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Zootaxa 3694 (2): 131–142 www.mapress.com /zootaxa /
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http://dx.doi.org/10.11646/zootaxa.3694.2.2 http://zoobank.org/urn:lsid:zoobank.org:pub:CBD951AE-A784-46B5-B212-22A7013838BA
Rediscovery and re-description of Ischnocnema nigriventris (Lutz, 1925) (Anura: Terrarana: Brachycephalidae) BIANCA V. M. BERNECK1, MARIANE TARGINO2 & PAULO CHRISTIANO DE ANCHIETTA GARCIA3 1
Departamento de Zoologia, Instituto de Biociências; Universidade Estadual Paulista “Júlio de Mesquita Filho”, Caixa Postal 199, Av. 24-A, 1515, Bela Vista, 13506–900 Rio Claro, Brazil. E-mail:
[email protected] 2 Departamento de Zoologia, Instituto de Biociências; Universidade de São Paulo, Rua do Matão, trav. 14, 321, Cidade Universitária, 05508-090 São Paulo, Brazil 3 Departamento de Zoologia, Instituto de Ciências Biológicas; Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, Pampulha, 31270–901 Belo Horizonte, Brazil
Abstract Besides its brief original description in 1925 and information provided by one specimen collected in the 1980s, nothing else is known for Ischnocnema nigriventris (Lutz, 1925). Also, the poor preservation of the type series has hindered the association of this name with any known population of Ischnocnema. Fieldwork in Bertioga municipality, state of São Paulo, Brazil, revealed a population of Ischnocnema to which we were able to apply the name Ischnocnema nigriventris. We report this rediscovery, re-describe the species on the basis of the newly found specimens, and describe its mating call. Ischnocnema nigriventris is allocated to the Ischnocnema lactea species series and we propose a diagnosis based on a combination of morphological character states. The species is diagnosed by prominent conical tubercles on the upper eyelid, inguinal region and hidden areas of the hind limbs with yellow mottling in males and orange mottling in females, and by its advertisement call composed of two to four non-pulsed notes, the first one differentiated from the others by its lower intensity and different frequency. Ischnocnema nigriventris is only known from Parque das Neblinas (Bertioga municipality), Paranapiacaba (Santo André municipality), and Boracéia (Salesópolis municipality), localities in the state of São Paulo, Brazil Key words: Ischnocnema; taxonomy; natural history; advertisement call; Brazilian Atlantic Forest
Introduction Ischnocnema nigriventris (Lutz, 1925) was briefly described in the original publication and reported to occur in the localities “Serra de Cubatão” (subsequently corrected to Paranapiacaba district in the Santo André municipality, state of São Paulo, Brazil, by Bokermann, 1966) and “Itatiaia” (state of Rio de Janeiro, Brazil). Heyer (1985) designated a lectotype, restricted the type locality to Paranapiacaba, and reported one additional specimen from Boracéia, state of São Paulo. The lectotype was briefly described by Heyer et al. (1990). Ischnocnema nigriventris was first allocated to the former Eleutherodactylus lacteus species group by Lynch (1968), a decision followed in subsequent works (Lynch, 1976; Heyer, 1985; Heyer et al. 1990; Hedges et al. 2008). Heinicke et al. (2007) resurrected the genus Ischnocnema for the former species groups of Eleutherodactylus distributed in the Atlantic Forest in Brazil (the E. guentheri, E. lacteus, E. parva, and E. ramagii groups). Some modifications in the content of these species series were made in subsequent works (Canedo et al 2010; Canedo and Haddad, 2012). Canedo and Haddad (2012) presented a molecular phylogenetic analysis of the genus Ischnocnema. The sample of the species identified as Ischnocnema cf. nigriventris corresponds to I. nigriventris as discussed in the present work, and it was placed by these authors in the Ischnocnema lactea species series, as sister taxon of Ischnocnema vizottoi + I. concolor. The brief and scarcely informative original description of Ischnocnema nigriventris, together with the bad state of conservation of the type specimens, made it difficult to associate this name with any known population of
Accepted by J. Padial: 10 Jul. 2013; published: 2 Aug. 2013
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Ischnocnema. Heyer (1985) and Heyer et al. (1990) provided relevant comments on the type series and a brief description of a single specimen from Boracéia. However, an extensive diagnosis distinguishing this species from other species of Ischnocnema, and information on morphological variation is still missing. Recently, fieldwork near the type locality at “Parque das Neblinas” (Bertioga municipality, state of São Paulo, Brazil), allowed us to observe and collect specimens assignable to Ischnocnema nigriventris (Lutz, 1925). Herein, we re-describe the species on the basis of twenty specimens, and provide data on intraspecific variation, vocalizations, and natural history.
