Bokermannohyla caramaschii

Pezzuti, Tiago Leite, Santos, Marcus Thadeu Teixeira, Martins, Sofia Velasquez, Leite, Felipe Sá Fortes, Garcia, Paulo Christiano Anchietta & Faivovich, Julián, 2015, The tadpoles of two species of the Bokermannohyla circumdata group (Hylidae, Cophomantini), Zootaxa 4048 (2), pp. 151-173 : 153-157

Bokermannohyla caramaschii

External morphology. Maximum total length 48.9 mm (at stage 37; Table 1 ). Body depressed (BH/BW = 0.84– 0.91), ovoid, or elliptical in dorsal view, 0.29–0.32 times TL; in lateral view, ventral contour slightly convex from peribranchial region to abdomen ( Fig. 1 A, B). Snout rounded in dorsal (BWN/BWE = 0.78–0.82) and lateral views. Eyes medium-sized (ED/BWE = 0.19–0.23), dorsally located (IOD/BWE = 0.63–0.73), dorsolaterally directed. Nostrils elliptical, medium-sized (ND/BL= 0.029–0.036), dorsally located, dorsolaterally directed, distance to snout 48–52% of eye-snout distance; elevated marginal rim, with well-developed trapezoidal to triangular fleshy projection on the medial margin, irregularly scalloped on lateral margin ( Fig. 1 E, F). Spiracle sinistral, lateral (SVD/BH = 0.46–0.62), posterodorsally directed, short (SL/BL = 0.04–0.07), opening at the Bokermannohyla caramaschii Bokermannohyla diamantina

Lot UFMG 1418 UFMG 1425 UFMG 1060

middle third of the body (SSD/BL = 0.52–0.61); internal wall fused to the body, with distal portion free and longer than the external wall ( Fig. 1 D). Intestinal tube circularly coiled, switchback point located at center of abdominal region ( Fig. 1 C). Vent tube dextral, posteriorly directed, twice as long as wide ( Fig. 1 G), fused to the ventral fin and positioned at its ventral margin. Oral disc medium-sized (ODW/BW = 0.30–0.38), ventrally positioned, with three posterior emarginations ( Fig. 2 ); 169–178 conical marginal papillae arranged in a single row, with its bases offset throughout the oral disc; narrow anterior gap present (about 0.17 of ODW); submarginal papillae absent; labial tooth row formula (LTRF) 2(2)/4(1), A2>A1, P1=P2>P3>P4; gaps in A-2 and P-1 about 0.2 and 0.08 mm, respectively; tooth density on P1 40–48 teeth/mm; absence of flaps with labial teeth laterally in the oral disc; jawsheaths wide, pigmented, finely serrated on the margins (22 to 28 triangular serrations on the upper jaw), upper jaw sheath arc-shaped and lower jaw sheath V-shaped, upper wider than lower. Tail low (MTH/TAL = 0.24–0.28); musculature robust (TMH/BH = 0.54–0.62); dorsal fin higher than ventral fin (DFH/VFH = 1.08–1.28); tail tip acute. Dorsal fin low (DFH/TAL = 0.07–0.09) with a slightly convex external margin; emerging at posterior third of the body with a low slope; maximum height at posterior third of tail. Ventral fin low (VFH/TAL = 0.06–0.07), with the external margin almost parallel to the longitudinal axis of the tail musculature; originates at base of tail, concealed by vent tube. Lateral line system distinct in life and in preserved specimens ( Figs. 3 , 4 ). All lines with transversally oriented stitches composed of two or three neuromasts. Supraorbital line with 15–16 stitches converging anteriorly on head, medial to nares, approaching the infraorbital series of 14–18 stitches. Infraorbital line begins behind eyes, extends anteriorly and is slightly curved in lateral profile ( Fig. 3 A, B). Posterior infraorbital line consists of a small aggregate series of five to seven stitches with no clear organization. Posterior supraorbital line composed of five stitches located near posterior portion of the supraorbital line. Angular line with 20–25 stitches, extends from below eyes to venter ( Fig. 3 A). Anterior oral line with 12–15 stitches, extends from lateral region of oral disc and approaches region of angular line, ventrally. Longitudinal oral line with 7–8 stitches, located between anterior region of anterior oral line and angular line. Two series of lines extend from mid body posteriorly throughout tail length ( Fig. 3 B): the first, dorsal line, with 13–15 stitches, located medially, converging before body-tail junction and continuing posteriorly with 22–27 stitches along dorsal fin base, until end of tail ( Fig.

