Zootaxa 4413 (2): 392–396 http://www.mapress.com/j/zt/ Copyright © 2018 Magnolia Press
ISSN 1175-5326 (print edition)
Correspondence
ZOOTAXA
ISSN 1175-5334 (online edition)
https://doi.org/10.11646/zootaxa.4413.2.12 http://zoobank.org/urn:lsid:zoobank.org:pub:8380DC32-B6B7-40D2-8FC3-48BFAA93A09E
Vocal repertoire of Ololygon pombali (Lourenço, Carvalho, Baêta, Pezzuti & Leite, 2013) (Anura: Hylidae) from its type locality, with notes on phenotypic variation DAVI LEE BANG 1,2,3 & ARIOVALDO ANTONIO GIARETTA1 1 Laboratório de Taxonomia, Sistemática e Evolução de Anuros Neotropicais, Universidade Federal de Uberlândia, Faculdade de Ciências Integradas do Pontal, Rua 20, 1600, Bairro Tupã, 38304-402. Ituiutaba, MG, Brazil; 2 Programa de Pós-Graduação em Biologia Comparada, Universidade de São Paulo, Departamento de Biologia/FFCLRP. Avenida dos Bandeirantes, 3900, 14040-901, Ribeirão Preto, SP, Brazil. 3 Corresponding author. E-mail:
[email protected]
A recent nomenclatural change based on molecular data (Duellman et al. 2016) resurrected genus Ololygon to accommodate all taxa in the former Scinax catharinae clade (Faivovich 2002; Faivovich et al. 2005). Most Ololygon species inhabit Coastal Atlantic rainforests in northeastern and southeastern Brazil (Duellman et al. 2016), but some species occur in the Cerrado Domain (Cardoso & Haddad 1982; Pombal et al. 2010; Lourenço et al. 2013). Ololygon pombali (Lourenço, Carvalho, Baêta, Pezzuti & Leite, 2013) is a small species only known from the southern portion of Parque Nacional da Serra da Canastra, in the municipality of Capitólio, state of Minas Gerais, southeastern Brazil. Here, we describe the vocal repertoire of Ololygon pombali and provide notes on dorsal color pattern variation, while briefly discussing their taxonomic implications. Fieldwork was conducted on 19 and 20 September 2016, at the type locality of Ololygon pombali, at Ribeirão da Capivara, Chapadão da Babilônia (20°36’14.74” S, 46°17’35.07” W; 1003 m a.s.l.), within Parque Nacional da Serra da Canastra. Males were found calling perched on marginal tree branches or bushes (0.3–0.5 m high) around a marginal pond connected to a perennial rivulet. Calling activity started after 03:00 a.m. and ceased at dawn; air temperature ranged between 18.5–24.0 °C. Vocalizations were recorded in the field using a Marantz PMD 671 digital recorder set at 44.1 kHz sampling rate and 16-bit resolution (mono .wav format) with a Sennheiser K6/ME67 directional microphone. Calls were analyzed using the software Raven Pro 1.5 (Bioacoustics Research Program 2014) with the following settings: window type = Hann; window size = 256 samples; 3 dB filter bandwidth = 270 Hz; overlap = 90%; hop size = 0.542 ms; DFT size = 1024 samples; spectral resolution = 46.9 Hz. Recordings were filtered from 0 to 400 Hz prior to analysis, in order to reduce background noise. Dominant frequency was obtained with the “Peak Frequency” function. Call-rise time of call type “A” was measured as the point of maximum amplitude of a call (“Peak Time” function) divided by its duration and multiplied by 100 to denote the percentage at which the call reaches its maximum amplitude. Note period was measured as the time from the beginning of a note to the beginning of the next; this trait was measured in the first, middle and penultimate note within a call type A. Other acoustic terminology and definitions followed Hepp et al. (2016) and Bang & Giaretta (2017). Sound figures were made in the Seewave package version 1.7.6 (Sueur et al. 2008) in R version 3.2.3 (R Core Team 2015), using the following settings: window = Hanning, overlap = 85% and FFT = 128. Nine specimens were collected, euthanized with 5% lidocaine, fixed in 10% formaldehyde, preserved in 70% ethanol, and deposited in the collection of frogs of Universidade Federal de Uberlândia (AAG-UFU 5588–5593, AAGUFU 5597–5599), in Uberlândia, Minas Gerais, Brazil. Audio files of original call recordings were deposited at the sound collection of AAG-UFU and are available upon request. Specimens collected were assigned to O. pombali for having (1) small size (male SVL 20.4–23.5 mm); (2) snout subelliptical, subovoid or rounded in dorsal view, rounded in lateral view; (3) dorsal skin with scattered granules or more granulose in some individuals; (4) lack of an externally developed and hypertrophied inguinal gland; (5) a dark brown, triangular or T-shaped blotch on interorbital region, and a black elliptical spot between eyes and nostrils; (6) dorsum with two dorsolateral elongated dark brown blotches from posterior margin of eye to mid-body and a chevron-shaped blotch on the sacral region. Differently from the original description (Lourenço et al. 2013), color pattern of dorsum varied among specimens, and three color variants were observed: brown background with dark blotches with silver/gray