Material and methods Specimens were collected during August, September, and November 2005, and in June 2009 at Parque das Neblinas, “Reserva Privada do Patrimônio Natural” (RPPN), a protected area belonging to the Ecofuturo Institute, a Non–Governmental Organization. The Park consists of 1.332,82 hectares covered by Atlantic Forest, with different degrees of human disturbance and presence of Eucalyptus spp. Collected and studied specimens are housed at the following herpetological collections (Appendix I): Célio F. B. Haddad (CFBH) at Universidade Estadual Paulista, Rio Claro, Brazil, Museu de Zoologia da Universidade de São Paulo (MZUSP), São Paulo, and the Adolpho Lutz at Museu Nacional (AL-MN), Rio de Janeiro. The following measurements were taken from preserved specimens: SVL (snout-vent length), HL (head length), HW (head width), ED (eye diameter), END (eye-nostril distance), IND (internasal distance), NSD (nostril to tip of snout distance), THL (thigh length), TBL (tibia length), and FL (foot length), following Duellman (1970); and AMD (distance between the anterior margins of the eyes), following Garcia et al (2003). All measurements are in millimeters and were measured using a digital caliper under a Nikon SMZ800 stereomicroscope. The terminology for disk morphology follows Savage (1987). Ovules were measured using a micrometric scale on a Zeiss SV11 stereomicroscope. Calls were recorded with a Marantz PMD-222 tape recorder and Audiotechnica AT835 directional microphone, and analyzed using Raven 1.4 (Cornell Lab of Ornithology Research Program Bioacoustics Workstation). Sounds were digitalized at 44.1 kHz and audio-spectrograms produced with frame length of 256 points FFT, frame overlap = 75% and Hamming function. We used five call parameters to describe the vocalizations (terminology follows Cocroft & Ryan 1995): call duration, note duration, note interval (measured directly at the waveform), frequency range (measured directly into spectrogram) and peak of frequency (obtained directly from the software), considered here as the dominant frequency. Recordings were housed at the Paulo Christiano de Anchietta Garcia (PCAG) collection of calls of the Laboratório de Herpetologia, Departamento de Zoologia, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil.
Ischnocnema nigriventris (Lutz, 1925) Hylaplesia nigriventris Lutz 1925: original description, type locality “Itatiaia and Serra do Cubatão”. Basanitia nigriventris—Bokermann, 1966: first combination with Basanitia. Modification of one of the type localities, “Serra do Cubatão” corrected to Paranapiacaba, Santo André municipality. Eleutherodactylus nigriventris—Lynch 1968: first combination with Eleutherodactylus. Eleutherodactylus nigroventris—Lynch 1976: Misspelling for Eleutherodactylus nigriventris. Eleutherodactylus nigriventris—Heyer, 1985: designation of a lectotype and restriction of the type locality to Paranapiacaba, Santo André municipality. Eleutherodactylus (Eleutherodactylus) nigriventris— Lynch & Duellman, 1997. Ischnocnema nigriventris—Heinicke, Duellman & Hedges, 2007: first combination with Ischnocnema.
Lectotype: AL-MN 719, a juvenile male from Paranapiacaba, Santo André municipality, state of São Paulo, Brazil, designated by Heyer (1985). Paralectotypes: AL-MN 721, USNM 96846, juveniles, both from Paranapiacaba, Santo André municipality, state of São Paulo, Brazil. AL-MN 720 juvenile of Ischnocnema guentheri (see Heyer, 1985) from Paranapiacaba, Santo André municipality, state of São Paulo, Brazil.
