Boana guarinimirim, Marinho & Bang & Vidigal & Giaretta, 2022

Marinho, Pedro, Bang, Davi L., Vidigal, Izadora & Giaretta, Ariovaldo A., 2022, A New Cryptic Species of Boana (Hylinae: Cophomantini) of the B. polytaenia Clade from the Brazilian Atlantic Forest, Journal of Herpetology 56 (3), pp. 278-293 : 280-287

Boana guarinimirim sp. nov.

( Fig. 2 )

Hypsiboas polytaenius ( Montesinos et al., 2012; Silva-Soares and Scherrer, 2013)

Boana polytaenia ( Zornosa-Torres et al., 2020)

Boana polytaenia ( Vasconcellos et al., 2021)

Boana sp. 3 ( Faivovich et al., 2021)

‘‘ Boana sp. 4 '' MT 823836 2.58 2.59 2.59 2.59 2.18 2.99 3.20 2.18 3.19 2.99 2.98 0.78 0.78 0.78 0.78 1.18 1.18 0.00 0.20 0.78 0.98 0.78

Holotype.— CFBH 46043 ( Fig. 2 ), an adult male collected in Brazil: State of Espírito Santo, Municipality of Castelo, Parque Estadual do Forno Grande , at Poços Amarelos (20831 0 1.21" S, 4185 0 19.85" W; 1,312 m) on 25 November 2021 by P. Marinho, T.R. Carvalho, and M.T.T. Santos .

Paratypes.—14 adult males. CFBH 46037 –42, collected with the holotype by the same collectors ; AAG-UFU 6772 –76 collected at the same locality of the holotype on 28 November 2019 by D.L. Bang, I. Vidigal, and P. Marinho ; AAG-UFU 6798 –00 collected in the surroundings of Parque Estadual do Forno Grande (20831 0 0.46"S, 4184 0 59.73"W; 1,115 m), on 28 November 2019 by D.L. Bang, I. Vidigal, and P. Marinho .

Diagnosis.— Boana guarinimirim sp. nov. can be distinguished from most of its congeners of the B. pulchella group by the following combination of characters: 1) dorsal pattern composed of longitudinal lines and stripes; 2) a small SVL of 24.1–28.1 mm (26.0 6 1.1; Table 3) in males; 3) no spots or vertical bars on hidden surfaces of legs, groin, and flanks; 4) presence of calcar appendage; 5) presence of supracloacal crest (characters 4, 5 in Fig. 3 ); 6) relatively conspicuous discs on fingers and toes; 7) HW 30–34% (32 6 1) of SVL; 8) vocal repertoire composed of two different types of calls: the ‘‘A'' call (a short and multipulsed note) and the ‘‘B'' call (a trilled note); 9) call dominant frequency (both call types) ranging from 4.5 to 6.6 kHz (5.8 6 0.5).

