Hyloxalus yasuni, Páez-Vacas & Coloma & Santos, 2010

Páez-Vacas, Mónica I., Coloma, Luis A. & Santos, Juan C., 2010, Systematics of the Hyloxalus bocagei complex (Anura: Dendrobatidae), description of two new cryptic species, and recognition of H. maculosus 2711, Zootaxa 2711, pp. 1-75 : 47-55

Hyloxalus yasuni new species

Hyloxalus bocagei (non Jiménez de la Espada)— Grant et al. 2006:136, 168.

Holotype. ( Fig. 17, virtual animation). QCAZ 32465 , adult male from Ecuador: Provincia Orellana: PUCE’s (Pontificia Universidad Católica del Ecuador) Yasuní Research Station (01° 40' 16.7" S, 76° 24' 01.8" W), 300 m above sea level, part of a series collected on 29 July 2006 by Myrian Rivera, Ítalo G. Tapia, and Mónica Reinoso-Recalde.

Paratopotypes. QCAZ 32455–67 , same data as holotype ; QCAZ 5100 , 5132 , obtained on 17–20 May 1994 by Stella de la Torre and Santiago R. Ron ; QCAZ 5319 , 5864 , obtained on 21 May–04 June 1994 by Stella de la Torre and Diego Tirira ; QCAZ 6659 , obtained on 01 January 1994 by Felipe Campos-Yánez ; QCAZ 8079–80 , 8081 , 8083 , 8284 , obtained on 21 January–09 February 1995 by Morley Read ; QCAZ 12098–12099 , obtained on 27 August 1996 by W. Chris Funk ; QCAZ 12102 , obtained on 31 December 1996 by W. Chris Funk ; QCAZ 13253 , obtained on 19 April 1999 by Santiago R. Ron ; QCAZ 13717 , 13723–27 , 18435 , 18706 , obtained on August 1999 by Santiago R. Ron and Dania Prado ; QCAZ 16779 , obtained on 08 August 2001 by Francisco Villamarín J .; QCAZ 18411–12 , 18497 , obtained on 16 February 2000 by Juan Carlos Santos ; QCAZ 18719 , obtained on 07 July 1997 by Santiago R. Ron ; QCAZ 19230–35 , 19250 , obtained on 20 February 2002 by Ítalo G. Tapia and Giovanni Carotti ; QCAZ 17849–52 , 17854 , 21264–67 , 21330 ; QCAZ 21432 , 21441–44 , 22480 , 22535 , 22554–60 , 22588–93 , 22625 , 22957 , 23825–27 , 24056–74 , 24230–36 , 24542 , 25053–55 , 25057–59 , 25061–65 , 25067–68 , 25070–83 , 30001–10 , obtained between April 2001 and September 2002 by Diego A. Paucar ; QCAZ 33379–80 , obtained on 23 April 2007 by Mónica I. Páez .

Referred specimens. QCAZ 31143–51 , 31153–55 , 31159 , 31161–63 , 31174–77 , 31268 , 31349 , Guagua Sumaco , 1095 m (0° 43' 32.7"S, 77° 33' 57.6"W), obtained on 15–16 December 2005 by Ítalo G. Tapia, Néstor Acosta-Buenaño, and Mónica I. Páez ; QCAZ 18679–80 , Loreto obtained on 23 October 1999 by Eduardo Kohn ; EPN 5752–54 , Parroquia San José de Dahuano, Comuna 24 de Mayo , 415 m (0°43'16" S, 77°25'24"W), obtained by Ana Almendáriz ; EPN 7514 , La Barquilla, obtained by Mario Yánez-Muñoz ; QCAZ 37261–37262 , 37629–34 , Lumbaqui , 547 m (0° 4' 47.676"N, 77° 21' 53.28"W), obtained on 25 July 2007 by Juan Carlos Santos, Natalia Biani, and Ítalo G. Tapia ; QCAZ 5865–66 , Reserva de Producción Faunística Cuyabeno , 260 m (0° 0' 34.92"S, 76° 10' 54.12"W), obtained on 01 April 1994 by Laurie J. Vitt and Peter A. Zani ; QCAZ 6340 , Reserva de Producción Faunística Cuyabeno , obtained on 01 September 1994 by Diego Tirira, Santiago R. Ron, and Edwin Carrillo , QCAZ 19161–62 , 19164–65 , Reserva de Producción Faunística Cuyabeno , 220–260 m, obtained on 03 February 2002 by Santiago R. Ron, Luis A. Coloma, and Ítalo G. Tapia ; QCAZ 13670 , Río Bermejo, 2 Km Northeast of Bermejo , 825 m (0° 10' 59.9982"N, 77° 22' 0.1194"W), obtained on 24 October 1999 by Jenny Naranjo .