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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 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
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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.
FIGURE 1. Ischnocnema nigriventris male (MZUSP 136689). Dorsal and lateral view of the head and ventral view of hand and foot. Scale: 5mm.
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.
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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]).
FIGURE 2. Intraspecific dorsal pattern variation of Ischnocnema nigriventris A. CFBH 23480; B. MZUSP 136693; C. MZUSP 136694; D. MZUSP 136695.
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).
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FIGURE 3. Ischnocnema nigriventris in life. Male, MZUSP 136725 SVL19.4mm (A and B). Female, MZUSP 136724 SVL24.5mm (C and D).
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
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).
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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 09 2005; 18:31h. Air temperature 16.5ºC.
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 03 2006; 23:45h. Air temperature 19.5ºC.
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).
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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. TABLE 2. Major differences in calls between Ischnocnema nigriventris and other species of Ischnocnema. I. nigriventris Call 1
I. nigriventris Call 2 (advertissment call)
(Heyer et al. 1990)
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)
I. randorum
TABLE 2. (Continued) I. vizottoi (Martins & Haddad, 2010)
I. manezinho (Castanho & Haddad, 2000)
I. sambaqui (Castanho & Haddad, 2000)
Number of notes/ call
1
11–13*
6–8*
Call duration (ms)
-
790–977
508–633
Call rate (Calls/s)
9.5 ± 2.2 (notes/min)
-
-
Note duration (ms)
38–72
17
48
Pulses p/call
-
-
-
Dominant frequency (Hz)
2780–3555
2400–2950
1800–2050
Other frequencies (Hz)
6585–7317
* Cited as pulses.
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.
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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.
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.
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FIGURE 7. Lectotype of Ischnocnema nigriventris (AL-MN 719).
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).
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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).
Acknowledgements We thank H. Zaher (MZUSP), J. P. Pombal Jr (MNRJ), and C. F. B. Haddad (CFBH) for the loan of specimens under their responsibility. Paulo Groke and Guilherme Dias (Ecofuturo Institute), for helping and allowing access to Parque das Neblinas. We are grateful to J. Faivovich, C. Canedo, V. Orrico, and U. Caramaschi for helpful suggestions. The distribution map was prepared by M. Segalla. C. O. R. Costa and M. Forlani for fieldwork help. We thank Dr. Padial and Dr. Pombal for helpful suggestions that greatly improved this manuscript. Berneck thanks FAPESP (Fundação de Amparo a Pesquisa do Estado de São Paulo 08/55235-4). PCA Garcia thanks Fapemig (Programa Pesquisador Mineiro) for financial support and CNPq for the productivity fellowship. MT thanks CNPq and FAPERJ for financial support.
