Abstracts
In this paper, we provide an updated diagnosis for Pseudopaludicola giarettai based on the morphometric and acoustic variation observed with the assessment of new populations, plus an expansion of its distribution range. Our results support that all acoustic variation observed might be attributed to intraspecific variation. The variation in body size and dorsal stripe patterns observed for Pseudopaludicola giarettai reinforces that the distinctive whistling advertisement call pattern is the most reliable evidence line to diagnose it from its congeners, whereas morphological (robust body, glandular dorsum) and morphometric (body size) features vary considerably within and among populations so that they should no longer be employed as diagnostic features of Pseudopaludicola giarettai.
Bioacoustics; Minas Gerais; Taxonomy.
Nesse trabalho, nós apresentamos uma diagnose atualizada para Pseudopaludicola giarettai a partir das variações morfométrica e acústica encontradas com a amostragem de novas populações, além da expansão de sua distribuição geográfica. Nossos resultados suportam que toda a variação acústica observada pode ser atribuída a variação intraespecífica. A variação em tamanho e padrão de faixas dorsais observada em Pseudopaludicola giarettai reforça que o padrão assobiado distintivo de canto de anúncio representa a linha de evidência mais confiável para diagnosticar a espécie de seus congêneres, enquanto as características morfológicas (corpo robusto, dorso glandular) e morfométricas (tamanho do corpo) variam consideravelmente dentro e entre populações de modo que não devem mais ser utilizadas como características diagnósticas para Pseudopaludicola giarettai.
Bioacústica; Minas Gerais; Taxonomia.
INTRODUCTION
The genus Pseudopaludicola currently comprises 18 species distributed throughout South America (Frost, 2014). This genus was traditionally defined by external morphology and osteological features (Lynch 1971, 1989). The monophyly of the genus was later assessed through phylogenetic analyses based on external morphology and osteology (Lobo, 1995), and, more recently, molecular data (Veiga-Menoncello et al., 2014). In both Lobo's (1995) and (Veiga-Menoncello et al.'s 2014) hypotheses, a few species were not tested for their phylogenetic position, including P. giarettai Carvalho, 2012, which possesses a unique, whistling advertisement call pattern in the genus, associated with a large size, robust body, warty dorsum, yellow vocal sac (Carvalho, 2012), a suite of features that is apparently more related to the "2n = 20" clade from Veiga-Menoncello et al. (2014), formed by P. ameghini Pansonato, Strüssman, Mudrek & Martins, 2013 and P. ternetzi Miranda-Ribeiro, 1937.
During recent field surveys (2013/2014) in the Cerrado of southeastern Brazil, we recorded and collected specimens of Pseudopaludicola assigned in the field to P. giarettai through its distinctive advertisement call pattern. We herein provide an updated diagnosis for P. giarettai based on the morphometric and acoustic variation observed with the assessment of new populations, plus an expansion of its distribution range.
MATERIAL AND METHODS
Field work was conducted in six municipalities of Minas Gerais State, southeastern Brazil: Buritis (15°21'29"S, 46°29'45"W; approx. 905 m a.s.l.); Buritizeiro (16°52'32"S, 45°05'02"W; approx. 700 m a.s.l.); Chapada Gaúcha, at the Parque Nacional Grande Sertão Veredas (15°10'51"S, 45°46'10"W; approx. 710 m a.s.l.); Coromandel (18°07'35"S, 47°11'60"W; approx. 730 m a.s.l.); Curvelo (18°46'09"S, 44°26'54"W; approx. 620 m a.s.l.); Unaí (16°43'33"S, 46°29'30"W; approx. 525 m a.s.l.). Examined specimens are listed in Appendix 1 APPENDIX 1 List of examined specimens Pseudopaludicola giarettai - BRAZIL: Minas Gerais: Curvelo (holotype: AAG-UFU 0312; paratypes: AAG-UFU 0309-0311, 0313-0316); Buritis (AAG-UFU 1772-1778); Buritizeiro (AAG-UFU 4580, MZUFV 14203-14210); Chapada Gaúcha (AAG-UFU 1920-1928); Coromandel (AAG-UFU 3565-3568); Unaí (MZUFV 14878-4883). .