3C); the second, middle-body line, with 20–22 stitches located laterally, joins the middle caudal series with 34–40 stitches. Along the approximate first third of tail this middle series projects dorsally reaching the dorsal fin base. A ventral body-line of 40–50 stitches extends anterodorsally from near vent tube forming a semicircle around spiracle, and after a small gap without neuromasts continues posteroventrally until mid abdominal region. A cumulus of neuromasts is present anterolateral to base of vent tube, near ventral line ( Fig. 3 D).

Coloration. In life, general pattern reddish to dark brown ( Fig. 4A ). Body with regularly scattered black spots; distal margin of spiracle lightly pigmented; iris reddish with irregularly scattered golden dots. Tail musculature finely reticulated with melanophores, and with irregular and dispersed dark spots, mainly on its anterior half; a longitudinal dark stripe starting from posterior end of body and extending posteriorly along medial caudal muscle line for first anterior 1/4 of tail; dorsal margin of caudal musculature with an interrupted narrow brown line; dorsal and ventral fins translucent, with irregularly scattered spots mainly on the dorsal fin. Neuromasts golden. In metamorphosing specimens, limbs light brown, with orange spots ( Fig. 4 B). In 10% formalin, the coloration fades and looses golden dots. Iris looses its golden tones and becomes black.

Variation. Two specimens in stages 29 and 33 have few submarginal papillae (1–2) randomly distributed laterally in the oral disc. Two individuals in stage 39, and one in stage 29, have LTRF 2(2)/3(1) ( Fig. 2 D). A specimen at stage 34 has a flap of labial teeth anterior to A1 ( Fig. 2 C). Three specimens have dorsal and ventral fins of the same height. The shape of the fleshy projections on the medial and lateral nostril margins is variable, even within the same specimen (i.e., right/left nostrils). There is no clear pattern of ontogenetic change in these characters.

Natural history notes. Bokermannohyla caramaschii tadpoles were found on the bottom of shallow, slowflowing muddy swamps associated with backwaters of permanent streams surrounded by semi-deciduous forests. The tadpoles are benthic and more active at night, when they can be found foraging among the sediment. Tadpoles in several developmental stages (including early stages) and froglets ( Fig. 4 B) were found in the same type of environment at both localities.

