rediscovery and re-description of ischnocnema nigriventris (lutz

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Accepted by J. Padial: 10 Jul. 2013; published: 2 Aug. 2013 ZOOTAXA ISSN 1175-5326 (print edition) ISSN 1175-5334 (online edition) Copyright © 2013 Magnolia Press Zootaxa 3694 (2): 131142 www.mapress.com/zootaxa/ Article 131 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. BERNECK 1 , MARIANE TARGINO 2 & PAULO CHRISTIANO DE ANCHIETTA GARCIA 3 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, Pam- pulha, 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 eye- lid, 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 municipal- ity), Paranapiacaba (Santo André municipality), and Boracéia (Salesópolis municipality), localities in the state of São Pau- lo, 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

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  • ZOOTAXA

    ISSN 1175-5326 (print edition)

    ISSN 1175-5334 (online edition)Copyright 2013 Magnolia Press

    Zootaxa 3694 (2): 131142 www.mapress.com/zootaxa/

    Article

    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

    1Departamento de Zoologia, Instituto de Biocincias; Universidade Estadual Paulista Jlio de Mesquita Filho, Caixa Postal 199,

    Av. 24-A, 1515, Bela Vista, 13506900 Rio Claro, Brazil. E-mail: [email protected] de Zoologia, Instituto de Biocincias; Universidade de So Paulo, Rua do Mato, trav. 14, 321, Cidade Universitria,

    05508-090 So Paulo, Brazil3Departamento de Zoologia, Instituto de Cincias Biolgicas; Universidade Federal de Minas Gerais, Av. Antnio Carlos, 6627, Pam-

    pulha, 31270901 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 So

    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 eye-

    lid, 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 municipal-

    ity), Paranapiacaba (Santo Andr municipality), and Boracia (Salespolis municipality), localities in the state of So Pau-

    lo, 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 Cubato (subsequently corrected to Paranapiacaba district in the Santo Andr municipality,

    state of So 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

    Boracia, state of So 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 131

  • Ischnocnema. Heyer (1985) and Heyer et al. (1990) provided relevant comments on the type series and a brief

    description of a single specimen from Boracia. 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 So 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 Patrimnio Natural (RPPN), a protected area belonging to the Ecofuturo Institute,

    a NonGovernmental 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): Clio F.

    B. Haddad (CFBH) at Universidade Estadual Paulista, Rio Claro, Brazil, Museu de Zoologia da Universidade de

    So Paulo (MZUSP), So 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 Laboratrio 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 Cubato.

    Basanitia nigriventrisBokermann, 1966: first combination with Basanitia. Modification of one of the type localities, Serra

    do Cubato corrected to Paranapiacaba, Santo Andr municipality.

    Eleutherodactylus nigriventrisLynch 1968: first combination with Eleutherodactylus.

    Eleutherodactylus nigroventrisLynch 1976: Misspelling for Eleutherodactylus nigriventris.

    Eleutherodactylus nigriventrisHeyer, 1985: designation of a lectotype and restriction of the type locality to Paranapiacaba,

    Santo Andr municipality.

    Eleutherodactylus (Eleutherodactylus) nigriventris Lynch & Duellman, 1997.

    Ischnocnema nigriventrisHeinicke, Duellman & Hedges, 2007: first combination with Ischnocnema.

    Lectotype: AL-MN 719, a juvenile male from Paranapiacaba, Santo Andr municipality, state of So Paulo,

    Brazil, designated by Heyer (1985).

    Paralectotypes: AL-MN 721, USNM 96846, juveniles, both from Paranapiacaba, Santo Andr municipality,

    state of So Paulo, Brazil. AL-MN 720 juvenile of Ischnocnema guentheri (see Heyer, 1985) from Paranapiacaba,

    Santo Andr municipality, state of So Paulo, Brazil.BERNECK ET AL. 132 Zootaxa 3694 (2) 2013 Magnolia Press

  • 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; sub-

    articular 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 IIIV 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 Zootaxa 3694 (2) 2013 Magnolia Press 133REDISCOVERY, RE-DESCRIPTION OF ISCHNOCNEMA NIGRIVENTRIS

  • 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. BERNECK ET AL. 134 Zootaxa 3694 (2) 2013 Magnolia Press

  • 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 1820 mm;

    presence of nuptial pads; and bright coloration in hidden areas in life (bigger size, I. sambaqui males 3240 mm,

    and I. manezinho males 2228 mm; absence of nuptial pads and bright colors in hidden areas in life). Zootaxa 3694 (2) 2013 Magnolia Press 135REDISCOVERY, RE-DESCRIPTION OF ISCHNOCNEMA NIGRIVENTRIS

  • 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).

