Ischnocnema bocaina, Taucce & Zaidan & Zaher & Garcia, 2019

Taucce, Pedro P. G., Zaidan, Bárbara F., Zaher, Hussam & Garcia, Paulo C. A., 2019, A new species of Ischnocnema Reinhardt and Lütken, 1862 (Anura: Brachycephalidae) of the I. lactea species series from southeastern Brazil, Zootaxa 4706 (4), pp. 531-545 : 533-537

Ischnocnema bocaina sp. nov.

urn:lsid:zoobank.org:act:64C9B836-EA8B-496F-B3B6-2BCFFE0CD1BA

Holotype. MZUSP 138663 , adult male, collected at Estação Ecológica do Bananal , municipality of Bananal, state of São Paulo, southeastern Brazil, by H. Zaher and P.C.A. Garcia on 18 January 2008.

Paratopotype. MZUSP 138664 , adult male, collected with the holotype .

Diagnosis. In the I. lactea species series by phylogenetic placement ( Fig. 1 ). Ischnocnema bocaina sp. nov. is distinguished from all other species of the I. lactea series by the following combination of characters: (1) medium size (SVL in males 18.6–19.0 mm); (2) snout rounded in dorsal view ( Fig. 2 ); (3) tip of the snout acuminate in lateral view ( Fig. 3 ); (4) dorsum smooth with granular flanks; (5) venter smooth; (6) head longer than wide; (7) eyelid tubercles absent; (8) dentigerous process of the vomer present; (9) vocal sac single, subgular, slightly expanded; (10) tips of Fingers II–IV expanded, truncated; (11) glandular-appearing nuptial pad on dorsal surface of the thumb, rounded, poorly-developed, whitish, extending to the posterior half of the thenar tubercle; (12) toe lengths formula I <II <V <III <IV; (13) calcar tubercle present, well-developed; (14) 9–18 notes per call; (15) advertisement call duration 1000–2010 ms; (16) note rate 8.1–9.0 notes/s; (17) dominant frequency 2325–2746 Hz; (18) nonpulsed advertisement call.

