Hyalinobatrachium mondolfii

Castroviejo-Fisher, Santiago, Vilà, Carles, Ayarzagüena, José, Blanc, Michel & Ernst, Raffael, 2011, Species diversity of Hyalinobatrachium glassfrogs (Amphibia: Centrolenidae) from the Guiana Shield, with the description of two new species, Zootaxa 3132, pp. 1-55 : 27-31

Hyalinobatrachium mondolfii

( Fig. 8 )

Señaris and Ayarzagüena, 2001: 1084.

Hyalinobatrachium sp. 1 Ernst et al.,2005: 183.

Type locality. First stream of Caño Acoima, tributary of Río Grande, slopes of Serranía de Imataca (08°22’N, 61°32’W; 15 m), Delta Amacuro, Venezuela.

Diagnosis. (1) Dentigerous process of vomer and vomerine teeth absent; (2) snout round in dorsal and lateral view; (3) tympanum covered by skin (not visible through skin); (4) dorsal skin from smooth to shagreened in life and preservative; (5) ventral skin granular, presence of small cloacal enameled warts; (6) parietal peritoneum transparent, pericardium, visceral and hepatic peritonea white, all other peritonea transparent; (7) liver bulbous; (8) humeral spine absent; (9) webbing formula of fingers III 2 – (1+ –1 1/2) IV; (10) webbing on feet I (1 1/4 – 1) – (1 3/4 – 1 1/4) II (1 1/4 – 1) – (2 – 1 1/2) III (1 1/4 – 1) – (2 – 1 3/4) IV (2 – 1 1/2) – (1 1/4 – 1) V; (11) enameled ulnar and tarsal folds; (12) nuptial excrescences Type-V, formed by a line of individual glands extended throughout the internal side of Finger I, this glands are also present in the lateral fringes of all fingers except the internal one of Finger III, prepollex not evident from external view; (13) Finger I longer than Finger II; (14) eye diameter larger than width of disc on Finger III; (15) color in life: dorsum with small yellow dots forming a light green reticulum dotted with dark and minute melanophores that in some specimens are more concentrated in the upper eyelid and specially around and between the nostrils where they form a brownish irregular patch, bones white; (16) color in preservative: dorsal surfaces cream with very small purple melanophores and white minuscule dots due to concentration of iridiophores that may or may not be lost; (17) irisgolden with small white spots and greyish-brown dots; (18) minute melanophores not extending throughout fingers and toes except base of Finger IV and Toe V; in life, tip of fingers and toes yellow; (19) advertisement call composed by a single tonal note lasting 0.18– 0.25 s, dominant frequency of 4989.6–5168.0. Hz, males mostly call from the underside of leaves; (20) fighting behavior unknown; (21) egg clutches deposited on the underside of leaves, males often on same leaf than eggs; (22) tadpole with sinistral spiracle, on longitudinal axis of the body and directed posteriorly; short and medial vent tube; (23) adult size between 19.9–22.8 (21.3 ± 0.8, N = 12) mm in males and 20.3–22.5 mm in two females.

Comparisons. The following unique combination of phenotypic characters differentiates Hyalinobatrachium mondolfii from all other species in the genus (but see below for exceptions): snout rounded in dorsal and lateral views, tympanic membrane and annulus not appreciable in life, pericardium white, hand webbing formula III 2 – (1+-1 1/2) IV, dorsal coloration in life light green with small yellow dots and minute melanophores, dorsal coloration in preservative pale cream dotted with minute melanophores and cream dots (could be lost in some specimens), iris coloration in life yellowish reticulated by dark flecks, coloration of bones in life white, coloration of hands and feet in life yellow, and a tonal single advertisement call without frequency modulation, lasting 0.18– 0.25 s and with dominant frequency of 4989.6–5168.0 Hz

Morphological, bioacoustic and genetic evidence allowing the differentiation between Hyalinobatrachium mondolfii and all other species of Hyalinobatrachium from the GS are summarized in Figs 2 , 3, 8 and Tables 1, 3. The species H. munozorum (Lynch & Duellman) and H. ruedai Ruiz-Carranza & Lynch are, as far as we know, morphologically undistinguishable among each other and with respect to H. mondolfii . Furthermore, their distributions are overlapping or adjacent with that of H. mondolfii . Castroviejo-Fisher et al. (2011) showed that H. munozorum and H. mondolfii might constitute independent evolving lineages on the basis of DNA sequences and, possibly, advertisement calls. Castroviejo-Fisher et al. (2011) also noted that their results should be interpreted with caution because sample size was particularly limited and the purported call of H. munozorum lacks a clear voucher specimen. Hyalinobatrachium ruedai is just known for the type series and there are no DNA sequences, tissue samples and/or bioacoustic information. With the data at hand we cannot resolve with enough confidence the taxonomic status of H. munozorum , H. mondolfii , and H. ruedai .

