Pholidobolus hillisi, Torres-Carvajal & Venegas & Lobos & Mafla-Endara & Sales Nunes, 2014

Torres-Carvajal, Omar, Venegas, Pablo J., Lobos, Simón E., Mafla-Endara, Paola & Sales Nunes, Pedro M., 2014, A new species of Pholidobolus (Squamata: Gymnophthalmidae) from the Andes of southern Ecuador, Amphibian & Reptile Conservation 8 (1), pp. 76-88 : 78-85

Pholidobolus hillisi sp. nov.

urn:lsid:zoobank.org:act:EB5A9DDD-742C-456F-B5C9-6E57EDEEE698

Proposed standard English name: Cuilanes of Hillis Proposed standard Spanish name: Cuilanes de Hillis

Holotype: QCAZ 4998 ( Figs. 1 , 2 ), adult male, Ecuador, Provincia Zamora-Chinchipe, near San Francisco Research Station on Loja-Zamora road, 3°57’57”S, 79°4’45”W, WGS84 , 1,840 m, 21 July 2012, collected by Santiago R. Ron, Andrés Merino, Fernando Ayala, Teresa Camacho, and Martin Cohen.

Paratypes (5): ECUADOR: Provincia Zamora-Chinchipe : QCAZ 4999 (adult male), 5000 (juvenile female), same data as holotype ; QCAZ 6840 (adult female), 6842 (adult female), 6844 (adult male), San Francisco Research Station , 3°58’14”S, 79°4’41”W , WGS84 , 1,840 m, 29 October 2004, 9 June 2005, and 29 September 2005, respectively, collected by Kristin Roos, Alban Pfeiffer, Andy Fries, Ulf Soltau, and Florian Werner.

Diagnosis: Pholidobolus hillisi is unique among species of Pholidobolus in having a distinct diagonal white stripe on each side of the chin, extending from the fourth genial to the fore limb ( Fig. 3 ). It further differs from all species of Pholidobolus , except P. affinis , in having three supraoculars (two in P. macbrydei , P. montium , and P. prefrontalis ). Pholidobolus affinis differs from the new species by having flanks with black reticulations on a reddish orange ground color (flanks brown in P. hillisi ; Fig. 4 ).

The new species also can be distinguished from P. montium and P. macbrydei by the presence of prefrontal scales (absent in the last two species). While P. hillisi shares with P. affinis and P. prefrontalis the presence of prefrontal scales, it differs from them in having a dark brown dorsum with a conspicuous light brown vertebral stripe (dorsum pale brown without a vertebral stripe in P. affinis and P. prefrontalis ; Fig. 4 ). Furthermore, P. hillisi has fewer dorsal scales in transverse rows (28–31) than P. affinis (45–55), P. montium (35–50), P. prefrontalis (37–46), and P. macbrydei (31–43).

Pholidobolus hillisi shares with all other recognized species of Pholidobolus the absence of a single transparent palpebral disc and the presence of a ventrolateral fold between fore and hind limbs. These characters distinguish members of Pholidobolus from members of its sister clade Macropholidus (Torres-Carvajal and Mafla-Endara 2013) .

Characterization: (1) Three supraoculars, anteriormost larger than posterior one; (2) prefrontals present; (3) femoral pores present in both sexes; (4) two to five opaque lower eyelid scales; (5) scales on dorsal surface of neck striated, becoming keeled from fore limbs to tail; (6) two or four rows of lateral granules at midbody; (7) 28–31 dorsal scales between occipital and posterior margin of hind limb; (8) lateral body fold present; (9) keeled ventrolateral scales on each side absent; (10) dorsum dark brown with a conspicuous narrow, pale brown, vertebral stripe that becomes grayish brown towards the tail; (11) labial stripe white; (12) sides of body dark brown; (13) white stripe along fore limb present; (14) a distinct diagonal white stripe on each side of the chin, extending from the fourth genial to the fore limb; (15) adult males with red flecks and ocelli (black with white center) dorsal to insertion of fore and hind limbs.

