Dendropsophus norandinus, Rivera-Correa, Mauricio & Gutiérrez-Cárdenas, Paul David Alfonso, 2012

Rivera-Correa, Mauricio & Gutiérrez-Cárdenas, Paul David Alfonso, 2012, A new highland species of treefrog of the Dendropsophus columbianus group (Anura: Hylidae) from the Andes of Colombia, Zootaxa 3486, pp. 50-62 : 51-59

Dendropsophus norandinus sp. nov.

( Fig. 2 )

Holotype. MHUA-A 3781, adult female, Colombia, departamento de Antioquia, municipio de Anorí, vereda El Roble, Bosque La Forzosa, 06º58’50’’N, 75º08’07’’W, ca. 1700 m a.s.l., November 14, 2003, collected by Mauricio Rivera and Paula Mejía.

Paratypes. 15 adult males (MHUA-A 3768-3777, 3786-3790) and seven adult females (MHUA-A 3778-80, 3782-85), collected with the holotype; MHUA-A 4092, adult female, Colombia, departamento de Antioquia, municipio de Anorí, vereda el Retiro, finca El Chaquiral, 6°58.8’ N, 75°7.83’W, ca. 1732 m a.s.l., November 26, 2005, collected by Taran Grant and Paul D. Gutiérrez. MHUA-A 5274, adult male, Colombia, departamento de Antioquia, municipio de Amalfi, vereda Salazar, Finca Bodega Vieja, ca. 1440 m a.s.l., July 6–7, 2006, collected by Marco Rada. MHUA-L 0 152, (13 tadpoles), Colombia, departamento de Antioquia, municipio de Anorí, vereda El Roble, Bosque La Forzosa, 06º58’50’’N, 75º08’07’’W, ca. 1700 m a.s.l., November 2005, collected by Paul D. Gutiérrez. MHUA-L 0 153, (9 tadpoles), Colombia, departamento de Antioquia, municipio de Amalfi, vereda Salazar, Finca Bodega Vieja, ca. 1440 m a.s.l., July 6–7, 2006, collected by Marco Rada.

Diagnosis. We assigned the new species to the genus Dendropsophus because of the reduced labial tooth row formula in tadpoles ( Duellman & Trueb 1983), overall similarity with other species of the genus ( Fig. 1 ) and DNA sequences similarity. A blast of a fragment (585 bp) of the 16S rRNA to sequences deposited in Genbank retrieved D. carnifex as the most similar sequence (Max ident = 94.88%). Dendropsophus norandinus is distinguished from other species of Dendropsophus by the following combination of traits: 1) SVL in adult females ( Fig. 2 ) 30.4–35.8 (n = 9), in adult males 24.8–27.8 (n = 15); 2) snout short, rounded in dorsal view and slightly rounded in lateral view, head wider than long; 3) canthus rostralis rounded in cross-section, loreal region slightly concave; 4) tympanum rounded, tympanic annulus distinct, upper edge covered by a supratympanic fold; 5) vomerine teeth prominent, left and right odontophores separated medially, between choanae; 6) skin on dorsal surfaces smooth, with some minute scattered tubercles; 7) axillary membrane present and developed; 8) discs relatively wide, webbing formulae of fingers I (2–2 1/2)–2- II 1 1/2–(2-–2 1/2) III (2-–2 1/2)– 2 IV, webbing formulae of toes I (1–1+)–(1 1/ 2–1 3/4) II 1 –(2–2-) III 1 –(2–2-) IV (2–2-)– 1 V; 9) bifid distal subarticular tubercle in the fourth finger; 10) in life, ventral surfaces cream with brown marks on the gula, throat, and the lateral areas of the belly in females; 11) medial area of the belly immaculate; 12) in life, dorsum reddish brown in females and cream or silver grey in males 13) in life, axilla and groin bright orange in females and pale yellow in males; 14) light gray iris with gold and copper chromatophores and purple dark blotches; 15) pupil horizontal, palpebral membrane translucent.

