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Accepted by V. Orrico: 15 Nov. 2013; published: 11 Dec. 2013 ZOOTAXA ISSN 1175-5326 (print edition) ISSN 1175-5334 (online edition) Copyright © 2013 Magnolia Press Zootaxa 3746 (2): 383392 www.mapress.com/zootaxa/ Article 383 http://dx.doi.org/10.11646/zootaxa.3746.2.8 http://zoobank.org/urn:lsid:zoobank.org:pub:38E6A09F-0CF4-46FB-84B7-7DF0369A02F8 New bioacoustic and distributional data on Bokermannohyla sapiranga Brandão et al., 2012 (Anura: Hylidae): revisiting its diagnosis in comparison with B. pseudopseudis (Miranda-Ribeiro, 1937) THIAGO RIBEIRO DE CARVALHO 1,2,3 , ARIOVALDO ANTONIO GIARETTA 1 , BERNARDO FRANCO DA VEIGA TEIXEIRA 1, 2 & LUCAS BORGES MARTINS 1, 2 1 Laboratório de Taxonomia, Sistemática e Ecologia Comportamental de Anuros Neotropicais. Faculdade de Ciências Integradas do Pontal, Universidade Federal de Uberlândia (UFU), Rua 20, 1600, 38304-402, Ituiutaba, Minas Gerais, Brasil 2 Programa de Pós-Graduação em Biologia Comparada, Universidade de São Paulo, Departamento de Biologia/FFCLRP. Avenida dos Bandeirantes, 3900, 14040-901, Ribeirão Preto, São Paulo, Brasil 3 Corresponding author. E-mail: [email protected] Abstract In this paper, we provide new bioacoustic and distributional data on Bokermannohyla sapiranga, as well as additional comparative bioacoustic data on topotypes of B. pseudopseudis, and re-evaluate the differential diagnosis of the former species with respect to the latter. Head shapes (dorsal and lateral views) presented such variation that should not be used to differentially diagnose them as originally proposed. On the other hand, the presence of a dermal ridge along outer tarsi, and color patterns of the eyes and dorsal surface of hand/toe disks still represent diagnostic characters between both spe- cies. We also found differences in temporal (call duration; notes per call), spectral (dominant frequency; harmonics), and structural (pulsed/non-pulsed note structure) traits of their calls. Distribution of B. sapiranga is extended eastward (Para- catu), which corresponds to the first record for the State of Minas Gerais, whereas B. pseudopseudis distribution seems to be restricted to rocky montane field environments of northern Goiás State. Key words: Advertisement call, Cerrado domain, rocky montane fields, taxonomy Introduction The Bokermannohyla pseudopseudis (Miranda-Ribeiro, 1937) species group (sensu Faivovich et al. 2005) currently comprises nine species distributed in highlands of central (Chapada dos Veadeiros and Planalto Central), southeastern (Serra da Canastra and Espinhaço mountain ranges), and northeastern Brazil (Chapada Diamantina), usually associated with rocky montane fields (Leite et al. 2011, 2012; Brandão et al. 2012). Bokermannohyla pseudopseudis was described from the Chapada dos Veadeiros, Alto Paraíso de Goiás Municipality, Goiás State (Miranda-Ribeiro 1953), and was thought to also occur southward in the Distrito Federal (Pombal & Caramaschi 1995). Recently, this southern population was named, Bokermannohyla sapiranga Brandão et al., 2012, and was reported to occur in a few municipalities of Goiás (Pirenópolis, Cristalina, and Catalão) in addition to its type locality, and had its advertisement call described from Distrito Federal and Pirenópolis (Brandão et al. 2012). In this paper, we provide new bioacoustic and distributional data on B. sapiranga and additional bioacoustic data on B. pseudopseudis, and a re-evaluation, mainly through a bioacoustic approach, of B. sapiranga differential diagnosis in comparison with B. pseudopseudis. Material and methods Specimens and calls of topotypes of B. pseudopseudis were obtained at the Fazenda São Bento (14°10′30.56′′ S;
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  • ZOOTAXA

    ISSN 1175-5326 (print edition)