Morphological Comparisons.— Boana guarinimirim sp. nov. can be distinguished from all species in the B. pulchella group, except from those in the B. polytaenia clade, by the combination of the following morphological traits: the presence of dorsal pattern composed of longitudinal lines and stripes (absent in B. aguilari , B. balzani , B. caipora , B. callipleura , B. cambui , B. cordobae , B. curupi B. cymbalum , B. ericae , B. freicanecae , B. gladiator , B. joaquini , B. marginata , B. marianitae , B. melanopleura , B. palaestes , B. poaju , B. prasina , B. pulchella , B. riojana , B. semiguttata , and B. stellae ); the smaller male SVL of 24.1–28.1 mm ( B. aguilari [33.7–43.8 mm], B. balzani [33.3–49.9 mm], B. bischoffi [36.0–47.0 mm], B. callipleura [37.2–43.3 mm], B. cordobae [39.0–50.0 mm], B. cymbalum [44.8– 46.2 mm], B. freicanecae [37.3–42.2 mm], B. gladiator [35.3–49.4 mm], B. goiana [29.0–33.0 mm], B. guentheri [33.0–40.0 mm], B. joaquini [40.3–56.4 mm], B. marginata [37.5–53.6 mm], B. marianitae [36.5–56.8 mm], B. melanopleura [43.6–50.0 mm], B. palaestes [36.2– 50.4 mm], B. poaju [33.5–42.7 mm], B. prasina [41.0–47.0 mm], B. pulchella [37.0–49.0 mm], B. riojana [48.0–56.0 mm], B. semiguttata [36.1–45.2 mm], and B. stellae [40.7–49.9 mm]); and the absence of vertical bars or spots on hidden parts of thighs, flanks, or groin (present in B. aguilari , B. balzani , B. bischoffi , B. caingua , B. caipora , B. callipleura , B. cordobae , B. curupi , B. cymbalum , B. ericae , B. gladiator , B. guentheri , B. joaquini , B. marianitae , B. melanopleura , B. poaju , B. prasina , B. pulchella , B. riojana , B. semiguttata , and B. stellae ; Boulenger, 1912; Bokermann, 1963; Barrio, 1965; Lutz, 1973; Heyer et al., 1990; Duellman et al., 1997; Cruz and Caramaschi, 1998, Garcia et al., 2001, 2003, 2007, 2008; Caramaschi and Cruz, 2004; Kwet, 2008; Köhler et al., 2010; Lehr et al., 2010; Pinheiro et al., 2016).

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From species of the B. polytaenia clade, B. guarinimirim sp. nov. can be distinguished by the presence of a calcar appendage and a distinct supracloacal crest ( Fig. 3 , absent in B. botumirim , B. buriti , B. cipoensis , B. jaguariaioensis , B. leptolineata , and B. stenocephala ); relatively more conspicuous discs on fingers and toes (less conspicuous in B. botumirim , B. jaguariaioensis , and B. stenocephala ), and the HW of 30–34% of SVL (mean of 27% in B. botumirim , 26% in B. buriti , 29% in B. jaguariaioensis , and 27% in B. stenocephala ). The male SVL of 24.1 to 28.1 mm of B. guarinimirim sp. nov. is smaller than B. buriti (28.2–31.9 mm; Lutz, 1968; Braun and Braun, 1977; Cruz and Caramaschi, 1998; Caramaschi and Cruz, 1999; Caramaschi et al., 2009; Caramaschi et al., 2010). B. guarinimirim cannot be distinguished from B. polytaenia and Boana sp. 4 in any of the analyzed morphological traits Vocal Repertoire.—The vocal repertoire of B. guarinimirim sp. nov. ( Fig. 4 A-B; Table 4) is composed of two types of calls, referred to as the ‘‘A'' and ‘‘B'' calls. The ‘‘A'' call is formed by a single and short multipulsed note and is commonly emitted alone or followed by a ‘‘B'' call but can also be emitted in pairs or in a series of consecutive ‘‘A'' calls. It lasts 18–84 ms (48 6 14) and reaches the amplitude peak at 1% to 76% (20 6 17) of its total duration. Pulses can be either well defined (with complete amplitude modulation, n = 27 calls) or poorly defined (concatenated pulses, n = 117 calls) along the call. In calls with well-defined pulses, the pulse rate ranges from 178 to 310 pulses per second (243 6 28), with 5–14 pulses per call. The dominant frequency always corresponds to the second harmonic and ranges from 4.6 to 6.6 kHz (6.2 6 0.6). The minimum frequency ranges from 4.4 to 6.2 kHz (5.4 6 0.5) and the maximum frequency from 5.0 to 7.2 kHz (6.3 6 0.6). The ‘‘B'' call is less common, and is usually preceded by an ‘‘A'' call, but can be emitted alone or followed by an ‘‘A'' call. The ‘‘B'' call lasts 381– 915 ms (574 6 136) and is composed of 5–11 pulses, which are emitted at irregular intervals of 2–284 ms (74 6 36). Pulses have durations of 2–16 ms (8 6 3). The ‘‘B'' call reaches its amplitude peak at 1–97% (48 6 35) of the total call duration. The dominant frequency corresponds to the second visible harmonic and ranges from 4.5 to 6.3 kHz (5.4 6 0.5). The minimum frequency ranges from 3.5 to 5.9 kHz (5.0 6 0.6) and the maximum frequency from 4.7 to 6.8 kHz (5.8 6 0.6).

