Bokermannohyla sapiranga Brandão, Magalhães, Garda, Campos, Sebben & Maciel, 2012, sp. nov.
Creators: name: Brandão, Reuber Albuquerque
name: Magalhães, Rafael Félix De
name: Garda, Adrian Antonio
name: Campos, Leandro Abrósio
name: Sebben, Antonio
name: Maciel, Natan Medeiros
Publisher: name: Zenodo
Year: 2012
Subjects: Biodiversity
Taxonomy
Animalia
Chordata
Amphibia
Anura
Hylidae
Bokermannohyla
Bokermannohyla sapiranga

description: Bokermannohyla sapiranga sp. nov.
(Figs. 1–2)
Holotype. Brazil, Distrito Federal, Reserva Ecológica do Roncador (15°55’49” S, 47°52’59” W, 1110m asl), CHUNB 62384, adult male, R.A. Brandão, R.D. Françoso, T. Marques, R.M. Japiassu, and L.R.A. Braga col., 10 December 2009.
Paratypes. Brazil, Distrito Federal, Brasília (15°52’25” S, 47°51’59” W, 1070m asl), CFBH 2248–2249, adult males, A. Sebben col., no date. CHUNB 14383–14384, adult females, A. Sebben col., 0 1 April 1986. CHUNB 38832, adult male, unknown collector, 0 1 May 1993. CHUNB 14377–14379, juveniles, B. A. Duar col., 0 4 November 1994. Distrito Federal, Poço Azul (15°34’36’’ S, 48°02’30’’ W, 1090m als), CHUNB 40854–40855, adult males, R. A. Brandão col., 0 5 October 1994. CHUNB 14369–14376, juveniles, R. A. Brandão col., 23 October 1994. Distrito Federal, Fazenda Água Limpa (15°56’44’’ S, 47°54’34’’ W, 1085m asl), CHUNB 25080, adult male, unknown collector, 23 November 2002. CHUNB 49652, adult male, P. H. Valdujo col., 14 February 2007. CHUNB 5079550796, adult males, G. R. Colli col., 27 November 2007. State of Goiás, Cristalina Municipality (16°44’30’’ S, 47°41’36’’ W, 1050m asl), CHUNB 8369, adult male, G. R. Colli col., no date. CHUNB 14387, adult male, R. A. Brandão, col., 22 May 1998. State of Goiás, Pirenópolis Municipality (15°49’08’’ S, 48°59’08’’ W, 880m asl), CHUNB 14386, adult male, R. A. Brandão col., 22 June 1998. CHUNB 14380, adult male, R. A. Brandão col., 0 1 September 1992. Reserva Particular do Patrimônio Natural Vaga Fogo (15°49’17’’ S, 48°59’44’’ W, 810m asl), CHUNB 14390, adult male, M. G. Zatz col., 0 3 January 1999. Cocalzinho Municipality, Parque Estadual dos Pireneus (15°48’16’’ S, 48°50’05’’ W, 1270m asl), CHUNB 14388, adult male, R. A. Brandão col., 28 December 1998. Novo Gama Municipality (16°03’24’’ S, 48°01’21’’ W, 1080m asl), CHUNB 14381, adult male, A. Sebben col., 10 November 1987.
Diagnosis. The new species is diagnosed by the following combination of features: Medium size for the Bokermannohyla pseudopseudis group; dorsal coloration brownish ochre with darker scattered blotches; large eyes, forelimbs robust and short, with hypertrophied forearms in males; orange to reddish iris (bronze in some individuals); snout rounded in lateral and dorsal views (slightly acuminated in lateral view in some individuals); poorly-developed tibial fold, call frequency ranging from 0.5 to 0.7 kHz.