References Bokermann, W.C.A. (1966) Lista anotada das localidades tipo de anfíbios Brasileiros. São Paulo, Serviço de Documentação, Universidade Rural São Paulo, 183 pp. Canedo, C. & Pimenta, B.V.S. (2010) New species of Ischnocnema (Anura, Brachycephalidae) from the Atlantic Rainforest of the State of Espírito Santo, Brazil. South American Journal of Herpetology, 5 (3), 199–206. http://dx.doi.org/10.2994/057.005.0305 Castanho, L.M. & Haddad, C.F.B. (2000) New species of Eleutherodactylus (Amphibia: Leptodactylidae) from Guaraqueçaba, Atlantic forest of Brazil. Copeia, 2000, 777–781. http://dx.doi.org/10.1643/0045-8511(2000)000[0777:nsoeal]2.0.co;2 Cei, J.M. (1980) Amphibians of Argentina. Monitore Zoologico Italiano, Nuova Serie, Monographia, 2, 1–609. http://dx.doi.org/10.1163/156853881x00465 Cochran, D.M. (1961) Type specimens of reptiles and amphibians in the U.S. National Museum. Bulletin of the United States National Museum, 220, 1–291. http://dx.doi.org/10.5479/si.03629236.220 Cocroft, R.B. & Ryan, M.J. (1995) Patterns of advertisement call evolution in toads and chorus frogs. Animal Behaviour, 49, 283–303. http://dx.doi.org/10.1006/anbe.1995.0043 Duellman, W.E. (2001) The hylid frogs of Middle America, Society for the Study of Amphibians and Reptiles, Ithaca, New York, USA, 1159 pp. Garcia, P.C.A, Vinciprova, G. & Haddad, C.F.B. (2003) The taxonomic status of Hyla pulchella joaquini (Anura: Hylidae) with description of its tadpole and vocalization. Herpetologica, 59, 3, 350–363. http://dx.doi.org/10.1655/01-54 Hedges, S.B., Duellman, W.E. & Heinicke M.P. (2008) New World direct-developing frogs (Anura: Terrarana): molecular phylogeny, classification, biogeography, and conservation. Zootaxa, 1737, 1–182. Heinicke, M.P., Duellman, W.E. & Hedges, S.B. (2007) Major Caribbean and Central American frog faunas originated by ancient oceanic dispersal. Proceedings of the National Academy of Sciences of the United States of America, 104 (24), 10092–10097. http://dx.doi.org/10.1073/pnas.0611051104
REDISCOVERY, RE-DESCRIPTION OF ISCHNOCNEMA NIGRIVENTRIS
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Heyer, W.R. (1984) Variation, systematics, and zoogeography of Eleutherodactylus guentheri and closely related species (Amphibia: Anura: Leptodactylidae). Smithsonian Contributions to Zoology, 402, 1–42. http://dx.doi.org/10.5479/si.00810282.402 Heyer, W.R. (1985) New species of frogs from Boracéia, São Paulo, Brazil. Proceedings of the Biological Society of Washington 98, 657–671. Heyer, W.R., Rand, A.S.C., Cruz, C.A.G., Peixoto, O.L. & Nelson C.E. (1990) Frogs of Boracéia. Arquivos de Zoologia, 31, 231–410. Langone, J.A. & Segalla, M.V. (1996) Una nueva especie de Eleutherodactylus del estado de Paraná, Brasil (Amphibia, Anura, Leptodactylidae). Comunicaciones Zoologicas del Museo de Historia Natural de Montevideo, 12 (185), 1–7. Lynch, J.D. (1968) The status of the nominal genera Basanitia and Phrynanodus from Brazil (Amphibia: Leptodactylidae). Copeia, 1968, 875–876. http://dx.doi.org/10.2307/1441865 Lynch, J.D. (1976) The species groups of the South American frogs of the genus Eleutherodactylus (Leptodactylidae). Occasional papers of the Museum of Natural History of the University of Kansas, 61, 1–24. Lynch, J.D. & Duellman, W.E. (1997) Frogs of the genus Eleutherodactylus in western Ecuador. Systematics, ecology, and biogeography. Natural History Museum University of Kansas, 23, 1–236. http://dx.doi.org/10.5962/bhl.title.7951 Lutz, A. (1925) Batraciens du Brésil. Comptes Rendus et Mémoires Hebdomadaires des