Myersiohyla neblinaria Faivovich & Mcdiarmid & Myers 2013, new species
Creators: name: Faivovich, Julián
name: Mcdiarmid, Roy W.
name: Myers, Charles W.
Publisher: name: Zenodo
Year: 2013
Subjects: Biodiversity
Taxonomy
Animalia
Chordata
Amphibia
Anura
Hylidae
Myersiohyla
Myersiohyla neblinaria

description: Myersiohyla neblinaria, new species
Figures 15–25
Hylid sp. nov. b – McDiarmid and Paolillo (1988). Species list.
Hylid sp. D (Neblina) – McDiarmid and Donnelly (2005). Species list.
Hyla inparquesi (non Ayarzagüena and Señaris, “1993” [1994]) – Faivovich et al. (2005). Misidentification of specimens from Cerro de la Neblina.
Myersiohyla inparquesi (non Ayarzagüena and Señaris,“1993” [1994]) – Faivovich et al. (2005). First combination with Myersiohyla.
HOLOTYPE: USNM 562071, adult ♂, with muscle tissue removed from left thigh. Venezuela: Departamento Amazonas: Cerro de la Neblina: Camp VII, 1730 m, collected by A. Gardner on February 1, 1985.
PARATOPOTYPES: USNM 562072, AMNH A-123715 (♀♀).
PARATYPES: Venezuela: Departamento Amazonas: Cerro de la Neblina: Camp I, 1820–1880 m: USNM 562070 (♀). Camp II, 2085–2100 m: AMNH A-131172 (♀). Camp XI, 1450 m: USNM 562073–562082 (♂♂).
ETYMOLOGY: The species name neblinaria is an adjective derived from the mountain name Neblina plus the Latin suffix -aria (fem. to agree with –hyla of genus name), denoting a place or a connection to a place.
DIAGNOSIS: Myersiohyla neblinaria is characterized by: (1) SVL of male 47.7–52.3; female SVL 54.0–61.6; (2) a single, thick, nuptial pad; (3) a row of tubercles in the forearm; (4) mental gland present but evident only through dissection; (5) thighs with longitudinal bars; (6) dorsum brown, with variable presence of a dorsal line and blotches; (7) m. depressor mandibulae without an origin on the dorsal fascia at the level of the m. levator scapulae; (8) unpigmented eggs; (9) tadpoles with a dorsoventrally flattened body; (10) fins reaching the base of the tail; (11) labial toothrow formula (LTRF) 16 (16)/21(1).
COMPARISON WITH OTHER SPECIES: Myersiohyla neblinaria is most similar to M. inparquesi but differs in having: hand and toe discs without sagittal black lines (present in M. inparquesi); larvae with dorsal and ventral tail fins reaching the base of the tail (extending only a third in M. inparquesi); larvae with scattered submarginal papillae in the upper and lower labium (apparently absent in M. inparquesi); and larval oral disc with a single row of marginal papillae (three rows in M. inparquesi). Furthermore, the advertisement call of M. neblinaria is composed of a single note with 7–9 pulses and a duration of 295–382 ms; in contrast, the advertisement call of M. inparquesi is composed of two notes, one of 6 pulses and a duration of 90 ms, and the other with 7 pulses and a duration of 80 ms (Ayarzagüena and Señaris, “1993” [1994]). Myersiohyla neblinaria differs from M. loveridgei in its larger SVL (M. neblinaria 47.7– 52.0 mm; M. loveridgei 42–45 mm; Rivero, 1961; “ 1971 ” [1972]), and in having a single nuptial pad (two in M. loveridgei). From M. aromatica it differs in having a single nuptial pad, instead of two (Ayarzagüena and Señaris, “1993” [1994]: 130); larger SVL (M. aromatica, 43.6–46.6 mm; M. neblinaria 47.7–52.0 mm); tadpole with dorsoventrally flattened body (globular in M. aromatica) and more rows of labial teeth (LTRF 10-13/ 14-18 in M. aromatica). M. neblinaria is distinguished from M. kanaima by its larger SVL (males: 37.0– 37.8 mm, ẍ= 37.4, n = 5; females: 46.3–48.0 mm, ẍ= 47.05, n = 4; Goin and Woodley, 1969, and this paper), more robust body (slender in M. kanaima), more developed prepollex (proportionally reduced in M. kanaima), more extensive and thick nuptial pad (reduced to the dorsal margin of the prepollex, and composed of a thin layer of glandular tissue, apparently without colored epidermal projections), unpigmented eggs (completely pigmented in M. kanaima), color pattern, tadpole with dorsoventrally flattened body (depressed in M. kanaima) and more rows of labial teeth (LTRF 2/ 4 in M. kanaima, but see discussion).
