Ischnocnema nigriventris

Berneck, Bianca V. M., Targino, Mariane & Garcia, Paulo Christiano De Anchietta, 2013, Rediscovery and re-description of Ischnocnema nigriventris (Lutz, 1925) (Anura: Terrarana: Brachycephalidae), Zootaxa 3694 (2), pp. 131-142 : 133-141

Re-description of Ischnocnema nigriventris

Ischnocnema nigriventris is allocated to the Ischnocnema lactea species series (sensu Canedo and Haddad, 2012). The species series includes species with tibia length <50% SVL, and finger disks from moderate to large.

A medium sized Ischnocnema , males 18–20 SVL, the two females are 24 SVL (see Table 1 for measurements); head wider than long; snout short and rounded in profile and nearly rounded in dorsal view ( Figure 1 ); large and prominent eyes, diameter smaller than interorbital distance and 40% of head length; on the upper eyelid several small and medium tubercles, one of them larger than the others; tympanic membrane undifferentiated and tympanic annulus hidden; supratympanic fold barely visible, starting behind the eye, covering the upper half of tympanic annulus and reaching the arm insertion; canthus rostralis distinct and straight, with sparse, small tubercles; usually two postrictal tubercles; nostril laterally oriented; internostril distance smaller than eye diameter, corresponding to 28% of head width; vomerine teeth small, in two rows of about five teeth each, lying between and posterior to the rounded choanae; tongue posteriorly free, male vocal slits lateral to the insertion of the tongue, single vocal sac not expanded externally; small premaxillary and maxillary teeth. Arms and fingers slender; Finger length III>IV>II>I; disk of first finger smaller than second; disks of the third and fourth wider than second; except for Finger I, which is rounded and not expanded, the others are expanded and are emarginated with ungual flap notched in dorsal view (see figs. 3 and 4 in Savage 1987); Fringes or webbing absent; palmar and thenar tubercles weakly developed; Finger I and Finger II with only one subarticular tubercle; Finger III and Finger IV with two subarticular tubercles; supernumerary tubercles absent; translucent nuptial pad on Finger I of most adult males (80%), divided into two parts: one obscures the medial margin of the thenar tubercle and the other occupies the medial margin of the base of the thumb. Legs slender; thigh and tibia slightly longer than SVL in males, and barely shorter than SVL in females; tibia length 50% of male SVL, and 48% of female SVL; feet not webbed, and foot length corresponding to 50% SVL; Toe length IV>V=III>II>I; Toe I disk is rounded and not expanded, the others are expanded emarginated disks, with ungual flap notched in dorsal view; inner metatarsal tubercle large, protruding, and ovoid; outer metatarsal tubercle small, conical and projecting; supernumerary metatarsal tubercles small and sparse; subarticular tubercles conical, projecting forward; calcar tubercle present and well developed. Dorsal skin shagreen with tubercles or warts, ranging in number, belly weakly areolate to areolate, flanks and posterior surface of thigh coarsely areolate.

In life, the dorsum is dark brown with lighter or darker brown blotches. Males have bright yellow mottling on a dark background on the inguinal region and hidden areas of hindlimbs, while in females the mottling is bright orange. At night, specimens showed a light brown belly while during daytime those same specimens showed a deeply dark brown belly. The dorsal and ventral areas of the iris are silver, and the medial transverse band is yellowish copper ( Fig. 3 ).

