thomasi , L. torresi , L. vallecurensis , and L. williamsi (all with SVL 50–80 mm). The presence of imbricate dorsal scales with keels differentiates L. qalaywa sp. nov. from species with smooth juxtaposed or sub-imbricate scales such as L. andinus , L. audituvelatus , L. balagueri , L. cazianiae , L. chiribaya , L. eleodori , L. erguetae , L. fabiani , L. foxi , L. gracielae , L. halonastes , L. insolitus , L. islugensis , L. jamesi , L. molinai , L. nigriceps , L. omorfi , L. patriciaiturrae , L. pleopholis , L. poconchilensis , L. poecilochromus , L. porosus , L. reichei , L. robertoi , L. robustus , L. rosenmanni , L. ruibali , L. schmidti , L. scrocchii , L. torresi , L. vallecurensis , L. victormoralesii , and L. vulcanus .

The new species differs from L. chiribaya , L. evaristoi , L. etheridgei , L. islugensis , L. insolitus , L. multicolor , L. omorfi , L. poconchilensis , L. pulcherrimus , L. robertoi , L. ruibali , and L. schmidti , by the absence of sky blue or celeste scales on the sides and dorsum of the body and tail. The number of scales around midbody in L. qalaywa sp. nov. varies between 52 and 58 (mean = 54.6), which differentiates it from several species of the group with more than 65 scales, such as L. andinus , L. annectens , L. audituvelatus , L. cazianiae , L. duellmani , L. eleodori , L. erguetae , L. forsteri , L. foxi , L. gracielae , L. halonastes , L. inti , L. molinai , L. multicolor , L. nigriceps , L. patriciaiturrae , L. pleopholis , L. poecilochromus , L. porosus , L. pulcherrimus , L. robertoi , L. rosenmanni , L. ruibali , L. schmidti , L. signifer , and L. vallecurensis . The number of ventral scales between the mental scale and the border of the vent in L. qalaywa sp. nov. varies between 71 and 83 (mean = 75.7), and is lower than the number in the following species (with more than 90 ventral scales): L. andinus , L. cazianiae , L. erguetae , L. foxi , L. gracielae , L. halonastes , L. inti , L. multicolor , L. nigriceps , L. pachecoi , L. patriciaiturrae , L. pleopholis , L. poecilochromus , L. porosus , L. robertoi , L. rosenmanni , L. torresi , and L. vallecurensis ; and higher than the number in the following species (with less than 70 ventral scales): L. dorbignyi , L. fittkaui , L. melanogaster , L. polystictus , and L. thomasi . Females of L. qalaywa sp. nov. exhibit precloacal pores in contrast to females of L. andinus , L. audituvelatus , L. aymararum , L. balagueri , L. duellmani , L. fabiani , L. fittkaui , L. griseus , L. hajeki , L. islugensis , L. jamesi , L. melanogaster , L. polystictus , L. puritamensis , L. reichei , L. robertoi , L. rosenmanni , L. ruibali , L. signifer , and L. vallecurensis (all lack precloacal pores). Additional measurements of morphometric characteristics in adult specimens are shown in Table 3 .

The coloration patterns of males and females (especially the deep yellow and orange color around the eye), of the palpebral scales, and on the posterior inner edge of the auditory meatus in females are character states that have not been reported in Liolaemus . This exclusive coloration pattern in both sexes was seen in different individuals throughout the year. Therefore, they differ from all known species in the L. montanus group.

