Fritziana izecksohni, Folly & Hepp & Carvalho-e-Silva, 2018

Folly, Manuella, Hepp, Fábio & Carvalho-e-Silva, Sergio P., 2018, A New Bromeligenous Species of Fritziana Mello-Leitão, 1937 (Amphibia: Anura: Hemiphractidae) from High Elevations in the Serra Dos Órgãos, Rio de Janeiro, Brazil, Herpetologica 74 (1), pp. 58-72 : 61-67

Fritziana izecksohni sp. nov.

( Figs. 2A , 3 , 4A,B , 5 )

Holotype. —An adult female (33.5 mm SVL), ZUFRJ 13978 ( Fig. 4A,B ), collected in a terrestrial bromeliad between the Abrigo IV and Pedra do Sino (22°27 ′ 37.1 ′′ S, 43°01 ′ 37.5 ′′ W; 2132 m a.s.l.), PARNASO , municipality of Teresópolis, state of Rio de Janeiro, Brazil, by Alice Magaldi, Fábio Hepp, Felipe Quintarelli, Pedro Feio, and Vanessa Araújo on 22 March 2013.

Paratypes. —Five males: three adult males (MNRJ 42602, 42606, and 42613) collected near Campo das Antas, PARNASO, municipality of Teresópolis, state of Rio de Janeiro, Brazil, by E. Gouveia on 20 January 1948 ; an adult male (ZUFRJ 14528) collected near a dam on the Beija-Flor River (22°27 ′ 48.8 ′′ S, 43°00 ′ 4.08 ′′ W; 1166 m a.s.l.), PARNA-SO, municipality of Teresópolis , state of Rio de Janeiro, Brazil, by Andressa M. Bezerra, Joice Ruggeri, and Manuella Folly, on 30 November 2013 ; and an adult male (ZUFRJ 13317) collected near Abrigo IV, Pedra do Sino (22°27 ′ 34.8 ′′ S, 43°01 ′ 42.2 ′′ W; 2146 m a.s.l.), PARNASO, municipality of Teresópolis , state of Rio de Janeiro, Brazil, by Cyro de Luna Dias , Joana Caram , Nathalie Citeli, and Manuella Folly on 24 September 2011 .

Diagnosis. —The radiograph ( Fig. 2A–D ) shows two diagnostic features for the genus Fritziana : large nasals, narrowly separated from the maxillae and premaxillae (see Duellman and Gray 1983), and quadratojugal not articulating with maxilla (see Castroviejo-Fisher et al. 2015). In addition to the osteological characters, the dorsolateral folds of the brood pouch of females of F. izecksohni (ZUFRJ 13978) matches the described pattern of the species of Fritziana (see Duellman and Gray 1983). The new species differs from the other species in the genus by the following combination of traits: (1) nostrils narrowly separated with 0.5 0.7 mm of IND/IOD (¯X ¼ 0.56 ± 0.07 mm); (2) diameter of tympanum equal to or larger than diameter of disc on third finger; (3) subarticular tubercles divided; (4) venter uniformly beige; (5) advertisement call with pulse groups composed of more than two pulses each; (6) advertisement call with longer first pulse group absent.

Comparisons with the other species. — Fritziana izecksohni differs from all other species of Fritziana by its dorsal coloration pattern, which is characterized by an interorbital triangle-shaped mark ( Figs. 3A , 4A ). Among the species that might have an interorbital triangle, F. ohausi has a marbled pattern on the dorsal and lateral surfaces, an interorbital brown triangle-shaped mark. Two stripes extend posteriorly from this interorbital mark; the stripes can be long and divergent, extending to the sacral region, short and divergent, or short and convergent (V-shaped mark). Fritziana goeldii has a brown interorbital hourglass-shaped mark extending to the middle of the body, and F. tonimi has, more commonly, an interorbital triangle and a posteriorly opened ‘‘V’’ or a bilobated mark reaching the insertion of the arm, or two dorsolateral lines originating on the snout, extending to the eye and tympanum, continuing posteriorly, and converging in the cloacal region, thereby forming a triangular shape (see fig. 4A,B of Walker et al. 2016). Fritziana ulei has an interorbital bronze pentagon-/hexagonshaped mark bordered by black ( Folly et al. 2014) and F. fissilis has a dorsal pattern consisting of beige with some small dark dots with patchy distribution ( Fig. 4C–E ).