Diagnosis. A species of the genus Hyloxalus as defined by Grant et al. (2006), based on the following features: (1) dorsal coloration cryptic, brown or black; (2) pale oblique lateral stripe present (although reduced); (3) pale dorsolateral stripe absent; (4) pale ventrolateral stripe absent; (5) dorsal skin texture posteriorly granular; (6) toe webbing extensive; (7) third finger of adults not swollen; (8) finger disc moderately expanded; (9) median lingual process absent; (10) larval vent tube dextral; (11) larval oral disc not umbelliform; (12) larval oral discs emarginated; (13) testes unpigmented; (14) dark throat collar absent.

A species with (1) mean SVL in adult males 23 mm (19–25.8, SD = 1.2 n = 78) and in adult females 25.5 mm (21.3–28.9, SD = 1.6, n = 70); (2) disc of Finger IV expanded less than 1.5 times the width of adjacent phalange; (3) Finger II shorter than Finger III; (4) fringes present on fingers; (5) disc of Toe IV expanded less than 1.5 times the width of adjacent phalange; (6) fringes present on toes; (7) outer metatarsal fold present or absent; (8) extensive toe webbing, formula I 1—(1½–2 +) II 1—(2–3) III (1–2 +)—(3–3½) IV (3–3½)—(1–2 -) V; (9) oblique lateral stripe reduced to a small bar or a series of 3–5 dots at groin level; (10) dorsum with three large blotches; (11) gular-chest region brown with white marks in adult males, cream-colored or with faint brown spots in adult females; (12) venter white with brown marks in adult males, cream in adult females; (13) sexual dimorphism in ventral coloration present; (14) tadpoles translucent with brown stippling, a belt-like mark on body-tail junction and, in vivo, two pale marks on each side of oral disc and two on each side of body at spiracle level; (15) tadpole spiracular opening oriented dorsoposteriorly; (16) call is a long trill composed of single pulsed notes.

Hyloxalus yasuni is similar to those species that exhibit extensive toe webbing and lack oblique lateral stripe ( H. abditaurantius , H. betancuri , H. chocoensis , H. edwardsi , H. faciopunctulatus , H. italoi , H. leucophaeus , H. maculosus , H. ruizi ). It is distinguished from these species by the following characters: H. abditaurantius has an orange spot on the calf, absent in H. yasuni . Hyloxalus betancuri lacks a tubercle posterior to mouth, ventral coloration in females (holotype CJS 2372, an adult female and the only specimen of the species known) is dark brown with small white dots, whereas females of H. yasuni are ventrally cream. Hyloxalus chocoensis has a squared dorsal mark and testes enlarged. Hyloxalus edwarsi and H. ruizi are distinguished from all species within the genus by having a cloacal funnel. Hyloxalus faciopunctulatus lacks a V- shaped dorsal blotch at scapular level. Hyloxalus leucophaeus lacks outer metatarsal fold and sexual dimorphism in ventral coloration. Hyloxalus maculosus differs in gular-chest region of adult males; they do not exhibit white spots over a dark brown background ( Figs. 3B, E and 5-7B, F). Specimens of H. italoi are very similar to H. yasuni , nevertheless, these two species differ in genetic sequences, tadpole morphology, and call parameters (see H. italoi Comments ).

Description of holotype. ( Fig. 17, virtual animation). Male, 23.2 mm; head slightly longer than wide; head length 40.3% of SVL; head width 37.3% of SVL; snout round in dorsal view, slightly angular in lateral view; loreal region slightly concave; nostrils slightly protuberant; eye-nostril distance 64.9% of eye length; supratympanic bulge subtle, covering upper edge of tympanum; tympanum diameter 39.3% of eye length.