Description of the holotype. Adult male ( MUBI 13286). SVL 85.54 mm. Head 1.08 times longer (20.24 mm) than wide (18.71 mm). Head height 15.9 mm. Neck width 20.5 mm. Eye diameter 4.67 mm. Interorbital distance 9.99 mm. Orbit-auditory meatus distance 8.71 mm. Auditory meatus 4.51 mm high, 1.53 mm wide. Orbit-commissure of mouth distance 7.35 mm. Internasal width 1.59 mm. Subocular scale length 5.3 mm. Trunk length 37.68 mm, width 28.7 mm. Tail length 110 mm. Femur length 16.03 mm, tibia 16.47 mm, and foot 22.8 mm. Humerus length 12.04 mm. Forearm length 10.91 mm. Hand length 14.11 mm. Pygal region length 7.67 mm, and cloacal region width 6.37 mm. Dorsal surface of head rough, with 13 scales, rostral 2.62 times longer (3.25 mm) than wide (1.24 mm). Mental larger (4.06 mm) than rostral, trapezoidal, surrounded by four scales. Nasal separated from rostral by two scales. Two internasals, longer than wide. Nasal surrounded by seven scales, separated from canthal by two scales. Six scales between frontal and rostral. Frontals divided into four scales. Interparietal larger than parietal, in contact with six scales. Preocular separated from lorilabials by one scale. Five superciliaries and 15 upper ciliaries scales. Three differential scales at anterior margin of auditory meatus. Six temporal scales. Five lorilabials in contact with subocular. Ten supralabials, which are not in contact with subocular. Seven supraoculars. Seven lorilabials. Six infralabials. Five chin shields, 4 th pair separated by six scales. Fiftysix scales around half of body. Fifty-four triangular dorsal body scales, imbricated, with an evident keel; fore and hind limbs and tail with lamellar scales, imbricated and keeled. Seventy-one ventral scales, from the mental to the cloacal region, following the ventral midline of the body, laminar, imbricated. Thirty imbricated gulars, not keeled. Neck with longitudinal fold with 43 granular, not keeled scales, ear fold and antehumeral fold present. Gular fold absent. Eighteen subdigital lamellae on the 4 th finger of the hand. Fourth toe with 23 subdigital lamellae with three keels, plantar scales with keels. Lamellar ventral tail, scales imbricated with a slight keel. Seven precloacal pores. Supernumerary pores present.

Coloration

Holotype coloration in preservative. Upper temporal area dark brown. Lower temporal region, supralabial, infralabial, lorilabial, and loreal scales white with dark edges. A transverse dark stain crossing the eye and the palpebral scales, the rest of it white. Lateral color of the neck white, back of the neck dark brown. Scales of body, limbs, and tail black with a white distal end. Irregular lines transverse to the body, white, with black edges, extending from one side of the body to the other. White spots on the back and sides of limbs, hands, tail, and scapular region. No vertebral line, dorsolateral bands, and ante-humeral arch. Sides of the body lighter below the lateral midline. Venter uniform, with white scales and black edges.

Color variation in life. Liolaemus qalaywa sp. nov. shows evident sexual dimorphism. In males, head varies considerably from brown to black. The back of the head is generally black or dark gray, in most cases darker than the sides of the head. The temporal region is similar in color to the back, but with lighter shades and in some specimens with white, yellow, or light gray spots. The supralabial, infralabial, and part of the lorilabial scales are always lighter than the rest of the head, sometimes immaculate or tinted with darker colors. The subocular, preocular, postocular, and loreal scales in most specimens are faint yellow, white, or light gray with light blue shades. The eyelid scales are always conspicuous, faint yellow, as are the posterior internal scales of the auditory meatus. In some specimens, the atrial scales, or part of them, also have the same yellow color as the palpebral scales. The general color of the body varies between chestnut and dark gray. Most of the dorsal scales of the body have a posterior end lighter than the anterior end, with yellow being the predominant color. The design of the dorsal body color pattern is diffuse and variable. Some males do not have paravertebral or lateral spots, while others exhibit thin, irregular, dark-colored transverse lines with a light back trim, with black and yellow being the most common combination. These lines can thicken or have a sub-quadrangular shape in the paravertebral region, and in some specimens the yellow lines fuse in the vertebral region. In the scapular region, numerous circular spots are highlighted, small in size and white, yellow, or light gray in color; these spots may also be present on the sides of the body, including some that are irregular or oblong in shape. The limbs and tail have the same pattern as the body. On the back of the limbs there are small light-colored spots, mostly intense yellow. The sides of the fingers and toes are faint yellow or white. In the antehumeral, pygal, and femoral regions, yellow shades stand out. Most specimens are white ventrally, but several specimens have black or dark gray scale edges in the mental, gular, pectoral, and abdominal regions. Some specimens have gray ventral scales with a light blue or light gray distal end. The tail generally changes to a lighter color after the first third. In females the coloration pattern is totally different and, unlike most Liolaemus species, the females have a more lively and showy coloration than males. The main difference is in the deep yellow color of the palpebral scales, those of the internal auditory meatus, the sides of the fingers and toes, as well as the back of the thighs and arms. As in males, the back of the head is darker than the sides. The predominant color on the back is dark brown. Small spots or white scales are present on the frontal and interparietal regions. The temporal region varies from brown to light gray. The supralabial, infralabial, and lorilabial scales are brown or light gray, with dark edges. The subocular, preocular, postocular, and loreal scales range from light gray to deep yellow. The color of the body varies from gray to brown and, like in the males, there are dark scales with a light distal end. The paravertebral spots are conspicuous and evident, generally black and diamond-shaped, which may be attached to a transverse black line that can extend to the vertebral zone and to the mediolateral line on the sides of the body. These paravertebral spots in some cases have a white anterior border. The sides of the body, humeral area, limbs, and tail have similar patterns as the males. Ventrally they are white or gray with some yellow undertones. In the gular and mental regions there may be dark spots and nuances, while on the belly some have iridescent scales that are greenish gray or bluish gray. The tail becomes darker distally.