Séances de la Société de Biologie et des ses Filiales, 2, 137–139. Martins, I.A. & Haddad C.F.B. (2010) A new species of Ischnocnema from highlands of the Atlantic forest, southeasteastern Brazil (Terrarana, Brachycephalidae). Zootaxa, 2617, 55–65. Miranda-Ribeiro, A. (1923) Basanitia lactea (Um novo batracchio das collecções do Museu Paulista). Revista do Museu Paulista, 13, 851–852. Miranda-Ribeiro, A. (1926) Notas para servirem ao estudo dos Gymnobatrachios (Anura) Brasileiros. Arquivos do Museu Nacional. Rio de Janeiro, 27, 1–227. Pombal, J.P Jr. & Cruz, C.A.G. (1999) Redescrição de Eleutherodactylus bolbodactylus (A.Lutz, 1925) e a posição taxonômica de E. gehrti (Miranda-Ribeiro, 1926) (Anura, Leptodactylidae). Boletim do Museu Nacional (N.S.) Zoologia, 404, 1–10. Savage, J.M. (1987) Systematics and distribution of the Mexican and Central American rainfrogs of the Eleutherodactylus gollmeri group (Amphibia: Leptodactylidae). Fieldiana Zoology, New Series, 33, 1–57. http://dx.doi.org/10.5962/bhl.title.2871 Targino, M. & Carvalho-e-Silva, S.P (2008) Redescrição de Ischnocnema holti (Cochran, 1948) (Amphibia, Anura, Brachycephalidae). Revista Brasileira de Zoologia, 25 (4), 716–723. http://dx.doi.org/10.1590/s0101-81752008000400017 Targino, M., Costa, P.N. & Carvalho-e-Silva, S.P. (2009) Two New Species of the Ischnocnema lactea Species Series from Itatiaia Highlands, Southeastern Brazil (Amphibia, Anura, Brachycephalidae). South American Journal of Herpetology, 4, 2, 139–150. http://dx.doi.org/10.2994/057.004.0205
APPENDIX I. Specimens examined. Ischnocnema nigriventris: MZUSP 37787; AL-MN 719 (lectotype) Paranapiacaba, São Paulo; AL-MN 720–21 (paralectotypes), Paranapiacaba, São Paulo; CFBH 23479–23481, Parque das Neblinas, Bertioga, São Paulo; 28950– 28952, Paranabiacaba, Santo André, São Paulo; MZUSP 135895–135898, 136689–136694, 136725 and MZUSP 136695 136724, Parque das Neblinas, Bertioga, São Paulo. Males measured CFBH 23479–23481; 28951; 28952. MZUSP 135895–135898; 136689–136694; 136725. Females measured: CFBH 23478 MZUSP 136695; 136724. Ischnocnema holti: CFBH10316, Itamonte, Minas Gerais. Ischnocnema gehrti: MNRJ 0105, (holotype), Paranapiacaba, Santo André, São Paulo. Ischnocnema lactea: MZUSP 828 (lectotype) Iguape, São Paulo. Ischnocnema sambaqui: MNRJ 21735 (holotype) Guaraqueçaba, Paraná; CFBH 2934–36 (paratypes), MNRJ 21733–21734 (paratypes). Ischnocnema venancioi MNRJ 44113, 44564, 53567, 53569–53571, 53590–53598, 53932, 56191–56215: Teresópolis, Rio de Janeiro; Ischnocnema spanios: MZUSP 23664 (holotype) Boracéia, Salesópolis, São Paulo. Ischnocnema randorum: MZUSP 59936 (holotype), MZUSP 36865 (paratype) Boracéia, Salesópolis, São Paulo. Ischnocnema manezinho: MNRJ 17478–79 (paratypes), ZUEC 9547 (paratype), CFBH 2979 Florianópolis, Santa Catarina; CFBH 3157 Corupá, Santa Catarina; CFBH 3158, São Bento do Sul. Paraná; CFBH 5481, Guaratuba, Paraná. Ischnocnema melanopygia: CFBH 16512, 16697 Itamonte, Minas Gerais. Ischnocnema concolor: MNRJ 57648; Parque Nacional do Itatiaia, Itatiaia, Rio de Janeiro. Ischnocnema bolbodactyla: AL-MN 445 (lectotype) Angra dos Reis, Rio de Janeiro; MNRJ 24131–24132, MNRJ 43390– 93 Parati, Rio de Janeiro. Ischnocnema bilineata: MNRJ 46476, 52873, Boa Nova, Bahia; MNRJ 40293, Canavieiras, Bahia; MNRJ 23776, Ilhéus, Bahia. Ischnocnema abdita: CFBH 2268–2270, 2278–2279, 22521–22522, Cariacica Espírito Santo; CFBH 22296–22298 Mimoso do Sul, Espírito Santo; CFBH 10840–10841, 10878–10879 Santa Teresa, Espírito Santo.
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