Description of holotype: Adult male (QCAZ 4998); snout-vent length 45. 52 mm; tail length 104 mm; dorsal and lateral head scales juxtaposed, finely wrinkled; rostral hexagonal, 2.09 times as wide as high; frontonasal pentagonal, wider than long, laterally in contact with nasal, smaller than frontal; prefrontals pentagonal, nearly as wide as long, with medial suture, laterally in contact with loreal and first superciliary; frontal hexagonal, longer than wide, slightly wider anteriorly, in contact with the prefrontals and supraoculars I and II on each side; frontoparietals pentagonal, longer than wide, with medial suture, each in contact laterally with supraoculars II and III; interparietal roughly hexagonal, lateral borders parallel to each other; parietals slightly smaller than interparietal, tetragonal and positioned anterolaterally to interparietal, each in contact laterally with supraocular III and dorsalmost postocular; postparietals three, medial scale smaller than laterals; supralabials seven, fourth longest and below the center of eye; infralabials five, fourth below the center of eye; temporals enlarged, irregularly hexagonal, juxtaposed, smooth; two large supratemporal scales, smooth; nasal divided, irregularly pentagonal, longer than wide, in contact with rostral anteriorly, first and second supralabials ventrally, frontonasal dorsally, loreal posterodorsally and frenocular posteroventrally; nostril on ventral aspect of nasal, directed lateroposteriorly, piercing nasal suture; loreal rectangular; frenocular enlarged, in contact with nasal, separating loreal from supralabials; supraoculars three, with the first being the largest; four elongate superciliaries, first one enlarged, in contact with loreal; palpebral disk divided into two scales, pigmented; suboculars three, elongated and similar in size; three postoculars, medial one smaller than the others; ear opening vertically oval, without denticulate margins; tympanum recessed into a shallow auditory meatus; mental semicircular, wider than long; postmental pentagonal, slightly wider than long, followed posteriorly by four pairs of genials, the anterior two in contact medially and the posterior two separated by postgenials; all genials in contact with infralabials; gulars imbricate, smooth, widened in two longitudinal rows; gular fold incomplete; posterior row of gulars (collar) with four scales, the medial two distinctly widened.

Scales on nape similar in size to dorsals, except for the anteriormost that are widened; scales on sides of neck small and granular; dorsal scales elongated, imbricate, arranged in transverse rows; scales on dorsal surface of neck striated, becoming keeled from fore limbs to the tail; number of dorsal scales between occipital and posterior margin of hind limbs 28; dorsal scale rows in a transverse line at midbody 30; one row of smooth, enlarged ventrolateral scales on each side; dorsals separated from ventrals by three rows of small scales at the level of the 13th row of ventrals; lateral body fold present; ventrals smooth, wider than long, arranged in 20 transverse rows between the collar fold and preanals; six ventral scales in a transverse row at midbody; subcaudals smooth; limbs overlap when adpressed against body; axillary region composed of granular scales; scales on dorsal surface of fore limb striated, imbricate; scales on ventral surface of fore limb granular; two thick, smooth thenar scales; supradigitals (left/right) 3/3 on finger I, 6/6 on II, 8/8 on III, 9/9 on IV, 6/6 on V; supradigitals 3/3 on toe I, 6/6 on II, 9/9 on III, 11/12 on IV, 8/8 on V; subdigital lamellae of fore limb single, 5/5 on finger I, 8/9 on II, 13/13 on III, 14/14 on IV, 8/9 on V; subdigital lamellae on toes I and II single, on toe III paired on the distal half, on toe IV all paired, on toe V paired at the base; number of subdigital lamellae (pairs when applicable) 6/5 on toe I, 9/9 on II, 13/14 on III, 19/20 on IV, 12/12 on V; groin region with small, imbricate scales; scales on dorsal surface of hind limbs striated and imbricated; scales on ventral surface of hind limbs smooth; scales on posterior surface of hind limbs granular; six femoral pores on each leg; preanal pores absent; cloacal plate paired, bordered by four scales anteriorly, of which the two medialmost are enlarged.

Measurements (mm) and proportions of the holotype: HL 12.6; HW 9.3; ShL 5.2; AGD 24.6; TL/SVL 1.72; HL/SVL 0.25; HW/SVL 0.18; ShL/SVL 0.10; AGD/SVL 0.48.

Hemipenial morphology ( Fig. 5 ): Both organs extend along approximately nine millimeters in length. The lobes of the organs are fully everted and each hemipenis is fully expanded.

The hemipenial body is roughly conical in shape, with the base distinctly thinner than the rest of the organ, ending in two small lobes with apical folds in the apex. The sulcus spermaticus is central in position, originating at the base of the organ, which bears a fleshy fold partially overlapping the sulcus spermaticus. From this point on, the sulcus proceeds in a straight line towards the lobes, and acquires an S-shape at the first third of the body. The sulcus becomes broader at halfway the length of the hemipenial body, and returns to its regular width at the apical region; it gets divided in two branches at the lobular crotch. Just before the crotch, the central region of the sulcus bears a tiny fleshy fold, which is not part of the sulcus division. From this point on, the two branches of the sulcus run on the medial regions of the lobes among conspicuous lobular folds. The sulcate face of the hemipenial body presents two nude areas, parallel to the sulcus spermaticus, which run throughout the hemipenial body, getting thinner and encircling the base of the lobes.