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

    Zootaxa 3746 (2): 383–392 www.mapress.com/zootaxa/

    Article

    http://dx.doi.org/10.11646/zootaxa.3746.2.8

    http://zoobank.org/urn:lsid:zoobank.org:pub:38E6A09F-0CF4-46FB-84B7-7DF0369A02F8

    New bioacoustic and distributional data on Bokermannohyla sapiranga Brandão

    et al., 2012 (Anura: Hylidae): revisiting its diagnosis in comparison with

    B. pseudopseudis (Miranda-Ribeiro, 1937)

    THIAGO RIBEIRO DE CARVALHO1,2,3, ARIOVALDO ANTONIO GIARETTA1,

    BERNARDO FRANCO DA VEIGA TEIXEIRA1, 2 & LUCAS BORGES MARTINS1, 2

    1Laboratório de Taxonomia, Sistemática e Ecologia Comportamental de Anuros Neotropicais. Faculdade de Ciências Integradas do

    Pontal, Universidade Federal de Uberlândia (UFU), Rua 20, 1600, 38304-402, Ituiutaba, Minas Gerais, Brasil2Programa de Pós-Graduação em Biologia Comparada, Universidade de São Paulo, Departamento de Biologia/FFCLRP. Avenida

    dos Bandeirantes, 3900, 14040-901, Ribeirão Preto, São Paulo, Brasil3Corresponding author. E-mail: [email protected]

    Abstract

    In this paper, we provide new bioacoustic and distributional data on Bokermannohyla sapiranga, as well as additional

    comparative bioacoustic data on topotypes of B. pseudopseudis, and re-evaluate the differential diagnosis of the former

    species with respect to the latter. Head shapes (dorsal and lateral views) presented such variation that should not be used

    to differentially diagnose them as originally proposed. On the other hand, the presence of a dermal ridge along outer tarsi,

    and color patterns of the eyes and dorsal surface of hand/toe disks still represent diagnostic characters between both spe-

    cies. We also found differences in temporal (call duration; notes per call), spectral (dominant frequency; harmonics), and

    structural (pulsed/non-pulsed note structure) traits of their calls. Distribution of B. sapiranga is extended eastward (Para-

    catu), which corresponds to the first record for the State of Minas Gerais, whereas B. pseudopseudis distribution seems to

    be restricted to rocky montane field environments of northern Goiás State.

    Key words: Advertisement call, Cerrado domain, rocky montane fields, taxonomy

    Introduction

    The Bokermannohyla pseudopseudis (Miranda-Ribeiro, 1937) species group (sensu Faivovich et al. 2005)

    currently comprises nine species distributed in highlands of central (Chapada dos Veadeiros and Planalto Central),

    southeastern (Serra da Canastra and Espinhaço mountain ranges), and northeastern Brazil (Chapada Diamantina),

    usually associated with rocky montane fields (Leite et al. 2011, 2012; Brandão et al. 2012). Bokermannohyla

    pseudopseudis was described from the Chapada dos Veadeiros, Alto Paraíso de Goiás Municipality, Goiás State

    (Miranda-Ribeiro 1953), and was thought to also occur southward in the Distrito Federal (Pombal & Caramaschi

    1995). Recently, this southern population was named, Bokermannohyla sapiranga Brandão et al., 2012, and was

    reported to occur in a few municipalities of Goiás (Pirenópolis, Cristalina, and Catalão) in addition to its type

    locality, and had its advertisement call described from Distrito Federal and Pirenópolis (Brandão et al. 2012).

    In this paper, we provide new bioacoustic and distributional data on B. sapiranga and additional bioacoustic

    data on B. pseudopseudis, and a re-evaluation, mainly through a bioacoustic approach, of B. sapiranga differential

    diagnosis in comparison with B. pseudopseudis.

    Material and methods

    Specimens and calls of topotypes of B. pseudopseudis were obtained at the Fazenda São Bento (14°10′30.56′′ S;

    Accepted by V. Orrico: 15 Nov. 2013; published: 11 Dec. 2013 383

  • 47°35′26.67′′ W; approximately 1290 m a.s.l.), Alto Paraíso de Goiás, northern Goiás, Brazil. Specimens and calls

    of B. sapiranga were obtained in four localities: 1) Parque Estadual de Caldas Novas [PESCAN (17°46′31.82′′ S;

    48°40′53.99′′ W, approximately 975 m a.s.l.)], Caldas Novas; 2) Pirenópolis (15°50′30.42′′ S; 48°58′05.89′′ W,

    approximately 800 m a.s.l.); 3) Cristalina (16°44′08.30′′ S; 47°35′29.78′′ W, approximately 1125 m a.s.l.), all three

    municipalities in Goiás (GO); and 4) Paracatu (17°27′03.23′′ S; 47°20′29.21′′ W; approximately 890 m a.s.l.),

    Minas Gerais State (MG).