Comparisons with similar species. Dendropsophus norandinus is most similar to the species of the D. columbianus and D. garagoensis groups than to species of the D. labialis group, and is distinguished from these by the following characteristics (those of D. norandinus in parenthesis). Dendropsophus bogerti (Cochran & Goin) and D. columbianus (Boettger) have head longer than wide (wider than long); finger webbing absent (present between fingers III and IV) and toe webbing never starting of the base of the disc (starting in the base of the disc of toes I, II, and III). Additionally, the females of Dendropsophus bogerti and D. columbianus in life have belly yellow or orange with brown blotches and reticulated pattern in the medial area, being more conspicuous in D. columbianus (cream belly with a spotted pattern and markings only in the flanks and never in medial area of belly; Fig. 3 B, C); tadpole with labial tooth row formula 1/2 and anterior region of caudal musculature less than 40% of body height (0/2 and musculature more wide, 60% of body height). Dendropsophus carnifex (Duellman) have head longer than wide (wider than long); yellow belly in life (cream belly); absence of axillary membrane (axillary membrane present); tadpole with labial tooth row formula 1/2 and anterior region of caudal musculature less than 50% of body height (0/2 and musculature more wide, 60% of body height) and a genetic distance of 5.12% in a fragment 585 pb of mitochondrial DNA sequences between D. carnifex and D. norandinus . Dendropsophus garagoensis (Kaplan) possesses a dorsolateral narrow light green stripe with brown borders from the tip of the snout to the groin (stripe absent); without dark flecks or marks in the gula (dark brown marks present; Fig. 3 D); toe webbing less extensive, I 2 – 2 1/2 II 1 1/2 – 3- III 1 1/2 – 3- IV 3 - – 1+ V [more extensive, I (1 – 1+) – (1 1/2 – 1 3/4) II 1 – (2 – 2-) III 1 – (2 – 2-) IV (2 – 2-) – 1 V]. Dendropsophus labialis (Peters) with snout short somewhat triangular in dorsal view (short and rounded); canthus rostralis moderately defined (rounded); loreal region nearly flat and slightly oblique (slightly concave); a black line extending from the canthus rostralis back over the tympanum to widen and fade out the body (absent); axillary membrane well developed bright blue (axillary membrane developed bright orange or pale yellow); axilla and groin blue (bright orange in females and pale yellow in males); vomerine teeth small, odontophores close together between choanae (vomerine teeth prominent, odontophores separated medially) and a genetic distance of 6.90% in a fragment 585 pb of mitochondrial DNA sequences between D. labialis and D. norandinus . Dendropsophus meridensis (Rivero) with black and yellow mottling or marbling on flanks, axilla, groin, ventral parts of the hind limbs, and posterior parts of thighs (absent); ventral surfaces yellowish orange (cream); tadpole with labial tooth row formula 2(2)/2 and oral disc with multiple rows of papillae (0/2 and a single row of papillae present) ( Rivero 1961; Mijares-Urrutia 1990). Dendropsophus padreluna (Kaplan & Ruiz) have black spots on anteroventral and posterodorsal surfaces of thighs (thighs without spots; Fig. 3 E); finger II> IV (finger II <IV); a dorsolateral striped extending from the canthus rostralis to the end of body (absent). Dendropsophus pelidna (Duellman) with snout long (short); head as wide as long (wider than long); webbing absent between fingers I and II (more extensive, I 2–2 - II); relative length of toes 1<2<3<5<4 (1<2<3=5<4); venter white with bluish gray suffusion (cream with brown marks in females); flanks areolate (smooth); throat coarsely granular (smooth); ventral surfaces of thighs coarsely granular (finely granular); axilla, groin and hidden surfaces of limbs mottled black and blue (bright orange in females and pale yellow in males); iris deep bronze (light gray) ( Duellman 1989). Dendropsophus praestans (Duellman & Trueb) possesses bluish grey groin with black spots (orange groin in females and pale or light yellow in males); lacks ulnar tubercles (always with ulnar tubercles); abundant spots in the medial area of the belly and thighs present (medial area of the belly and thighs immaculate; Fig. 3 F;). Dendropsophus virolinensis (Kaplan & Ruiz) has dorsolateral stripe narrow of uniform widths and bordered by black pigment (stripe absent); an indistinct tympanic annulus (tympanic annulus distinct and conspicuous); absence of axillary membrane (axillary membrane present).

Description of holotype. Adult female; SVL 35.8; head slightly narrower than the body, wider than long (HW/ HL = 1.17%; Table 1); snout short, rounded in dorsal view ( Fig. 4 A), slightly rounded in lateral view ( Fig. 4 B); distance from nostril to eye less than diameter of eye ( END /ED = 0.76%); canthus rostralis indistinct, rounded; loreal region slightly concave, slightly sloping to upper lip; internarial area depressed; nostrils barely protuberant, openings directed laterally; eye large, its diameter about three times depth of lip below eye; tympanic membrane round, distinct, its diameter about one third of eye length, separated from eye by a distance equal to its diameter; tympanic annulus distinct ventrally, barely hidden dorsally; supratympanic fold evident conspicuous, inclined posteroventrally.