In preservative, dorsal coloration ranges from dark brown to light brown, and some specimens may show many sparse patches ( Fig 2 ). The belly and gular region range from light brown to dark brown, always with a lot of sparse dark spots. The most common venter feature is dark and areolate (76%). The head is brown with lateral beige bars rising from the ventral margin of maxilla to eye ventral portion; sparse beige blotches cover the maxilla region, and a dark brown stripe outlines the supratympanic fold. Some specimens may show a vertebral white line that can be wide (5%) or slender (29%) ( Fig. 2 A and D). This line extends from snout to vent. Other specimens show a large dorsolateral band starting behind the eyes and reaching the proximal quarter of the thigh, leg, and feet (17%) ( Fig. 2 B and C). Some specimens show a W-shaped dark brown mark between the eyes ( Fig. 2 B). A cream interorbital bar is sometimes present ( Fig. 2 C and D), as well as a semilunar cream mark at the tip of the snout ( Fig. 2 B and D). Some specimens exhibit transversal dark brown stripes in the dorsal surfaces of hind limbs while, in others, the stripes are randomly disposed. The bright yellow and orange regions become white in preservative. All brown coloration becomes lighter brown in preservative.

Diagnosis. Ischnocnema nigriventris can be distinguished from other Ischnocnema by the following combination of character states: (1) snout short and nearly rounded in dorsal view and rounded in profile view; (2) head wider than long; (3) prominent conical tubercles on the upper eyelid; (4) first finger shorter than second; (5) disks on fingers II–IV expanded and emarginated, with ungual flap notched in dorsal view; (6) translucent, double glandular nuptial pad on the thumbs of males; (7) vomerine teeth present; (8) single vocal sac not expanded externally; (9) skin on dorsum shagreen with tubercles or warts, flanks, belly and posterior portion of thighs areolate (10) prominent calcar on the heel; tibia length <55% SVL; (11) In life, iris silver with a ventral yellowish copper band; inguinal region and hidden areas of hind limbs with yellow mottling in males and orange mottling in females; (12) advertisement call composed of two to four non-pulsed notes with the first one differentiated by its lower intensity and frequency.

Comparison with other species of Ischnocnema . Ischnocnema nigriventris is distinguished from all other species of the I. lactea species as follows (character states for other members of the series in parenthesis): upper eyelid tubercles large, conical (absent, or present as low and small rounded granules); expanded disks in fingers II– IV (Finger IV with no expanded disk in I. concolor and I. vizottoi ); nuptial pads present (absent in, I. melanopygia , and I. spanios ; not reported in I. paranaensis ; I. lactea is only known from its female holotype; the condition is unknown for the poorly preserved male holotype of I. gehrti ; not reported in the original description of I. vizottoi but observable as a translucent inconspicuous glandular pad); well-developed calcar tubercles (absent in I. concolor , and I. paranaensis ; unknown in I. lactea , and I. gerhti whose type specimens are in bad condition); vomerine teeth present (absent in I. randorum and I. paranaensis ); palmar tubercles inconspicuous but present (indistinct in I. spanios and I. paranaensis ); dorsum shagreen with tubercles or warts (smooth in I. concolor , I.

vizottoi , I. melanopygia , I. gehrti , I. lactea , I. paranaensis , I. spanios , and I. randorum ); in life, bright yellow or orange mottling or as blotches in the inguinal region and hidden areas of hind limbs (no bright coloration in these areas occur in I. concolor , I. vizottoi , and I. paranaensis ; the coloration in life is unknown for I. lactea and I. gehrti ; I holti presents red or orange coloration in the inguinal region but not mottled or as blotches); iris silver with a ventral yellowish copper band (iris green in I. holti , dorsally bluish in I. spanios , golden to lemon yellow in I. randorum , I. melanopygia , I. concolor , and I vizottoi , and dark violet in I. lactea ; not reported for I. gehrti and I. paranaensis ); snout nearly rounded in dorsal view (truncate in I. gehrti , the others are also nearly rounded, rounded or sub-acuminate with no substantial difference; head wider than long (head longer than wide in I. melanopygia , I. randorum , and I. spanios ).

Ischnocnema nigriventris differs from species in the I. guentheri species series by having a tibia length shorter than 55% of SVL; snout nearly rounded in dorsal view; disks expanded and emarginated; translucent glandular nuptial pads. ( I. guentheri species series: legs with tibia length> 60% SVL; acuminate snout in dorsal view; disks usually small or slightly expanded, large only in I. hoehnei and I. vinhai ; and conspicuous white glandular nuptial pads, unknown in I. vinhai ; see Heyer, 1984; Hedges et al. 2008; Canedo et al. 2010).