    Examined specimens, including type material (in bold) and topotypical material (underlined), are listed in

    Appendix 1. Examined specimens are housed in the following Brazilian zoological collections: Coleção de Anuros

    do Museu de Biodiversidade do Cerrado, Universidade Federal de Uberlândia (AAG-UFU), Uberlândia, Minas

    Gerais, and Coleção Herpetológica da Universidade de Brasília (CHUNB), Brasília, Distrito Federal. Head shape

    terminology follows Heyer et al. (1990). Considering that both species were evaluated through a morphometric

    approach in the original description of B. sapiranga (see Brandão et al. 2012), we mainly focused our interspecific

    comparisons through a bioacoustic approach. Given this, our morphological description is brief, focusing mainly

    on the set of morphological characters and color patterns originally employed as part of the diagnosis of B.

    sapiranga (Brandão et al. 2012).

    Advertisement calls were recorded with digital equipment (Boss BR 864, M-audio Microtrack II, Marantz

    PMD 670 and 671) set at a sampling rate of 44.1 or 48.0 kHz and a resolution of 16 bits (mono WAVE format file),

    coupled to directional microphones (Sennheiser K6/ME67 or K6/ME66). Bioacoustic terminology follows

    Duellman and Trueb (1994).

    Calls were analyzed on a personal computer with Windows XP Professional operating system using the

    software Raven Pro version 1.5, 64-bit version (Bioacoustics Research Program 2012). Temporal traits were

    measured from oscillograms; spectral traits (dominant frequency) were measured from spectrograms, obtained in

    the software (Peak Frequency measurement function). Raven Pro settings: window type = Hanning; window size

    (FFT) = 1024 samples; time resolution = 21.3 ms; 3 dB filter bandwidth = 67.4 Hz; brightness = 50%; contrast =

    50%; overlap = 85%; hop size = 3.21 ms; DFT size (locked) = 1024 samples; grid spacing (spectral resolution) =

    43.1 or 46.9 Hz. Sound figures were obtained using Seewave 1.6.4 (Sueur et al. 2008), package of R 2.15.1

    platform, 64-bit version (R Development Core Team 2012). Seewave settings: window name (Fourier transform

    window) = Hanning; window length = 1024 samples; overlap = 85%. Analyzed sound files are listed in Appendix

    2. Voucher specimens: B. pseudopseudis (topotypical specimens)—AAG-UFU 0103–0104 (Alto Paraíso de Goiás,

    GO); B. sapiranga (non-topotypical specimens)—AAG-UFU 0101, 4563, 4565 (Caldas Novas, GO); AAG-UFU

    1537–1538 (Paracatu, MG).

    Recordings from Distrito Federal and Pirenópolis that were analyzed and figured in the original description of

    B. sapiranga (Brandão et al. 2012) were supplied by R. H. Matsushita, and were reanalyzed with the same software

    (Soundruler version 0.9.6.0; Gridi-Papp 2007) using the same settings, seeking for possible differences in spectral

    (harmonics) and structural (pulses) traits. We used the same setting of Brandão et al. (2012) for FFT length (256

    samples); other settings were not specified in the original contribution, software defaults were then considered

    (defaults in parentheses): window type (Hanning), overlap (90%), contrast (70%).

    Results

    Morphology and color patterns. Topotypical (N = 47) and non-topotypical (N = 4) specimens (both live and

    preserved) of Bokermannohyla pseudopseudis (figs. 1A–B) have a pale or brownish gray dorsal coloration with

    blotches that may form a lichenous-like pattern, and evident (continuous) white-colored dermal ridges along outer

    tarsi; in live specimens, dorsal surfaces of hand and toe disks with a light (whitish cream) coloration, and bronze/

    golden eyes. In contrast, type material (holotype and two paratypes, as stated in Brandão et al. 2012) and additional

    non-topotypical (N = 9) specimens (both live and preserved) of B. sapiranga (figs. 1C–D) have a uniform brown

    dorsal coloration with darker spots and/or blotches, dorsal surfaces of hand and toe disks with dark (grayish brown)

    coloration—i.e. just like that one of B. pseudopseudis, but darker)—and ill-defined (fragmented) ridges or granular

    rows along outer tarsi, or smooth outer tarsi; in live specimens, red or reddish orange eyes. Head shape better fits a

    rounded (dorsal and lateral views) outline in both species (fig. 2); see Appendix 1 for examined specimens.