Comparison with other species. We based the comparisons both on collection specimens and literature data (references follow in parenthesis at the end of each species comparison). The new species differs from I. concolor by its larger size ( I. bocaina sp. nov. males 18.6–19.0 mm SVL; I. concolor males 15.0– 18.4 mm SVL); smooth venter (slightly areolate in I. concolor ); rounded snout in dorsal view (subacuminate in I. concolor ); acuminate snout in lateral view (rounded in I. concolor ); slightly expanded vocal sac (moderately expanded in I. concolor ); tips of Fingers II–IV well-developed and truncate (moderately developed and rounded in I. concolor ); toe lengths formula I <II <V <III <IV (I <II <III <V <IV in I. concolor ); and well-developed calcar tubercle (calcar tubercle absent in I. concolor ; Targino et al. 2009). Ischnocnema bocaina sp. nov. differs from I. gehrti by its rounded snout in dorsal view (truncate in I. gehrti ) and its acuminate snout in lateral view (subacuminate in I. gehrti ; Pombal & Cruz 1999). From I. holti , the new species differs by its smooth venter (slightly areolate in I. holti ); head longer than wide (wider than long in I. holti ); acuminate snout in lateral view (rounded in I. holti ); slightly expanded vocal sac (not expanded in I. holti ); whitish nuptial pad (translucent in I. holti ); and toe lengths formula I <II <V <III <IV (I <II <III <V <IV in I. holti ; Targino & Carvalho-e-Silva 2008). Ischnocnema bocaina sp. nov. differs from I. lactea by its smaller size ( I. bocaina sp. nov. males 18.6–19.0 mm SVL; I. lactea males 19.6–26.7 mm SVL); its smooth dorsum and venter (rugose and moderately granular in I. lactea ); acuminate snout in lateral view (obtuse in I. lactea ); the absence of upper eyelid tubercles (present in I. lactea ); its single nuptial pad (double in I. lactea ); its toe lengths formula I <II <V <III <IV (I <II <III <V <IV in I. lactea ); and the advertisement call with 9–18 non- pulsed notes (one pulsed note in I. lactea ; Silva-Soares et al. 2018). The new species differs from I. melanopygia by its smooth venter (venter slightly areolate in I. melanopygia ); snout rounded in dorsal and acuminate in lateral views (respectively subacuminate and rounded in I. melanopygia ); and its slightly expanded vocal sac (not expanded in I. melanopygia ; Targino et al. 2009). Ischnocnema bocaina sp. nov. differs from I. nigriventris by its smooth dorsum and venter (respectively shagreen with tubercles or warts and weakly areolate in I. nigriventris ); head longer than wide (wider than long in I. nigriventris ); snout rounded in dorsal and acuminate in lateral views (respectively nearly-rounded and rounded in I. nigriventris ); by the absence of upper eyelid tubercles (present in I. nigriventris ); by the slightly expanded vocal sac (not expanded in I. nigriventris ); its toe lengths formula I <II <V <III <IV (I <II <III = V <IV in I. nigriventris ); and the advertisement call with 9–18 notes and call duration of 1000–2010 ms (2–4 notes and 194–565 ms in I. nigriventris ; Berneck et al. 2013). The head longer than wide (as long as wide in I. paranaensis ); snout acuminate in lateral view (rounded in I. paranaensis ); vomerine teeth present (absent in I. paranaensis ); toe lengths formula I <II <V <III <IV (I <II <III <V <IV in I. paranaensis ); and well-developed calcar tubercle differ I. bocaina sp. nov. from I. paranaensis (calcar absent in I. paranaensis ; Langone & Segalla 1996). Ischnocnema bocaina sp. nov. differs from I. randorum by its larger size ( I. bocaina sp. nov. males 18.6–19.0 mm SVL; I. randorum males 11.8–15.0 mm SVL); its smooth venter (weakly granular in I. randorum ); rounded snout in dorsal and acuminate in lateral views (respectively subovoid and rounded in I. randorum ); the presence of dentigerous processes of the vomer (absent in I. randorum ); its slightly expanded vocal sac (greatly expanded in I. randorum ); its toe lengths formula I <II <V <III <IV (I <II <III <V <IV in I. randorum ); and the nonpulsed advertisement call with 9–18 notes, note rate 8.1–9.0 notes/s, and dominant frequency 2325–2756 Hz (pulsed single note advertisement call with note rate 1.3–2.6 and dominant frequency 3800–5200 Hz in I. randorum ; Heyer 1985; Heyer et al. 1990). Ischnocnema bocaina sp. nov differs from I. spanios , its sister species, by its larger size ( I. bocaina sp. nov. males 18.6–19.0 mm SVL; I. spanios males 14.7–15.3 mm SVL); its rounded snout in dorsal and acuminate in lateral views (respectively subovoid and rounded in I. spanios ); its slightly expanded vocal sac (not expanded in I. spanios ); the presence of a nuptial pad (absent in I. spanios ); and its toe lengths formula I <II <V <III <IV (I <II <III = V <IV in I. spanios ; Heyer 1985; Heyer et al. 1990). Finally, I. bocaina sp. nov. differs from I. vizottoi by its larger size ( I. bocaina sp. nov. males 18.6–19.0 mm SVL; I. vizottoi males 13.3–16.6 mm SVL); its smooth dorsum and venter (respectively slightly rugose and granular in I. vizottoi ); its rounded snout in dorsal and acuminate in lateral views (respectively sub-elliptical and acuminate-rounded in I. vizottoi ); its slightly expanded vocal sac (moderately expanded in I. vizottoi ); its toe lengths formula I <II <V <III <IV (I <II <III = V <IV in I. vizottoi ); its well-developed calcar tubercle (small or absent in I. vizottoi ); and its advertisement call with 9–18 notes, call duration 1000–2010 ms and dominant frequency 2325–2756 Hz (advertisement call with a single note, call duration 38–72 ms, and dominant frequency 3417–3763 Hz in I. vizottoi ; Martins & Haddad 2010).

Genetic distances of mitochondrial 16S rRNA fragment within and between members of the Ischnocnema lactea species series are given in Table 1 .

Description of holotype. Adult male with vocal slits, subgular vocal sac, and nuptial pads; medium-size (SVL = 18.6 mm). Head slightly longer than wide; head length 36% of the SVL, head width 34% of the SVL; snout round- ed in dorsal view, acuminate in lateral view; nostril elliptical, slightly protuberant, oriented laterally, located near the tip of snout; canthus rostralis slightly distinct, curved; loreal region slightly concave; two poorly-developed, rounded, postrictal tubercles on each side about the same size; eye protuberant, oriented laterally; eye diameter 42% of head length; palpebral tubercles absent; tympanum barely distinct, rounded; tympanic membrane undifferentiated; annulus present, barely visible externally, its dorsal portion hidden; tympanum diameter 45% of eye diameter; supratympanic fold absent; vocal slits present; vocal sac subgular, distinct, one visible fold on each side of the jaw; tongue large, elliptical, without posterior notch; choanae elliptical, larger than the dentigerous processes of the vomer; dentigerous processes of the vomer round, located posteromedially to choanae, medially separated by a gap approximately the same size as one dentigerous process; vomerine teeth present.