    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 2.83.3 seconds (Figure 4). Note duration is 3041 ms (36.1 3.8 ms, n = 8 calls of two individuals).

    The frequency spectrum is 20043685 Hz and the peak frequency (= dominant frequency) is 29283014 Hz (2965

    46.0, n = 8 calls of two individuals).

    Measurements Males (n=16) Females (n=3)

    SVL 19.0 0.6, 18.220.2 24.6 0.1, 24.524.7

    HL 6.6 0.4, 6.27.4 8.1 0.3, 7.78.4

    HW 6.9 0.2, 6.47.2 8.6 0.1, 8.48.7

    ED 2.6 0.2, 2.33.1 3 0.0, 3.03.1

    END 1.9 0.2, 1.12.1 2.5 0.0, 2.52.6

    AMD 3.6 0.2, 3.33.8 4.5 0.0, 4.44.5

    IND 1.9 0.10, 1.72.0 2.4 0.1, 2.32.6

    NSD 1.1 0.1, 1.01.4 1.4 0.1, 1.41.5

    THL 9.5 0.4, 8.910.4 11.5 0.3, 11.211.9

    TBL 10 0.4, 9.310.5 11.9 0.2, 11.612.2

    FL 9.7 0.5, 8.810.5 12.2 0.3, 11.812.6BERNECK ET AL. 136 Zootaxa 3694 (2) 2013 Magnolia Press

  • FIGURE 4. Spectrogram (above) and waveform (below) of the putative territorial call of Ischnocnema nigriventris (MZUSP

    136694) from Parque das Neblinas, Bertioga, state of So Paulo, Brazil, recorded on September 09 2005; 18:31h. Air

    temperature 16.5C.

    FIGURE 5. Spectrogram (above) and waveform (below) of the putative advertisement call of Ischnocnema nigriventris

    (MZUSP 135895) from Parque das Neblinas, Bertioga, state of So Paulo, Brazil, recorded on November 03 2006; 23:45h. Air

    temperature 19.5C.

    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 194565 ms, the frequency spectrum is 19553932

    Hz, and the peak frequency is 27562928 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 1133% lower than the others) and lower

    frequency range (the first note ranged from 21512774 Hz). Note duration is similar, the first note is 3089 ms

    (54.2 2.0 ms) and the others are 2888 ms (41.7 2.0 ms). The interval between the notes is 113157 ms (132

    12 ms). Zootaxa 3694 (2) 2013 Magnolia Press 137REDISCOVERY, RE-DESCRIPTION OF ISCHNOCNEMA NIGRIVENTRIS

  • 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.

    TABLE 2. (Continued)

    * 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: 2.53.2 ( =2.8mm).

    Distribution. Ischnocnema nigriventris is only known from the Parque das Neblinas (Bertioga municipality),

    Paranapiacaba (Santo Andr municipality), and Boracia (Salespolis municipality), all localities in the Serra do

    Mar, eastern So 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 Cubato and Itatiaia, for

    the distribution of the species. Cochran (1961) lists one cotype, measuring 6.5 mm total length, from Serra de

    Cubato 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 Andr, state of So 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.

    I. nigriventris

    Call 1

    I. nigriventris

    Call 2 (advertissment call)

    I. randorum

    (Heyer et al. 1990)

    Number of notes/ call 1 24 38

    Call duration (ms) - 194565 20005000

    Call rate (Calls/s) - - 0.10.2

    Note duration (ms) 3041 2888 40100

    Pulses p/call - - 410

    Dominant frequency (Hz) 20043685 19553932 38005200

    Other frequencies (Hz) - -

    I. vizottoi

    (Martins & Haddad, 2010)

    I. manezinho

    (Castanho & Haddad, 2000)

    I. sambaqui

    (Castanho & Haddad, 2000)