    CARVALHO ET AL. 384 · Zootaxa 3746 (2) © 2013 Magnolia Press

  • FIGURE 1. A−B) Adult male topotypes of Bokermannohyla pseudopseudis: A) voucher AAG-UFU 0103 (SVL 51.0 mm), B) AAG-UFU 1628 (SVL 49.3 mm); C−D) Adult males of Bokermannohyla sapiranga: C) voucher AAG-UFU 0101 (SVL 44.9 mm) from Caldas Novas (GO); and D) voucher AAG-UFU 1538 (SVL 43.7 mm) from Paracatu (MG).

    Bokermannohyla sapiranga advertisement call. Twelve males were recorded (189 analyzed calls).

    Bioacoustic data for each locality are summarized in Table 1. Advertisement call (figs. 3–4) comprises 3–8 non-

    pulsed notes with up to 12 harmonics emitted from 3–9 calls/minute. Advertisement call varies from 0.41–1.25 s,

    and intercall interval from 4.09–20.25 s. Each note varies from 55–146 ms, and internote interval from 50–138 ms.

    Dominant frequency peaks from 516–797 Hz and corresponds to the fundamental frequency (1st harmonic). Three

    individuals from Caldas Novas (GO) had notes with deep and irregular amplitude modulations throughout their

    duration (fig. 4).

    Bokermannohyla pseudopseudis advertisement call. Two males were recorded (32 analyzed calls).

    Advertisement call (fig. 5; Table 1) comprises 12–18 (mean 15.2, SD = 1.9) non-pulsed notes with up to 12

    harmonics emitted from 5–8 calls/minute (mean 6.5, SD = 2.1). Advertisement call varies from 2.12–3.65 s (mean

    2.82, SD = 0.56), and intercall interval from 3.99–12.43 s (mean 6.99, SD = 2.23). Each note varies from 80–122

    ms (mean 98.8, SD = 7.5), and internote interval from 70–132 ms (mean 87.4, SD = 9.0). Dominant frequency

    peaks from 469–656 Hz (mean 559.6, SD = 62.3) and corresponds to the fundamental frequency (1st harmonic).

    Calling habitat. Males of both species were found calling from the ground, either exposed or hidden in rock

    crevices, in habitats that were always associated with rock outcrops in both seasonal and permanent flowing water.

    Males could call from places covered with a shallow water film (< 1 cm deep). Some of the calling habitats (rock

    outcrops with flowing water) were associated with shadowy environments (gallery forests), other with open field

    environments.

    Zootaxa 3746 (2) © 2013 Magnolia Press · 385NEW BIOACOUSTIC AND DISTRIBUTION DATA ON B. SAPIRANGA

  • TABLE 1. Advertisement call traits and recording air temperatures of topotypes of Bokermannohyla pseudopseudis, and

    four populations of Bokermannohyla sapiranga. Mean+SD (range). N = number of recorded males (number of analyzed

    calls).

    Discussion

    The assessment of new data on specimens of Bokermannohyla sapiranga from additional localities updates its

    diagnosis with respect to B. pseudopseudis (Brandão et al. 2012). Head shapes (dorsal and lateral views) among the

    examined specimens of both species (see Appendix 1) better fit a rounded outline (see fig. 2). Specimens of B.

    sapiranga have a narrower head (fig. 2C), which might lead one to attribute a sub-ovoid outline in dorsal view,

    whereas specimens of B. pseudopseudis have more prominent nostrils and oblique loreal region (fig. 2A), which

    might lead one to attribute a truncate outline. Given this, we suggest this character should not be employed as a

    useful diagnostic character henceforth. Even so, differences among morphological measurements were found in the

    original description (head proportions and toe disk diameter; see Tables 1–3 in Brandão et al. 2012), and should

    potentially be more straightforward to diagnose both species than head shape actually is.

    In contrast, the color patterns of the eyes and dorsal surface of hand/toe disks are distinctive between both

    species even considering the additional non-topotypical specimens of B. sapiranga of the present study, which still

    represent diagnostic characters. Even so, it is worth mentioning that these character states should preferentially be

    assessed from live or newly preserved specimens, taking into consideration a possible loss of coloration, as we

    could observe among the examined preserved specimens.