The new species has divided subarticular tubercles on fingers IV and V and toes IV and V, differing from F. goeldii , F. ohausi , F. tonimi , and F. ulei (undivided subarticular tubercles on fingers and toes in these species). The new species has an average head width larger than the head length (HW/HL: ¯X ¼ 1.09 ± 0.004, n ¼ 5) differing from F. tonimi , which has a narrower head (HW/HL: ¯X ¼ 0.83 ± 0.08, n ¼ 3). Fritziana izecksohni differs from F. ohausi in its reproductive behavior of releasing tadpoles into water accumulated in bromeliads (tadpoles deposited in water accumulated in bamboo holes in F. ohausi ; Duellman and Gray 1983) and by having the nostrils more narrowly separated than in F. ohausi (IND/IOD ¼ 0.56 in F. izecksohni , and 0.82 in F. ohausi ). Fritziana izecksohni differs from F. fissilis by the tip of the snout being mucronate (snout outline rounded to nearly rounded, not mucronate in F. fissilis ) and by having larger females (SVL 33.5 mm in F. izecksohni and 27.4–28.0 mm in F. fissilis ). The new species has an average tympanum diameter larger than that of the disc on the third finger (TYD/DD3: ¯X ¼ 1.1 ± 0.13, n ¼ 5), differing from F. fissilis (TYD/DD3 0.80 ± 0.08, n ¼ 2) and F. ohausi (TYD/DD3: ¯X ¼ 0.70 ± 0.11, n ¼ 38), which have small tympanum diameters.

Description of holotype. —Dorsolateral folds of dorsal pouch partially developed ( Fig. 4A,B ). Skin on dorsal surfaces mostly smooth, head well tuberculated. SVL 33.5 mm, head slightly longer than wide (HL/HW ¼ 1.03). Snout mucronate in dorsal view, rounded in lateral view ( Fig. 3D ). Nostrils oval, lateral, closer to the tip of snout (NSD ¼ 1.3 mm) than to anterior corner of orbit; internarial distance equivalent to around 50% of interorbital distance (IND/IOD ¼ 0.45) and 21% of head width (IND/HW ¼ 0.21). Eye diameter (ED ¼ 3.7 mm) equivalent to 31% of the head length (ED/HL ¼ 0.31). Canthus rostralis distinct, rounded; loreal region concave. Tongue oval. Vomerine teeth between choanal openings. Tympanum distinct, large (TYD ¼ 1.6 mm), 43% of the diameter of the eye and equal to the diameter of disc on third finger (TYD/DD3 ¼ 1). Supratympanic fold well developed, extending from eye to insertion of arm. Outer margins of hand, arm, thigh, shank, knee, and tarsus crenulated. Arms long and thick; lengths of fingers II <III <V <IV; discs on fingers well developed; fingers not webbed; subarticular tubercles large, divided ( Fig. 3B,C ); six large palmar tubercles; number of tubercles on fingers II, III, IV, and V are 8, 4, 4, and 2, respectively. Relative toe lengths: I <II <V <III <IV; vestigial webbing between toes I and II; webbing formula, I 2–3 1/3 II 2 2/3–3 III 2–3 1/2 IV 4 1/2–3 2/3 V. Number of tubercles on toes I, II, III, IV, and V are 3, 4, 4, 6, and 2, respectively; five palmar tubercles. Venter granular.

Measurements of holotype (mm). —SVL 33.5; HL 11.9; HW 11.5; IND 2.4; IOD 5.1; ED 3.7; END 3.4; NSD 1.3; TYD 1.6; ARL 9.1; FRL 7.8; HNL 10.8; FIL 7.5; DD3 1.6; THL 16.4; SL 18.4; FL 25.4; TL 9.5.

Color of holotype in life. —Dorsal surface yellow to green, marked with dark brown dots ( Fig. 4A ); white interorbital triangle-shaped mark. Golden iris with narrow black lines forming a complex net. Forelimbs beige, with small brown spots. Thigh and shank beige with brown spots. Hind limbs beige, with narrow brown transverse bars. Ventral surface beige ( Fig. 4B ).

Color of holotype in preservative. —The coloration pattern was maintained with the white interorbital triangleshaped mark clear. Color of the dorsal surface became paler and color of the ventral surface remained beige, but lighter. Thigh and shank became a lighter beige but still with brown spots.

Variation. —Head longer than wide (HL/HW: 1.2 1.3, n ¼ 5); snout rounded (n ¼ 1) or semicircular (n ¼ 4) in dorsal view; internarial distance 54% of interorbital distance (IND/ IOD ¼ 0.5 0.6, n ¼ 5) and 19% of head width (IND/HW ¼ 0.17 0.20, n ¼ 5); eyes large (ED: ¯X ¼ 4.0 ± 1.0 mm, n ¼ 5), 52% of head length (ED/HL ¼ 0.44 0.74, n ¼ 5); tympanum distinct and small (TYD: ¯X ¼ 1.6 ± 0.3 mm, n ¼ 5), corresponding to 32% of eye diameter, and the diameter can be equal to or larger than the diameter of digit on third finger; female (holotype) is slightly larger than males ( Table 2 ). Male SVL ranges from 21.5 to 29.4 mm (n ¼ 5); males with single, median, and subgular vocal sac.