DESCRIPTION OF THE HOLOTYPE (figs. 15a, 16–17): Body robust; head slightly longer than wide; as wide as body; head width 33% SVL; head length 36% SVL. Snout in dorsal view rounded, in profile truncate; canthus rostralis rounded; loreal region concave; lips not flared; nares slightly protuberant, directed dorsolaterally, and posterior to anterior margin of lower jaw. Internarial region and top of head slightly depressed. Interorbital distance shorter than eyelid. Eye prominent, its diameter 125% eye-nostril distance. Tympanum rounded, its diameter 39% eye diameter. Supratympanic fold heavy, beginning behind eye and extending to anterior margin of insertion of arm, obscuring dorsal margin of tympanic membrane.
Vomerine teeth in two medially convergent series that contour posterior margin of choanae giving shallow S- shape to each series; 16 teeth on right and 13 on left. Choanae kidney shaped; separated by distance larger than their maximum diameter. Tongue ovoid, attached overall (narrowly free around lateral and posterior margin), posterior margin entire. Vocal slits present, longitudinal, originating at sides of tongue and extending to corners of mouth.
Vocal sac not evident externally. Glandular tissue on mental area visible at 60×, but otherwise not evident externally.
Forearm robust and prominent. Row of low, irregularly spaced tubercles along ventrolateral edge of forearm. Fingers long and slender, with clearly defined circumferential groove, pad smaller (~75%) than disc; width of disc on third finger similar to tympanum diameter. Relative lengths of fingers 1<2<4<3. Fingers webbed basally, without dermal fringes; webbing formula of outer fingers II 2⅓–3½ III 3 + –3 + IV. Subarticular tubercles large; distal tubercle of finger IV irregularly shaped, others round. Large supernumerary tubercles, round or irregularly shaped. Outer metacarpal tubercle small and bifid, nearly round. Inner metacarpal tubercle large, elliptical. Prepollex enlarged, semicircular. Nuptial pad present, covering internal margin of thumb and dorsal margin of enlarged prepollex; consisting of thick, cream glandular pad, covered by minute dark epidermal projections (fig. 18).
FIG. 17. Ventral view of hand and foot of the holotype of Myersiohyla neblinaria (USNM 562071).
Scale bar = 5 mm.
Hind limbs moderately robust; tibia length 55% of SVL; foot length 43% SVL. Calcar absent; tarsal fold absent, but skin subtly thickened. Inner metatarsal tubercle large, elliptical; outer metatarsal tubercle round. Toes short, bearing discs smaller than those on fingers; disc of toe I smaller than others; relative length 1<2<3≈5<4; webbing formula I 2–2 II 1½–2½ III 2–3 IV 2½–1½ V. Subarticular tubercles large, round. Few flat supernumerary tubercles in longitudinal series at base of toes. Cloacal opening directed posteroventrally at midlevel of thighs; several flat tubercles scattered laterally and below cloaca. Dorsal skin smooth, finely granular on abdomen. Pectoral fold absent.
MEASUREMENTS OF HOLOTYPE (all in mm): SVL 49.8; HL 18.0; HW 16.8; IND 4; IO 5.4; ED 5.9; EN 4.7; TD 2.3; TL 27.7; FL 21.3.
COLORATION OF HOLOTYPE in life: No field notes are available for the holotype. Visible details from a color slide of RWM, here reproduced as figure 15A, differ little from the coloration in preservative.