Ischnocnema nigriventris differs from species in the I. parva species series by its shagreen dorsum with tubercles. Finger I smaller than Finger II; disks expanded and emarginated; and translucent and glandular nuptial pads. ( I. parva species series: smooth dorsum; Finger I as long as Finger II; small and pointed disks; and conspicuous white glandular nuptial pads [contra Hedges et al. 2008]).

Ischnocnema nigriventris differs from the I. verrucosa species series by its rounded snout in dorsal view; Finger I shorter than II; and expanded disks. ( I. verrucosa species series: snout sub acuminate in dorsal view; Finger I as long as II; and small disks, Hedges et al. 2008; Canedo et al. 2010).

Ischnocnema nigriventris differs from I. manezinho and I. sambaqui , recently removed from the I. lactea species series and not allocated to any series (Canedo and Haddad, 2012), by its smaller size, males 18–20 mm; presence of nuptial pads; and bright coloration in hidden areas in life (bigger size, I. sambaqui males 32–40 mm, and I. manezinho males 22–28 mm; absence of nuptial pads and bright colors in hidden areas in life).

Vocalization. Two calls were recorded for two specimens of Ischnocnema nigriventris . The first (considered a territorial call due to continuous and high emission rate) consists of a single, non-pulsed note emitted at regular intervals of 2.8–3.3 seconds ( Figure 4 ). Note duration is 30–41 ms (36.1 ± 3.8 ms, n = 8 calls of two individuals). The frequency spectrum is 2004–3685 Hz and the peak frequency (= dominant frequency) is 2928–3014 Hz (2965 ± 46.0, n = 8 calls of two individuals).

The second call ( Figure 5 ), considered here as the advertisement call, shows two to four non-pulsed notes, emitted after long irregular intervals. The duration of the call is 194–565 ms, the frequency spectrum is 1955–3932 Hz, and the peak frequency is 2756–2928 Hz (n = 19 calls of three individuals). The first note differs from the others by its lower intensity (the amplitude of the first note is about 11–33% lower than the others) and lower frequency range (the first note ranged from 2151–2774 Hz). Note duration is similar, the first note is 30–89 ms (54.2 ± 2.0 ms) and the others are 28–88 ms (41.7 ± 2.0 ms). The interval between the notes is 113–157 ms (132 ± 12 ms).

The major differences in call with respect to other Ischnocnema from I. lactea series (sensu Canedo and Haddad, 2012) and I. manezinho and I. sambaqui (former I. lactea series and unassigned to species series in Canedo and Haddad, 2012) are shown in Table 2 .

I. nigriventris I. nigriventris I. randorum Call 1 Call 2 (advertissment call) (Heyer et al. 1990) Natural history. Ischnocnema nigriventris starts its vocalization activity just before dusk, with its territorial call. The males are usually found perching on trees or shrubs. On some occasions we found males calling from about three meters above the ground. On others, a couple in amplexus was observed moving on the leaf litter. Individuals were found active all year round, even during the dry season (June), although they were more abundant in September during the early stages of the rainy season when the forest was very humid. Two dissected females contained large, unpigmented ovarian ovules. One (CFBH23478) with 20 ovules, nine in the left ovary and eleven in the right, and the second (MZUSP136724) with 18 ovules in total. Ovule diameter: 2.5–3.2 (x = 2.8mm).

Distribution. Ischnocnema nigriventris is only known from the Parque das Neblinas (Bertioga municipality), Paranapiacaba (Santo André municipality), and Boracéia (Salesópolis municipality), all localities in the Serra do Mar, eastern São Paulo State, Brazil ( Figure 6 ).