Variation in the dorsal pattern occurs in the direction, width, and continuity of the stripes of the dorsal pattern ( Fig. 5 ). The gray and white stripes from the dorsal pattern may be slightly curved at some parts, may have wider sections, may have short interruptions ( Fig. 5A ; MNRJ 48613 and 48606), or even be so interrupted that the dark stripe is divided into irregular brown spots bordered by white inverted-triangle shape ( Fig. 5B ; ZUFRJ 14528).

Regarding the 16S mitochondrial gene, we found a relatively high intraspecific divergence for F. izecksohni ( Fig. 1 ). This molecular divergence was even higher than interspecific divergences.

Advertisement call. —We classified all analyzed calls as advertisement calls because we found little variation among sampled calls ( Fig. 6 ). Each call ( Figs. 7 , 8 , 9G–I ) is composed of a sequence of pulse groups. Usually, the first pulse group has the lowest amplitude and thenceforth the amplitude gradually increases group by group until the amplitude peak. The amplitude peak often occurs with the last pulse group; however, it can be between the middle and the end of the call (i.e., with a decreasing amplitude period at the end of the call). The pulse-group period varies from 0.027 to 0.455 s (¯X ¼ 0.169 ± 0.057 s, mode ¼ 0.158 s, n ¼ 281). The pulse groups are composed of 1 to 35 pulses per group (¯X ¼ 4.6 ± 3.7, mode ¼ 3, n ¼ 331). The number of pulses per call varies from 10 to 47 (¯X ¼ 30.3 ± 8.3, mode ¼ 23, n ¼ 50). The pulse duration varies from 0.003 to 0.019 s (¯X ¼ 0.007 ± 0.001 s, mode ¼ 0.006 s, n ¼ 1517). The pulse interval varies from 0.001 to 0.048 s (¯X ¼ 0.007 ± 0.003 s, mode ¼ 0.005 s, n ¼ 1186). The pulse period varies from 0.006 to 0.054 s (¯X ¼ 0.013 ± 0.002 s, mode ¼ 0.012 s, n ¼ 1186). In the first one or two pulse groups, the relative amplitude between the pulses is similar to the common amplitude pattern of the call (i.e., with amplitude peak at the end). The rest of the pulse groups show an inverse pattern, with the first pulse having the peak amplitude, which decreases gradually pulse by pulse until the end of the group. Some calls are emitted with short intervals in between, resulting in call series. The call rate with calls regularly emitted was 0.5 calls per second (n ¼ 1). Although the pulses have a wide frequency band (1500–14,000 Hz), a harmonic series is notable (frequency bands more energetic in spectrogram), with up to six harmonics. The dominant frequency of the call corresponds to the fundamental one. Each pulse group sounds like a rattle. Occasionally a longer single pulse is emitted at the end of the call, resembling a short whistle ( Fig. 7 ).

Comparison with advertisement calls of species of Fritziana ( Table 1 ). —The advertisement call of F. izecksohni resembles that of F. goeldii in the typically quite regular pulse-group durations and many pulses (often more than two) per pulse group. The call of F. izecksohni can be distinguished from that of F. aff. fissilis sp. 1 (sensu Franz and de Mello 2015) by having a dominant frequency up to 2500 Hz (vs. higher than 3000 Hz in F. aff. fissilis sp. 1; Table 1 , Fig. 9 ); from that of F. fissilis by absence of a longer first pulse group followed by very short pulse groups (vs. present in F. fissilis ; Fig. 9 ; cf. Duellman and Gray 1983); and from that of F. ohausi by the presence of more than two pulses per pulse group (vs. pulse groups with up to two pulses in F. ohausi ; Fig. 9 ). The advertisement call of F. ulei is unknown ( Folly et al. 2014).

Etymology. —The specific epithet is a patronym in honor of Dr. Eugenio Izecksohn (1932–2013), who was a great herpetologist, describing 27 species of amphibians and having eight species described in his honor so far. He was professor of zoology at Universidade Federal Rural do Rio de Janeiro, state of Rio de Janeiro, Brazil from 1954 to 1992.

Distribution. —Areas in Serra dos Órgãos range ( Fig. 10 ): southeastern Brazil, state of Rio de Janeiro, municipality of Teresópolis (1166–2146 m a.s.l).

Natural history. —Specimens were found in bromeliads ( Bromeliaceae ), mostly from high elevations near Pedra do Sino (PARNASO), except for one specimen that was found at 1166 m. a.s.l.. The species is very abundant, being heard and found in bromeliads around Pedra do Sino, and currently is the only species of the genus Fritziana known to occur exclusively above 1166 m in PARNASO.

