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
References
Angulo, A. & Reichle, S. (2008) Acoustic signals, species diagnosis, and species concepts: the case of a new cryptic species of Leptodactylus (Amphibia, Anura, Leptodactylidae) from the Chapare Region, Bolivia. Zoological Journal of the Linnean Society, 152, 59–77. http://dx.doi.org/10.1111/j.1096-3642.2007.00338.x
Bioacoustics Research Program (2012) Raven Pro: Interactive Sound Analysis Software, version 1.5. The Cornell Lab of Ornithology, Ithaca, New York. Available from: http://www.birds.cornell.edu/raven (accessed on 11 Dec 2012)
Brandão, R.A., Magalhães, R.F., Garda, A.A., Campos, L.A., Sebben, A. & Maciel, N.M. (2012) A new species of Bokermannohyla (Anura: Hylidae) from highlands of Central Brazil. Zootaxa, 3527, 28–42.
Duellman, W.E. & Trueb, L. (1994) Biology of Amphibians. The John Hopkins University Press, Baltimore, Maryland, 670 pp.Eterovick, P.C. & Brandão, R.A. (2001) A description of the tadpoles and advertisement calls of members of the Hyla
pseudopseudis group. Journal of Herpetology, 35 (3), 442–450. http://dx.doi.org/10.2307/1565962
Faivovich, J., Haddad, C.F.B., Garcia, P.C.A., Frost, D.R., Campbell, J.A. & Wheeler, W.C. (2005) Systematic Review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision. Bulletim of the American Museum Natural History, 294, 1–240. http://dx.doi.org/10.1206/0003-0090(2005)294[0001:srotff]2.0.co;2
Gridi-Papp, M. (2007) Sound Ruler. Version 0.9.6.0. Available from: http://soundruler.sourceforge.net (accessed on 21 August 2013)
Guimarães, L.D., Lima, L.P., Juliano, R.F. & Bastos, R.P. (2001) Vocalizações de espécies de anuros (Amphibia) no Brasil Central. Boletim do Museu Nacional, Nova Série, 474, 1–14.
Heyer, W.R., Rand, A.S., Cruz, C.A.G., Peixoto, O.L. & Nelson, C.E. (1990) Frogs of Boracéia. Arquivos de Zoologia, 31 (4), 231–410.
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
Miranda-Ribeiro, A. (1937) Alguns batrachios novos das collecções do Museu Nacional. O Campo, Rio de Janeiro, Maio, 66–69.
Miranda-Ribeiro, P. (1953) Tipos das espécies e subespécies do Prof. Alípio de Miranda Ribeiro depositadas no Museu Nacional (com uma relação dos gêneros, espécies e subespécies descritos). Arquivos do Museu Nacional, 42, 389–418.
Pombal Jr., J.P. & Caramaschi, U. (1995) Posição taxonômica de Hyla pseudopseudis Miranda-Ribeiro, 1937 e Hyla saxicolaBokermann, 1964 (Anura, Hylidae). Boletim do Museu Nacional, Nova Série, Zoologia, 363, 1–8.
R Development Core Team (2012) The R Project for Statistical Computing. Vienna, Austria. Available from: http://www.r-project.org/ (accessed on 30 Jan 2013)
Sueur, J., Aubin, T. & Simonis, C. (2008) Seewave: a free modular tool for sound analysis and synthesis. Bioacoustics, 18, 213–226. http://dx.doi.org/10.1080/09524622.2008.9753600
Watkins, W.A. (1968) The harmonic interval: fact or artifact in spectral analysis of pulse trains. In: Tavolga, W.N. (Ed.), Marine Bio-acoustis. Vol. 2. Pergamon Press, Oxford, pp. 183–212.
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
/ColorImageDict > /JPEG2000ColorACSImageDict > /JPEG2000ColorImageDict > /AntiAliasGrayImages false /CropGrayImages true /GrayImageMinResolution 300 /GrayImageMinResolutionPolicy /OK /DownsampleGrayImages true /GrayImageDownsampleType /Bicubic /GrayImageResolution 300 /GrayImageDepth -1 /GrayImageMinDownsampleDepth 2 /GrayImageDownsampleThreshold 2.00000 /EncodeGrayImages true /GrayImageFilter /DCTEncode /AutoFilterGrayImages true /GrayImageAutoFilterStrategy /JPEG /GrayACSImageDict > /GrayImageDict > /JPEG2000GrayACSImageDict > /JPEG2000GrayImageDict > /AntiAliasMonoImages false /CropMonoImages true /MonoImageMinResolution 1200 /MonoImageMinResolutionPolicy /OK /DownsampleMonoImages true /MonoImageDownsampleType /Bicubic /MonoImageResolution 1200 /MonoImageDepth -1 /MonoImageDownsampleThreshold 1.50000 /EncodeMonoImages true /MonoImageFilter /CCITTFaxEncode /MonoImageDict > /AllowPSXObjects false /CheckCompliance [ /None ] /PDFX1aCheck false /PDFX3Check false /PDFXCompliantPDFOnly false /PDFXNoTrimBoxError true /PDFXTrimBoxToMediaBoxOffset [ 0.00000 0.00000 0.00000 0.00000 ] /PDFXSetBleedBoxToMediaBox true /PDFXBleedBoxToTrimBoxOffset [ 0.00000 0.00000 0.00000 0.00000 ] /PDFXOutputIntentProfile () /PDFXOutputConditionIdentifier () /PDFXOutputCondition () /PDFXRegistryName () /PDFXTrapped /False
/Description > /Namespace [ (Adobe) (Common) (1.0) ] /OtherNamespaces [ > /FormElements false /GenerateStructure true /IncludeBookmarks false /IncludeHyperlinks false /IncludeInteractive false /IncludeLayers false /IncludeProfiles true /MultimediaHandling /UseObjectSettings /Namespace [ (Adobe) (CreativeSuite) (2.0) ] /PDFXOutputIntentProfileSelector /NA /PreserveEditing true /UntaggedCMYKHandling /LeaveUntagged /UntaggedRGBHandling /LeaveUntagged /UseDocumentBleed false >> ]>> setdistillerparams> setpagedevice