Arm length 22.1% of SVL; Finger II shorter than Finger III; fingers unwebbed; fringes on finger discrete; terminal discs expanded, less than 1.5 times diameter of adjacent phalange; subarticular tubercles small, round, those of Fingers II and III slightly oval; outer metacarpal tubercle large, round and protuberant; inner metacarpal tubercle at base of thumb, elliptical, protuberant, approximately one third the size of outer metacarpal tubercle; depigmentation on the outer edge of metacarpus absent. Tibia length 45.7% of SVL; foot length 42.2% of SVL; outer metatarsal fold absent; inner sigmoid tarsal fold present on distal half of tarsus; outer metatarsal tubercle round; inner metatarsal fold larger than inner, elliptical; translucent protuberance between the two metatarsal tubercles; toes more than a half webbed, toe webbing formula I 1—2 II 1— 2½ III 1 + —3 + IV 3½—1½ V; lateral fringes on toes extensive; terminal discs expanded, less than 1.5 times diameter of adjacent phalange; subarticular tubercles small, round; supernumerary tubercles absent.

Skin of dorsum, limbs, flanks and venter smooth; scattered tubercles on posterior portion of dorsum and flanks; tubercle posterior to mouth; anal sheath conspicuous. Tongue twice as long as wide, thinner and broader posteriorly, posterior two thirds not attached to mouth’s floor. Testis white.

Color in preservative (~70% ethanol). Dorsum of head and body dark brown; a darker brown interorbital blotch, a V- shaped mark at scapular level, and a band-like mark at sacral level; flanks dark brown with white spots towards the venter; dark brown stripe from posterior corner of eye to arm-body junction. Loreal region brown with scattered diffuse bronze spots. Pale oblique lateral stripe nearly absent, reduced to a short and diffuse cream-colored band. Forelimbs dark brown, transverse bars not visible, a dark brown band on dorsal surface of arm, a cream spot on dorsal surface of arm at arm-body junction, fingers dark brown; dorsal surface of hind limbs dark brown, transverse bars subtle, a dark brown spot behind the knee; groin dark brown; ventral surface of hind limbs brown, cream-colored proximally. Gular-chest region dark brown with small white spots, larger spots on chin; venter cream flecked with brown; short dark brown spots at axilla, axillas translucent. Palmar and plantar surfaces dark brown; toe webbing translucent.

Color in life. QCAZ 33379 (adult female, Fig. 4E). Iris black with coppery reticulations. Dorsum brown, slightly reddish; dorsal blotches dark brown; longitudinal reddish brown stripes posterior to each eye; loreal region brown with cream spots; flanks dark brown with white spots towards the venter. Tubercle posterior to mouth creamy white. Oblique lateral stripe reduced to a short cream-colored band anterior to the groin. Dorsal surfaces of hind limbs reddish brown; white spot at the arm-body junction; transverse bars dark brown. Gularchest region cream flecked with brown; venter white; dorsal surfaces of limbs translucent; palmar and plantar surfaces brown; webbing whitish translucent (MIP field notes, 23 April 2007).

QCAZ 33380 (adult male, Fig. 3E). Darker than female ( QCAZ 33379 ). Reddish brown thigh marks. Ventrally, gular-chest region dark brown with white spots, venter cream flecked with dark brown ( MIP field notes, 23 April 2007) .

Variation. Variation in measurements is given in Table 7. Variation in color patterns is depicted on Figs. 5F – 7F. Toe webbing formula I 1—(1½–2 +) II 1—(2–3) III (1–2 +)—(3–3½) IV (3–3½)—(1–2 -) V. Specimens from the type locality (n = 113: 58 males, 55 females) exhibit a keel on outer edge of metacarpus (75% of specimens). Outer metatarsal fold present in 77% of specimens. In some specimens, cream spots or dots present on loreal region (e.g. QCAZ 32459 ). Females paler than males in dorsal coloration. Gular-chest region dark brown in males, pale dots present or absent; cream slightly flecked with brown in females. Venter brown marbled or completely cream in males, cream or slightly flecked with brown in females .

Fifty-one juveniles (QCAZ 5319, 6659, 8080–8081, 8083, 8284, 12098, 12102, 13253, 13723, 13725– 13727, 16779, 18411–18412, 18497, 19233–19235, 19250, 19910–19911, 21330, 22593, 23825, 24231– 24236, 25053–25055, 25061–25062, 25067, 25073–25075, 25077–25079, 32279, 32397–32399, 32457, 32463) with SVL between 9–23.3 mm (mean = 15.8) have the same coloration patterns of adult specimens. In recently metamorphosed specimens, venter translucent and dorsal surface of limbs cream-colored. As development proceeds, the venter acquires cream coloration and limbs become brown. Nine recently metamorphosed specimens (QCAZ 5153, 5320–5322, 25079, 32397–32399, 35738) have SVL of 9.6–10.9 mm (mean = 10.4).