Oral cavity morphology. Buccal roof— roof sub-triangular, about 1.2 times longer than wide ( Fig. 5 A). One to three prenarial arena papillae with undulated margins disposed as transversal ridge along prenarial arena midline. Maximal internal nares length about 33% of Buccal Roof Width (BRW); internarial distance about 8% of BRW. Nares oriented 45º from midline; anterior wall short and thick with irregular margin; posterior wall (narial valves) large, wide and with distinct papillae; narial valves extending forward, covering almost completely the internal nares, but only a small portion of the vacuities. Large elliptical, smoothly concave, and shallow vacuities attached anteromedially to internal nares. Postnarial arena with one or two pairs of papillae distributed in an inverted V-shape, with posterior and external papillae larger than those more anterior and medial; three to five randomly distributed pustulations present. Median ridge trapezoidal to triangular with six to seven blunt, short papillae on anterior surface. One pair of medium-sized lateral ridge papillae with three to four secondary projections. Buccal Roof Arena (BRA) hexagonal with 7–14 short buccal roof arena papillae distributed mainly posterolaterally. In addition, 6–10 digitiform lateral roof papillae on each side. BRA with 288–310 homogeneously distributed pustulations. Secretory pits distinct in glandular zone, mainly posterolaterally in the dorsal velum. Dorsal velum large, discontinuous at midline (gap corresponding to 41% of BRW); irregular, discrete marginal papillae present. Buccal Floor — floor triangular, 1.2 times wider than long ( Fig. 5 B). Three pairs of infralabial papillae; two large hand-like papillae located anteriorly, and one pair of short digitiform papillae posteriorly. Some pustulations present antero-laterally. One pair of tall, digitiform lingual papillae present. Buccal Floor Arena (BFA) triangular, surrounded by 49–52 long, digitiform papillae. These papillae are disposed in two rows, one medially from anterior region of buccal pockets to median region of BFA, and one extending laterally and more obliquely following the anterior margin of ventral velum, towards the posterior region of BFA; larger papillae located anteriorly; two or three large papillae bifurcated. BFA with 197–210 pustulations, more concentrated posteriorly. Buccal pockets about 6 times wider than high, transversally oriented, deep, its width about 33% of Buccal Floor Width (BFW). Five or six short, conical prepocket papillae on each side. Ventral velum height about 31% of BFW. Posterior margin scalloped, with six distinct peaks over filter cavities; peaks 6% of BFW; median notch depth about 9% of BFW. Secretory pits distinct when stained with methylene blue, more concentrated on posterior margin of ventral velum but absent on median notch region. Glottis large, 20% visible, width about 10% of the BFW; thick and broad lips.

Figures

FIGURE 1. Bokermannohyla caramaschii (UFMG 1418) at stage 35: (A) lateral, (B) dorsal, and (C) ventral views. Scale bar = 10 mm. Details of (D) spiracular aperture, (E, F) margin of right nostrils with trapezoidal and triangular fleshy projections, respectively. Scale bars = 0.5 mm. (G) vent tube. Scale bar = 2 mm.

FIGURE 2. Oral discs of Bokermannohyla caramaschii (UFMG 1418): a closed (A) and opened (B) typical oral disc of a specimen at stage 37. Note the three posterior emarginations and the reduced P 4. (C) Unusual presence of flap with labial teeth anteriorly to A 1 in a specimen at stage 34. (D) The less common LTRF 2 (2) / 3 (1) of an individual at stage 29. Scale bars = 1 mm.

FIGURE 3. The lateral line system of Bokermannohyla caramaschii (UFMG 1418) in a stage 36 specimen. (A) Lateral view of body indicating the angular (AN), infraorbital (IO), longitudinal oral (LOR), anterior oral (AOR), posterior supraorbital (PSO), and ventral (V) lines. (B) Dorsal view of body showing the supraorbital (SO), infraorbital (IO), posterior infraorbital (PIO), middle (M), and dorsal (D) lines. Scale bars = 2 mm. (C) Detail of the tail and the distribution of the dorsal (D) and middle (M) lines. Scale bar = 10 mm. (D) Detail of the vent tube region of body showing the ventral line of neuromasts (V) and, encircled, the associated ventrolateral cumulus of neuromasts (N). Scale bar = 1 mm.

FIGURE 5. SEM micrographs of oral roof (A) and floor (B) of Bokermannohyla caramaschii at stage 37 (UFMG 1418). Scale bars = 2 mm. (1) Detail of the anterior region of roof: prenarial arena papillae (prnp); anteromedial vacuity of internal nares (amv); internal nares (in); narial valve projection (nvp); lateral ridge papilla (lrp); median ridge (mr); postnarial papillae (ptnp). (2) Detail of the posterior region of roof: lateral roof papillae (lrp); buccal roof arena (bra); buccal roof arena papillae (brap); dorsal velum (dv); secretory pits (sp). (3) Detail of the anterior region of floor: infralabial papillae (ilp); lingual papillae (lpa); lingual anlage (la). (4) Detail of the posterior region of floor: buccal floor arena (bfa); buccal floor arena papillae (bfap); buccal pocket (bp); prepocket papillae (ppp); vv (ventral velum); median notch (mn); glottis (g). Scale bars = 1 mm.