COLORATION IN OF HOLOTYPE IN PRESERVATIVE: Dorsally brown, turning darker brown toward the flanks, and with many large, irregular tan blotches; these blotches are smaller on the sides. Thick dark brown to black uniform line from tip of the snout to approximately the distal tip of urostyle. Dark, poorly defined, diffuse canthal stripe. Discs dorsally dark gray, contrasting with the brown coloration of the limbs. Hind limbs dorsally and ventrally brown; each thigh with five tan dorsal longitudinal stripes with diffuse margins that extend into the hidden areas. Shank with irregular tan blotches, some of which look dorsally continuous with those on thigh, smaller blotches on the outer surface of the foot. The only pattern present on rear surfaces of thighs are the posterior margins of the tan bars. A few tan blotches surround the cloacal region. Paracloacal tubercles tan. Ventral surfaces of body and limbs brown; subarticular, palmar, and thenar tubercles light gray. Irregular series of small tan blotches across abdomen below the pectoral region.
VARIATION OF PARATYPES: Morphologically the paratypes are similar to the holotype. The variation in toe-webbing formula can be expressed as: I (2–2½)–(2–2½) II (1 + –2 -)–(2½–3) III (1½–2)–(2–3) IV (2½–3)–(1 + –2 -) V. Vomerine teeth (n = 12): 12-17 (right, ẍ = 14.1) and 11-16 (left, ẍ = 13.4). The structure that has been described in the holotype as a subtle dermal ridge along the tarsus is equally subtle in most paratypes, with the exception of three females (AMNH A-131172, USNM 562070 and 562072), where it is quite distinct, and proximally forms a few flat tubercles.
Most notable variation involves the coloration and color pattern, particularly regarding presence and extent of blotches (figs. 15, 19–20). We describe the variation according to the camps at which specimens were collected. Unless otherwise stated, all descriptions refer to preserved specimens. Camp I. The single specimen collected at Camp I (USNM 562070), an adult female, has a barely defined dorsal pattern, being light tan with a diffuse darker reticulum. Exposed surfaces of shank and foot are light tan as well, with diffuse brown blotches. Thighs dark brown with light tan blotches. Undersides of hind limbs and forelimbs reddish brown. Abdomen and throat creamy; areas surrounding the insertion of the arms dark brown. Diffuse line borders the lower jaw. An irregular brown line extends from the mandibular symphysis up to the beginning of the pectoral region. Camp VII. Coloration of two females differs notably from the holotype. USNM 562072 is dorsally tan, becoming brown on the sides. It lacks the dorsal line and other discernible pattern, with the exception of some irregular, small, tan blotches on the sides. Coloration of this frog during the day was noted by Cocroft (field notes, Dec. 2, 1985) as: iris coppery yellow with black reticulations; dorsal surfaces of fore- and hind limbs tan; dorsum from snout to vent brownish tan, fading to lighter tan laterally in center of body; feet mottled light tan and dark brown dorsally, toe pads dorsally dark brown, almost black in center outlined with light tan, brownish gray ventrally; sides and ventral surfaces lavender brown mottled with light tan; anterior and posterior thighs same as sides; toe webbing dark brown; light tan upper lips; tympanum coppery brown. In AMNH A-123715 the dorsal pattern is reversed with respect to the holotype, with the ground coloration being tan and the blotches, which are smaller and fewer, being brown. Middorsal dorsal dark line present. Seven longitudinal bars on the thighs. In his field notes Myers described this specimen in life as “Brown with vague darker blotching and blackish brown vertebral line. Flanks and thigh mottled and banded tan and purplish brown. Ventral surfaces purplish brown with suffusion of tan across chest. Iris golden yellow with black reticulation (conspicuous but not sharply defined).” Camp XI. Nine of the 10 specimens collected in Camp XI have the dark vertebral line. With the exception of USNM 562079, all are like the holotype in the dark brown flanks with tan blotches of variable size. Most variation involves the dorsal and thigh pattern, and the hues of brown and tan. On specimens USNM 562073– 74, USNM 562076, and USNM 562079–80, the dorsal pattern is barely distinguishable. USNM 562075 is completely light tan without dorsal blotches. Specimens USNM 562077–78 and USNM 562081–82 have dorsal blotches, but their pattern is reversed from that of the holotype, with their ground coloration being tan or light tan and the blotches brown.