Forelimbs not hypertrophied; axillary membrane present, extending along proximal two fifths of upper arm; minute ulnar tubercles present along the ventrolateral edge of the forearm; fingers short, bearing round discs, wider than digit; relative length of fingers I<II<IV<III ( Fig. 4 C); distal subarticular tubercle in fourth finger bifid; supernumerary tubercles very small, barely detectable; palmar tubercle flat, elliptical; thenar tubercle large, flat, elliptical; nuptial excrescences absent; finger webbing formula I 2–2 - II 1 1/2–2- III 2 -– 2 IV ( Fig. 4 C). Hind limbs long, slender, lacking calcar tubercles, tarsal fold absent, but some tarsal tubercles presents; toes moderately long, bearing round discs, slightly smaller than finger discs; relative length of toes 1<2<3=5<4 ( Fig. 4 D); outer metatarsal tubercle small, round, inconspicuous; inner metatarsal tubercle large, flat, elliptical; subarticular tubercles small, subconical; supernumerary tubercles minute, subconical, numerous on proximal segments of each digit; toe webbing formula I 1–1 1/ 2 II 1– 2 III 1–2- IV 2– 1 V ( Fig. 4 D).

Skin on head, dorsum, and dorsal surfaces of limbs smooth with few scattered minute tubercles; skin on flanks, throat and neck smooth; skin on belly coarsely granular; skin on another ventral surfaces and proximal area of thighs finely granular. Cloacal opening directed posteriorly at upper level of thighs; cloacal sheath short, covering upper edge of cloacal opening; cloacal folds absent; minutes scattered cloacal tubercles present. Vomerine odontophores prominent, posteromedially inclined, moderately separated medially, between posterior border of choanae, bearing each, five vomerine teeth; tongue approximately round, barely notched and free posteriorly; pectoral fold absent.

Coloration of holotype in life. Coloration between night and daylight was not observed to vary. Dorsal surfaces of head, body, and limbs reddish brown with numerous small and scattered dark brown spots and markings. Region around nostrils dark brown; supratympanic fold dark brown, tympanic annulus pale brown, tympanic region dark brown; upper lip slightly pale brown, with scattered melanophores and distinct cream spots below the eye; light gray iris with gold and copper chromatophores and purple dark blotches; eyelid without pigmentation. Axilla, groin, anterior and posterior surfaces of thigh, and anterior surface of shank bright orange; flanks whitish with few dark brown blotches; gula, throat and lateral region of belly cream with brown scattered spots, medial area of belly immaculate; ventral surfaces of hands, feet, and webbing yellowish.

Coloration of holotype in preservative. Dorsum reddish brown with a similar pattern of dark brown markings and spots as in the life specimen; head dark reddish brown laterally; flanks posteriorly whitish with spots and blotches brown; supratympanic fold and tympanic region reddish; upper lip slightly pale, with scattered melanophores and distinct white spots below the eye; axilla, groin, anterior and posterior surfaces of thigh, and anterior surface of shank pink; flanks whitish with irregular brown blotches; gula, throat and lateral region of belly cream with brown scattered spots, center of belly without spots; ventral surfaces of hands, feet, and webbing cream.

Measurements of holotype (in mm). SVL 35.8; TBL 16.9; HW 11.9; HL 10.2; IOD 4.4; IND 2.8; END 2.6; NSD 1.3; ED 3.4; TD 1.7; TFD 1.9; FTD 1.8; THL 16.9; FL 23.7.

Variation and sexual dimorphism. Variation of measurements and body proportions is given in Table 1. The variation on finger webbing formulae is I (2 – 2 1/2) – 2- II 1 1/2 – (2- – 2 1/2) III (2- – 2 1/2) – 2 IV, and the variation on toe webbing formulae is I (1 – 1+) – (1 1/2 – 1 3/4) II 1 – (2 – 2-) III 1 – (2 – 2-) IV (2 – 2-) – 1 V. The adults males have vocal slits extending from mid lateral base of tongue to posterior level of it; vocal sac single, median, subgular. This new species has an evident sexual dimorphism in the color pattern in life. The female dorsum is reddish brown or cream (cream and silver grey with blotches and brown and yellow spots in males); in males, axilla, groin, anterior and posterior surfaces of thigh, and anterior surface of shank are pale yellow. Some individuals, mainly females, possess an X-shaped pattern brown dark, which extends from the posteromedial edge of the orbit along the dorsum. Most juveniles with dark brown dorsal transverse bands and on entire hind limbs, additionally, canthus rostralis and region around nares brown dark, lips speckled; most individuals have white spots below the eye, in some cases these spots extend toward inferior postocular region.

