Introduction

Animal communication plays an important role in sexual attraction, reproductive success, parental care, and anti-predatory defense (Krebs and Davies, 1996). The importance of acoustic signals in natural and sexual selection, and diversification of species have extensively been documented (Cocroft and Ryan, 1995; Gerhardt and Huber, 2002; Robillard, Höbel and Gerhardt, 2006). Acoustic signals related to species recognition and mate choice are liable for strong selective pressures (see Erdtmann and Amézquita, 2009). Other biotic (e.g., size,

closely related taxa occurring in syntopy) and abiotic (e.g., temperature, habitat structure, and microhabitat of vocalization) features might also have an influence on the evolution of acoustic signals (Wells, 1977; Gerhardt, 1992).

Differences in acoustic signals in anurans are an important pre-zygotic barrier (Blair, 1955, 1958; Fouquette, 1960; Littlejohn, 1965), evidencing their usefulness in species recognition and complementary information for taxonomic studies (Heyer et al., 1996; Padial et al., 2008; Carvalho, 2012). The advertisement call is the main acoustic signal given by males during the breeding season, and often conveys more than one type of message (Gerhardt, 1992). Also, it usually serves two main functions: the attraction of conspecific females, and the advertisement of a male’s position to other conspecific males, which helps maintaining spacing between calling males (Blair, 1958; Wells, 2007). Moreover, the advertisement call comprises additional sets of information related to size. For instance, individual discrimination of calling males (Narins et al., 2007; Gasser, Amézquita and Hödl, 2009).

The genus Chiasmocleis currently comprises 25 species distributed in Central America and South

Herpetology Notes, volume 6: 439-446 (2013) (published online on 23 September 2013)

Intraspecific variability of the advertisement call of Chiasmocleis albopunctata (Anura: Microhylidae): note structure as an

additional diagnostic character within the genus

Thiago Ribeiro de Carvalho 1, 2, *, Bernardo Franco da Veiga Teixeira 1, 2, Lucas Borges Martins 1, 2 and Ariovaldo Antonio Giaretta 1

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.

* Corresponding author: thiago_decarvalho@yahoo.com.br

Abstract. We analyzed the intraspecific variability of the advertisement call of Chiasmocleis albopunctata and provide an additional diagnostic character (note structure) for this species to distinguish it from other congener species. Specimens and vocalizations were obtained in Teresina de Goiás, northern State of Goiás, central Brazil. The advertisement call consists of long series of multipulsed notes emitted at irregular intervals. Note structure consists of two distinctive pulse groups, the first one is usually formed by two pulses or rarely by one pulse, often with greater amplitude; and the second one, which is formed by the remaining pulses (5–8). An increment in amplitude can be observed in the second pulse group, particularly in the last pulse. The pulse groups are separated by a short interval (< 10 ms). Our bioacoustic data embraced almost all the range of values in temporal and spectral traits from previous descriptions. The distinctive two-pulse group note structure of C. albopunctata distinguishes it from all congeners with described calls, except for C. mehelyi. Our study sheds light on the usefulness of bioacoustic databases as a reliable source of data that could enhance further taxonomic and systematic studies.

Keywords. Bioacoustics, Cerrado, Goiás.

Thiago Ribeiro de Carvalho et al..440

America north and east of the Andes (Frost, 2013). Most of its comprising taxa had their calls already described (Santana et al., 2009; Forlani et al., 2013). The call of C. albopunctata was first described based on a single individual from Bolivia (De la Riva, Marquez and Bosch, 1996). Oliveira-Filho and Giaretta (2006) described its call from a second population based on two individuals from Uberlândia (Minas Gerais), southeastern Brazil.

In this paper, we analyzed the intraspecific variability of the advertisement call of Chiasmocleis albopunctata based on data from central Brazil and compared it with bioacoustic information available. We also provide an additional diagnostic character (note structure) for this species that distinguishes it from congeneric species.

Materials and Methods

Vocalizations were obtained in two localities from central Brazil: Teresina de Goiás (13°52′ S; 47°15′ W; c. 835 m a.s.l.), northern Goiás, in November 2012; and Caldas Novas (17°46’ S, 48°39’ W; c. 880 m a.s.l.), southern Goiás, in November 2011. Seven males were recorded from Teresina de Goiás (N = 21 analyzed calls; 590 analyzed notes) on 16 November 2012 and one male from Caldas Novas (N = 1 analyzed call; 50 analyzed notes) on 26 November 2011. All individuals were recorded after strong rainfalls on the same day or one day before. Males were calling partially submerged from rain-filled puddles grasped in grassy vegetation.

