Bokermannohyla napolii, Carvalho, Thiago Ribeiro De, Giaretta, Ariovaldo Antonio & Magrini, Leandro, 2012

Carvalho, Thiago Ribeiro De, Giaretta, Ariovaldo Antonio & Magrini, Leandro, 2012, A new species of the Bokermannohyla circumdata group (Anura: Hylidae) from southeastern Brazil, with bioacoustic data on seven species of the genus, Zootaxa 3321, pp. 37-55 : 39-46

Bokermannohyla napolii sp. nov.

Figures 1 , 2 (left), and 3

Holotype. UFMG 3333 (Ex-AAG-UFU 4767), adult male, collected at the Estação de Pesquisa e Desenvolvimento Ambiental Galheiro (EPDA-Galheiro; 19o12ʹS; 47 o0 8 ʹW, 845 m a.s.l.), Municipality of Perdizes, State of Minas Gerais, southeastern Brazil, on 16 October 2009, by A. A. Giaretta, T. R. de Carvalho, L. B. Martins, and B. F. V. Teixeira. Paratopotypes. Five adult males: AAG-UFU 4774–4775, UFMG 3334 (Ex-AAG-UFU 4770), and ZUEC 16610 (Ex-AAG-UFU 4771), collected with the holotype; AAG-UFU 0 860, on 3 December 2011, by A. A. Giaretta. Three adult females: AAG-UFU 4773, UFMG 3335 (Ex-AAG-UFU 4769), ZUEC 16609 (Ex-AAG-UFU 4768), collected with the holotype.

Diagnosis. Bokermannohyla is currently supported only by molecular data, and a thorough morphological study of the genus still needs to be done ( Faivovich et al. 2005, 2009). Thus, we assign B. napolii sp. nov. to this genus on the basis of its phenotypic similarity to other species in the genus. Bokermannohyla napolii sp. nov. is assigned to the B. circumdata species group as it has transverse dark brown stripes on dorsum, simple (not dichotomized or anastomosed) dark brown transverse stripes on posterior surfaces of thighs and flanks, single (not bifid) large sharp prepollex, and adult males having hypertrophied forearms. The new taxon is diagnosed by the following combination of traits: (1) medium size (adult SVL 49.7–55.0 mm); (2) head wider than longer; (3) dark brown transverse stripes on dorsum; (4) dark brown vertical bars on posterior and superior surfaces of thighs; (5) vocal slits present in adult males; (6) bifid/divided distal tubercle of finger III in males, and bifid/divided distal tubercle of finger IV in males and females; (7) distinctive advertisement call pattern (see call description section).

Brazil); B. circumdata from the Municipality of Chiador (State of Minas Gerais, Brazil), and District of Paranapiacaba (State of

São Paulo, Brazil); and B. napolii sp. nov. from the type locality. Mean + standard deviation (minimum–maximum). N = num-

ber of recorded males.

Variables Bokermannohyla Bokermannohyla Bokermannohyla Bokermannohyla luctuosa circumdata (MG) circumdata (SP) napolii sp. nov. N=1 N=1 N=1 N=6

Advertisement call 607.7+48.2 (550–708) __ __ 619.7+71.7 (460–807)

duration (ms)

Note types A/B 110.8+11.1 (97–138) __ __ 133.3+17.2 (82–167)

internote interval (ms)

Note type A duration 57.2+20.3 (23–93) 95.0+15.3 (71–120) __ 93.4+15.6 (53–156)

(ms)

Note type A dominant 0.57+0.09 (0.49–0.65) 0.48+0.12 (0.33– __ 0.43+0.07 (0.39–0.56) /

frequencies (kHz) / 0.66) / 0.73+0.05 0.77+0.06 (0.73–0.90)

harmonics (0.70–0.80) / 1.47+0.05 (1.34–1.51) / 1.82+0.08 (1.68–1.85)

Advertisement call 6.8+2.4 (4–8) __ 11.1+2.4 (8–14) 6.7+4.6 (1–14)

rate (calls/minute)

Note type B duration 440.6+46.6 (371–526) 778.0+42.4 (748– 495.3+55.8 (235–544) 399.5+77.4 (242–550)

(ms) 808)

Note type B dominant 0.47 / 0.88+0.04 (0.82– 0.47+0.07 (0.42– 0.54+0.04 (0.52–0.61) / 0.51+0.06 (0.47–0.65) /

frequencies (kHz) / 0.90) / 1.23+0.06 (1.16– 0.52) / 0.89 1.05+0.05 (0.98–1.08) / 1.17+0.14 (0.82–1.34)

harmonics 1.34) / 1.65+0.04 (1.59– 1.46+0.03 (1.45–1.55) / 1.57+0.07 (1.42–1.68) / 1.68) / 1.98+0.09 (1.85– 2.05+0.04 (2.04–2.11) 2.02)