In referred specimens from Guagua Sumaco (n = 21: 14 males, 7 females), transverse bars on hind limbs are more contrasting than in specimens from the type locality. Loreal region is the same color of dorsum or paler; pale dots absent. Gular-chest region in an adult male is cream-colored with scattered brown spots and a collar-like mark. Dorsum of referred specimens from Reserva de Producción Faunística Cuyabeno (n = 7: 3 males, 4 females) is light brown, thus, dorsal marks are more conspicuous than in other localities; light brown stripes posterior to eyes. Loreal region is slightly lighter than dorsum, scattered pale dots in some specimens. The chest is white; venter and ventral surfaces of limbs are yellow marbled in both sexes. Two males with gular-chest region cream flecked with brown. Referred specimens from Lumbaqui (n = 6: 2 males, 4 females) are very similar to the topotypes. Loreal region is slightly paler than dorsum; pale dots absent. Measurements of three populations are given in Table 11 .

Tadpole. The following description is based on a single specimen in Stage 27 ( QCAZ 33189 a, Fig. 18). Tadpole corresponds to a series of dorsal tadpoles carried on back of adult male QCAZ 32466 , obtained at forest at PUCE’s Yasuní Research Station along with the species holotype ( QCAZ 32465 ). All measurements provided are in millimeters. Total length 23.5; body ovoid, ventrally depressed; body length 8.0 (34% of total length), width at spiracle 5.0, height taken posterior of eyes 3.7; snout round in dorsal and lateral views .

Nostrils very small, inconspicuous, directed anterolaterally, openings circular; opening 0.8 from tip of snout; internarial distance (taken at internal edge of each nostril) 1.5; distance from narial opening to anterior edge of eye 0.8. Eyes directed dorsolaterally, slightly leaning anteriorly; eye length 1.0, width 0.9; interorbital distance from internal edge of each eye 1.6.

Spiracle sinistral 5.0 from tip of snout (62.5% of total length); inner wall free in its distal portion; length 0.8, width at base 0.8; opening directed dorsoposteriorly and with a diameter of 0.4. Vent tube totally bounded and dextrally to ventral fin, length 1.2, width 0.5; opening circular.

Tail length 15.5 (66% of total length); tail musculature narrowing gradually, tip pointed reaches tail terminus; myotomes visible at distal half; muscle width at body-tail junction 2.5, muscle height 2.7; tail height at midtail 5.3; dorsal and ventral fin originate at body-tail junction, but dorsal fin edge becomes evident at one fourth of tail lenght; dorsal fin height 1.8, ventral fin height 1.5; distal margin of tail pointed, subtly directed upwards. Lateral line system not visible.

Oral disc ventrally located, emarginated on both sides ( Fig. 10D); transverse width 1.9 (37.9% of body width); border of disc surrounded with 62 marginal papillae: 41 ventral papillae and 21 located laterally (10 at left side and 11 at right side); a submarginal papillae at right side of inferior labium; ventral marginal papillae aligned, but alternate papillae project to opposite directions; single anterior gap of papillae 1.0.

Anterior and posterior jaw sheaths serrated through their entire length; serrations less profound as they move away from center; anterior jaw sheath transverse width, including lateral processes, 0.8 (44% of oral disc width); anterior and posterior edge of anterior jaw sheath winding; posterior jaw sheath V-shaped, transverse width 0.6 (32% of oral disc width).

Labia tooth row formula 2(2)/3(1); anterior tooth row A-1 length 1.4, number of teeth 107; A-2 length 1.3 and 35 teeth at each side of gap; A-2 gap length 0.1; P-1 gap 0.04; posterior tooth row P-1 length 1.3, 70 teeth (35 at each side of gap); P-2 length 1.4 and 83 teeth; P-3 length 1.2 and 83 teeth.

Color in preservative (~10% formalin). Dorsum and flanks translucent, tail musculature white; brown stippling covering integument and muscle. Integument less stippled than muscle. Ventrally translucent; region between mouth and gut heavily stippled; venter less stippled. Spiracle and vent tube translucent.

Tail musculature white, translucent at posterior portion; brown spots on entire extension of dorsal surface; ventrally and laterally subtly stippled; fins translucent with scattered brown spots.