Calls were recorded using digital equipment (M-Audio Microtrack II and Marantz PMD 671) set at a sampling rate of 48.0 kHz and a resolution of 16 bits (mono WAVE file format), coupled to directional microphones (Sennheiser K6/ME66 and K6/ME67, respectively). At two study sites (Buritizeiro and Unaí), calls were recorded using an Olympus DM-420 Digital Voice Recorder coupled to an Audio-Technica Pro stereo condenser microphone set at a sampling rate of 32 kHz and a resolution of 24 bits (stereo WMA file format). Sound files were converted to mono WAVE file format prior to perform any sound analysis. Calls from two municipalities were provided by Diego J. Santana: i) Muriaé (Minas Gerais State; see Santana et al., 2009), and ii) Flores de Goiás (Goiás State); recordings perfectly fitted P. giarettai distinctive calling pattern, so both populations were assigned by us to P. giarettai, but we excluded these data from acoustic comparisons since just a few calls of one male from each site were recorded.
Calls were analyzed with the software Raven Pro version 1.5, 32-bit version (Bioacoustics Research Program, 2012). Temporal and spectral traits were measured from spectrograms; temporal traits were manually measured, and spectral traits (dominant and other frequencies) were obtained with the Peak Frequency measurement. Raven Pro settings: window type = Hann; window size = 1024 samples; 3 dB filter bandwidth = 67.4 Hz; brightness = 50%; contrast = 50%; overlap (locked) = 85%; hop size (temporal resolution = 3.21 ms); DFT size (locked) = 1024 samples (spectral resolution = 46.9 Hz). Calls of P. giarettai from its original description (Carvalho, 2012) were reanalyzed under the analytical standards and software settings presented earlier. Acoustic terminology is defined in Table 1. Mean and standard deviation (SD) given along the text and tables were calculated from individual mean values.
The overall thermal dependency of temporal variables of the advertisement call of P. giarettai was performed in two steps using Vegan package (Oksanen et al., 2013) version 2.0-10, R platform (R Core Team, 2014): a Principal Component Analysis (PCA) was performed on a correlation matrix from untransformed individual mean values. Then, a correlation analysis between recording air temperature and the first component scores (PC1) was performed to identify potential temperature-dependent variables. This statistical approach was not likewise applied to calling male size (SVL) dependency of spectral traits of its call due to the lack of either a minimum sample size or a non-correspondence of voucher males and recordings. See Appendices 2 APPENDIX 2 Mean individual values, scores, eigenvalues, and proportional explained variation (%) of the first three principal components. CUR (Curvelo), BUR (Buritis), BUZ (Buritizeiro), CHG (Chapada Gaúcha), COR (Coromandel), UNA (Unaí). T = recording air temperature (°C), CD = call duration (s), CI = call interval (s), CRT = call rise time (s), CRS = call rate/s, DF = dominant frequency (Hz), FM = frequency modulation (Hz). Individuals T CD CI CRT CRS DF FM PC1 PC2 PC3 CUR 1 24.0 0.179 0.406 119.0 1.8 4436.2 1516.4 0.446 0.015 -0.088 CUR 2 33.0 0.180 0.229 114.7 2.2 4365.0 1468.2 -0.347 0.392 -0.175 CUR 3 33.0 0.177 0.206 120.8 2.2 4376.2 1331.6 -0.426 0.113 0.144 CUR 4 35.0 0.152 0.194 64.8 2.6 4109.1 1453.4 -1.358 0.440 -0.539 CUR 5 35.0 0.167 0.216 65.0 2.6 