MEASUREMENTS OF THE PARATYPES (all in mm, ẍ ± 1 standard error): Males (n = 9): SVL 47.7–52.3 (ẍ = 50.5 ± 0.4); HL 17.9–18.9 (ẍ = 18.4 ± 0.1); HW 16.8.0 – 18.1 (ẍ = 17.4 ± 0.1); IND 3.7–5.0 (ẍ = 4.0 ± 0.1); IO 4.9–5.6 (ẍ = 5.2 ± 0.1); ED 5.0 – 6.5 (ẍ = 5.7 ± 0.1); EN 4.1 – 5.2 (ẍ = 4.6 ± 0.1); TD 2.3 – 2.6 (ẍ = 2.5 ± 0.1); TL 26.0–28.3 (ẍ = 27.6 ± 0.2); FL 19.7 – 21.8 (ẍ = 20.5 ± 0.2). Immature male (USNM 562081): SVL 40.0; HL 15.0; HW 14.0; IND 3.4; IO 4.7; ED 4.8; EN 3.9; TD 1.9; TL 23.1; FL 15.9. Females (n = 4): SVL 54.0 – 61.6 (ẍ = 58.9 ± 1.7); HL 20.4 – 22.3 (ẍ = 21.5 ± 0.4); HW 19.1 – 21.0 (ẍ = 20.3 ± 0.4); IND 4.6 – 5.0 (ẍ = 4.8 ± 0.1); IO 5.9 – 7.4 (ẍ = 6.4 ± 0.4); ED 5.5 – 6.9 (ẍ = 6.3 ± 0.3); EN 5.2 – 5.8 (ẍ = 5.4 ± 0.1); TD 2.6 – 3.1 (ẍ = 2.9 ± 0.1); TL 31.1 – 34.7 (ẍ = 33.3 ± 0.8); FL 22.6 – 25.8 (ẍ = 24.2 ± 0.7).
REMARKS: The presence of a mental gland is not externally evident in male paratypes of Myersiohyla neblinaria, but is evident under high power magnification (60×) or through dissections. Superficial dissections in male USNM 562074 reveal a roughly circular patch of glandular tissue in the dermis of the mental region (fig. 21). A dissection of female USNM 562072 did not indicate the presence of a mental gland.
The vocal sac appears to be single and subgular, as indicated by the slightly distended sacs of USNM 562073, USNM 562076–77, and USNM 562080. The forearm is robust and prominent in all males, and proportionally slender in females. The prepollex is equally enlarged in males and females (figs. 17, 22). Two specimens partially dissected when tissue samples were removed (USNM 562072 ♀, and USNM 562077 ♂) show a translucent peritoneum and unpigmented urinary bladder. The female (SVL 60.2 mm) has large, unpigmented ovarian eggs. The dissected right ovary (left one not dissected) contained 119 eggs with largest diameter of 2.7– 2.9 mm (ẍ= 2.8; s = 0.08; n = 15). The male has elongated, almost cylindrical, unpigmented testes. Females are proportionally larger than males (SVL 54.0– 61.6 mm, males 47.7–52.3 mm). Superficial dissections in male USNM 562074 reveal that the m. intermandibularis has a large diamond-shaped aponeurosis; its fibers barely contact the oval and araphic m. submentalis. Supplementary elements of the m. intermandibularis absent. The m. depressor mandibulae originates from the zygomatic ramus of the squamosal, and, contiguously, from the posterior margin of the tympanic annuli; the tympanic fibers are not differentiated as a slip. There are no fibers originating from the dorsal fascia at the level of the m. levator scapulae.
ECOLOGY AND NATURAL HISTORY: Near Camp I, Buck found an adult female (USNM 562070) asleep during the day in a leaf axil of Bonnetia maguireorum (Theaceae) on a small ridge northeast of Camp I (fig. 23). At Camp VII, a gravid female (USNM 562072) was collected on a vine in the forest and produced copious amounts of a milky white exudate on its back after capture. Specimens from Camp XI were collected by McDiarmid, Cocroft, and Paolillo along a small (1–4 m wide) forest stream with large boulders and cascades. On February 25, 1985, USNM 562073 was recorded as it called beside a cascade in a clump of grass growing out of a sloping, mossy rock face about 1 m from the water; three other males (USNM 562074, USNM 562077–78) were on leaves and in grass clumps near cascades on sloping rocks along the same stream. USNM 562075– 76, USNM 562079–80, USNM 562082 were all collected from a rocky grotto along the same stream on the following night. An immature male (see below) was collected on a leaf of a small plant about 15 m from the stream that same night.