Remarks. A group of specimens coming from Guyana (Ernst et al. 2005) shows morphological similarities with Hyalinobatrachium mondolfii from the type locality in Venezuela, but with variations in color (in life and preservative). The fragment of mtDNA studied shows that both phenotypes share the same haplotype and they cluster together forming a clade. Also, their advertisement calls show no differences. We consider both phenotypes to belong to the same species and consequently assign them to H. mondolfii . The new population differs in the following characters (in parentheses characters for this population): golden iris (iris golden with small white areas and with greyish-brown dots spreading concentrically from pupil, where they appear at higher density); without concentrations of melanophores in dorsal surfaces (melanophores more concentrated in the upper eyelid and specially around and between the nostrils where they form a brownish irregular patch).

Señaris and Ayarzagüena (2005) described Hyalinobatrachium mondolfii as having granular dorsal skin and very granular skin around the tympanum. However, all specimens of H. mondolfii that we have studied (even those coming from the type locality of H. mondolfii ) have slightly shagreened dorsal skin and granular skin in the tympanic area. This could indicate that skin texture varies between individuals or that this dorsal granular skin appears at particular ontogenetic/reproductive states, as shown for skin structures in some species of Cochranella (e.g. Harvey and Noonan 2005). Hence, dorsal granular skin does not appear to be a distinctive character to differentiate H. mondolfii from other species of Hyalinobatrachium from the GS as suggested by Señaris and Ayarzagüena (2005).

Additional records of Hyalinobatrachium mondolfii in Guyana come from two localities in Iwokrama Forest: Turtle mountain (04° 43' 51.5" N, 58° 43' 27.2" W; MTD 47920, male) and the field Station (04° 40' 17.46" N, 58° 41' 06.56" W, MTD 47920, 48189–92, all males except MTD 48190, female). In January 2010 we found three specimens of Hyalinobatrachium mondolfii in Quebrada El Sufragio (04°0'11.42" S, 69°53'44.05" W; 116 m), Leticia, Amazonas, Colombia that represent the first record for the country. The three specimens were adult males that where calling (advertisement calls recorded) from the upper side of leaves. Although the data is not included in the analyses here presented, direct comparison with other specimens and calls of H. mondolfii allowed us to assign them to this species. Lynch (2005) also found this species in the surroundings of Leticia and reported it as Hyalinobatrachium sp.

Specimens reported as Cochranella sp. for Para, Brazil ( Avila-Pires et al. 2010) are here identified as members of Hyalinobatrachium mondolfii . This identification was based on photographs generously provided by M. S. Hoogmoed.

Biology and tadpole. Señaris and Ayarzagüena (2005) provide information about the position of calling males, number of eggs per clutch and advertisement call in Venezuela. Description of the advertisement call from specimens from Guyana and Venezuela is provided in Table 3 and Fig. 2 . Information from the new population from Guyana is as follows: males have frequently been observed next to their nesting sites. Clutches at varying stages of development (usually two) were found on the underside of leaves with a single calling male. Nest and associated calling sites were usually located at heights of 4–5 m in trees overhanging fast flowing segments of medium sized black water creeks, particularly Maiko Creek and its tributaries, Mabura Hill Forest Reserve (MHFR). There is no indication of males staying by the clutches during the day. In two cases calling sites were revisited during the day, however, only “abandoned” clutches without males were encountered. Whether or not males revisited these clutches in following nights was not confirmed.

Up to five males were recorded calling from the same tree usually during and after rain. Clutches consist of transparent gelatinous circular masses containing eggs 17–24 (19.6 ± 2.7; N = 5). A calling male (SMNS 12256) recorded on April 26, 2003, at the MHFR, was observed in the proximity (≤ 5 cm) of two clutches of different developmental stages. One clutch contained 19 eggs at stages 18–19 ( Gosner 1960), whereas the second clutch contained 17 undeveloped eggs. Egg and jelly color did not differ between these ontogenetic stages. The largest clutch recorded contained 24 eggs, at developmental stage 21–22 ( Gosner 1960), and tadpoles were about to hatch. This clutch was located on the underside of a leaf in a small tree overhanging Maiko Creek and was guarded by a calling male (SMNS 12258). A clutch guarded by a calling male (SMNS 12257) was collected in March 2004 and contained 19 eggs at stage 20–21. The clutch was transferred to a plastic terrarium and tadpoles were preserved in 70 % alcohol after hatching (no collection number assigned, SMNS 12257 also refers to the tadpole series).

An amplectant pair (SMNS 12259–60) that was caught in May 2004 and subsequently transferred to a plastic aquarium, remained in amplexus for several hours before spawning. The clutch, containing 19 eggs, was attached to the wall of the container but was apparently not fertilized as eggs did not develop in consequent days and finally started molding.