Comparison with other species of the Bokermannohyla pseudopseudis species group. Bokermannohyla sapiranga differs from B. alvarengai (in parentheses) by having: 1) snout rounded in dorsal and lateral views (truncate snout in dorsal view and vertical in lateral view); 2) head slightly longer than wide (head wider than long); 3) tympanic fold present (absent); 4) tibial fold less conspicuous, not extending from the metacarpal external tubercle to the elbow (very conspicuous tibial fold, from the elbow to the basis of the external metacarpal tubercle); 5) dorsum with several scattered blotches (dorsum without pattern or large dark patches); 6) dorsum blotches extending to the inguinal region (inguinal region without blotches or pattern); 7) thigh bars poorly defined (conspicuous); 8) hidden surfaces of thighs with bars (hidden surfaces thighs without blotches, bars or patterns); 9) vent tubercles small, inconspicuous, and white (vent tubercles conspicuous); 10) gular region with small circular and darker blotches (gular region immaculate). Bokermannohyla sapiranga differs from B. flavopicta (in parentheses) by having: 1) dorsal background brownish with dark brown blotches (dorsal pattern lichenous-like, composed of small dark brown blotches in a light gray to light brown background); 2) similar head width and head length (heads wider than longer); 3) glandular tissues on mental region not evident (evident glandular tissues on mental region); 4) absence of yellow dots on the body in live individuals (small yellow dots present on lips, eyelids, loreal and gular regions, supratympanic fold, fore and hind limbs, flanks, and anal flap in live individuals); 5) smaller females [39.8–54.5 (N=14) in B. sapiranga; 60.2–61.6 (N=2) in B. flavopicta]. The new species differs from B. ibitiguara (in parentheses) by having: 1) snout rounded in dorsal view (truncate in dorsal view); 2) presence of several darker blotches on the gular region, that sometimes reach the chest (gular region immaculate white); 3) bars on legs poorly defined, becoming paler on hidden surfaces of thighs, and resembling diffuse blotches; 4) same pattern on the flanks and inguinal regions (transversal bars conspicuous, narrower, and regularly spaced in legs, flanks, and inguinal region); 5) dorsal coloration brown, with regular and darker blotches (dorsal color tan without blotches); 6) males with conspicuously hypertrophied forearms (males with forearm less hypertrophied). Bokermannohyla sapiranga differs from B. itapoty (in parentheses) by having: 1) tarsal fold poorly developed, from the metacarpal external tubercle to 4/5 of forearm length (tarsal fold more evident, from the metacarpal external tubercle to the elbow); 2) snout rounded in lateral and dorsal views (snout truncate in lateral and dorsal views); 3) tympanum oval-shaped (tympanum round); 4) absence of white spots on the dorsum, canthus rostralis, and loreal region (presence of white spots in some individuals); 5) presence of blotches on the hidden surface of thighs (thighs dark brown, without any bars or spots); 6) evident hypertrophied forearms in males (discrete hypertrophy in forearms of males). Bokermannohyla sapiranga differs from B. oxente (in parentheses) by having: 1) forearms of adult males more robust and hypertrophied (forearm width 3.65±0.35, range: 3.08–3.97, N=9 for B. oxente and 5.83±0.70, range 5.02–7.68, N=13 for B. sapiranga); 2) large dark blotches on dorsum (not present); 3) developed prepollex (less developed prepollex); 4) hidden surface of thighs with blotches (hidden thigh surface brownish, without blotches); 5) cloacal flap without white supracloacal stripe (white supracloacal stripe present). Bokermannohyla sapiranga can be distinguished from B. pseudopseudis (in parentheses) by having: 1) rounded snout in dorsal view (snout truncate in dorsal view) and rounded or slightly acuminated in lateral view (vertical); 2) iris red, orange, or bronze (iris yellowish or golden); 3) less conspicuous tarsal fold (more conspicuous); 4) dorsal surface of the fingers and toes discs grayish brown (whitish). Bokermannohyla sapiranga differs from B. sagarana (in parentheses) by having: 1) snout profile truncate in dorsal and lateral views (rounded in dorsal view, truncate in lateral view); 2) dorsal background brownish with dark brown blotches (lichenous-like dorsal color pattern: light gray with darker and lighter blotches of irregular shape); 3) bars on dorsal thigh surface brownish, poorly defined (dark gray perpendicular bars covering dorsal surface of thighs, highly contrasted with the background color). Bokermannohyla sapiranga differs from B. saxicola (in parentheses) by having: 1) snout profile rounded in dorsal and lateral view (rounded in dorsal view, truncate in lateral view); 2) brownish dorsum (dorsum light gray with darker blotches); 3) bars on thighs reaching the hidden outer surface, but poorly defined (bars on hidden thigh surface narrow, well defined); 4) head slender (head robust); conspicuous arm hypertrophy in males (discrete hypertrophy in males forearm); 5) absence of light stripe on the cloacal flap (light stripe on cloacal flap present); 6) forelimbs robust (forelimbs width: 5.83±0.70, range 5.02–7.68, N= 17 in B. sapiranga; forelimbs width 3.78±0.51, range 2.96–4.60, N= 7 in B. saxicola); 8) prepollex well developed (prepollex less developed).