Two of three females (USNM 562070, SVL 59.8; USNM 562072, SVL 60.2) collected on February 10, 1984, and February 10, 1985, respectively, were gravid. A comparable-sized female (AMNH A-123715, SVL 61.6 mm) collected on November 29, 1984 also was gravid. The fourth female (AMNH A-131172), collected February 9–11, 1984, was smaller (SVL 54.0 mm) and had oocytes in very early stages of development, suggesting that she was approaching maturity. Most collected males (SVL 47.7–52.3 mm, n = 10) had well-developed nuptial pads and presumably were capable of breeding. Calling males were heard in late February 1985 at Camp XI. A single smaller male (USNM 562081, SVL 40.0 mm) collected at the same time and place lacked nuptial pads and likely was immature.
VOCALIZATION: The advertisement call of a male paratype (USNM 562073) calling alone was recorded in February along a cascading stream near Camp XI (fig. 24). The frog was calling at the base of a clump of grass, about 1 m from the water. The recording includes 31 notes being continuously given in 80 sec of tape (the recording may contain only the terminal part of a long call).
The call is a long train of well-spaced notes given at a rate of 23.4 notes/min. Note duration is about 0.3–0.4 sec (295–382 ms, ẍ = 338 ± 21 ms, n = 20). The individual note is composed of 7–9 pulses (ẍ = 8.05 ± 0.69, n = 20 notes) that are resolvable even by narrowband analysis (fig. 24C). The individual note is a brief musical trill, being narrowly tuned with frequency rising about 113–151 Hz throughout the note from 1522–1560 Hz at initiation to 1673 Hz at the end (n = 9 notes analyzed).
Ayarzagüena and Señaris (“1993” [1994]) described the advertisement call of Myersiohyla inparquesi as a train of 240 ms, composed of two notes, the first with six pulses (90 ms) and the second with seven pulses (70 ms). The call was described as spanning the spectrum between 1200–2000 Hz, with a harmonic at 4400 Hz and the fundamental frequency at 1740 Hz. The call repetition rate was 20 notes/min. While no illustrations or temperature data were provided by Ayarzagüena and Señaris, their description suggests a call quite different from that of M. neblinaria.
Although Myersiohyla neblinaria and M. aromatica are readily diagnosable by several morphological characters (see diagnosis), the calls seem similar. The call of M. aromatica was described by Ayarzagüena and Señaris (“1993” [1994]), on the basis of recordings done at 19° C. The call was composed of single notes with an average duration of 420 ms, with 10–11 wellspaced pulses, a dominant frequency of 2000 Hz, and a bandwidth between 1250 and 2600 Hz. The note repetition rate was 44 notes/min.
TADPOLE: The uncorrected pairwise distances of 16S sequences (table 2), between the tadpole (USNM 562732) and those of the holotype, and paratypes (USNM 562072, USNM 562074) are 0%–0.2%. Conversely, they are 12.3%–13.6% different from the sequences of available specimens of M. chamaeleo. Considering the identical or almost identical sequences, we consider this tadpole and all others with the same general morphology (see below) to be larvae of M. neblinaria.
Five larvae of Myersiohyla neblinaria in stage 25 were taken in the stream below Camp IX. They were found among rocks in shallow water (~ 5 cm deep) in slow-moving portions of the stream by day and night. A few tadpoles presumed to be of the same species (greenish gray) were seen at Camp VII (Cocroft, field notes) but none were collected. Specimens from Camp XI are quite fragile (possibly because of problems with the formalin [low pH?] at the time of fixation), especially the largest individual (USNM 562370) that was illustrated shortly after its capture and shown in figure 25. Since that time, the specimen has progressively deteriorated, particularly in that its tooth rows are separating from the tooth ridges; otherwise the remainder of the specimen is in good condition. Based on notes on the LTRF taken when the specimen was illustrated and additional observations, we describe it below and compare it with other available specimens.