4080.9 1284.3 -1.243 -0.001 -0.625 CUR 6 35.0 0.170 0.219 109.5 2.5 4212.2 1344.9 -0.786 0.040 -0.199 CUR 7 24.0 0.180 0.322 122.4 2.2 4330.3 1380.1 -0.097 -0.118 -0.104 CUR 8 24.0 0.190 0.327 126.2 1.9 4444.5 1331.6 0.255 -0.185 0.072 BUR 1 24.8 0.206 0.364 155.9 1.9 4234.7 1136.9 0.525 -1.089 -0.255 BUR 2 23.5 0.200 0.335 141.9 1.9 4488.5 1117.9 0.411 -0.696 0.403 BUR 3 23.5 0.235 0.478 160.7 1.4 4310.6 1313.3 1.499 -0.978 -0.855 BUZ 1 26.0 0.222 0.243 118.5 2.0 4896.3 1741.6 -0.909 -1.003 0.207 BUZ 2 26.0 0.225 0.334 144.5 1.9 4751.7 1633.0 -0.975 0.149 -0.857 CHG 1 36.0 0.185 0.304 116.7 2.1 4845.0 1627.9 0.473 1.639 -0.037 CHG 2 36.0 0.168 0.308 86.4 2.0 4895.6 1415.7 0.877 0.839 -0.146 CHG 3 36.0 0.219 0.309 80.6 1.9 4250.6 1358.6 0.209 1.124 0.634 CHG 4 36.0 0.175 0.340 119.1 2.0 4918.1 1411.0 -0.081 0.781 1.178 CHG 5 34.0 0.209 0.372 133.7 1.7 4467.5 1408.7 0.070 -0.017 -1.196 CHG 6 34.0 0.207 0.282 105.8 2.0 4477.2 1444.4 0.275 0.568 1.300 CHG 7 34.0 0.188 0.285 113.0 2.1 4562.5 1256.1 0.736 -0.145 -0.291 CHG 8 34.0 0.171 0.225 99.5 2.4 4152.6 913.7 0.118 0.392 -0.417 CHG 9 34.0 0.172 0.268 52.0 2.4 4117.2 1377.7 -0.064 0.008 0.437 COR 1 24.7 0.192 0.379 102.3 1.7 4352.7 1612.8 0.432 0.285 -0.749 COR 2 24.7 0.202 0.376 131.5 1.7 4293.0 1295.0 0.573 -0.629 -0.430 UNA 1 28.0 0.149 0.264 90.3 2.3 4279.0 827.0 -0.944 -1.174 0.952 UNA 2 28.0 0.173 0.363 128.7 1.8 4765.6 986.0 0.331 -0.751 1.637 Eigenvalues - - - - - - - 3.268 1.229 0.749 % variation - - - - - - - 54.5 20.5 12.5 -3 APPENDIX 3 Eigenvectors from P. giarettai acoustic traits in the first three principal components. Acoustic traits Eigenvectors PC1 PC2 PC3 Call duration 1.161 0.124 -0.596 Call interval 1.212 -0.432 -0.023 Call rise time 1.163 -0.347 0.242 Call rate/s -1.352 0.213 0.017 Dominant frequency 0.706 0.786 0.939 Frequency modulation 0.418 1.234 -0.482 for the first three principal component scores, eigenvalues, eigenvectors, proportional explained variation, and mean individual values. Further, the potential association between linear geographic distance and variation in acoustic traits was assessed through a Mantel test applied on Euclidean distance matrices with 10,000 Monte Carlo permutations, using ade4 package (Dray & Dufour, 2007) version 1.6-2, R platform.
Specimens are housed in the Collection of Amphibians of the Museu de Biodiversidade do Cerrado, Universidade Federal de Uberlândia (AAG-UFU), Municipality of Uberlândia, and at the Museu de Zoologia João Moojen, Universidade Federal de Viçosa (MZUFV), Municipality of Viçosa, both in Minas Gerais, Brazil. Call voucher males were registered under the following accession numbers: AAG-UFU 1772 (Buritis), AAG-UFU 1920-1924 (Chapada Gaúcha), AAG-UFU 3565 (Coromandel), AAG-UFU 0309-0313 (Curvelo), MZUFV 14207, 14210 (Buritizeiro), MZUFV 14878, 14882 (Unaí).
RESULTS AND DISCUSSION
Distribution
Pseudopaludicola giarettai was previously reported only for its type locality (Curvelo) and from Buritizeiro, ca. 160 km northward to the type locality (Carvalho, 2012). We extend its distribution range to localities in northwestern Minas Gerais (Buritis, Chapada Gaúcha, and Unaí), ca. 300 km westward (Coromandel), and ca. 340 km southeastward (Muriaé) to its type locality. Besides, Flores de Goiás, located in northern Goiás (central Brazil), represents the first record outside Minas Gerais, ca. 550 km northwestward to P. giarettai type locality (Fig. 1).