The advertisement calls were recorded with digital recorders (M-audio Microtrack II or Marantz PMD 671) set at 48.0 kHz sample rate and a resolution of 16 bits (mono WAVE file format), coupled to Sennheiser K6/ME66 directional microphones, positioned at a mean distance of 1.5 meters from the calling males. Bioacoustic traits were analyzed with Raven Pro 1.5, 64-bit version (Bioacoustics Research Program, 2012). Temporal traits (call duration, note duration, internote

interval, pulses/note, notes/second, and notes/minute) were measured from spectrograms. Dominant frequency was obtained from the software (Peak Frequency measurement function). Raven Pro settings: window type = Hanning; window size = 256 samples; brightness = 50%; contrast = 50%; overlap = 85%; DFT size = 256 samples; grid spacing = 188 Hz. Sound figures were obtained with Seewave 1.6.4 (Sueur, Albin and Simonis, 2008), package of R 2.15.1 (R Development Core Team, 2012). Seewave settings: window name (Fourier transform window) = Hanning; window length = 256 samples; overlap = 85%. Terminology follows Duellman and Trueb (1994). Mean and standard deviation (SD) given in the text and tables were calculated from individual mean values, due to different samples for each recorded individual, whereas the range encompassed the minimum and maximum values for all call sample variation.

Within-male variation for each bioacoustic trait was expressed as coefficients of variation [(CV = SD/mean) x 100]. For each male, the coefficient of variation (CV) of each bioacoustic trait was calculated taking all individual call samples into account. The average coefficient of variation was calculated for each trait from CV values for each male. Bioacoustic traits with low within-male coefficients of variation (usually less than 5%) were classified as static and traits with higher coefficients of variation (usually greater than 12%) as dynamic (Gerhardt, 1991). Notes per minute were only estimated once for each individual, so that individual SD and CV values were zero.

All seven males from Teresina de Goiás were recorded at the same time (Table 1), in addition to a small number of recorded males from the population of Caldas Novas (N = 1). Voucher and additionalVoucher and additional examined specimens are housed in the Coleção de Anuros do Museu de Biodiversidade do Cerrado at 1

Table 1. Advertisement call traits and recording temperatures of four populations of Chiasmocleis albopunctata. Mean±SD (range). N = number 1

of recorded specimens (number of analyzed notes).2

3

Bioacoustic traits Present study Teresina de Goiás (GO)

N=7 (590)

Present study Caldas Novas (GO)

N=1 (50)

De la Riva, Marquez and Bosch (1996) Santa Cruz (Bolivia)

N=1 (15)

Oliveira-Filho & Giaretta (2006) Uberlândia (MG)

N=2 (10) Call duration (s) 17.2±4.6 (5.8–34.2) 25.0 Up to 23 seconds 11.8±0.9 (5.2–17.7) Notes/call 202.9±56.3 (69–400) 298 ---- ---- Note duration (ms) 53.2+2.1 (33–61) 56.2+1.3 (54–59) 51.9±8.5 (24–60) 60.0±4.0 (50–60) Internote interval (ms) 31.6±1.8 (28–36) 27.7±1.3 (26–30) ---- ---- Pulses/note 8.7±0.6 (6–10) 8.4±0.5 (8–9) 7.1±0.8 (5–8) 9 Notes/second 11.8±0.4 (11–13) 12 ---- ---- Notes/minute 709.7±21.3 (683–749) 714 643.9±90.8 (585–908) 462.0±55.2 (423–501) Dominant frequency (kHz) 4.52±0.17 (3.94–4.88) 4.26±0.15 (4.13–4.48) 4.43±0.10 (4.31–4.66) 4.31 Air temperature (°C) 22.3 20.0 24 22.2 Water temperature (°C) 23.8 23.0 ---- 22.1

4

Table 1. Advertisement call traits and recording temperatures of four populations ofAdvertisement call traits and recording temperatures of four populations of Chiasmocleis albopunctata. Mean±SD (range). N = number of recorded specimens (number of analyzed notes).