    An additional diagnostic character that could be assessed in preserved specimens is the differential dorsal

    coloration pattern in B. sapiranga (typically uniform brown dorsum with darker spots and/or blotches) in

    comparison to a pale or brownish gray lichenous-like pattern in B. pseudopseudis (Brandão et al. 2012). In

    addition, the evident white ridge on outer tarsi of B. pseudopseudis distinguishes it from B. sapiranga, which has

    discrete granules that may form rows, or the absence of distinctive patterns on outer tarsi (i.e. smooth).

    We found differences in temporal traits (call duration and notes per call) comparing bioacoustic data of B.

    sapiranga and B. pseudopseudis (Table 1), in addition to previous acoustic information on B. pseudopseudis and B.

    sapiranga (Eterovick & Brandão 2001; Guimarães et al. 2001; Brandão et al. 2012), and we assume they might be

    regarded as diagnostic bioacoustic characters between both species as well (Tables 1–2). On the contrary, the

    referred spectral (dominant frequency; absence of harmonics in B. sapiranga; Brandão et al. 2012) and structural

    B. pseudopseudis B. sapiranga

    Chapada dos Veadeiros (GO)N=2 (32)

    Caldas Novas (GO)N=8 (125)

    Cristalina (GO)N=1 (11)

    Pirenópolis (GO)N=1 (27)

    Paracatu (MG)N=2 (26)

    Call duration (s) 2.82+0.56(2.12–3.65)

    0.75+0.06(0.41–0.95)

    0.56+0.08(0.49–0.67)

    0.78+0.12(0.58–1.02)

    1.00+0.08(0.63–1.25)

    Intercall interval (s) 6.99+2.23(3.99–12.43)

    10.82+2.93(5.70–18.74)

    8.85+1.80(6.70–10.98)

    10.29+1.81(7.83–13.17)

    6.20+0.36(4.09–20.25)

    Notes/call 15.2+1.9(12–18)

    5.0+0.5(3–6)

    4.3+0.5(4–5)

    4.9+0.5(4–6)

    7.0+0.2(5–8)

    Note duration (ms) 98.8+7.5(80–122)

    83.5+13.2(55–146)

    73.2+6.0(56–88)

    91.5+6.7(77–102)

    78.6+1.7(57–97)

    Internote interval (ms) 87.4+9.0(70–132)

    86.3+9.9(53–126)

    67.0+9.3(51–86)

    81.8+13.3(60–125)

    72.4+15.4(50–138)

    Calls/minute 6.5+2.1(5–8)

    5.7+1.9(3–9)

    5.5+2.1(4–7)

    4.5+1.0(3–5)

    8.5+0.7(7–9)

    Dominant frequency (Hz)

    559.6+62.3(469–656)

    654.7+27.5(516–750)

    687.5+25.6(609–703)

    651.0+15.6(609–656)

    737.0+84.8(656–797)

    Harmonics 10–12 2–12 9 12 7

    Temperature (°C) 21.6–22.3 21.0–26.5 24.1 21.0 22.6

    CARVALHO ET AL. 386 · Zootaxa 3746 (2) © 2013 Magnolia Press

  • (pulsed notes in B. sapiranga; Brandão et al. 2012) traits no longer represent diagnostic characters between both

    species, given that we assessed calls of both species (inclusive of those in the original description) as consisting of

    series of non-pulsed notes with up to 12 visible harmonics, and overlapping dominant frequency (Tables 1–2).

    TABLE 2. Comparative advertisement call data (range of values) of Bokermannohyla pseudopseudis and

    Bokermannohyla sapiranga (N = number of recorded males).

    * Locality and the number of males recorded were based on R.A. Brandão personal communication.

    FIGURE 2. Head shapes (dorsal and lateral views) of (A−B) Bokermannohyla pseudopseudis (topotype AAG-UFU 0104; Alto Paraíso de Goiás, GO), and (C−D) Bokermannohyla sapiranga (AAG-UFU 4564; Caldas Novas, GO). Scale bar = 10 mm.

    B. pseudopseudis B. sapiranga

    Present study(Alto Paraíso de Goiás)N=2

    Eterovick & Brandão (2001)(Alto Paraíso de Goiás)N=1*

    Present study(All four populations)N=12

    Brandão et al. (2012)(Brasília and Pirenópolis)N=2

    Guimarães et al. (2001)(as Hyla pseudopseudis)N=2

    Call duration (s) 2.12–3.65 About 2.6 0.41–1.25 0.38–1.20 0.66–0.88

    Notes/call 12–18 9–10 3–8 3–7 5–6

    Harmonics Up to 12 Unreported Up to 12 No harmonics Up to 5

    Zootaxa 3746 (2) © 2013 Magnolia Press · 387NEW BIOACOUSTIC AND DISTRIBUTION DATA ON B. SAPIRANGA