Distribution map of Pseudopaludicola giarettai. Star (Type locality: Curvelo, MG); Circles (localities in Minas Gerais): 1 (Buritis), 2 (Chapada Gaúcha), 3 (Unaí), 4 (Buritizeiro), 5 (Coromandel), 6 (Conceição do Mato Dentro; Pimenta et al., 2014), 7 (Muriaé; Santana et al., 2009); Triangle (Flores de Goiás, GO). MG = Minas Gerais; GO = Goiás
Color patterns and body size
Although the holotype of P. giarettai neither possesses vertebral pin-stripe nor dorsolateral stripes, some paratypes, on the other hand, possess at least one of the two characters (Carvalho, 2012). In other populations, the presence of these characters was more regularly observed (Table 2; Fig. 2). Regarding body size, P. giarettai was considered one of the largest Pseudopaludicola species according to its original description (Carvalho, 2012): adult male SVL 16.2-18.0 mm. However, adult males from Buritis (SVL 13.8-16.3 mm; N = 6), Buritizeiro (SVL 13.4-15.9 mm; N = 7), Chapada Gaúcha (SVL 13.5-14.7 mm; N = 7), and Unaí (SVL 14.7-16.2 mm; N = 6) are remarkably smaller than P. giarettai type series (Table 3), whereas the only adult male collected in Coromandel has a relatively larger size (SVL 16.7 mm), which fits male size range of its type series (Table 3).
Presence of vertebral (pin-stripe) and/or dorsolateral stripes in adult specimens of Pseudopaludicola giarettai from six localities of Minas Gerais, southeastern Brazil. N = number of examined specimens; * Type specimens.
Adult specimens of P. giarettai in life from: Above - Parque Nacional Grande Sertão Veredas, Chapada Gaúcha, Minas Gerais (voucher male AAG-UFU 1920: CRC = 14.6 mm); Below - Coromandel (female AAG-UFU 3566: CRC 18.8 mm)
Summary of snout-vent length (SVL) ranges (mm) for adult specimens of Pseudopaludicola giarettai from six localities of Minas Gerais, southeastern Brazil. Sample sizes in parentheses; * Type locality.
Advertisement call redescription (type locality: Curvelo, Minas Gerais)
Eight males were recorded (N = 400 calls). Advertisement call (Table 4; Figs. 3-4) consists of a whistle, i.e. non-pulsed signal, with a remarkable ascendant frequency modulation throughout its duration. Calls may have a slight upward amplitude modulation in their half or last third duration (see oscillogram in Fig. 4) or upward and downward amplitude modulations in their first third or half duration (see oscillogram in Fig. 3). Fundamental frequency (1st harmonic) always corresponds to the carrier frequency, and up to four higher harmonically related frequencies can be observed. Call duration varies from 101-212 ms (mean 174.4; SD = 11.5), whose rise time varies from 61-143 ms (mean 105.3; SD = 25.4), which corresponds approximately to 60% of average call duration. Call interval varies from 158-781 ms (mean 264.8; SD = 76.8). Call rate varies from 1.77-2.61 per second (mean 2.24; SD = 0.30). Dominant frequency (= fundamental frequency) varies from 3984-4594 Hz (mean 4294.3; SD = 142.6), with frequency modulation varying from 1214-1582 Hz (mean 1388.8; SD = 81.3); second, third, and fourth harmonic frequencies peak from 7172-9094 Hz, 10969-13922 Hz, and 15094-18281 Hz, respectively. Fifth harmonic was not measured once it can be incomplete in spectrogram screen [maximum frequency measurement allowed by a 48-kHz sampling rate (Nyquist of sampling rate) = 24 kHz].
Acoustic traits for Pseudopaludicola giarettai from Curvelo (type locality), and five additional municipalities of Minas Gerais, southeastern Brazil. Mean ± SD (minimum-maximum). N = number of recorded males (number of analyzed calls). H = harmonic peak frequency. * Dominant frequency (= Fundamental frequency); ** Obtained from calls of one male.