Harmonic groups/note 12.2+1.3 (10–15) __ 15.7+1.6 (7–16) 2.5+1.2 (1–5)

Comparisons with other species. Bokermannohyla napolii sp. nov. (adult male SVL 52.5–55.0 mm; adult female SVL 49.7–53.7 mm) is set apart by its larger size from the small-sized (combined SVL 30.1–47.6 mm; cf. Napoli 2000) species of the B. circumdata group [ B. astartea (Bokermann 1967) , B. feioi ( Napoli & Caramaschi 2004) , B. ibitipoca ( Caramaschi & Feio 1990) , B. izecksohni ( Jim & Caramaschi 1979) , B. nanuzae , B. ravida ( Caramaschi, Napoli & Bernardes 2001) , and B. sazimai ].

Bokermannohyla napolii sp. nov. has a wider than longer head, whereas the head in B. ahenea ( Napoli & Caramaschi 2004) , B. capra Napoli and Pimenta (2009) , B. feioi , B. hylax , and B. lucianae ( Napoli & Pimenta 2003) is longer than wider. The new species is also distinguished by having dark brown transverse stripes on dorsum and limbs, which are immaculate in B. ahenea , B. astartea , B. carvalhoi , and B. gouveai ( Peixoto & Cruz 1992) ; immaculate or with weak dark brown transverse bands in B. capra , B. diamantina Napoli and Juncá (2006) , B. izecksohni , and B. lucianae ; and with a reticulated pattern in B. sazimai . Furthermore, the new taxon is distinguished by having dark brown vertical bars on posterior surface of thighs, which is immaculate in B. feioi , B. gouveai , B. nanuzae , and B. lucianae ; fragmented in B. carvalhoi , and anastomosed in B. vulcaniae ( Vasconcelos & Giaretta 2003) . From B. caramaschii ( Napoli 2005) and B. izecksohni , the new species is also distinguished by having vocal slits in adult males (absent in the other two species).

The distal bifid/divided subarticular tubercles of fingers III and IV in males, and finger IV in males and females (fig. 2) diagnose B. napolii sp. nov. from B. ahenea , B. astartea , B. carvalhoi , B. feioi , B. gouveai , B. hylax , B. ibitipoca , B. izecksohni , B. luctuosa , B. nanuzae , B. sazimai , and B. vulcaniae .

The advertisement call of Bokermannohyla napolii sp. nov. differs from that of all species of the B. circumdata group with calls described so far (unknown advertisement calls: B. ahenea , B. caramaschii , B. gouveai , B. izecksohni , B. ravida , and B. vulcaniae ), except B. circumdata and B. luctuosa , due to its harmonic structure. The advertisement call of the new species (figs. 6 A–B) most resembles the call pattern of B. circumdata (fig. 6 C) and B. luctuosa (fig. 6 D). Advertisement calls of B. circumdata , B. luctuosa , and B. napolii sp. nov. are composed of a short note followed by a long note. The first two have long notes composed of several disjunctive and/or juxtaposed harmonic groups, whereas the long note of B. napolii sp. nov. has fewer well-defined harmonic groups (1–5) with more sound intensity at the beginning of the note, or ill-defined harmonic groups with increasingly weaker sound intensity along its extent.

Description of holotype. Adult male (UFMG 3333; figs. 1, 2(left), and 3). Body robust; head wider than longer. Snout rounded in dorsal and lateral views (figs. 3 A-B, respectively); nostrils directed laterally, much closer to the tip of snout than to the eye; canthus rostralis distinct; loreal region slightly concave; tympanum circular, 83% of the eye diameter; supra-tympanic fold present; pupil horizontal; vocal sac single, subgular, expanded; vocal slits present; tongue round; vomerine teeth in two almost contiguous, slightly arched series between choanae. Crenulated ridge on outer surface of forearms; forearm hypertrophied; finger lengths when put together I<II<IV<III (fig. 3 C); disks of fingers II, III, and IV larger than that of I; disk of finger III 75 % of the tympanum diameter; distal subarticular tubercles of fingers I and II ovoid, those of fingers III and IV bifid/divided; nuptial pads present; pollical tubercle large, elongated; prepollex well-developed, spine curved, completely covered by skin; inner metacarpal tubercle region formed by several smaller granular tubercles; palmar tubercle developed, elongated, divided; supernumerary tubercles present on the palm of hand; hand webbing formula I 2–3 II 2 -–2 2/3 III 2 1/2– 2 IV. Toe lengths when put together I<II<V<III<IV (fig. 3 D); disks of toes III, IV, and V larger than those of I and II; disk of toe IV 68 % of the tympanum diameter; toe webbing formula I 1–2 - II 1–2 III 1–2 + IV 2 +– 1 V; inner metatarsal tubercle ovoid, outer metatarsal tubercle barely distinct; toes fringed; supernumerary tubercles on the sole of foot; subarticular tubercles of toes rounded; inner tarsal fold weak, extending along full length of the tarsus; outer surface of tarsi. Dorsal surfaces and flanks smooth; belly granular; supra-vent granular ridge defined; discrete pointed dermal protuberance on outer heel present.