    Number of notes/ call 1 1113* 68*

    Call duration (ms) - 790977 508633

    Call rate (Calls/s) 9.5 2.2 (notes/min) - -

    Note duration (ms) 3872 17 48

    Pulses p/call - - -

    Dominant frequency (Hz) 27803555 24002950 18002050

    Other frequencies (Hz) 65857317

    x

    BERNECK ET AL. 138 Zootaxa 3694 (2) 2013 Magnolia Press

  • FIGURE 6. Map showing the geographical distribution of Ischnocnema nigriventris. The square is Boracia, Salespolis; the

    triangle is Parque das Neblinas, Bertioga and the circle is the type-locality, Paranapiacaba, Santo Andr. All localities in the

    state of So 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 Cubato 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. Zootaxa 3694 (2) 2013 Magnolia Press 139REDISCOVERY, RE-DESCRIPTION OF ISCHNOCNEMA NIGRIVENTRIS

  • 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 Cubato Alto Itatiaia (see text).BERNECK ET AL. 140 Zootaxa 3694 (2) 2013 Magnolia Press

  • 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

    (MirandaRibeiro, 1926). The type of Ischnocnema lactea is from Iguape, state of So Paulo, SVL 32 mm, and the

    description makes no reference to bright coloration in life or palpebral tubercles (MirandaRibeiro, 1923). The

    type of Ischnocnema paranaensis is from Pico Paran, state of Paran, 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 (Fundao de Amparo a Pesquisa do Estado de So 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 anfbios Brasileiros. So Paulo, Servio de Documentao,

    Universidade Rural So Paulo, 183 pp.

    Canedo, C. & Pimenta, B.V.S. (2010) New species of Ischnocnema (Anura, Brachycephalidae) from the Atlantic Rainforest of

    the State of Esprito Santo, Brazil. South American Journal of Herpetology, 5 (3), 199206.

    http://dx.doi.org/10.2994/057.005.0305

    Castanho, L.M. & Haddad, C.F.B. (2000) New species of Eleutherodactylus (Amphibia: Leptodactylidae) from Guaraqueaba,

    Atlantic forest of Brazil. Copeia, 2000, 777781.

    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, 1609.

    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, 1291.

    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,

    283303.

    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, 350363.

    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, 1182.

    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),

    1009210097.

    http://dx.doi.org/10.1073/pnas.0611051104 Zootaxa 3694 (2) 2013 Magnolia Press 141REDISCOVERY, RE-DESCRIPTION OF ISCHNOCNEMA NIGRIVENTRIS

    http://dx.doi.org/10.1643/0045-8511(2000)000[0777:nsoeal]2.0.co;2http://dx.doi.org/10.1643/0045-8511(2000)000[0777:nsoeal]2.0.co;2http://research.amnh.org/vz/herpetology/amphibia/?action=names&a_id=4196http://research.amnh.org/vz/herpetology/amphibia/?action=names&p_id=9http://research.amnh.org/vz/herpetology/amphibia/?action=names&p_id=9

  • Heyer, W.R. (1984) Variation, systematics, and zoogeography of Eleutherodactylus guentheri and closely related species

    (Amphibia: Anura: Leptodactylidae). Smithsonian Contributions to Zoology, 402, 142.

    http://dx.doi.org/10.5479/si.00810282.402

    Heyer, W.R. (1985) New species of frogs from Boracia, So Paulo, Brazil. Proceedings of the Biological Society of

    Washington 98, 657671.

    Heyer, W.R., Rand, A.S.C., Cruz, C.A.G., Peixoto, O.L. & Nelson C.E. (1990) Frogs of Boracia. Arquivos de Zoologia, 31,

    231410.

    Langone, J.A. & Segalla, M.V. (1996) Una nueva especie de Eleutherodactylus del estado de Paran, Brasil (Amphibia, Anura,

    Leptodactylidae). Comunicaciones Zoologicas del Museo de Historia Natural de Montevideo, 12 (185), 17.

    Lynch, J.D. (1968) The status of the nominal genera Basanitia and Phrynanodus from Brazil (Amphibia: Leptodactylidae).

    Copeia, 1968, 875876.

    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, 124.