Figures

FIG. 2.—A male Fritziana izecksohni (A; ZUFRJ 13317), a male F. goeldii (B; UNIRIO 2538), a male F. ohausi (C; ZUFRJ 14094), and a male F. fissilis (D; ZUFRJ 14093) from municipality of Teresópolis, state of Rio de Janeiro; and a female F. ulei (E; ZUFRJ 13337) from municipality of Nova Friburgo, state of Rio de Janeiro. Radiographs with nasals and sphenethmoid as assigned on panel A. Note the spaces (hatched) between the nasals and maxillae. Mouths of the five specimens are opened. Scale bars ¼ 2 mm.

FIG. 3.—Dorsal view of the body (A), ventral view of the right foot (B), ventral view of the right hand (C), and lateral view of the head (D) from the holotype of Fritziana izecksohni (ZUFRJ 13978), an adult female from municipality of Teresópolis, state of Rio de Janeiro. Scale bars: 10 mm in A; 1 mm in B, C, D.

FIG. 4.—Dorsal (A) and ventral (B) views of the holotype of Fritziana izecksohni (ZUFRJ 13978) in life from Parque Nacional da Serra dos Órgãos, Teresópolis, state of Rio de Janeiro. Note the outline of a white exclamation-shaped mark on the dorsum and the slight development of the dorsolateral folds. Dorsal view (C) of F. fissilis (IVBC156) in life from Nova Friburgo, state of Rio de Janeiro (photo credit: B. Handam). Dorsal (D) and ventral (E) views of the lectotype of F. fissilis (MZUSP 30) from Nova Friburgo, state of Rio de Janeiro. A color version of this figure is available online.

FIG. 5.—Sketches of dorsal pattern variation of male paratypes (A: MNRJ 48613, SVL 21.5 mm; B: ZUFRJ 14528, SVL 25.1 mm) of Fritziana izecksohni. Note the interrupted pattern of an inverted triangle on the dorsum that differs from the holotype pattern seen in Fig. 4A.

FIG. 1.—Bayesian analysis tree for 16S sequence (GTR þ G; lnL ¼ 6452.395) of species of Fritziana. Posterior probability nodal support values (>0.8) from the Bayesian consensus tree are labeled above the branches. Different colors correspond to the conspecific lineages analyzed. Photos provided by R. Pontes (F. ohausi), B. Handam (F. fissilis), L.F.G. Peixoto (F. goeldii), and J.L. Gasparini (F. tonimi). A color version of this figure is available online.

FIG. 6.—Distribution of 50 calls from one voucher specimen of Fritziana izecksohni (ZUFRJ 13317) along the first and second axes of a principal component analysis (PCA) generated from 10 acoustical variables with 95% confidence ellipses. Note that there are no clear gaps within the variation. See text for explanations of the acronyms for the call variables.

FIG. 7.—Oscillogram (A) and spectrogram (B) of one advertisement call of Fritziana izecksohni (adult male ZUFRJ 13317) from municipality of Teresópolis, state of Rio de Janeiro. Oscillogram (C) and spectrogram (D) of the two pulse types, from left to right, short and long pulse (see text) belonging to the same specimen as depicted in panels A and B. Final longer pulse marked with asterisks. Spectrograms with Hann window function, window size 512 samples, overlap 99%, and amplitude plotted on a logarithmic scale.

FIG. 8.—Oscillogram (A) and spectrogram (B) of five advertisement calls of Fritziana izecksohni from municipality of Teresópolis, state of Rio de Janeiro. From left to right, note the decrease of pulse-group number per call and increase of pulse-group duration and pulse number (see text). Spectrogram with Hann window function, window size 512 samples, overlap 99%, and amplitude plotted on a logarithmic scale.

FIG. 9.—Oscillograms (A, D, G, J), spectrograms (B, E, H, K), and power spectra (C, F, I, L) of one advertisement call of each available Fritziana species: F. fissilis (A–C) from municipality of Teresópolis, state of Rio de Janeiro; F. goeldii (D–F) from municipality of Teresópolis, state of Rio de Janeiro; F. izecksohni (G–I) from municipality of Teresópolis, state of Rio de Janeiro; and F. ohausi (J–L) from municipality of Petropólis, state of Rio de Janeiro. Spectrograms and power spectra with Hann window function, window size 512 samples, overlap 99%, and amplitude plotted on a logarithmic scale.

FIG. 10.—Geographic distribution of the species of Fritziana in Brazil (upper-left inset). Fritziana aff. fissilis sp. 1 sensu Franz and de Mello (2015), and F. aff. fissilis sp. 2 sensu Castroviejo-Fisher et al. (2015).