FIGURE 4. A tadpole at stage 37 (A) and a froglet (B) of Bokermannohyla caramaschii in life (UFMG 1418).

Tables

TABLE 1. Measurements (in mm) of tadpoles of Bokermannohyla caramaschii from Santa Teresa, State of Espírito Santo (UFMG 1418, 1425), and Bokermannohyla diamantina from Rio de Contas, State of Bahia (UFMG 1060), for some groups of Gosner (1960) stages. Data presented as mean ± standard deviation (range). For abbreviations, see text.

Stage (n)	29–33 (6)	35–38 (5)	39 (2)	30–35 (3)	27–30 (5)	33–35 (5)	36–38 (5)
TL	39.3 ± 0.8 (38.4–40)	45.4±2.8 (41.2–48.9)	(47.7–48.4)	46.5±2.2 (44.7–48.9)	41.8±3.0 (37.9–44.9)	43.3±1.3 (41.5–44.9)	43.8±1.3 (42.5–46.1)
BL	13.1±0.3 (12.8–13.6)	13.8±0.9 (12.7–15.1)	(13.4–15.6)	14.3±0.9 (13.6–15.3)	12.9±0.4 (12.4–13.6)	13.3±0.9 (11.6–13.9)	13.8±0.2 (13.4–14.1)
TAL	26.2±1.1 (24.8–27)	31.6±2.1 (28.0–34.2)	(32.7–34.2)	32.2±1.3 (31.1–33.7)	28.9±2.9 (25.2–32.5)	29.9±1.0 (28.8–31.2)	30.0±1.2 (28.8–32.1)
MTH	7.3±0.6 (6.5–8.1)	8.2±0.4 (7.9–8.9)	(8.3–8.6)	8.7±0.8 (7.9–9.5)	8.6±0.4 (8.2–9.3)	8.2±0.1 (8.0–8.5)	8.5±0.5 (7.8–9.4)
DFH	2.4±0.1 (2.3–2.5)	2.6±0.2 (2.3–2.3)	(2.3–2.6)	2.7±0.2 (2.4–2.8)	2.9±0.2 (2.6–3.1)	2.7±0.2 (2.5–3.0)	2.7±0.2 (2.4–3.0)
VFH	1.9±0.1 (1.8–2.1)	2.2±0.1 (2.0–2.4)	(1.9–2.1)	2.2±0.1 (2.0–2.3)	2.2±0.1 (2.0–2.4)	2.2±0.1 (2.0–2.4)	2.2±0.2 (2.0–2.6)
TMH	3.9±0.2 (3.7–4.2)	4.3±0.2 (4.0–4.5)	(4.5–4.5)	4.8±0.6 (4.2–5.4)	4.3±0.2 (4.0–4.6)	4.1±0.1 (3.9–4.3)	4.3±0.2 (4.1–4.6)
BH	6.8±0.3 (6.4–7.1)	7.3±0.7 (6.5–8.3)	(6.5–7.7)	7.9±0.6 (7.2–8.5)	7.5±0.6 (6.5–8.1)	7.7±0.6 (6.6–8.3)	7.7±0.5 (6.7–8.2)
SL	0.9±0.1 (0.8–1)	0.8±0.1 (0.6–0.9)	(0.7–0.9)	1.0±0.1 (0.9–1.0)	0.8±0.1 (0.7–1.0)	0.7±0.1 (0.7–0.9)	0.8±0.1 (0.7–1.0)