Description of holotype. Body robust (Fig. 1 and 2 A); head slightly longer than wider; snout rounded in lateral (Fig. 2 B) and in dorsal views; nostrils slightly protuberant, nostril aperture oval; eyes large, slightly protruding laterally; tympanum large, rounded; maximum eye length 1.5 times the maximum tympanum length; supratympanic fold evident, well-developed, extending from the posterior eye margin to the shoulder, at the level of the inferior tympanum margin. Vocal sac not externally expanded; vocal slits present; tongue large, wider than longer, almost cordiform; vomerine teeth disposed in two continuous rows, placed posterior to the choanae, forming an open angle (ten on the right and 9 on the left side); choanae large, almost circular, apart from each other; hypertrophied forearms (Fig. 1 and Fig. 2 B–C); external forearm fold evident, extending from the elbow to the wrist; well-developed prepollex, with a sharp spine, not exposed; slender fingers; subarticular tubercles simple, round, and well-developed; few round and discrete palmar tubercles; a large external metacarpal tubercle, fanshaped, partially divided in three parts (united at the basis) by two grooves on the internal margin; finger pads ovoid, single, well-developed; relative finger lengths IV>II>III>V; webbing hand formula II–III2 -–3- IV3–2 +V (Fig. 2 C); nuptial excrescence small, discrete, round, placed on the dorsal surface of finger II basis, at the prepollex junction; legs slender, thigh longer than tibia (Fig. 2 D); tarsal folds evident; internal tarsal fold from the posterior margin of the internal metatarsal tubercle to the heel (Fig. 2 D); external metatarsal fold less developed, extending two thirds the tarsal length from the first phalanx of toe V; internal metatarsal tubercle well developed, ovoid; external metatarsal tubercle small and round; subarticular tubercles simple and round; plantar tubercles small, discrete, round; relative toe length IV>V>III>II>I; web foot formula I1 +– 2II 1+– 1III 1+– 2IV 2– 1V (Fig. 2 E). Toe discs slightly less developed than finger discs; dorsal texture moderately granular; ventral region, chest, lateral flanks, and ventral thigh surface densely granular (Fig. 2 D); ventral tibia and ventral mandible surfaces smooth; vent region dark; an evident fold delimits the dorsum and the cloacal flap.
Measurements of holotype (in mm). SVL: 46.98, HL: 16.25, HW: 16.86, ED: 5.51, IOD: 7.86, END: 4.46, IND: 4.53, NSD: 3.28, TD: 2.95, PPL: 4.68, FDD: 1.90, TGL: 22.91, TBL: 25.52, FTL: 23.47, TDD: 1.83, FL: 7.48, FW: 5.75, HD: 15.72, AL: 6.56, TAL: 12.93.
Color in preservative. Dorsum brownish gray, with large dark brown or gray blotches; large dorsal dark brown blotches similar in size; flanks light gray with large dark brown or gray blotches; venter immaculate, whitish; gular region with several pale, brownish blotches; ventral tarsal surface brownish gray; dorsal surface of limbs brownish gray; ventral surfaces of toe discs white; hidden surfaces of the thighs dark brown.
Color in life. Dorsum and limbs brownish, with large darker brown blotches; iris reddish (Fig. 1 A), tympanum and foot webbing brownish; venter light ochre.
Morphometric analyses. Measurements of Bokermannohyla sapiranga are shown in Table 1.
To evaluate morphometric differences between B. sapiranga and B. pseudopseudis we used the model selection with shape variables. In this case, eight models were selected, all combining more than nine variables (Table 2). Just two models presented AICw value greater than 15.0. However, all the models selected share several variables. The variables snout-vent length, eye diameter, and tibia length were less important to explain the average model (Table 3). These variables were not recovered in any of the eight models selected by the AIC criterion (Table 2). The average model explained less than half of the differences between B. pseudopseudis and B. sapiranga (r² = 0.413; r² adjusted = 0.291). The variables head length, interorbital distance, head width, and fourth toe disc diameter were the four most important selected by the average model (Table 3), suggesting that the differences between B. pseudopseudis and the new species were related to the head proportions and size of the toe discs.
The PCA suggests that Bokermannohyla pseudopseudis and B. sapiranga are slightly different on general morphology (Fig. 3). The first two scores of the PCA account for 61.34% of the variance. The first component accounts for 40.48% of the variance and showed higher positive values for nostril-snout distance and interorbital distance, and higher negative values for third finger disc diameter, and fourth toe disc diameter (Table 4). The second component accounts for 20.86% of the variance, presenting higher positive value for third finger disc diameter, and higher negative value for tympanum diameter.