Intraspecific variability of the advertisement call of Chiasmocleis albopunctata 441

the Universidade Federal de Uberlândia (AAG-UFU), Uberlândia, Minas Gerais. Snout-vent length (SVL;Snout-vent length (SVL; sensu Duellman, 1970) was measured with calipers to the nearest 0.1 mm. Voucher specimens: AAG-UFUVoucher specimens: AAG-UFU 0840 (Caldas Novas), 1380–1382 (Teresina de Goiás); additional examined specimens: AAG-UFU 1383–1396 (Teresina de Goiás).

Results

Species identification. The series of 17 adult specimens (16 males and one female) from Teresina de Goiás was assigned to Chiasmocleis albopunctata based on the following morphological and coloration characters presented in its redescription (Caramaschi and Cruz, 1997): 1) Adult male SVL 21.9–27.0 mm (24.6 ± 1.5; N = 16); 2) lack of occipital fold, postorbital fold present (Figure 1); 3) dorsal coloration dark gray with whitish bar on snout, extending along canthus rostralis, superior palpebra, and fragmented as irregular blotches on dorsum, arms and legs (Figure 1); 4) ventral coloration gray with large, well-delimited, and irregularly distributed whitish blotches; 5) fingers

and toes free, lacking disks, and slightly fringed. The voucher male from Caldas Novas (SVL 25.0 mm) also fits the set of diagnostic morphological and coloration characters presented above.

Advertisement call (Teresina de Goiás). Comparative data of the single male recorded from Caldas Novas are summarized in Table 1. The advertisement call (Figure 2) consists of long series of multipulsed notes emitted at irregular intervals and with a slight increment in amplitude in the first notes of each series. Call duration varies from 5.8–34.2 s (17.2 ± 4.6), composed of 69–400 notes (203 ± 56.3). Note structure consists of two distinctive pulse groups (Figure 3): the first one is usually formed by two pulses or rarely by one pulse, but often with a greater amplitude; and the second one is formed by 5−8 pulses, with an increment in amplitude, which is more evident in the last pulse. Pulse groups are separated by a short interval (< 10 ms). Each note is composed of 6–10 pulses (8.7 ± 0.6). Note duration varies from 33–61 ms (53.2 ± 2.1), with internote interval from 28–36 ms (31.6 ± 1.8), emitted at a rate of 11–13 notes/second (11.8 ± 0.4), and at a rate of 683–749 notes/minute (709.7 ± 21.3). Dominant frequency peaks from 3.94 to 4.88 kHz (4.52 ± 0.17). Sound energy concentrates at the central portion of each note (Figure 3A), which is weaker along lower and higher frequencies, so that there are three (Figure 3B) or two (Figure 3C) emphasized frequency bands in each note. Other emphasized frequency band can be assessed at a higher frequency (Figures 2B, 3A), peaking from 11.81 to 14.06 kHz (13.65 ± 0.16). The first note of each advertisement call is often different in note structure among six out the seven males by not having the typical two-pulse group pattern, as well as less sound energy. We refer to these notes herein as introductory notes (Figure 2B), which correspond to the increment in amplitude at the beginning of each advertisement call. Introductory notes (N = 13 notes from six males) last from 26–54 ms (40.1 ± 10.4). Notes are composed of 5–10 pulses (7.3 ± 2.2) or even ill-defined pulses. Dominant frequency peaks from 2.63 to 3.94 kHz (3.57 ± 0.41).

Call variation within males. There was variation in all call traits, except for the number of notes per minute (Table 2). Variation was highest for call duration (average CV = 31.2%) and notes per call (average CV = 35.8%). These were classified as dynamic traits. Note duration (average CV = 3.0), internote interval (average CV = 4.0), pulses per note (average CV = 4.3), notes per second (average CV = 4.2), and dominant frequency (average CV = 1.6) were classified as static traits, since they had the lowest variation.

Figure 1. Voucher male specimens ofVoucher male specimens of Chiasmocleis albopunctata from Teresina de Goiás, central Brazil: (A) AAG-UFU 1380 (SVL 21.9 mm), and (B) AAG-UFU 1381 (SVL 23.4 mm).

DiscussionDespite the widespread distribution of Chiasmocleis

albopunctata (Silva et al., 2009; Forlani et al., 2011), only four populations had their advertisement calls described so far. A previous study from southeastern Brazil (Oliveira-Filho and Giaretta, 2006) found remarkable differences in quantitative data compared to calls from Bolivia (De la Riva, Marquez and Bosch, 1996), leading the former authors to suggest that these populations maybe represent different taxa. Both studies were based on small samples (a few notes from one or two individuals), which might have hampered the assessment of a greater bioacoustic variability, especially in temporal traits. Our data from central Brazil were based on a larger sample and embraced almost all the range of values from previous descriptions. That allowed us to assign the differences in quantitative data of all four populations to intraspecific variability.