Measurement Males (n = 15) Females (n = 9)

SVL 24.8–27.8 (26.5 ± 0.9) 30.4–35.8 (32.9 ± 1.7) TBL 11.9–13.7 (13.0 ± 0.6) 15.0–16.9 (15.8 ± 0.9) HW 8.2–10.2 (9.4 ± 0.5) 10.7–11.8 (11.3 ± 0.3) HL 7.1–8.9 (8.1 ± 0.4) 9.0–10.2 (9.8 ± 0.4) IOD 3.7–4.1 (3.1 ± 0.2) 3.6–4.8 (4.1 ± 0.4) IND 1.8–2.4 (2.1 ± 0.1) 2.3–2.7 (2.5 ± 0.1) END 1.7–2.5 (2.1 ± 0.2) 2.3–2.7 (2.5 ± 0.1) NSD 0.8–1.2 (1.0 ± 0.1) 1.1–1.3 (1.3 ± 0.1) ED 2.6–3.2 (2.8 ± 0.2) 2.9–3.5 (3.2 ± 0.2) TD 0.9–1.5 (1.3 ± 0.1) 1.3–1.6 (1.5 ± 0.1) TFD 0.9–1.5 (1.3 ± 0.2) 1.5–1.9 (1.8 ± 0.1) FTD 1.1–1.6 (1.2 ± 0.2) 1.2–1.8 (1.7 ± 0.2) THL 11.5–13.4 12.6 ± 0.6) 14.8–16.6 15.6 ± 0.7) FL 16.3–19.5 18.2 ± 1.0) 20.4–23.9 22.2 (± 1.2)

Tadpole. MHUA-L 0153-1 (stage 39, Fig. 5 , Table 2). Body ovoid, wider than deep, body length approximately 38% of total length ( Fig. 5 A); snout rounded in dorsal and profile view; eyes large approximately 30% of body height, directed laterally; nostrils moderately large, elliptical, located frontally, directed anteroventrally, midway between eye and tip of snout; spiracle sinistral, short, directed posterodorsally, distance from opening to snout 66% of body length; neuromasts of the lateral line system evident mainly of supraorbital, infraorbital, ventral body and dorsal body lines; intestines located approximately at the center of abdominal region, intestines ventrally visible and coiled clockwise; cloacal tube very short, dextral. Caudal musculature robust, in the anterior region correspond to 60% of body height, tapering to a point posteriorly; dorsal fin beginning at posterior edge of body, slightly more arched than ventral fin; fins deepest at about midlength of tail; tail acute. Oral disc very small 25% of body width, anteroventral, directed frontally upper jaw sheath wide, arch-shaped, with no lateral processes; marginal papillae single laterally and ventrally, marginal papillae interrupted dorsomedially in the anterior labium forming a wide gap ( Fig. 5 D); lower jaw sheath broadly U-shaped; labial tooth row formula 0/2; P- 1 larger than P-2; teeth of P-1 larger than P-2; one toothless ridge present on anterior (upper) labium, broadly arched.

In life, dorsal and lateral view body brown; anterior region ventrally dark brown, with very small spots black, turning translucent posteriorly just in the joint with the tail. Intestines reddish brown; iris reddish copper; tail musculature pale brown, fins light orange or light yellow, both with irregular brown blotches forming reticulations in some specimens; posterior region of tail musculature dark brown while the fin is translucent. In preservative, colors on the fins become creamy or light gray.

Etymology. The specific epithet norandinus is composed by the prefix nor from “norte” (Spanish word for “north”), and the New Latin noun andinus meaning “Andes”. The specific name in reference to the septentrional distribution of this species in South America, and a tribute to Andean mountains of Colombia.