SVD	3.7±0.4 (3.2–4.3)	4.3±0.5 (3.8–5.0)	(4.1–4.2)	4.5±0.4 (4.1–4.9)	4.0±0.4 (3.7–4.5)	4.3±0.6 (3.7–5.2)	4.2±0.5 (3.5–5.0)
SSD	7.8±0.5 (7.3–9)	8.0±0.5 (7.3–8.8)	(6.6–9.6)	9.0±0.6 (8.3–9.4)	7.8±0.4 (7.2–8.4)	7.7±0.4 (7.0–8.1)	8.0±0.5 (7.3–8.8)
ED	1.2±0.1 (1.1–1.3)	1.4±0.1 (1.3–1.6)	(1.4–1.8)	1.3±0.2 (1.2–1.6)	1.2±0.1 (1.1–1.3)	1.2±0.1 (1.1–1.4)	1.5±0.0 (1.4–1.5)
BW	7.8±0.2 (7.6–8)	8.5±0.9 (7.2–9.9)	(8.6–9.4)	9.2±0.8 (8.6–10.1)	9.6±0.9 (8.2–10.5)	10.0±0.7 (8.5–10.5)	10.2±0.6 (9.0–10.7)
BWN	4.9±0.2 (4.7–5.1)	5.3±0.4 (4.8–5.6)	(5.0–5.0)	5.5±0.7 (4.8–6.3)	5.0±0.2 (4.7–5.3)	4.9±0.3 (4.7–5.4)	5.2±0.1 (5.0–5.4)
BWE	6.2±0.1 (6.1–6.3)	6.6±0.4 (6.1–7.2)	(6.6–6.9)	7.0±0.6 (6.5–7.7)	6.5±0.3 (6.2–7.0)	6.5±0.2 (6.3–6.7)	6.8±0.3 (6.5–7.2)
TMW	3.5±0.2 (3.2–3.7)	3.8±0.2 (3.6–4.1)	(4.3–6.6)	3.9±0.3 (3.6–4.2)	4.1±0.2 (3.8–4.3)	3.9±0.2 (3.7–4.1)	4.2±0.2 (4.0–4.5)
END	1.8±0.1 (1.7–2.0)	2.0±0.1 (1.8–2.2)	(2.0–2.1)	2.0±0.1 (1.9–2.1)	1.9±0.1 (1.9–2.1)	2.0±0.1 (1.8–2.1)	2.2±0.1 (2.1–2.4)
ESD	3.8±0.0 (3.8–3.8)	3.9±0.3 (3.7–4.4)	(3.4–4.0)	4.0±0.2 (3.8–4.2)	3.9±0.1 (3.8–4.1)	3.9±0.2 (3.6–4.2)	4.3±0.1 (4.1–4.4)
NSD	2.0±0.1 (1.9–2.0)	2.0±0.2 (1.8–2.2)	(1.4–1.9)	2.0±0.1 (1.9–2.1)	1.9±0.1 (1.9–2.1)	2.0±0.2 (1.8–2.2)	2.0±0.1 (2.0–2.2)
ND	0.5±0.0 (0.5–0.5)	0.4±0.0 (0.4–0.5)	(0.4–0.4)	0.4±0.0 (0.4–0.4)	0.4±0.0 (0.4–0.5)	0.42±0.0 (0.3–0.5)	0.4±0.0 (0.3–0.5)
IND	2.4±0.1 (2.2–2.6)	2.6±0.1 (2.4–2.8)	(2.5–2.7)	2.8±0.1 (2.7–2.9)	2.6±0.1 (2.5–2.9)	2.7±0.0 (2.7–2.8)	2.7±0.1 (2.6–2.8)
IOD	4.2±0.1 (4–4.3)	4.4±0.2 (4.0–4.8)	(4.3–4.8)	4.6±0.4 (4.4–5.0)	4.4±0.2 (4.2–4.6)	4.4±0.1 (4.3–4.6)	4.8±0.1 (4.7–4.8)
ODW	2.6±0.2 (2.5–2.9)	2.9±0.1 (2.7–3.1)	(2.7–3.0)	2.8±0.2 (2.6–3.1)	2.8±0.1 (2.6–2.9)	2.9±0.2 (2.6–3.1)	2.9±0.2 (2.7–3.2)