Description: A tadpole (USNM 562370, fig. 25) in stage 25 from Camp XI has the following measurements (all in mm): total length 76.0; body length 27.0; basal tail muscle height 7.8; basal tail muscle width 7.8; maximum dorsal fin height 2.8, this point being 20 mm away from body; maximum ventral fin height 2.8, this point being 24.4 mm away from body; body width 16.7; body depth 12.1; eye diameter 2.0; pupil diameter 0.8; interorbital distance 5.0; internarial distance 4.9; snout to nostril distance 6.5; snout to eye 2.5; snout to spiracle 21.7; oral disc diameter 14.9.
Oral disc enlarged and ventral; marginal papillae in single row, with contiguous papillae in offset disposition, but sometimes also forming second row. Few submarginal papillae scattered between distal labial tooth rows and labial edge. LTRF 16(16)/21(1). Gaps in rows A-16 and P-1 small, of about equal width. Teeth on proximal (closest to mouth) rows wider than teeth on distal rows; distal teeth 2–3 times more numerous per mm. Tooth density on P-1 about 35 teeth/mm. Upper jaw sheath long and slender, with uniform and small serrations. Lower jaw sheath wide, V- shaped, about four times as wide as upper jaw sheath, and with low, rounded serrations.
Body dorsoventrally flattened anteriorly, ovoid posteriorly. Eyes small, dorsolateral. Snout slightly truncated in dorsal view, gently slopping in profile. Nostrils relatively small (about 60% of eye diameter), with fleshy rim and two medial, contiguous, triangular projections, anterior one quite prominent and about twice as large as the posterior one. Spiracle lateral, sinistral, its inner wall fused with body wall along its distal half; opening oriented slightly dorsally. Vent tube dextral, twice as long as wide, fused with lower fin; angular aperture. Dorsal fin originating on terminal eighth of the body, anterior to origin of tail; lower fin originating at base of tail. Neuromasts not visible but presumably present and undetected because of the almost complete loss of pigmentation as an artifact of fixation. Melanophores also not visible but presumably present (see below).
Some variation was observed in comparing the described specimen (USNM 562370) with four other smaller specimens also in stage 25 (USNM 562731: TTL 48 mm, LTRF 14/15; USNM 567732: TTL? [tail taken for tissue], LTRF 14/18; USNM 562731[2]: TTL 41 and 22 mm, LTRF 13/15 and 9/10, respectively). We did not observe the second, minor triangular projection from the nostril rim in these specimens. Further studies will determine whether these projections are the same structures noticed by Mijares-Urrutia (1992) and Sanchez (2010) on several species of Hyloscirtus. Coloration of the body of USNM 567732 (a tissue voucher that was frozen in the field in liquid nitrogen) when it was thawed and preserved (Sept., 2005) was overall greenish with extensive concentrations of pigment on the head and body and patches of iridophores above the eyes; scattered patches of greenish color on the snout; neuromasts not visible and perhaps absent; melanophores (not visible in the other field-fixed specimens) visible and rodlike.
The LTRF of 16/21 reported for the largest tadpole (fig. 25) represents the largest labial toothrow formula known; it was erroneously reported as 17/21 and the largest value in hylids by Altig and McDiarmid (1999b: 308). The only tadpoles having large formulae that are close to the one reported here are those of M. inparquesi (a maximum of 14/21), M. aromatica (a maximum of 13/18), and the Hyloscirtus armatus group (a maximum of 14/17, Cadle and Altig, 1991; Lotters et al., 2005). Interestingly, the smaller tadpoles of M. neblinaria also have smaller formulae (ranging from 9/10 to 14/18). This apparent positive association between increased total length and LTRF could be related to a similar observation recently reported by Sanchez (2010) in tadpoles of Hyloscirtus; however, the underlying mechanism of ontogenetic increase in the number of labial tooth rows requires further study.
description: Published as part of Faivovich, Julián, Mcdiarmid, Roy W. & Myers, Charles W., 2013, Two new species of Myersiohyla (Anura: Hylidae) from Cerro de la Neblina, Venezuela, with comments on other species of the genus, pp. 1-63 in American Museum Novitates 2013 (3792) on pages 25-37, DOI: 10.1206/3792.1, http://zenodo.org/record/4597569