Notes per minute was the only trait with a greater variability, in which the population from Uberlândia had a remarkably lower rate in comparison with the other three populations. This difference might be attributed to social context, such as the density of conspecific calling males, or the presence of receptive females, which usually increases emission rate, or even the presence of possible predators, which usually decreases emission rate (Wells, 2007). Within-male variation in call traits of C. albopunctata followed the pattern previously found for other anuran species (Tárano, 2001), in which the dominant frequency usually has the lowest coefficients of variation. In contrast, call duration had the highest coefficients of variation and is classified as a dynamic trait.

The note structure of the advertisement call of C. albopunctata is distinctive within the genus, except for C. mehelyi (Hartmann, Hartmann and Haddad, 2002).

Thiago Ribeiro de Carvalho et al..442

Figure 2. (A) Oscillogram section (24.2 seconds) showing a 293-note advertisement call of(A) Oscillogram section (24.2 seconds) showing a 293-note advertisement call of Chiasmocleis albopunctata from Teresina de Goiás, central Brazil (voucher AAG-UFU 1381; SVL 23.4 mm); (B) spectrogram (above) and oscillogram (below) showing the first six notes in A. The first is introductory, defined by lacking the distinctive note structure of two distinctive pulse groups, followed by five two-pulse group notes. Air temperature 22.3 °C, water temperature 23.8 °C; recorded at 20:57h, on 16 Nov 2012. Sound file: Chiasmoc_albopunTeresGoiasGO3cTRC_AAGm671.

Figure 3. Spectrograms(above)andcorresponding(below)ofcomparativenotes (sectionof threemediannotes)of theadvertisementSpectrograms (above) and corresponding (below) of comparative notes (section of three median notes) of the advertisement call of Chiasmocleis albopunctata from (A) Teresina de Goiás (voucher AAG-UFU 1381; SVL 23.4 mm); Air temperature 22.3 °C, water temperature 23.8 °C; recorded at 20:57h, on 16 Nov 2012. Sound file: Chiasmoc_albopunTeresGoiasGO3cTRC_AAGm671; (B) Caldas Novas (voucher AAG-UFU 0840; SVL 25.0 mm); Air temperature 20.0 °C, water temperature 23.0 °C, recorded at 21:43h, on 26 Nov 2011. Sound file: Chiasmoc_albopunCNovasGO1AAGm671; and (C) Uberlândia (unvouchered recording); Air temperature 24.4 °C, water temperature 25.4 °C, recorded at approximately 22:50h, on 19 Mar 2011. Sound file: Chiasmoc_albopunUberlMG6aAAGm.

Intraspecific variability of the advertisement call of Chiasmocleis albopunctata 443

The presence of such a distinctive note structure in both species was reported earlier (Forlani et al., 2013). Note structure may then be employed as an additional diagnostic character to distinguish C. albopunctata from congeners.

In this sense, it is noteworthy to state that the call of C. supercilialbus was reported to have a structure of ‘two set pulses’ by the original authors (Morales and McDiarmid, 2009). However, we could not associate it to a note structure with two well-defined pulse groups, inasmuch as the sound figure provided in the original description did not depict an isolated note. The call of C. mantiqueira (Santana et al., 2012) is composed of non-pulsed notes in comparison with the multipulsed note structure of C. albopunctata. Furthermore, note duration of C. albopunctata (24–61 ms; Table 3) is shorter than those of C. atlantica (64–186 ms; Wogel et al., 2004), C. cordeiroi (70–140 ms; Forlani et al., 2013), C. crucis (105–179 ms; Forlani et al., 2013), and C. shudikarensis (98 ms; Lescure and Marty, 2000). It also has fewer

number of pulses (5–10 pulses/note in C. albopunctata) in comparison with C. cordeiroi (13–24 pulses/note) and C. crucis (14–23 pulses/note), and higher dominant frequency (3.94–4.88 kHz in C. albopunctata) in comparison with C. atlantica (3.32–3.75 kHz; Wogel et al., 2004), C. avilapiresae (2.94–3.50 kHz; Barros et al., 2010), C. bassleri (3.27 kHz; Santana et al., 2009), C. shudikarensis (3.38–3.75 kHz; Lescure and Marty, 2000), C. supercilialbus (3.10 kHz; Morales and McDiarmid, 2009), and C. ventrimaculata (3.35–3.70 kHz; Nelson, 1973). In this context, it is noteworthy that the call described from Itaguaí (Rio de Janeiro; Nelson, 1973) and assigned to Chiasmocleis bicegoi, currently in the synonym of C. albopunctata (Caramaschi and Cruz, 1997), should probably correspond to C. carvalhoi (Caramaschi and Cruz, 1997).