Remarks. Lutz (1925) did not designate type specimens in the original description of Hylaplesia nigriventris , only provided a single measurement (SVL 21mm), and mentioned two localities, Serra de Cubatão and Itatiaia, for the distribution of the species. Cochran (1961) lists one cotype, measuring 6.5 mm total length, from Serra de Cubatão and deposited in the United States Natural History Museum (USNM 96846). Bokermann (1966) cited two specimens labeled as cotypes from Adolpho Lutz Collection (AL-MN 720 and 721) and corrected the type locality to Paranapiacaba in Santo André, state of São Paulo, Brazil. Heyer (1985) found three specimens, labeled as cotypes, in the Adolpho Lutz Collection, AL-MN 719 (SVL 17.8 mm), AL-MN 720 (SVL 8.2 mm), and AL-MN 721 (SVL 7.0 mm), all from Paranapiacaba. The specimen AL-MN 720 was identified as a juvenile of Eleutherodactylus guentheri (now Ischnocnema guentheri ) and, since none of these specimens reached the size informed in the original description, Heyer (1985) considered that this may be the length of the lost specimen from Itatiaia. From the remaining syntypes, he designated AL-MN 719 as lectotype ( Figure 7). In the same work, he associated the lectotype with the specimen MZUSP 37787 from Boraceia, clearly cospecific with specimens studied herein.

However, we found an unpublished illustration at the Museu Nacional, Rio de Janeiro, having the following handwritten information “ Hylaplesia nigriventris , 21 mm. n. esp. Campo Bello, Alto da Serra de Cubatão Alto Itatiaia” ( Figure 8 ). The illustrated specimen seems to exactly match the original description, on the basis of its color pattern and the recorded length (“ 21mm ”). As none of the syntypes from Paranapiacaba reach 21mm SVL, this illustrated specimen could be the lost syntype from Itatiaia. The illustration does not show any bright coloration on the inguinal region and hidden areas of the hind limbs, nor the presence of a calcar on the heels, or tubercles on the upper eyelid, as found on the extant syntypes of I. nigriventris and our freshly collected specimens.

For those reasons, the specimens studied herein and the syntypes from Paranapiacaba may not be conspecific with the figured specimen and, consequently, with the original description, probably from the Itatiaia specimen, as already pointed by Heyer (1985). Since the specimens from Paranapiacaba are the only ones available, and considering that a lectotype has already been designated by Heyer (1985), in accordance with the Article 74.1.3 of the I.C.Z.N., the name I. nigriventris is attributed to the syntypes, all from Paranapiacaba. The remaining lectotype and paralectotypes are juveniles, their color pattern is completely dark, and most of their fingers and toes are missing ( Fig. 7). The specimens we collected share the following characters with them: series of warty tubercles on the upper eyelid and dorsum; presence of prominent calcar on the heels; and the expanded emarginated disks, with ungual flap notched in dorsal view.

There are three species of the Ischnocnema lactea species series in Itatiaia, I. melanopygia , I. concolor , and I. holti (Targino & Carvalho-e-Silva, 2008; Targino et al. 2009). The illustrated specimen ( Fig. 8 ) does not seem to correspond to any of them, although the expanded disks and W-shaped marking between the eyes may resemble I. holti . However, the shape of the head is different (rounded in I. holti , as shown in the illustration). The illustrated specimen has expanded disks on the first finger and toe: we consider this a mistake since this character does not occur in any known species of Ischnocnema .

There are three species of the I. lactea series that are still known only from their type specimens, generally poorly preserved. These are I. gehrti , I. lactea , and I. paranaensis . The type locality of I. gehrti is also Paranapiacaba, but the type has smooth skin, truncate snout in dorsal view (as already observed by Pombal & Cruz, 1999), and has no palpebral tubercles. These character states are also listed in the original description of I. gehrti (Miranda–Ribeiro, 1926). The type of Ischnocnema lactea is from Iguape, state of São Paulo, SVL 32 mm, and the description makes no reference to bright coloration in life or palpebral tubercles (Miranda–Ribeiro, 1923). The type of Ischnocnema paranaensis is from Pico Paraná, state of Paraná, and it has smooth skin, vomerine teeth absent, palpebral and calcar tubercles absent (Langone & Segalla, 1996).