Measurements of holotype. Morphometric characters (mm) and ratios (%) in relation to SVL (52.5 mm): HL 19.2 (36.6), HW 19.6 (37.3), ED 4.8 (9.1), TD 4.0 (7.6), END 5.1 (9.7), TL 28.5 (54.3), SL 29.0 (55.2), FL 24.5 (46.7), HAL 18.6 (35.4), 3FD 3.0 (5.7), 4TD 2.7 (5.1).

Color of holotype in life (fig. 1). Dorsal surfaces uniformly pale cream, with subtly darker transverse stripes; a few white dots and blotches on dorsal surfaces and flanks; background color of the hidden parts of thighs and arms bluish and violet, with 8–9 dark brown vertical bars on posterior and superior surfaces; dorsal surface of shanks with 4–6 dark brown transverse stripes; flanks with subtle violet bars on a yellow marked region; inguinal region tending to the same color (violet) of the hidden parts of thighs, with a few dark brown transverse bars; supra-vent crenulated ridge white; crenulated ridge on outer forearm white; throat, chest, and belly light cream; iris gold, pupil black; tympanum tends to violet.

Color of holotype in preservative. Dorsum dark grayish brown with some faded parts on dorsum and limbs, and dark brown transverse stripes barely distinct on dorsum; a few white blotches scattered on dorsum, limbs, and flanks; hidden parts of thighs and arms light gray, their posterior and superior surfaces with 8–9 dark brown vertical bars; anterior surface of thighs immaculate; dorsal surface of shanks with 4–6 dark brown transverse stripes, sometimes fragmented; dark brown transverse stripes on dorsal surface of forearms indistinct; background color of flanks light gray, with a few dark brown reticulations, especially on inguinal region; supra-vent crenulated ridge white; crenulated ridge on outer forearm white; throat, chest, belly, and ventral surfaces of limbs cream, gular region with dark brown punctuations bordering lower jaw, region of tubercles and webbing of hands and feet slightly gray; tympanum brown, slightly lighter than dorsal coloration pattern.

Variation. Dorsum varies in color from medium brown (females) to dark gray (males) in ethanol preserved specimens. Number of dark brown vertical bars on dorsal surfaces of forearms (3–4), thighs (6–10), shanks (4–7), and tarsi (3–4). Dark brown transverse stripes on dorsal surfaces may be barely distinct. The male specimen AAG- UFU 0 860 has no distinctive transverse stripes on dorsal surfaces. The presence and extent of white blotches on dorsum and limbs are variable, being completely absent in AAG-UFU 4775. Type series, except the holotype and AAG-UFU 0 860, has a dark brown vertebral stripe, sometimes restricted to the first half of dorsal length. One female (AAG-UFU 4773) has distal subarticular tubercles of finger III divided; one male (AAG-UFU 4774) has distal subarticular tubercles fingers III and IV cordiform. Two male specimens (AAG-UFU 4775 and ZUEC 16610) have distal subarticular tubercles of finger I divided.