Tadpole description. All examined specimens (N = 18) belong to a single clutch (SMNS 12257); stages 25– 26 of Gosner (1960). Typical exotroph, lotic, fossorial tadpole (eco-morphological guild after Altig and Johnston, 1989). Elongate, vermiform habitus ( Fig. 6 ). Body ovoid, longer than wide (length approximately twice the width; BL/BW = 2.0), depth less than width (depth approximately half the width; BH/BW = 0.6); snout rounded in dorsal and lateral view; eyes dorsal, near sagittal line; pupils visible in dorsal view; dorsal surface flattened, oral disc anteroventral; belly flat; nostrils not protuberant, spiracle sinistral, on longitudinal axis of body, hardly visible, directed posteriorly; spiracular tube short (approx. 1 mm) triangular; cloacal tube medial, short; caudal musculature robust; caudal fins about half the width of caudal musculature at widest point (ventrally and dorsally), narrower at origin of tail muscle, expanding distally. Tail tip slightly pointed. Measurements are presented in Table 4 .

Oral disc large with well-developed anterior and posterior folds; posterior fold strongly fringed, anterior fold only distinctly fringed on lateral edges; both anterior and posterior jaw sheath wide and heavily serrated. Tooth rows are distinctly keratinized. Labial tooth row formula 2(2)/3. Labial papillae are large and irregularly fringed especially on posterior labium. Size reduced on anterior labium. Oral disc emarginated ( Fig. 9).

Tadpoles of Hyalinobatrachium mondolfii are easily distinguishable from tadpoles of the two sympatric centrolenid species ( H. cappellei and H. iaspidiense ) by their bright pink color in life ( Fig. 6 ), probably due to high concentrations of haemoglobin visible through large blood sinuses, indication of an adaptation to fossorial lotic habits. Color in preservative yellowish-white. Dorsal surface of body covered with dark brown melanophores; entire length of dorsal and caudal fins clear, however, covered with irregular but distinct white-pigmented spots bordering tail musculature. Ventral skin transparent. Eyes appear as sickle-shaped black-pigmented ring; lens off-white.

Ecology and distribution. The species inhabits lowland rain forest of the eastern Guiana Shield (15–200 m) and the western Amazon. It has exclusively been found in vegetation associated with streams. Here we showed that Hyalinobatrachium mondolfii has a wider distribution than originally thought, occurring in Bolivia (Castroviejo- Fisher et al. 2011), Brazil (this work), Colombia (this work), French Guiana (this work), Guyana, Suriname (this work) and Venezuela. Hyalinobatrachium mondolfii , like H. iaspidiense , has a broad distribution through the lowland Amazon rainforests.

Figures

FIGURES 2. Comparative oscillograms and spectograms of advertisement calls of Hyalinobatrachium species from the Guiana Shield and H. fleischmanni: (A) H. fleischmanni from Panama, audio from Ibañez et al. (1999); (B) H. kawense sp. nov. from French Guiana, MNCN 44825; (C) H. cappellei Venezuela, MHNLS 17328; (D) H. cappellei French Guiana, audio from Marty and Gaucher (1999); (E) H. iaspidiense from Venezuela, MHNLS 13495; (F) H. iaspidiense from French Guiana, audio from Marty and Gaucher (1999); (G) H. mesai, holotype; (H) H. tricolor sp. nov. from type locality in French Guiana, uncollected specimen; (I) H. mondolfii from Venezuela, MHNLS 17120; (J) H. taylori from Venezuela, MHNLS 13496.

FIGURES 6. Tadpoles of (A) Hyalinobatrachium cappellei, (B) H. iaspidiense; (C, D) H. mondolfii. RE (A, B), MB (C, D).

FIGURES 8. Adult males of Hyalinobatrachium mondolfii. (A) Topotype, MHNLS 17122, SVL = 22.2 mm; (B) MNHN 2011.0126, SVL = 23.0 mm; (C) MTD 48148, SVL = 22.0 mm; (D, E) SMNS 12255, SVL = 20.7 mm; (F) egg clutch on the underside of a leaf. Photographs by SCF (A), MB (B – C, F) and RE (D – E).

Tables

TABLE 4. Morphological features (mean ± SD, range) of Hyalinobatrachium mondolfii tadpoles (N = 18, stages 25 – 26). TL = total length; BL = body length; TAL = tail length; BW = body width; BH = body height; ED = horizontal eye diameter; IOD = interorbital distance; ESD = eye snout distance; TMH = tail muscle height; TH = total tail height; TFH = dorsal tail fin height.

Parameter	Average ± SD	Range
TL	14.9 ± 1.08	13.0–17.0
BL TAL TAL/TL BW BH	4.7 ± 0.49 10.2 ± 0.69 0.7 ± 0.02 2.3 ± 0.14 1.3 ± 0.14	4.0–5.5 9.0–11.5 0.66–0.71 2.1–2.5 1.1–1.5
ED	0.2 ± 0.02	0.2–0.3
IOD	0.6 ± 0.04	0.5–0.6
ESD	1.1 ± 0.09	1.0–1.2
TMH TH TFH	1.0 ± 0.07 1.8 ± 0.22 0.4 ± 0.10	0.8–1.1 1.5–2.1 0.3–0.6