    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, 1236.

    http://dx.doi.org/10.5962/bhl.title.7951

    Lutz, A. (1925) Batraciens du Brsil. Comptes Rendus et Mmoires Hebdomadaires des Sances de la Socit de Biologie et

    des ses Filiales, 2, 137139.

    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, 5565.

    Miranda-Ribeiro, A. (1923) Basanitia lactea (Um novo batracchio das colleces do Museu Paulista). Revista do Museu

    Paulista, 13, 851852.

    Miranda-Ribeiro, A. (1926) Notas para servirem ao estudo dos Gymnobatrachios (Anura) Brasileiros. Arquivos do Museu

    Nacional. Rio de Janeiro, 27, 1227.

    Pombal, J.P Jr. & Cruz, C.A.G. (1999) Redescrio de Eleutherodactylus bolbodactylus (A.Lutz, 1925) e a posio taxonmica

    de E. gehrti (Miranda-Ribeiro, 1926) (Anura, Leptodactylidae). Boletim do Museu Nacional (N.S.) Zoologia, 404, 110.

    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, 157.

    http://dx.doi.org/10.5962/bhl.title.2871

    Targino, M. & Carvalho-e-Silva, S.P (2008) Redescrio de Ischnocnema holti (Cochran, 1948) (Amphibia, Anura,

    Brachycephalidae). Revista Brasileira de Zoologia, 25 (4), 716723.

    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, 139150.

    http://dx.doi.org/10.2994/057.004.0205

    APPENDIX I. Specimens examined.

    Ischnocnema nigriventris: MZUSP 37787; AL-MN 719 (lectotype) Paranapiacaba, So Paulo; AL-MN 72021

    (paralectotypes), Paranapiacaba, So Paulo; CFBH 2347923481, Parque das Neblinas, Bertioga, So Paulo; 28950

    28952, Paranabiacaba, Santo Andr, So Paulo; MZUSP 135895135898, 136689136694, 136725 and MZUSP 136695

    136724, Parque das Neblinas, Bertioga, So Paulo. Males measured CFBH 2347923481; 28951; 28952. MZUSP

    135895135898; 136689136694; 136725. Females measured: CFBH 23478 MZUSP 136695; 136724. Ischnocnema

    holti: CFBH10316, Itamonte, Minas Gerais. Ischnocnema gehrti: MNRJ 0105, (holotype), Paranapiacaba, Santo Andr,

    So Paulo. Ischnocnema lactea: MZUSP 828 (lectotype) Iguape, So Paulo. Ischnocnema sambaqui: MNRJ 21735

    (holotype) Guaraqueaba, Paran; CFBH 293436 (paratypes), MNRJ 2173321734 (paratypes). Ischnocnema venancioi

    MNRJ 44113, 44564, 53567, 5356953571, 5359053598, 53932, 5619156215: Terespolis, Rio de Janeiro;

    Ischnocnema spanios: MZUSP 23664 (holotype) Boracia, Salespolis, So Paulo. Ischnocnema randorum: MZUSP

    59936 (holotype), MZUSP 36865 (paratype) Boracia, Salespolis, So Paulo. Ischnocnema manezinho: MNRJ 1747879

    (paratypes), ZUEC 9547 (paratype), CFBH 2979 Florianpolis, Santa Catarina; CFBH 3157 Corup, Santa Catarina;

    CFBH 3158, So Bento do Sul. Paran; CFBH 5481, Guaratuba, Paran. 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 2413124132, MNRJ 43390

    93 Parati, Rio de Janeiro. Ischnocnema bilineata: MNRJ 46476, 52873, Boa Nova, Bahia; MNRJ 40293, Canavieiras,

    Bahia; MNRJ 23776, Ilhus, Bahia. Ischnocnema abdita: CFBH 22682270, 22782279, 2252122522, Cariacica

    Esprito Santo; CFBH 2229622298 Mimoso do Sul, Esprito Santo; CFBH 1084010841, 1087810879 Santa Teresa,

    Esprito Santo.BERNECK ET AL. 142 Zootaxa 3694 (2) 2013 Magnolia Press

    http://research.a

    AbstractIntroductionMaterial and methodsIschnocnema nigriventris (Lutz, 1925)Re-description of Ischnocnema nigriventrisAcknowledgementsReferences

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