Etymology. The specific epithet Qalaywa, refers to the Quechua word for the Liolaemus lizards from the high Peruvian Andes.

Distribution and natural history. All known specimens and observations of L. qalaywa sp. nov. come from the 12 localities of the type series, in the southeastern Department of Apurimac, Peru, at elevations between 3,740 –4,615 m asl ( Figs. 4–5 ). This species inhabits high Andean puna ( Figs. 4–5 ). Within the geographical distribution of L. qalaywa sp. nov., four vegetation units were determined: Wetlands, Puna Lawn, Grassland, and Bushes. The common floristic composition of each unit is as follows—Wetlands: Distichia muscoides, Zameoscirpus muticus, Carex sp. , Eleocharis albibracteata , Calamagrostis rigescens , and Oritrophium limnophyllum ; Puna Lawn: Aciachne acicularis , Calamagrostis vicunarum , Paranephelius ovatus , and Trichophorum rigidum ; Grassland: Jarava ichu , Festuca dolichophylla , and Calamagrostis sp. ; and Bushes: Ribes sp. , Gynoxis sp. , Escallonia myrtylloides , and Berberis sp. Liolaemus qalaywa sp. nov. inhabits all the vegetation units, but in wetlands the presence of lizards is restricted to the edges. During intensive field work in the study area, the presence of adult individuals was registered throughout the year; newborns (with presence of abdominal scar) appeared from November to March, and immatures were found from December to March. In December, some couples showing reproductive behavior were observed. The species presents a viviparous reproduction; an embryo was found inside the body of an adult female. Sympatric amphibian and reptile species include Gastrotheca marsupiata , Pleurodema marmoratum , Telmatobius cf. jelskii , Liolaemus aff. incaicus , and Tachymenis peruviana .

Individuals were registered and collected during the dry and wet seasons, in natural rocky areas (under rocks when hiding and on rocks when active). One of the authors spent 82 person-hours of search time, between 0815 and 1500 hrs distributed from 2013 to 2019; and the total captures (catch and release) were 249 individuals, 147 in the wet season and 102 in the dry season (97 males, 113 females, and 39 immatures). The average results of our records in areas with different degrees of impact per hour of effort varied: in natural areas without anthropic intervention, five individuals/hour of search were registered; in natural areas with little human impact, three; in agricultural areas (which include sectors with stones or rocky outcrops) 1.5; and in very impacted areas (including areas with removal of land and vegetation, like mining, roads, and buildings) the result was zero individuals per hour. In general, our observations show that L. qalaywa sp. nov. is abundant in sectors where the habitat remains intact, especially in areas with the presence of natural rock outcrops and scattered stones which serve as permanent or temporary shelters. However, in areas with the presence of agricultural, livestock, and open-pit mining activities, abundance tends to decrease, as the lizards maintain their populations at the perimeters of zones with anthropic activities.

Individuals of this species are capable of building their own burrows and taking advantage of the burrows of other animals, such as tarantulas and mice; in the same way, arachnids, insects, and small mammals use the lizard’s shelters. Several individuals were observed thermoregulating on small and medium-sized stones, and on stony sandy substrate and grass-like vegetation, always near their shelters. The peak of activity was during 0900–1100 hrs.

The presence of ectoparasites of the family Trombiculidae was recorded throughout the year; however, the presence and density of ectoparasites seemed to be lower during December–March, increasing in number during April–November. The ectoparasites were found distributed in the mite pocket, tympanic duct, prefemoral region, inguinal pocket, and axillary pocket.

An adult male individual of L. qalaywa sp. nov. was registered eating a frog of the species Pleurodema marmoratum , when it was under a stone. Other individuals were seen consuming insect larvae.

Male-male interactions were observed, including aggressive behavior by back arching, followed by a mutual lateral presentation that ends with one lizard charging and biting the other, and the persecution from the winner to the loser. Also, when the lizards sense danger, such as when researchers try to capture them, they show back arching and opening of the mouth, producing an exhalation-like sound.