Natural History. Despite extensive fieldworks since 2001, this species was only heard (found) in 2009, during an explosive breeding event. Afterwards, a few males were heard once at the end of 2011. Males started calling late at night (around 01:00 AM), and a few males were heard still calling at nearly midday on the next day. They gathered around a muddy slow-watered section of a stream at the forest border. Males (N = 10) were calling from the ground or perched on low (<1 m high) vegetation. Egg clutches (N = 4; fig. 4) were laid 5–10 cm deep and hidden among dead broad leaves under water. Eggs were adhered to each other so that the entire egg mass (fresh, <6 hours) could be removed from water using both hands to scoop it up. Number of eggs per clutch ranged from 373 to 742 (mean 637, SD = 176, N = 4 egg clutches); yolk diameter ranged from 1.2 to 2.3 mm (mean 1.8, SD = 0.3, N = 3 egg clutches); gelatinous capsules ranged from 3.8 to 5.4 mm (mean 4.4, SD = 0.6, N = 4 egg clutches). Three collected females released ovocytes inside plastic bags: yolk diameter ranged from 1.5 to 2.2 (mean 2.0, SD = 0.6); gelatinous capsules ranged from 3.1 to 5.4 mm (mean 4.2, SD = 0.5). Some males had their backs scratched (fig. 1), probably as a result of agonistic interactions. The new species occurs simpatrically with Bokermannohyla sazimai , Hypsiboas faber (Wied-Neuwied) , Hypsiboas goianus (Lutz) , Hypsiboas lundii (Burmeister) , and Scinax canastrensis (Cardoso & Haddad) .

Geographic distribution. Bokermannohyla napolii sp. nov. is known only from the type locality. (fig. 5).

Etymology. The name is a noun in the genitive case honoring Marcelo F. Napoli for his extensive contribution to the knowledge of the genus Bokermannohyla .

Vocalizations of Bokermannohyla napolii sp. nov. Six males recorded (N = 76 advertisement call samples; N = 43 aggressive call samples). Quantitative traits are summarized in Table 2. Advertisement call is composed of two note types (referred herein to as note types A and B; figs. 6 A-B) emitted consecutively at a rate of 1–14 calls/minute (mean 6.7, SD = 4.6). Additional notes B may eventually be emitted just after a typical A/B sequence though. Advertisement call duration (notes A + B) was 460–807 ms (mean 619.7, SD = 71.7). Note A is a short note (53– 156 ms; mean 93.4, SD = 15.6) with 5–6 harmonics. Dominant frequencies from 0.39–0.56 kHz (mean 0.43, SD = 0.07), from 0.73–0.90 kHz (mean 0.77, SD = 0.06), from 1.34–1.51 kHz (mean 1.47, SD = 0.05), and from 1.68– 1.85 kHz (mean 1.82, SD = 0.08), which correspond to the first four harmonics. Note B is a long note (242–550 ms; mean 399.5, SD = 77.4) with a harmonic structure (5–6 harmonics; sometimes ill-defined), and sound intensity concentrated the most on the first part of the note, and sound intensity modulations forming 1–5 disjunctive or juxtaposed harmonic groups (mean 2.5, SD = 1.2) along its extent, or with ill-defined harmonic structure (N = 8 note samples). A/B internote interval from 82–167 ms (mean 133.3, SD = 17.2). Dominant frequencies from 0.47–0.65 kHz (mean 0.51, SD = 0.06), from 0.82–1.34 kHz (mean 1.17, SD = 0.14), from 1.42–1.68 kHz (mean 1.57, SD = 0.07), and from 2.02–2.11 kHz (mean 2.05, SD = 0.04), which correspond to the first four harmonics.

We have also identified a third note type (referred herein to as note type C; fig. 7 A) that should possibly be attributed to a kind of aggressive call (sensu Wells 2007) because it has an ill-defined lower sound intensity structure with remarkable differences in temporal traits (longer duration) in comparison with note B, yet similar in spectral traits (dominant frequencies). Besides, this aggressive call has no distinguishable harmonic structure as in notes A and B of the advertisement call. Note C is emitted at a rate of 12–26 notes/minute (mean 20.0, SD = 5.7) alone or just after a note A. The emission rate of advertisement calls of a given male was inversely proportional to the emission rate of aggressive calls. Note C duration was 437–1,120 ms (mean 763.9, SD = 210.4) with A/C internote interval from 90–128 ms (mean 115.3, SD = 14.6). Despite the absence of well-defined harmonic structure, dominant frequencies coincided with those of note type A.

Figures

FIGURE 1. Adult specimens of Bokermannohyla napolii sp. nov. in life. Specimens from the Estação de Pesquisa e Desenvolvimento Ambiental Galheiro (EPDA-Galheiro), Municipality of Perdizes, State of Minas Gerais, Brazil. Upper, holotype UFMG 3333; Lower, female paratopotype ZUEC 16609.

FIGURE 2. Ventral view of hands of adult male specimens of Bokermannohyla napolii sp. nov. (left: ZUEC 16610) and B. luctuosa (right: AAG-UFU 0473). The arrows point to the divided tubercles of fingers III and IV in B. napolii sp. nov.