Geographic distribution and natural history. Dendropsophus norandinus is known from only three localities in the northeastern part of the Cordillera Central: in the vereda El Roble (type locality) and vereda El Retiro, both at municipio de Anorí and in the vereda Salazar, municipio de Amalfí (06º57´N, 75º03´W, 1420 m a.s.l.), both municipalities in the departamento de Antioquia, Colombia ( Fig. 6 ). Altitudinal range is between 1420–1950 m a.s.l. The type locality and the locality from municipio de Amalfí are distanced approximately to each other 10 km, separated by the Porce river valley. Individuals of D. norandinus inhabit semi-permanent swamps, with abundant grasses, in pasturelands. Most males called from the emerging vegetation, near the water surface during or immediately after light rains, while females remain hidden in the aquatic vegetation. Some males called during the day, but their activity peak is between 19:00 and 02:00 h. Amplexus is axillar and clutches are laid under water attached to the submerged vegetation. Some individuals were found in secondary forest, along the creeks. In the shallow swamps, D. norandinus is syntopic with Leptodactylus colombiensis (Heyer) and an undescribed species of Scinax . An adult female of D. norandinus was found in the stomach of Leptodeira septentrionalis Kennicott (MHUA 14315).

TL 28.1–32.0 (30.2 ± 1.1) BL 10.9–11.9 (11.3 ± 0.3)

BH 6.3–7.2 (6.7 ± 0.2)

OD 1.8–2.1 (2.0 ± 0.1)

ND 0.3–0.4 (0.3 ± 0.0)

BW 6.6–7.8 (7.2 ± 0.3)

IO 5.2–5.7 (5.4 ± 0.2)

IN 3.2–3.9 (3.6 ± 0.1)

NS 1.9–2.1 (2.0 ± 0.1)

ES 3.5–4.0 (3.8 ± 0.1)

SS 6.8–7.4 (7.1 ± 0.2)

ODL 1.7–1.9 (1.8 ± 0.0)

TMH 3.1–4.3 (3.8 ± 0.3)

MTH 6.2–7.8 (7.1 ± 0.3)

Figures

FIGURE 1. Living specimens of some high Andean species of genus Dendropsophus. A) D. bogerti, Medellín, Antioquia, Colombia (MRC 999, SVL = 32.6 mm, female); B) D. carnifex, Maquipucuna, Pichincha, Ecuador (QCAZ 42387, SVL = 32.6 mm, female); C) D. columbianus, Calima, Valle del Cauca, Colombia (MRC 920, SVL = 33.2 mm, female); D) D. garagoensis, Garagoa, Boyacá, Colombia (MRC 730, SVL = 28.3 mm, female); E) D. labialis, San Juanito, Meta, Colombia (MRC 644, SVL = 42.6 mm, male); F) D. meridensis, Merida, Venezuela (voucher number unknown); G) D. padreluna, Fusagasuga, Cundinamarca, Colombia (specimen not collected); H) D. virolinensis, Virolín, Santander, Colombia (MAR 2298, SVL = 25.4 mm, male). The specimens are not to scale. Photos: M. Rivera-Correa (A, C-D) S. Ron (B); M. Rada (E, H); F. Rojas-Runjaic (F); H. Bernal (G).

FIGURE 2. Dendropsophus norandinus sp. nov. (MHUA-A 4092, paratype, adult female in life, SVL = 35.6 mm). Photo: T. Grant.

FIGURE 3. Ventral color patterns of females of some Dendropsophus species from the highlands of the Andes of Colombia. (A) Dendropsophus norandinus sp. nov. MHUA-A 3781 (holotype); (B) D. bogerti MHUA-A 4599; (C) D. columbianus MHUA-A 3583; (D) D. garagoensis ICN 17803; (E) D. padreluna ICN 22021 (paratype); (F) D. praestans ICN 7559. The specimens are not to scale. Photos: M. Rivera-Correa.

FIGURE 4. Drawings of holotype of Dendropsophus norandinus sp. nov. (MHUA-A 3781). (A) Lateral, and (B) dorsal views of the head; (C) palmar, (D) plantar views of left hand and foot. Scale bar = 5 mm. Drawings: M. Rivera-Correa.

FIGURE 5. Tadpole of Dendropsophus norandinus sp. nov. from the type locality (MHUA-L 0153 - 1). (A) lateral, (B) dorsal, (C) ventral views; scale bar = 5 mm; (D) Oral disc, scale bar = 1 mm. Photos and drawing: M. Rivera-Correa.

FIGURE 6. Map showing the known distribution of Dendropsophus norandinus sp. nov. The star indicates the only two know localities, which are separated by 10 Km.