Figures

Fig. 2. Details of the holotype of Liolaemus qalaywa sp. nov. MUBI 13286 (SVL = 85.54 mm, Tail = 110 mm): (A) dorsal and (B) ventral views of body, (C) lateral, (D) dorsal, and (E) ventral views of head, (F) ventral view of precloacal pores, (G) ventral aspect of right hand, (H) ventral aspect of right foot, (I) keeled dorsal body scales, (J) ventral body scales. Scale = 5 mm.

Fig. 3. (A, C, E, G) Adult male of Liolaemus qalaywa sp. nov. (unvouchered specimen; SVL = 91.9 mm, Tail = 121.1 mm); (B, D, F, H) Adult female of Liolaemus qalaywa sp. nov. (MUBI 13260 paratype; SVL = 85.53 mm, Tail = 110.78 mm). Both individuals are from Ñahuinlla, Department of Apurimac, 4,010 m asl.

Fig. 1. Phylogenetic tree obtained using Bayesian Methods (BM).

Fig. 4. Habitat of Liolaemus qalaywa sp. nov. from localities in the Department of Apurimac: (A) Quequello; (B) Ñahuinlla; (C) Huanquere; (D) Choaquere; (E) Queuña; (F) Ccomerococha; (G) Huanacopampa.

Fig. 5. Geographic distribution of 17 formally described species, and three candidate species of Liolaemus. Symbols with a black dot in the middle represent the type locality of each species. Species with quotation marks in names belong to the candidate species.

Tables

Table 3. Measurements (in mm) of morphological characteristics in adult specimens of Liolaemus qalaywa sp. nov. * broken tail, ** regenerated tail.

Museum code	MUBI 13286	MUSA 5600	MUBI 13287	MUBI 13264	MUBI 13260	MUBI 12100	MUBI 12084	MUBI 12081	MUBI 12080
Stage of development	Adult	Subadult	Adult	Adult	Adult	Adult	Adult	Subadult	Subadult
Sex	Male	Male	Female	Female	Female	Female	Female	Female	Female
Type material	Holotype	Paratype	Paratype	Paratype	Paratype	Paratype	Paratype	Paratype	Paratype
Snout-vent length	85.54	79.25	79.35	77.23	85.53	79.43	79.75	68.51	74.78
Head length	20.24	18.86	18.09	16.85	19.34	17.23	18.20	16.04	16.89
Head width	18.71	13.35	17.32	15.46	16.71	15.45	15.75	14.10	15.66
Head height	15.90	10.64	12.36	12.54	12.10	12.50	11.64	9.68	11.03
Interorbital distance	9.99	8.25	9.16	8.90	9.30	8.99	9.06	8.50	8.99
Tail length	110.00	103.44	86.15 (*)	108.57	110.78	59.45 (**)	64.44 (**)	87.87	99.88
Cloacal opening width	12.76	9.56	10.74	10.64	11.64	9.69	13.14	10.77	11.49
Body width	28.70	17.42	26.85	24.41	34.34	29.34	30.28	22.06	26.18
Width of base of tail	37.68	33.67	40.20	38.28	37.34	42.76	36.52	28.87	32.61
Femur length	16.03	15.16	13.60	14.32	15.48	13.63	14.36	12.37	13.79
Tibia length	16.47	15.86	14.41	13.98	14.36	13.21	13.94	13.04	13.41
Foot length	22.80	19.12	19.67	19.24	20.17	18.62	19.03	18.00	19.65
Length of claw of the 4th toe	14.39	11.35	12.61	12.53	12.92	11.11	12.18	11.50	12.22
Humerus length	12.04	10.73	8.74	9.78	10.15	9.26	9.62	7.45	9.08
Humerus width	7.03	3.91	5.90	5.45	5.93	5.24	5.27	4.65	5.00
Radio length	10.91	9.93	9.45	9.68	9.54	8.63	8.99	8.76	8.84
Hand length	14.11	10.27	14.02	12.88	11.84	11.07	10.96	10.88	12.53
Tympanum height	4.51	3.57	3.91	3.85	4.16	3.64	3.72	3.36	3.18
Tympanum length	1.53	1.72	1.07	1.20	1.66	1.18	1.62	1.49	1.27
Neck width	20.50	13.10	17.40	15.62	17.44	15.11	17.43	14.46	18.00