  • FIGURE 3. Spectrograms (above) and corresponding oscillograms (below) of the advertisement call of Bokermannohyla sapiranga from A) Caldas Novas (GO); sound file: Bokerm_sapirCNovasGO8bAAGm671; 21:03h; air 21.0 °C, water 23.0 °C; 4 Nov 2012; B) Paracatu (MG); sound file: Bokerm_sapirParacatuMG1TRC_AAGm671; 19:29h; air 22.6 °C, water 24.1 °C; 6 Dec 2012; C) Cristalina (GO); sound file: Bokerm_sapirCristalGO1aAAGm; 19:05h; air 24.1 °C, water 24.1 °C; 4 Dec 2010; D) Pirenópolis (GO); sound file: Bokerm_sapirPirenopGO1dAAGm; 19:54h; air 21.0 °C, water 21.0 °C; 12 Feb 2011.

    FIGURE 4. Spectrogram (above) and corresponding oscillogram (below) of the advertisement call of Bokermannohyla sapiranga from Caldas Novas (GO) evidencing notes with deep and irregular amplitude modulations. Sound file: Bokerm_sapirCNovasGO6dAAGm671; 19:21h; air 25.0 °C, water 21.0 °C; 30 Oct 2012.

    CARVALHO ET AL. 388 · Zootaxa 3746 (2) © 2013 Magnolia Press

  • FIGURE 5. Oscillogram section showing an 18-note advertisement call (3.59 seconds) of a topotype of Bokermannohyla pseudopseudis, and spectrogram (above) and corresponding oscillogram (below) detailing four notes in A, identified by a red outline. Sound file: Bokerm_pseudopVeadGO1cAAGm; 19:41h; air 22.3 °C, water 23.0 °C; 2 Dec 2010.

    Eterovick and Brandão (2001) presented a frequency range from 0.4 to 2.4 kHz for B. pseudopseudis. These

    authors considered all sound energy portrayed in the spectrum (probably from 5 harmonics; see fig. 2 in Eterovick

    & Brandão 2001) instead of giving values for the dominant and other frequencies separately. In fact, dominant

    frequency for both B. pseudopseudis and B. sapiranga is restricted to values lower than 1 kHz (Table 1). We could

    attribute quantitative differences between B. sapiranga calls from Brasília and Pirenópolis provided in Brandão et

    al. (2012) to intraspecific variation, once we assessed a larger call sample from additional populations, all of them

    assigned to B. sapiranga based on adult morphology, color patterns, or bioacoustic information (Tables 1–2).

    In the original description (fig. 4A in Brandão et al. 2012), the absence of visible harmonics should possibly be

    attributed to recordings made with a low sound input (Angulo & Reichle 2008). Concerning the presence of pulsed

    notes, we found notes with deep and irregular amplitude modulations (AM) among calls of three recorded males of

    B. sapiranga (fig. 4), in which the sound energy in spectrograms is uniform along the harmonics with no regular

    intervals (pulsed structure portrayed in spectrogram) throughout each note. This AM pattern was not classified as a

    ‘pulsed structure’, which might be defined as a particular case of AM, wherein the carrier frequency is gated at a

    pulsed rate (“regular amplitude modulations throughout a given note/call”; Watkins 1968). This irregular AM

    pattern, infrequent in our call sample, does not fall into the aforementioned AM particular case, in which the

    commonly used term ‘pulsed’ might be applied. Furthermore, B. sapiranga and B. pseudopseudis calls are heard in

    the field as series of pure notes (non-pulsed to the human ear), resembling an owl low-pitched hoot.

    Bokermannohyla sapiranga was previously reported to occur in five municipalities of Goiás (Catalão,

    Cristalina, Nova Gama, Pirenópolis), including its type locality (Distrito Federal) (Brandão et al. 2012). Among

    our study sites, two localities (Caldas Novas, GO; Paracatu, MG) represent new distribution records for B.

    sapiranga. Guimarães et al. (2001) reported on a population of B. pseudopseudis in Silvânia (Goiás), which

    actually represents an additional distribution record for B. sapiranga instead based on bioacoustic information

    (Table 2). Our new distributional data on B. sapiranga extends its currently recognized geographic distribution

    Zootaxa 3746 (2) © 2013 Magnolia Press · 389NEW BIOACOUSTIC AND DISTRIBUTION DATA ON B. SAPIRANGA

  • eastward (fig. 6): Paracatu represents the easternmost distribution point, 75 km east to its previously easternmost

    record (Cristalina), and the first record for Minas Gerais, southeastern Brazil. B. sapiranga is widespread in central

    and southern Goiás, in addition to northwestern Minas Gerais (fig. 6), whereas B. pseudopseudis seems to be

    associated with the Chapada dos Veadeiros and Serra da Mesa rocky montane environments of northern Goiás.