Either the limited availability of detailed quantitative data (e.g., Nelson, 1973) or the use of non-standard terminology (e.g., Morales and McDiarmid, 2009) restrict a comprehensive comparison of the advertisement calls of Chiasmocleis species. But, at the same time, it reinforces the necessity of new call descriptions and redescriptions and sheds light on the usefulness of bioacoustic databases as a reliable source of data that could enhance further taxonomic and systematic studies.

Acknowledgements. This study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG). T.R.C. received a fellowship fromT.R.C. received a fellowship from

1

Table 2. Within-male variation in call traits of Chiasmocleis albopunctata from Teresina de Goiás, central Brazil (seven recorded males). Range 1

of variation in parentheses. 2

Call traits Average CV (%) Trait type Call duration (s) 31.2 (21.6–60.0) Dynamic Notes per call 35.8 (24.2–73.4) Dynamic Note duration (ms) 3.0 (1.8–5.2) Static Internote interval (ms) 4.0 (2.8–5.0) Static Pulses per note 4.3 (3.0–5.7) Static Notes per second 4.2 (0–6.8) Static Dominant frequency (kHz) 1.6 (0–2.5) Static

3

Table 2. Within-male variation in call traits of Chiasmocleis albopunctata from Teresina de Goiás, central Brazil (seven recorded males). Range of variation in parentheses.

1

Table 3. Comparative advertisement call data (range of values) of Chiasmocleis species. 1

Note duration (ms) Pulses/note Dominant frequency (kHz) Source C. albopunctata 24–61 5–10 3.94–4.88 Present study; De la Riva, Marquez and Bosch (1996);

Oliveira-Filho and Giaretta (2006) C. atlantica 64–186 7–22 3.32–3.75 Wogel, Abrunhosa and Prado (2004) C. avilapiresae 43–117 7–18 2.94–3.50 Barros et al. (2010) C. bassleri 39–74 3–6 3.27 Santana et al. (2009) C. capixaba 47–61 8–10 4.61–4.87 Wogel, Abrunhosa and Prado (2004) C. carvalhoi 42–54 8–10 4.69–4.96 Wogel, Abrunhosa and Prado (2004) C. cordeiroi 70–140 13–24 4.50–4.90 Forlani et al. (2013) C. crucis 105–179 14–23 4.07–4.44 Forlani et al. (2013) C. hudsoni* 71–126 5–8 4.26–4.87 Rodrigues et al. (2008) C. leucosticta ---- ---- 3.40–4.00 Nelson (1973) C. mantiqueira 12–72 Non-pulsed 1.88–4.94 Santana et al. (2012) C. mehelyi ---- 7–11 4.70–5.40 Hartmann, Hartmann and Haddad (2002) C. panamensis ---- ---- 4.80–5.50 Nelson (1973) C. schubarti ---- ---- 3.70–4.10 Nelson (1973) C. shudikarensis 98 ---- 3.38–3.75 Lescure and Marty (2000) C. supercilialbus ---- ---- 3.10 Morales and McDiarmid (2009) C. ventrimaculata ---- ---- 3.35–3.70 Nelson (1973)

* Introductory notes were not included in the range of values; see Rodrigues et al. (2008). 2

Table 3. Comparative advertisement call data (range of values) of Chiasmocleis species.

Thiago Ribeiro de Carvalho et al..444

FAPESP, B.F.V.T. received a fellowship from CAPES, L.B.M. received a fellowship from CNPq, A.A.G. received a grant from CNPq. Collection permits were granted by Instituto ChicoCollection permits were granted by Instituto Chico Mendes through the online platform Sistema de Autorização e Informação em Biodiversidade (ICMBio/SISBIO 30059–3 and ICMBio/SISBIO 02015.008064/02–51).

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Accepted by Diogo Provete

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