Forelimb slender; palmar tubercle barely distinct, cordiform, its diameter approximately equal that of the thenar tubercle; thenar tubercle barely distinct, elliptical; glandular-appearing nuptial pad on dorsal surface of the thumb, round, poorly-developed, whitish, extending to the posterior half of the thenar tubercle; palm smooth; supernumerary tubercles absent; single subarticular tubercles flat, rounded, large; fingers slender, without fringes; tip of Finger I slightly expanded, rounded; tip of Finger II moderately expanded, truncated; tips of Fingers III and IV fairly expanded, truncated, with ungual flaps indented; Finger I half the size of Finger II; finger lengths formula I <II <IV <III.

Hindlimb slightly robust; shank slightly longer than thigh; tibia length 49% of SVL; thigh length 48% of SVL; moderately-developed, conical calcar tubercle present; tarsal folds absent; foot length 47 % of SVL; inner metatarsal tubercle elliptical, twice as large as outer metatarsal tubercle; outer metatarsal tubercle rounded; sole of foot smooth; supernumerary tubercles absent; single subarticular tubercles present, flat, rounded; toes long, slender, without fringes; tips of Toes I and V slightly expanded, rounded; tips of Toes II–IV moderately expanded, truncated, ungual flaps indented on Fingers III and IV; toe lengths formula I <II <V <III <IV.

Dorsal skin smooth; venter smooth; flanks granulated; posterior portion of ventral surface of thighs coarsely shagreen; discoidal and thoracic folds present.

Coloration of holotype. Dorsum diffused marbled rust, brown, and dark-brown, with two medial white spots at the shoulder girdle ( Fig. 4 ); head with clear brown stripe between eyes; lips with sparse white spots; flanks diffused marbled rust, brown, and dark-brown; posterior half with sparse white spots; dorsal surfaces of the limbs banded brown and dark-brown with sparse rust blotches. Venter, venter surfaces of the limbs, and gular region marbled light-brown, brown, and rust; gular region darker than rest of the ventral region. Posterior surfaces of thighs brown. In preservative, rust becomes nut-brown and all other colors become lighter.

Measurements of holotype (in millimeters). SVL 18.6; HL 6.6; HW 6.3; ED 2.8; TD 1.3; END 1.5; IND 1.8; AMD 3.8; FAL 3.7; HAL 5.3; 3FD 1.1; THL 8.9; TL 9.1; TAL 4.7; FL 8.8; 4TD 0.8.

Variation. The paratopotype is somewhat faded, but it is overall similar to the holotype, except that its dentigerous processes of the vomer are barely distinct (distinct in the holotype). It also lacks the two medial white spots at the shoulder girdle. Measurements of the paratopotype (in millimeters): SVL 19.0; HL 7.3; HW 7.0; ED 2.7; TD 1.1; END 2.1; IND 2.0; AMD 3.4; FAL 3.6; HAL 5.6; 3FD 1.1; THL 9.4; TL 9.4; TAL 5.1; FL 8.8; 4TD 1.0.

Phylogenetic relationships and genetic distances. The Bayesian inference and the maximum likelihood analyses yielded similar topologies ( Fig. 1 ). We recovered the I. lactea species series with high support (1.0 of posterior probability and 98% of bootstrap), with I. bocaina sp. nov. as the sister species of I. spanios , also with high support (1.0 of posterior probability and 98% of bootstrap). The uncorrected pairwise distance of partial 16S rRNA between these two species was among the lowest of all species pairs (6.3–6.9%, Table 1 ).

Etymology. The specific epithet refers to the Bocaina Mountain Range (Serra da Bocaina, in Portuguese), where the type locality of the species is located, in recognition of the great biodiversity importance of this mountain range. The name is used here as a noun in apposition.