Advertisement call. The advertisement call of Bokermannohyla sapiranga from the type locality (Brasília municipality) consists of series of 5 to 7 notes with no harmonic structure (Fig. 4). Some notes show a pulsed structure (Fig. 4 A). Mean call duration was 997±16.4 ms (range = 759–1202 ms, N=5, Fig. 4 A). Mean note duration was 98.4±9.3 ms (range = 85–116 ms), and mean internote interval was 110±16.5 ms (range = 92–132 ms, Fig. 4 A). Dominant frequency did not vary (645.9 Hz, Fig. 4 B). Temporal call parameters from Brasília were slightly longer when compared to calls from Pirenópolis, in number of notes (3–5), mean call duration 520±14.2 ms (range = 380–790 ms) (N=13) and duration of notes (mean note duration = 67.5±6.2 ms, ranging 75–85 ms). Mean dominant frequency was also slightly shorter in Pirenópolis 559.9±49.7 Hz (range = 516.8–602.9 Hz).
The call of B. sapiranga is similar to calls of other species in the B. pseudopseudis group (Table 5). It is more similar to B. pseudopseudis, but readily separated from it by lacking the harmonic structure showed by B. pseudopseudis (pulsionated in B. sapiranga), along with differences in spectral features, number and duration of notes, and call length (Table 5). The maximum frequency in B. sapiranga is under 1.0 kHz, whereas in B. pseudopseudis it may reach 2.4 kHz (Eterovick & Brandão, 2001; Lugli & Haddad, 2006b). Mean call duration of B. pseudopseudis was 2.6s (Eterovick & Brandão 2001), while ranging 0.4– 1.2 s in B. sapiranga.
pure notes, without B. pseudopseudis 3 5–10 64 –84 56.4–71.8 0.4–2.4 up to five visible pulses
most notes are
B. sapiranga 4 5–7 85 –116 92–132 0.5–0.7 not present pulsed
Three main pure notes, without B. saxicola 5 25–25 22 –441 602 0.9–4.5 harmonics visible pulses Source for comparisons: 1 Cardoso (1983); 2 Lugli & Haddad (2006b); 3 Eterovick & Brandão (2001); 4Present work (call parameters based in the specimen recorded from Brasília municipality, type locality); 5 Bokermann (1964) and Eterovick & Brandão (2001).
Etymology. In Tupi indigenous language, sapiranga means red eye, an allusion to the reddish iris in the most individuals of the species. The specific epipeth is also homage to Marco (Sapiranga) Freitas, for his continuous efforts to popularize the Brazilian herpetofauna.
Distribution. Bokermannohyla sapiranga is known from the type locality (Brasília, Distrito Federal), and the Municipalities of Cristalina, Novo Gama, Catalão, and Pirenópolis, State of Goiás (Fig. 5).
Ecology and natural history notes. Bokermannohyla sapiranga and B. pseudopseudis are species associated with streams and rivulets with fast water flow in highlands of Central Brazil. Basking behavior was observed for both species, in Brasília (B. sapiranga) (Fig. 6 A) and Parque Nacional da Chapada dos Veadeiros (B. pseudopseudis). However, they present some ecological differences. Bokermannohyla pseudopseudis uses streams in open areas and rivulets with rocky beds, while B. sapiranga besides using similar habitats in some localities (e.g. Pirenópolis, Cristalina, and Brasília Municipalities) also occurs in dense wet gallery forest, calling near small waterfalls formed by roots and logs along rivulet (Brasília Municipality). In these habitats, tadpoles are found in pools and backwaters with mud beds. We never found B. pseudopseudis using such kind of habitat. As other species of the B. pseudopseudis group, B. sapiranga shows low ability to perch on the vegetation. Most individuals were observed on rocks, soil, or dead logs. In Brasília Municipality, Ameerega flavopicta, Aplastodiscus aff. perviridis, Barycholos ternetzi, Hypsiboas lundii, Hypsiboas goianus, Rhinella cerradensis, Rhinella rubescens, and Scinax skaios can be found in the same habitats where B. sapiranga occurs.
description: Published as part of Brandão, Reuber Albuquerque, Magalhães, Rafael Félix De, Garda, Adrian Antonio, Campos, Leandro Abrósio, Sebben, Antonio & Maciel, Natan Medeiros, 2012, A new species of Bokermannohyla (Anura: Hylidae) from highlands of Central Brazil, pp. 28-42 in Zootaxa 3527 on pages 30-38, DOI: 10.5281/zenodo.213546