Figures

FIGURE 1. Ischnocnema nigriventris male (MZUSP 136689). Dorsal and lateral view of the head and ventral view of hand and foot. Scale: 5 mm.

FIGURE 2. Intraspecific dorsal pattern variation of Ischnocnema nigriventris A. CFBH 23480; B. MZUSP 136693; C. MZUSP 136694; D. MZUSP 136695.

FIGURE 3. Ischnocnema nigriventris in life. Male, MZUSP 136725 SVL 19.4 mm (A and B). Female, MZUSP 136724 SVL 24.5 mm (C and D).

FIGURE 4. Spectrogram (above) and waveform (below) of the putative territorial call of Ischnocnema nigriventris (MZUSP 136694) from Parque das Neblinas, Bertioga, state of São Paulo, Brazil, recorded on September 0 9 2005; 18: 31 h. Air temperature 16.5 ºC.

FIGURE 5. Spectrogram (above) and waveform (below) of the putative advertisement call of Ischnocnema nigriventris (MZUSP 135895) from Parque das Neblinas, Bertioga, state of São Paulo, Brazil, recorded on November 0 3 2006; 23: 45 h. Air temperature 19.5 ºC.

FIGURE 6. Map showing the geographical distribution of Ischnocnema nigriventris. The square is Boracéia, Salesópolis; the triangle is Parque das Neblinas, Bertioga and the circle is the type-locality, Paranapiacaba, Santo André. All localities in the state of São Paulo, Brazil.

FIGURE 8. Illustration housed at Museu Nacional, Rio de Janeiro: “ Hylaplesia nigriventris, 21 mm. n. esp. Campo Bello, Alto da Serra do Cubatão Alto Itatiaia ” (see text).

Tables

TABLE 1. Measurements, in millimeters, for 19 specimens of Ischnocnema nigriventris (mean ± standard deviation and range). SVL (snout-vent length); HL (head length); HW (head width); ED (eye diameter); END (eye-nostril distance); AMD (distance between the anterior margins of eyes); IND (internasal distance); NSD (nostril to tip of snout distance); THL (thigh length), TBL (tibia length) and FL (foot length).

Measurements	Males (n=16)	Females (n=3)
SVL	19.0 ± 0.6, 18.2–20.2	24.6 ± 0.1, 24.5–24.7
HL	6.6 ± 0.4, 6.2–7.4	8.1 ± 0.3, 7.7–8.4
HW	6.9 ± 0.2, 6.4–7.2	8.6 ± 0.1, 8.4–8.7
ED	2.6 ± 0.2, 2.3–3.1	3 ± 0.0, 3.0–3.1
END	1.9 ± 0.2, 1.1–2.1	2.5 ± 0.0, 2.5–2.6
AMD	3.6 ± 0.2, 3.3–3.8	4.5 ± 0.0, 4.4–4.5
IND	1.9 ± 0.10, 1.7–2.0	2.4 ± 0.1, 2.3–2.6
NSD	1.1 ± 0.1, 1.0–1.4	1.4 ± 0.1, 1.4–1.5
THL	9.5 ± 0.4, 8.9–10.4	11.5 ± 0.3, 11.2–11.9
TBL	10 ± 0.4, 9.3–10.5	11.9 ± 0.2, 11.6–12.2
FL	9.7 ± 0.5, 8.8–10.5	12.2 ± 0.3, 11.8–12.6

TABLE 2. Major differences in calls between Ischnocnema nigriventris and other species of Ischnocnema.

Number of notes/ call 1	2–4	3–8
Call duration (ms) -	194–565	2000–5000
Call rate (Calls/s) -	-	0.1–0.2
Note duration (ms) 30–41	28–88	40–100
Pulses p/call -	-	4–10
Dominant frequency (Hz) 2004–3685	1955–3932	3800–5200
Other frequencies (Hz)	-	-
TABLE 2. (Continued)