Advertisement call of P. giarettai from the type locality (Curvelo, Minas Gerais). From top to bottom: oscillogram section (ca. 1.6 s) depicting calling pattern, waveform, spectrogram, and power spectrum of the second advertisement from oscillogram section. Sound energy with relative amplitude below 40 dB was clipped to zero dB to remove background noise from power spectrum
Advertisement call of P. giarettai from the Parque Nacional Grande Sertão Veredas (Chapada Gaúcha, Minas Gerais). From top to bottom: oscillogram section (ca. 1.6 s) depicting calling pattern, waveform, spectrogram, and power spectrum of the second advertisement from oscillogram section. Sound energy with relative amplitude below 40 dB was clipped to zero dB to remove background noise from power spectrum
Acoustic comparisons
Despite the advertisement call pattern shared among all populations, i.e. non-pulsed signal with notable ascendant frequency modulation throughout its duration, dominant frequency coincident with fundamental frequency, and higher harmonically related frequencies typically observed, quantitative (temporal and spectral) traits of P. giarettai call varied within and among populations (Table 4; Fig. 5). The first three PC axes explained approximately 87% of the overall variation. Type specimens and from Buritizeiro were partially separated from the other populations along PC1 (ca. 55% explained variation) mainly by temporal traits of call (higher call rate, and shorter call duration and interval), as well as faster call rise time, whereas type specimens and from Chapada Gaúcha were completely separated along PC2 (ca. 21% explained variation) from specimens from Buritizeiro and Unaí, mainly by a wider frequency modulation.
Scatterplot of the first two principal component scores (PCs) from acoustic traits of six populations of P. giarettai. Yellow (Curvelo; type locality); purple (Chapada Gaúcha); green (Coromandel); red (Buritis); blue (Buritizeiro); pink (Unaí)
Considering acoustic variation represented in Fig. 5, it is possible to assume that the between-population variation was not great enough to discriminate any as a potential independent group with respect to acoustic information, thus we attributed it to intraspecific variation only. Populations from Coromandel, Buritis, and Unaí showed within-population acoustic variation that should possibly be explained by an insufficient sample size of recorded males (N = 2 males). The Mantel test showed no significant association between geographic distance and acoustic variation (Mantel r = -0.04; p = 0.77).
Effect of temperature on temporal traits of call
Air temperature could not explain the overall variation observed in all three temporal traits analyzed of P. giarettai call (F1,24 = 3.61; df = 24; p = 0.07).
Revised diagnosis
Considering the newly assessed intraspecific variation in dorsal stripe patterns, as well as morphometric and acoustic data of P. giarettai, an updated diagnosis is provided as follows: Pseudopaludicola giarettai is assigned to the genus Pseudopaludicola by the presence of distal hypertrophied antebrachial tubercles. The distinctive whistling advertisement call pattern of P. giarettai diagnoses it from all congeneric species with described calls (unknown calls: P. ceratophyes, P. llanera, and P. pusilla). This non-pulsed call structure distinguishes P. giarettai from the pulsed calls of P. ameghini (Pansonato et al., 2013), P. atragula (Pansonato et al., 2014a), P. boliviana (Duré et al., 2004), P. falcipes (Haddad & Cardoso, 1987), P. mineira (Pereira & Nascimento, 2004), P. murundu (Toledo et al., 2010), P. mystacalis (Pansonato et al., 2013), P. saltica (Pansonato et al., 2013), and P. ternetzi (Cardozo & Toledo, 2013). Regarding Pseudopaludicola species with non-pulsed structure (P. canga, P. facureae, P. hyleaustralis, and P. parnaiba), P. giarettai can easily be distinguished from all four species by its distinctive long-lasting (combined value range: 101-260 ms; Table 3) whistling call with a remarkable ascendant frequency modulation, and emitted in an intermittent calling pattern, whereas calls of all four species are emitted in a trilled calling pattern (well-defined series of non-pulsed notes) with short-lasting notes (maximum note duration: 50 ms; see Table 2 in Pansonato et al., 2012), having no or slight frequency modulation (Giaretta & Kokubum, 2003; Pansonato et al., 2012; Andrade & Carvalho, 2013; Roberto et al., 2013).
Notes on natural history
Males tend to call during daytime and decrease or cease call activity after nightfall. Males call on the margins of artificial ponds or slow-flowing streamlets with clean water and muddy/sandy bottom, either on water surface among grassy vegetation or at their border on the ground, almost always in association with Buriti (Mauritia flexuosa) palm grove marshes (Fig. 6).