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Acoustic Comparisons.—The call of Boana guarinimirim sp. nov. can be distinguished from the call of B. caingua , B. callipleura , B. cambui , B. cordobae , B. freicanecae , B. goiana , B. melanopleura , B. pulchella , and B. riojana by being pulsed (nonpulsed in those species; Baraquet et al., 2007, 2014; Köhler et al., 2010; Lehr et al., 2010; Pinheiro et al., 2012; Batista et al., 2015; Furtado et al., 2016; Pinheiro et al., 2016; Marinho et al., 2020). Species of the B. pulchella group with pulsed calls, except those in the B. polytaenia clade, are B. aguilari , B. balzani , B. bischoffi , B. caipora , B. callipleura , B. curupi , B. ericae , B. gladiator , B. guentheri , B. joaquini , B. marginata , B. marianitae , B. palaestes , B. poaju , B. prasina , B. semiguttata , and B. stellae . The advertisement call of B. guarinimirim can be distinguished from those species, except from B. bischoffi and B. ericae , by being composed of two types of calls (a single and pulsed call, or a series of similar calls in those species; Duellman et al., 1997; Garcia et al., 2001, 2003, 2007, 2008; Antunes et al., 2008; Garcia and Haddad, 2008; Kwet, 2008; Köhler et al., 2010; Lehr et al., 2010; Pombal, 2010; Delgado and Haddad, 2015; Forti et al., 2019). From B. bischoffi and B. ericae , the calls of B. guarinimirim can be distinguished by its higher dominant frequency of 4.5–6.6 kHz (1.4–2.1 kHz in calls of B. bischoffi and 2.0–3.6 kHz in calls of B. ericae ; Garcia and Haddad, 2008; Pombal, 2010). Additionally, the vocal repertoire of B. ericae is composed of three types of calls: calls ‘‘A,'' ‘‘B,'' and ‘‘C.'' The ‘‘C'' call consists of a trill of pulses similar to the ‘‘B'' call of B. guarinimirim sp. nov. and can be distinguished from it by the longer duration of 381–915 ms in the ‘‘B'' call of B. guarinimirim sp. nov. (‘‘C'' call duration of 104–560 ms in B. ericae ).

Among species within the Boana polytaenia clade, the calls of B. buriti and B. cipoensis remains undescribed. The calls of B. guarinimirim sp. nov. can be distinguished from the calls of B. botumirim and B. stenocephala by the higher dominant frequency of 4.5–6.6 kHz (dominant frequency of 3.3–4.1 kHz in ‘‘A'' calls of B. botumirim and B. stenocephala ; Caramaschi et al., 2009; Martins et al., 2016) and by being composed of two distinct call types (‘‘B'' call unknown in B. botumirim ). Also, the call of B. guarinimirim can be distinguished from the calls of B. jaguariaioensis and B. stenenocephala by the ‘‘A'' call being composed of only one note (‘‘A'' call composed by a sequence of short notes in B. jaguariaioensis and B. stenocephala ; Martins et al., 2016; Guerra et al., 2017). The described calls of B. leptolineata ( Forti et al., 2019) cannot be distinguished from the calls of B. guarinimirim based on any of the analyzed traits; however, these species are easily distinguished by morphological features and are not closely related ( Faivovich et al., 2021). Although the DAPC analysis pointed to a discrimination between B. guarinimirim and its distant taxon B. polytaenia ( Fig. 1B ), we could not find any acoustic trait that did not overlap in our analysis (Table 4). Additionally, B. guarinimirim could not be distinguished from Boana sp. 4 based on acoustic traits.