Vocalization. We recorded two types of calls, call 1 (n = 11; Fig. 5A ; Table2 ) and call 2 (n = 10; Fig. 5B ; Table 2 ). The first one was composed of 9 to 18 non-pulsed notes (= 15.6 ± 2.3), with the energy gradually increasing in each note through the call, until reaching a peak typically on the penultimate or last note ( Fig. 5A ). Call 1 duration ranged from 1000 to 2010 ms (= 1760 ± 260) and call rise time ranged from 91.6–99.4% (= 97.8 ± 2.2) of the call. Note repetition rate was 8.1–9.0 notes/s (= 8.3± 0.3) and note repetition rate acceleration ranged from –13.2 to 0.2 (= –6.1 ± 4.4). Dominant Frequency was 2325–2756 Hz (= 2576 ± 146). Call 2 was composed of one non-pulsed note, with duration ranging from 13 to 14 ms (= 13.7 ± 0.0) and Dominant Frequency ranging from 2756–2842 Hz (= 2834 ± 27). We considered call 1 the advertisement call and call 2 the territorial call because of the similarities of each call with the advertisement and territorial calls of I. nigriventris ( Berneck et al. 2013) .

Natural history notes. The collectors found the two type specimens calling perched on trees about 50 cm above the ground, right after a heavy rain. The call activity started about one hour before dusk, together with two other Ischnocnema species from the I. guentheri and I. parva species series, but the new species ceased to call earlier, about one hour after dusk.

Geographic distribution. Ischnocnema bocaina sp. nov. is known only from the type locality: Estação Ecológica do Bananal, municipality of Bananal, state of São Paulo, southeastern Brazil ( Fig. 6 ).

Figures

FIGURE 1. The 50% majority rule consensus tree from Bayesian inference of mitochondrial 16S rRNA gene (16S) showing the relationships within the Ischnocnema lactea species series. Numbers above branches indicate posterior probabilities and numbers below branches indicate maximum likelihood nonparametric bootstrap values. We only show bootstrap values above 50%.

FIGURE 2. Dorsal (left) and ventral (right) views of Ischnocnema bocaina sp. nov. holotype (MZUSP 138663). Scale bar = 10 mm. Photos by B. F. Zaidan.

FIGURE 3. Lateral view of the head (above), ventral view of the foot (below, left), and ventral view of the hand (below, right) of Ischnocnema bocaina sp. nov. holotype (MZUSP 138663). Scale bar = 2 mm. Photos by B. F. Zaidan.

FIGURE 4. Live specimen of Ischnocnema bocaina sp. nov., holotype (MZUSP 138663). Photo by P. C. A. Garcia.

FIGURE 5. Spectrogram (above) and oscillogram (below) of the two types of calls of Ischnocnema bocaina sp. nov.: (A) advertisement call and (B) territorial call. Respectively recordings CBUFMG 1017 and 1016, 18 January 2008.

FIGURE 6. Map showing the type locality of Ischnocnema bocaina sp. nov. (indicated by a black square): Estação Ecológica do Bananal, municipality of Bananal, state of São Paulo, southeastern Brazil. Elevations above 500 and 1000 m are shaded gray.

Tables

TABLE 1. Uncorrected pairwise genetic distances (given in percentage) of mitochondrial 16S rRNA fragment (ca. 600bp) within (in bold) and between members of the Ischnocnema lactea species series. Within species distances are in bold. Data are shown as min–max where appropriate.

	I. bocaina	I. spanios	I. nigriven-	I. randorum	I. concolor	I. vizottoi	I. melano-	I. holti	I.
	sp. nov.		tris				pygia		lactea
I. bocaina	NA
sp. nov.
I. spanios	6.3–6.9	0.0–1.9
		(n = 6)
I. nigriventris	13.6–13.7	12.0–12.5	0.0–0.2
			(n = 3)
I. randorum	12.1	12.0–12.2	10.0–10.1	0.0
				(n = 2)
I. concolor	13.6	12.2–12.7	7.0	8.6	0.0
(n = 2)
I. vizottoi	14.1	12.5–13.1	6.7–7.0	8.9	1.4	0.0
						(n = 2)
I. melanopy-	10.7	10.9–11.1	10.5–10.7	9.8	10.0	10.2	0.0
gia							(n = 2)
I. holti	13.6	15.1–15.5	13.9–14.5	12.6	13.7	12.9	12.0	0.0
								(n = 2)
I. lactea	13.9–14.8	14.9–16.2	15.5–16.4	12.6–13.2	13.1–14.2	12.9–14.0	12.7–13.2	9.2–10.2	0.0–2.7
									(n = 7)