Color in life. ( Fig. 11D). Body light brown with golden glitter on dorsum. Two short brown stripes, one anterior and the other posterior to the eye. Tail cream-colored with brown and golden spots; dorsal spots conspicuous in anterodorsal portion of tail; tail gradually becomes translucent, small iridescent spots in posterior portion of tail. A belt-like mark at body-tail junction. Ventrally, translucent with golden dots; brown spots on anterior portion of abdomen. Two conspicuous pale marks at each side of oral disc, and two at each side of the body at spiracle level. These marks are visible at ventral and lateral views ( Fig. 11D).

Variation. Fifteen (15) tadpoles in Stages 25–37 were examined; however, not every stage is represented in the sample. Variation of 17 measurements is given in Table 12.

Hyloxalus yasuni tadpoles exhibit the same color pattern as adult specimens in every developmental stage. The tail terminus is not always projected anteriorly. Fins are slender in Stage 25. P-1 gap sometimes is absent or teeth proximal to this space converge orienting to the front ( Fig. 10D). Submarginal papillae absent in the rest of specimens examined. Two metamorphs (Stage 41, QCAZ 18756, 18942) exhibit dorsal pattern of adult specimens.

Comparisons. Tadpoles of Hyloxalus yasuni are very similar to H. italoi . Nonetheless, they differ in morphometric variables (MANOVA, F = 15.437, df = 30, df2 = 361.705, p <0.001, n = 137). Moreover, H. yasuni has brown stippling in body and tail; whereas, H. italoi has large blotches with diffuse edges ( Figs. 14, 18).

Tadpoles of Hyloxalus yasuni differ from tadpoles of H. bocagei and H. maculosus in morphometric variables (MANOVA, F = 15.437, df = 30, df2 = 361.705, p <0.001, n = 137). Additionally, H. yasuni is larger than H. bocagei (t -test, t = -3.4, df = 82, p <0.001); body/tail proportion is larger (t -test, t = -7.3, df = 82, p <0.001); tail musculature is more robust (t -test, t = -7.07, p <0.001); eyes are larger (t -test, t = -6.1, df = 82, p <0.001); body is more elongated; fewer marginal papillae (t -test, t = 7.08, df = 82, p <0.001); anterior edge of anterior jaw sheath winding, round in H. bocagei ( Fig. 10); in vivo, tadpoles of H. bocagei have two pale ventral spots at anterior portion of body and a mark at dorsal fin origin; whereas, H. yasuni lacks those marks but exhibit two pale marks at each side of oral disc and two at each side of body at spiracle level ( Fig. 11). Hyloxalus maculosus has a dorsal tail blotch; spiracle directed laterally (dorsoposteriorly in H. yasuni ); tail musculature reaches tail terminus; body less elongate (t -test, t = 4.332, df = 33, p <0.001); more ventral papillae on oral disc (t -test, t = 5.229, df = 33, p <0.001); labia immaculate (blotches on H. yasuni ); anterior margin of anterior jaw sheath is convex (winding in H. yasuni ); in life, H. maculosus exhibits only two pale marks at each side of oral disc ( Fig. 11).

Etymology. The specific name yasuni is meant as a noun in apposition. It is derived from the Yasuní National Park, the type locality of the species and the larger protected area in Ecuador. The Yasuní National Park holds one of the richest amphibian faunas of the world that includes 150 species ( Duellman 1988; Ron 2001–2008); thus, its conservation is pivotal and of global significance ( Bass et al. 2010). This name is also used to call attention to the Yasuní-ITT Initiative (Iniciativa Yasuní ITT 2009), a revolutionary idea to keep oil underground and protect the planet’s climate and biodiversity (http://www.yasuni-itt.gov.ec). According to Kohn (2002:451), this species has a common name given by Kichwa people from Ávila Viejo (Provincia Orellana): “yaku telele” (yaku, water in Kichwa; telele, onomatopoeic word for the calling of some frog species).

Comments. Referred specimens from Guagua Sumaco (Río Pingullo of Santos et al. 2009), R. P. F. Cuyabeno, Lumbaqui, and Bermejo are similar morphologically and they are included under Hyloxalus yasuni because of their phylogenetic proximity based on molecular data ( Fig. 1; Santos et al. 2009). However, patristic distances between these populations are high (3.7–4.4% in mitochondrial genes 12S, 16S and Cytochrome b, Santos 2002; Santos et al. 2009); therefore, it is feasible that they are not conespecific ( Fig. 1, Tables 2 and 3). For further information, see H. italoi Comments and Phylogeny and Chronogram and Ancestral Area Resconstruction sections ( Tables 2 and 3; Figs. 1).