Comments.—Although not diagnostic, the analyzed males of B. guarinimirim tend to have a smaller SVL range of 24.1–28.1 mm while the SVL of males of B. polytaenia reaches larger values (23.2–34.7 mm; Table 3). Another tendency is that the ‘‘A'' calls of individuals from the type locality of B. guarinimirim tend to be shorter and exhibit an ‘‘A'' call envelope with a descending amplitude modulation along pulses ( Fig. 5A ). However, we could not consider it as diagnostic for the species because we observed considerable envelope variation in the ‘‘A'' call of B. guarinimirim ( Fig. 5B–C ) and in call duration of B. polytaenia (Table 4).

Description of the Holotype.— Adult male ( Figs. 2 , 6 ); SVL 24.1; body slender; head wider than body, slightly longer than wider (HL/HW = 1.11); snout rounded in dorsal view (SL/HL = 0.37; SL/HW = 0.41), and in profile; END shorter than ED (END/ED = 0.55); canthus rostralis distinct, slightly curved in dorsal view; loreal region oblique, slightly concave; internarial region not depressed; nostrils not protuberant, dorsolaterally directed; interorbital area flat, shorter than ED (IOD/ED = 0.94), shorter than HW (IOD/HW = 0.36). Eyes large and protuberant (ED/HL = 0.35; ED/HW = 0.39); palpebral membrane translucent, without reticulations, pigmented on its lower portion and margin. Supratympanic fold absent. Tympanum small (TD/ED = 0.42), inconspicuous, directed laterally. Arm slender, lacking an axillary membrane; forearm slightly hypertrophied in comparison with the arm, with a dermal ridge along the ventral side extending from the proximal limit of hand to the elbow. Fingers bearing round discs; disc diameter on finger III narrower than tympanum (3FD/TD 0.74); relative finger length: I, II, IV, III; webbing formula I–II 2 - – 3 III–IV; lateral fringes on fingers absent; subarticular tubercles distinct, circular, nonbifid, and rounded in ventral view; supernumerary tubercles present on fingers and palm; outer metacarpal tubercle rounded, almost indiscernible from supernumerary tubercles ( Fig. 2C ). Nuptial pad absent; prepollex enlarged and pointed as a curved bony spine. Hind limbs long and slender (THL/SVL = 0.42; TL/SVL = 0.53); tarsal dermal ridge extending from the inner metatarsal tubercle to heel; calcar appendage present on both heels, small. Toes long, with round discs, the 4th disc diameter slightly smaller than that on finger (4TD/3FD = 0.90); relative toe length I <II <III = V <IV; webbing formula I2 + –2 + II 1 + –2 + III 2–3 + IV 2 + –1 + V; presence of lateral fringes on toes. Presence of a dermal ridge extending from the base of the disc to the heel. Subarticular tubercles circular, slightly conical in profile; numerous supernumerary tubercles present on toes and sole; outer metatarsal tubercle rounded in ventral view, inner metatarsal elliptical in ventral view ( Fig. 2D ). Dorsal skin smooth. Pectoral, abdominal areas, and ventral surfaces of thighs granular. Pectoral fold absent. Cloacal opening directed posteroventrally at upper level of thighs; cloacal sheath (veil) absent; a white supracloacal dermal ridge present; cloacal tubercles present around vent, scattered, extending to midlevel of thighs. Tongue ovoid, barely free behind; dentigerous processes of vomers prominent, in two separate series between and slightly behind choanae, bearing four (right) and three (left) visible teeth. Choanae elliptical. Vocal slits extending from midlateral base of tongue, almost reaching the angle of jaws. Vocal sac single, median, subgular.

Distribution.— Boana guarinimirim sp. nov. occurs in the Northern Mantiqueira Mountain range ( Fig. 8 ) in the municipalities of Castelo (ES), Divino de São Lourenço (ES), Domingos Martins (ES), Pedra Menina (ES), Carangola (MG), Vargem Alta (ES), and Caratinga (MG). The distribution range of B. guarinimirim comprises at least three protected areas: Parque Estadual do Forno Grande, Parque Estadual da Pedra Azul, and the Parque Nacional do Caparaó, where it was previously recognized as B. polytaenia ( Montesinos et al., 2012; Silva-Soares and Scherrer, 2013; Zornosa-Torres et al., 2020).