The lateral and asulcate faces of the hemipenial body are ornamented with 28–30 rows of roughly equidistant flounces with calcareous spinules. The first four rows are straight, with a large series of spinules on the central aspect of the asulcate face, and small isolated series of 5-6 spinules bordering the nude areas parallel to the sulcus spermaticus. A V-shaped nude area at the central asulcate face of the body separates the remaining flounces. The fifth and sixth flounces are also interrupted laterally by an extension of the basal nude area. From the seventh to the apical-most one, the flounces cross the lateral aspects of the organ from the sulcate to the asulcate face, initially in roughly straight lines, gradually assuming chevronshapes and getting reduced in length towards the apex of the organ.

The region between the asulcate and the lateral surfaces is marked by a conspicuous unevenness forming a bulge, which is shared by closely related species, such as Macropholidus annectens , M. huancabambae , M. ruthveni , Pholidobolus affinis , P. macbrydei , P. montium , and P. prefrontalis ( Nunes, 2011) .

Color of holotype in preservative: Dorsal background uniformly dark brown with a narrow light brown vertebral stripe extending from occiput onto tail; vertebral stripe slightly wider anteriorly; dorsal surface of head light brown medially (rostral, frontonasal, prefrontals, frontal and frontoparietals) and dark brown laterally (including supraoculars); white supralabial longitudinal stripe extending from first supralabial to fore limb; lateral aspect of neck dark brown with a dorsolateral light brown stripe that extends posteriorly along the flanks to the hind limbs; ventrolateral aspect of head and neck with a longitudinal white stripe extending posteriorly from fourth genial to insertion of fore limb and then laterally along

Torres-Carvajal et al.

upper arm; fore limbs with scattered ocelli (black with white center); flanks grayish brown with two dorsolateral stripes, the dorsal one light brown and the ventral one dark brown; tail light brown dorsally and dark brown on the sides; two and three well-defined, small ocelli (black with white center) dorsal to insertion of fore and hind limbs, respectively; ventral surface of head gray, with dirty cream genials and scattered brown marks; chest, belly and ventral surface of limbs and tail dark gray.

Variation: Measurements and scale counts of Pholidobolus hillisi are presented in Table 1. Superciliaries usually four, five in QCAZ 6840 ; supralabials usually seven (eight of left side of specimen QCAZ 6840 ) . Rows of lateral granules at midbody two ( QCAZ 4999 , 6844 ) to four ( QCAZ 6842 ) . Three specimens including the holotype, with a ventrolateral row of smooth enlarged scales ( QCAZ 4999 , 6840 ) . Specimen QCAZ 6842 has a tiny scale separating the cloacal scales posteriorly; all four scales bordering the cloacal plate anteriorly are similar in size in two specimens ( QCAZ 4999 , 6844 ) , whereas the lateralmost scales overlap the cloacal scales in one specimen ( QCAZ 6840 ) .

No variation was observed in color pattern in preservative among adult males. They can be distinguished from females by the presence of ocelli and pale flecks around insertion of fore and hind limbs. Moreover, the characteristic diagonal white stripe on each side of the chin that extends from the fourth genial to the forearm is more conspicuous in males than in females. Females are larger (maximum SVL 55. 7 mm, n =3) than males (maximum SVL 51. 1 mm, n =3).

Coloration in life of an adult male paratype ( QCAZ 4999 ) was similar to the holotype’s coloration in preservative described above, except that specimen QCAZ 4999 had small red flecks both at insertion of fore limbs extending onto sides of neck and at insertion of hind limbs extending onto base of tail. In addition, the lateral white stripe that starts on first supralabial extends further posteriorly along flanks in specimen QCAZ 4999 ( Fig. 4 ) .

Phylogenetic relationships: The maximum clade credibility tree resulting from the chronophylogenetic analysis supports inclusion of the new species within the Pholidobolus clade (Torres-Carvajal and Mafla-Endara 2013) with strong support (PP = 0.96; Fig. 6 ). Phylogenetic relationships among other species of Pholidobolus and species of Macropholidus are identical to those obtained by Torres-Carvajal and Mafla-Endara (2013). Macropholidus ruthveni is sister (PP = 0.99) to a clade containing both M. annectens and M. huancabambae (PP = 1). Pholidobolus macbrydei is sister (PP = 0.91) to a clade with the three remaining species of Pholidobolus ; the latter clade included P. prefrontalis as sister (PP = 0.99) to a clade containing P. affinis and P. montium as sister taxa (PP = 0.99). In contrast to the results reported by Torres-Carvajal and Mafla-Endara (2013), the chronophylogenetic tree inferred in this paper suggests that the diversification of the clades Macropholidus and Pholidobolus occurred at about the same time ( Fig. 6 ).