    FIGURE 6. Distribution of Bokermannohyla sapiranga and Bokermannohyla pseudopseudis on a topographic map: Bokermannohyla sapiranga—Star = Type locality (Distrito Federal); black circles = additional records based on the present study and Guimarães et al. (2001), Brandão et al. (2012); red circles = new records (Caldas Novas, GO; Paracatu, MG). Bokermannohyla pseudopseudis—Square = type locality (Chapada dos Veadeiros, GO), black triangles = additional records in the present study (Appendix I) and based on Pombal and Caramaschi (1995). State abbreviations: DF (Distrito Federal); GO (Goiás); MG (Minas Gerais).

    Acknowledgements

    We thank K. G. Facure and W. R. Silva for assistance in the field, G. R. Colli for making available specimens under

    his care, R. Matsushita, N. M. Maciel, and R. A. Brandão for making available sound files and/or additional

    suggestions, V. G. D. Orrico and two anonymous reviewers, whose comments greatly improved this study. This

    work was supported by Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Conselho

    Nacional de Desenvolvimento Científico e Tecnológico (CNPq). A research grant conceded by CNPq to A.A.G.,

    fellowships by FAPESP (T.R.C.; 2012/15763–7), CAPES (B.F.V.T.; Demanda Social), and CNPq (L.B.M.;

    152548/2011–4). Collection permits were granted by Instituto Chico Mendes through the online platform Sistema

    de Autorização e Informação em Biodiversidade (ICMBio/SISBIO 02015.008064/02–51 and ICMBio/SISBIO

    29954–2).

    CARVALHO ET AL. 390 · Zootaxa 3746 (2) © 2013 Magnolia Press

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    Leite, F.S.F., Pezzuti, T.L. & Drummond, L.O. (2011) A new species of Bokermannohyla from the Espinhaço Range, State of Minas Gerais, Southeastern Brazil. Herpetologica, 67 (4), 440–448. http://dx.doi.org/10.1655/herpetologica-d-11-00017.1

    Leite, F.S.F., Pezzuti, T.L. & Garcia, P.C.A. (2012) A new species of the Bokermannohyla pseudopseudis group from the Espinhaço Range, Central Bahia, Brazil (Anura: Hylidae). Herpetologica, 68 (3), 401–409. http://dx.doi.org/10.1655/herpetologica-d-11-00006.1

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    APPENDIX 1. Examined specimens.

    Bokermannohyla ibitiguara—BRAZIL: MINAS GERAIS: Capitólio (AAG-UFU 4746; 4849–4852); São Roque de Minas (AAG-UFU 2141; 0060–0062);

    Bokermannohyla oxente—BRAZIL: BAHIA: Piatã (AAG-UFU 1684–1685);Bokermannohyla pseudopseudis—BRAZIL: GOIÁS: Alto Paraíso de Goiás (AAG-UFU 0103–0104, 1326; CHUNB 511, 514–

    517, 519–521, 425, 453–454, 484, 523–528, 14065, 14382, 14389, 14385, 17527–17528, 17531–17532, 32619, 42522, 43650, 47516, 58873–58874, 58876, 58878–58879, 59086, 58789, 58791–58794, 62512, 62518, 69153); Minaçu (CHUNB 14367–14368, 14394–14395);

    Bokermannohyla sapiranga—BRAZIL: DISTRITO FEDERAL: Brasília (Holotype: CHUNB 62384); GOIÁS: Caldas Novas (AAG-UFU 4352, 4563–4565, 0101); Novo Gama (CHUNB 65405–65406); Pirenópolis (Paratypes: CHUNB 14387, 14390); MINAS GERAIS: Paracatu (AAG-UFU 1537–1538);

    Bokermannohyla saxicola—BRAZIL: MINAS GERAIS: Santana do Riacho (AAG-UFU 0026).