Natural History.—In the type locality, specimens were collected in rocky outcrop shrubs around small ponds formed by a stream inside the Parque Estadual do Forno Grande and in an open and marshy area in the surroundings of the park, which had a slow stream flooding an anthropized area covered with shrubs and grasses. Although we did not observe any male–male combat, males likely use their modified prepollex bone to fight against other males, leaving scars that can be noticed on the back of the specimens ( Fig. 7 ), as previously described for other species of the B. pulchella group (e.g., Menin et al., 2004).

Etymology.—‘‘Guarinimirim'' is a combination of two words in the Tupi–Guarani language: ‘‘guarinĩ,'' which means ‘‘warrior,'' is an allusion to the species' fighting behavior and ‘‘mirim,'' which means ‘‘little'' ( Carvalho, 1987), is an allusion to the small SVL of males in comparison with congeners and other Cophomantini species with such a modified prepollex (also known as ‘‘gladiator frogs''; Kluge, 1979; Hedges et al., 2019).

Figures

FIG. 2. Holotype of Boana guarinimirim sp. nov. (CFBH 46043) from Castelo, Parque Estadual do Forno Grande (Espírito Santo, Brazil): (A) dorsal and (B) ventral views (SVL = 24.1 mm), (C) hand and (D) foot.

FIG. 3. Comparison of (A) Boana guarinimirim sp. nov. with other species in the B. polytaenia clade: (B) B. cipoensis (AAG-UFU 0027), (C) B. buriti (AAG-UFU 0433), and (D) B. stenocephala (AAG-UFU 4827). Arrows in (A) indicate the supracloacal crest and the calcar appendage, absent in B–D. Specimens are not to scale.

FIG. 4. Advertisement calls (spectrograms and corresponding oscillograms) of (A–B) B. guarinimirim sp. nov. (sound files: Boana_guarinimirimFornoGrandeES2aPM_AAGm671 and Boana_guarinimirimFornoGrandeES3aPM_AAGm671, respectively); (C–D) Boana sp. 4 (sound file: Boana_sp.4BJAmparoMG3aAAGm671); and (E–F) B. polytaenia (sound file: Boana_polytaeniaNovFriburRJ1bLBM_AAGmt). See Appendix 2 for additional information on sound files.

FIG. 1. Scatterplot of the two first axes of discriminant analyses of principal components (DAPC) on the (A) morphometric (9 first Principal Components, ca. 95% retained variance) and (B) acoustic (5 first Principal Components, ca. 95% retained variance) datasets of the tree partitions.

FIG. 5. Oscillograms depicting the variation in the envelope structure of the ‘‘A'' calls of Boana guarinimirim sp. nov. (A) ‘‘A'' call with a decreasing amplitude modulation; a short (B) and a long (C) ‘‘A'' call with irregular amplitude modulations (sound files: Boana_guarinimirimFornoGrandeES2aIV_AAG671; Boana_guarinimirimFornoGrandeES4aPM_AAGm671 and FNJV0040231, respectively).

FIG. 6. Holotype (CFBH 46043) of Boana guarinimirim sp. nov. in life. (A) Dorsolateral; (B) ventral and (C) dorsolateral view showing the coloration of hidden surfaces of thighs.

FIG. 8. Distribution of five species within the B. polytaenia clade in southeastern Brazil (Faivovich et al., 2021; Santos et al., 2009), including that of B. guarinimirim sp. nov.

FIG. 7. Color variation of Boana guarinimirim sp. nov. in life. Dorsolateral view of the paratypes AAG-UFU 6773 (top left), AAG-UFU 6800 (top right), AAG-UFU 6772 (bottom left), and dorsal view of AAG-UFU 6774. Scratch markings produced during aggressive interactions can be noticed on the dorsum of specimens.