Distribution and ecology: Pholidobolus hillisi inhabits low montane forests in the eastern slopes of the Andes of southern Ecuador. This area represents a weather di- vide between the humid Amazon and the dry Inter-Ande- an regions ( Beck et al. 2008). The new species is known from Provincia Zamora-Chinchipe, at 1,840 m ( Fig. 7 ), in the deep valley of the Zamora river. The only gymnophthalmid species known to occur in sympatry with P. hillisi is Alopoglossus buckleyi , although P. macbrydei is parapatrically distributed ( Fig. 7 ). Two specimens (QCAZ 4998, 4999) were found under logs and rocks next to the Zamora river between 1130 hrs and 1145 hrs, whereas another specimen (QCAZ 5000) was basking on a rock next to the road at 1200 hrs. Other specimens (QCAZ 6840, 6842, 6844) were found and captured by a domestic cat around the San Francisco Research Station in pasture with interspersed shrubs.

Etymology: The specific epithet hillisi is a noun in the genitive case and is a patronym for David M. Hillis, who has had a great impact in the development of the field of molecular systematics (e.g., Hillis et al. 1996). In particular, he published a classic paper on evolutionary genetics of Pholidobolus lizards, where he compared some phylogenetic tree reconstruction techniques and emphasized the importance of phylogenetics in biogeography ( Hillis 1985).

Remarks: The Andes of southern Ecuador and northern Peru between 4°S and 7°S consist of relatively low-ele- vation mountains that create a mixture of environments. This region, known as the Huancabamba Depression, has long been recognized as a major biogeographic barrier for Andean organisms (e.g., Cadle 1991; Duellman 1979; Vuilleumier 1969). Although all species of Pholidobolus , except P. macbrydei , are restricted to the southern part of the northern Andes (i.e., Ecuador and southern Colombia), the new species described herein occurs on the northern limit of the Huancabamba Depression.

The Huancabamba Depression seems to have influenced the radiation of several Andean lizard clades, such as Stenocercus , Riama , Macropholidus , and Pholidobolus ( Doan 2003; Torres-Carvajal 2007; Torres-Carvajal and Mafla-Endara 2013). Except for Macropholidus , these clades have diversified along the northern Andes, suggesting that common geological or climatic events have influenced these radiations. The phylogenetic tree presented in this paper further supports the idea of a south-to-north sequence of speciation events ( Doan 2003; Torres-Carvajal 2007) which is congruent with the recent south-to-north uplift of the northern Andes (Simpson 1979; Aleman and Ramos 2000).

Acknowledgments. —We thank Santiago R. Ron for photographs and Andrea Varela for assembling some of the figures. Special thanks to Tiffany Doan and an anonymous reviewer for their valuable comments. OTC received funds from Secretaría de Educación Superior, Ciencia, Tecnología e Innovación (SENESCYT). PMSN is grateful to Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for financial support (Grant # 2012/00492-8). Specimens were collected under collection permit 001-11 IC-FAU-DNB/MA issued by Ministe- rio de Ambiente del Ecuador.

Figures

Fig. 1. Holotype (QCAZ 4998; SVL = 45.52 mm) of Pholidobolus hillisi sp. nov. in dorsal (A) and ventral (B) views. Photographs by OTC.

Fig. 2. Head of the holotype (QCAZ 4998) of Pholidobolus hillisi sp. nov. in dorsal (A), lateral (B), and ventral (C) views. Photo- graphs by OTC.

Fig. 3. Head of five species of Pholidobolus in ventral view. (A) P. affinis; (B) P. hillisi sp. nov.; (C) P. macbrydei; (D) P. montium; (E) P. prefrontalis. Photographs by OTC.

Fig. 4. Five species of Pholidobolus from Ecuador. (A) P. affinis; (B) P. macbrydei; (C) P. montium; (D) P. prefrontalis; (E) P. hillisi sp. nov. Photographs by OTC (A, B, C, D) and S. R. Ron (E).

Fig. 5. Left hemipenis of Pholidobolus hillisi sp. nov. (QCAZ 4999) in sulcate (left), lateral (middle), and asulcate (right) views. Photographs by P. Nunes.

Fig. 6. Maximum clade credibility tree inferred from the analysis of a dataset containing three mitochondrial genes under uncor- related, log normally distributed rates; branch lengths are in substitutions per site. Posterior probability values are shown above branches; asterisks correspond to values of 1.

Fig. 7.Distribution of Pholidobolus in Ecuador. P.affinis (white circles); P. macbrydei (blue circles); P. montium (green circles); P. prefrontalis (orange circles); P. hillisi sp. nov (red circle).