    Zootaxa 3746 (2) © 2013 Magnolia Press · 391NEW BIOACOUSTIC AND DISTRIBUTION DATA ON B. SAPIRANGA

    http://dx.doi.org/10.1206/0003-0090(2005)294[0001:srotff]2.0.co;2http://www.r-project.orghttp://www.r-project.orghttp://dx.doi.org/10.1111/j.1096-3642.2007.00338.xhttp://dx.doi.org/10.1111/j.1096-3642.2007.00338.xhttp://dx.doi.org/10.2307/1565962http://dx.doi.org/10.2307/1565962http://dx.doi.org/10.1206/0003-0090%282005%29294%5b0001:srotff%5d2.0.co;2http://dx.doi.org/10.1206/0003-0090%282005%29294%5b0001:srotff%5d2.0.co;2http://dx.doi.org/10.1655/herpetologica-d-11-00017.1http://dx.doi.org/10.1655/herpetologica-d-11-00017.1http://dx.doi.org/10.1655/herpetologica-d-11-00006.1http://dx.doi.org/10.1655/herpetologica-d-11-00006.1http://dx.doi.org/10.1080/09524622.2008.9753600http://dx.doi.org/10.1080/09524622.2008.9753600http://dx.doi.org/10.1080/09524622.2008.9753600http://dx.doi.org/10.1575/1912/2726

  • APPENDIX 2. List of analyzed sound files of Bokermannohyla pseudopseudis and Bokermannohyla sapiranga for each

    locality.

    Species Locality Sound file Voucher

    Bokermannohyla

    pseudopseudis

    Chapada dos Veadeiros (GO)

    Bokerm_pseudopVeadGO1aAAGm AAG-UFU 0103 or 0104

    Bokerm_pseudopVeadGO1bAAGm AAG-UFU 0103 or 0104

    Bokerm_pseudopVeadGO1cAAGm AAG-UFU 0103 or 0104

    Bokerm_pseudopVeadGO2aAAGm AAG-UFU 0103 or 0104

    Bokerm_pseudopVeadGO2bAAGm AAG-UFU 0103 or 0104

    Bokermannohyla

    sapiranga

    Caldas Novas (GO) Bokerm_sapirCNovasGO1AAGmt Unvouchered

    Bokerm_sapirCNovasGO2LM_AAGb Unvouchered

    Bokerm_sapirCNovasGO3AAGb AAG-UFU 4563 or 4565

    Bokerm_sapirCNovasGO4LM_AAGb Unvouchered

    Bokerm_sapirCNovasGO5aAAGm AAG-UFU 0101

    Bokerm_sapirCNovasGO5bAAGm AAG-UFU 0101

    Bokerm_sapirCNovasGO5cAAGm AAG-UFU 0101

    Bokerm_sapirCNovasGO5dAAGm AAG-UFU 0101

    Bokerm_sapirCNovasGO6aAAGm671 Unvouchered

    Bokerm_sapirCNovasGO6bAAGm671 Unvouchered

    Bokerm_sapirCNovasGO6cAAGm671 Unvouchered

    Bokerm_sapirCNovasGO6dAAGm671 Unvouchered

    Bokerm_sapirCNovasGO6eAAGmt Unvouchered

    Bokerm_sapirCNovasGO7aAAGm671 Unvouchered

    Bokerm_sapirCNovasGO7bAAGmt Unvouchered

    Bokerm_sapirCNovasGO7cAAGmt Unvouchered

    Bokerm_sapirCNovasGO7dAAGmt Unvouchered

    Bokerm_sapirCNovasGO7eAAGmt Unvouchered

    Bokerm_sapirCNovasGO8aAAGm671 Unvouchered

    Bokerm_sapirCNovasGO8bAAGm671 Unvouchered

    Cristalina (GO) Bokerm_sapirCristalGO1aAAGm Unvouchered

    Bokerm_sapirCristalGO1bAAGm Unvouchered

    Pirenópolis (GO) Bokerm_sapirPirenopGO1aAAGm Unvouchered

    Bokerm_sapirPirenopGO1bAAGm Unvouchered

    Bokerm_sapirPirenopGO1cAAGm Unvouchered

    Bokerm_sapirPirenopGO1dAAGm Unvouchered

    Paracatu (MG) Bokerm_sapirParacatuMG1TRC_AAGm671 AAG-UFU 1537

    Bokerm_sapirParacatuMG2BFVT_AAGmt AAG-UFU 1538

    CARVALHO ET AL. 392 · Zootaxa 3746 (2) © 2013 Magnolia Press

    AbstractIntroductionMaterial and methodsDiscussionAcknowledgementsReferences

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