Typical breeding habitat of P. giarettai: a permanent pond associated with a Buriti palm grove marsh at the Parque Nacional Grande Sertão Veredas (Municipality of Chapada Gaúcha), northwestern Minas Gerais, southeastern Brazil
DISCUSSION
A better sample of calls from each population should be assessed prior to any assumption on the association of temperature and temporal traits of P. giarettai call, as well as to test the effect of water temperature on them, given that this species may call on water surface in association with vegetation. Although the exploratory test (PCA) recovered acoustic variation both within and among populations of P. giarettai, it was insufficient to raise doubts on the assignment of all populations enclosed in a single taxonomic unit. Thus, our results support that all acoustic variation observed might be attributed to intraspecific variation.
The remarkable morphological and morphometric intraspecific variation observed for P. giarettai reinforces that the distinctive advertisement call pattern is the most straightforward evidence line, perhaps the unique unambiguous character, to diagnose it from its congeners, whereas morphological (robust body, glandular dorsum) and morphometric (body size) features show such variation, especially for non-topotypical populations, so that they should no longer be employed as reliable diagnostic features for P. giarettai. Still, the color feature of yellow vocal sac was observed in all specimens of P. giarettai, which might be helpful to distinguish this species besides its distinctive whistling advertisement call.
Morphological/morphometric features might have little contribution to assess specific identity of Pseudopaludicola, whereas acoustic information has revealed cryptic diversity and has contributed to the reassessment of taxonomic status within this Neotropical frog group. In the last four years, six species were described (in chronological order: P. giarettai, P. hyleaustralis, P. facureae, P. parnaiba, P. pocoto, and P. atragula; Carvalho, 2012; Pansonato et al., 2012, 2014a; Andrade & Carvalho, 2013; Roberto et al., 2013; Magalhães et al., 2014), one revalidated (P. ameghini; Pansonato et al., 2013), and two invalidated (P. riopiedadensis and P. serrana; Cardozo & Toledo, 2013; Pansonato et al., 2014b) taking into account this line of evidence. Therefore, it is essential to obtain, whenever it is possible, the association of advertisement call pattern to Pseudopaludicola specimens to unambiguous assessment of their species identity.
ACKNOWLEDGEMENTS
This study was supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa no estado de Minas Gerais (FAPEMIG), and Fundação de Amparo à Pesquisa no estado de São Paulo (FAPESP). A research grant conceded by CNPq to AAG. Fellowships by CAPES (BFVT, LBG), CNPq (LBM), and FAPESP (TRC). Special thanks go to PARNA Grande Sertão Veredas staff, who assisted with logistics during fieldwork; Diego J. Santana and Leandro A. Drummond, who kindly provided acoustic and distributional information, Marco Antônio Peixoto for field assistance in Buritizeiro, Renato N. Feio for making available specimens under his care. Collection permit was granted by Instituto Chico Mendes through the online platform Sistema de Autorização e Informação em Biodiversidade (ICMBio/SISBIO 30059-4).
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APPENDIX 1
List of examined specimens
Pseudopaludicola giarettai - BRAZIL: Minas Gerais: Curvelo (holotype: AAG-UFU 0312; paratypes: AAG-UFU 0309-0311, 0313-0316); Buritis (AAG-UFU 1772-1778); Buritizeiro (AAG-UFU 4580, MZUFV 14203-14210); Chapada Gaúcha (AAG-UFU 1920-1928); Coromandel (AAG-UFU 3565-3568); Unaí (MZUFV 14878-4883).
APPENDIX 2
Mean individual values, scores, eigenvalues, and proportional explained variation (%) of the first three principal components. CUR (Curvelo), BUR (Buritis), BUZ (Buritizeiro), CHG (Chapada Gaúcha), COR (Coromandel), UNA (Unaí). T = recording air temperature (°C), CD = call duration (s), CI = call interval (s), CRT = call rise time (s), CRS = call rate/s, DF = dominant frequency (Hz), FM = frequency modulation (Hz).
APPENDIX 3
Eigenvectors from P. giarettai acoustic traits in the first three principal components.
Publication Dates
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Publication in this collection
2015
History
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Accepted
08 Apr 2015