392 Accepted by P. Simoes: 16 Mar. 2018; published: 23 Apr. 2018
bordering (Fig. 1A); brown background with dark blotches with no borders (Fig. 1B); light brown background with blotches with little or no color contrast (Fig. 1C). The vocal repertoire of nine recorded males consists of three types of notes: 1) short squawk-like notes, 2) long squawk-like notes, and 3) click-like notes. These notes are emitted in different arrangements, and the most common emitted arrangement is herein referred as call type “A”, and therefore assumed to be the advertisement call (sensu Hepp et al. 2017). Values of call parameters described below are presented as ‘range (mean ± SD)’. Call type A consists of a sequence of short squawk-like notes (Fig. 1D) that increase in amplitude along call duration, reaching maximum amplitude in its middle-to-final portion (call-rise time = 45.6–99.2%; n = 24 calls). Call duration ranges between 534–1619 ms (918.3 ± 276.0 ms; n = 24 calls) and calls have 6–15 notes (9.9 ± 2.4 notes) that are emitted at rates of 8.3–11.5 notes/s (10.3 ± 0.8 notes/s). Each short squawk-like note within a call type A has ascending amplitude modulation (Fig. 1E), reaching its maximum approximately in its first third or half portion, decreasing towards the end. Note duration within a call type A ranges between 18–48 ms (35.4 ± 6.7 ms; n = 71 notes) and have 5–15 pulses (10.0 ± 2.4 pulses) that are emitted at rates of 142.8–437.5 pulses/s (275.9 ± 60.2 pulses/s). Pulses within notes may have complete or incomplete amplitude modulation. First pulse of each note always separated from the others by complete amplitude modulation. First note period has a duration of 73–118 ms (94.3 ± 10.6 ms); middle note period has a duration of 77–112 ms (91.5 ± 9.1 ms); and last note period has a duration of 96–298 ms (124.4 ± 39.4 ms), being often the longest. There is a slight shift in dominant frequency from the first to the last note within a call: first note = 2437–4078 Hz (2981 ± 409 Hz), middle note = 2718–4031 Hz (3317 ± 320 Hz), last note = 2906–4078 Hz (3443 ± 328 Hz). Dominant frequency of the entire call ranges between 2906–4078 Hz (3474 ± 305 Hz). A variation of call type A (n = 3 males; Fig. 1F) may be emitted by males when in close-range interactions with other males. Calls with longer duration are herein referred as “extensive calls”. These calls are characterized by the absence of remarkable shifts in amplitude along call. Call duration ranges from 1776 to 3019 ms (2319 ± 393 ms; n = 7 calls). Calls have 17–30 notes (23.3 ± 4.5 notes) and are emitted at rates of 9.1–10.7 notes/s (9.8 ± 0.6 notes/s). Note duration ranges between 28–56 ms (40.4 ± 7.5 ms; n = 21 notes) and notes have 3–10 pulses (7.1 ± 2.0 pulses) emitted at rates of 74.1–257.1 pulses/s (154.6 ± 48.3 pulses/s). First note period has a duration of 78–150 ms (94 ± 25 ms); middle note period has a duration of 84–138 ms (110 ± 18 ms); and last note period has a duration of 101–157 ms (120 ± 18 ms). Dominant frequency of the entire call ranges from 3515 to 3937 Hz (3734 ± 178 Hz). Click-like (n = 5 males) and long squawk-like (n = 7 males) notes (Fig. 1G) are emitted sporadically and are assumed to be aggressive signals since they are emitted in close-range interactions between males. They can be emitted alone, in association with one another, or before or shortly after a call type A. The long squawk-like note (n = 16 notes) is formed by a train of pulses with highly variable duration, ranging between 153–708 ms (361 ± 137 ms) and containing 18–71 pulses (38.6 ± 16.5 pulses) emitted at rates of 93.2–162.5 pulses/s (124.4 ± 19.4 pulses/s). This note can have a first low-amplitude portion, followed by a last third portion with increased amplitude, decreasing afterwards. Alternatively, this note can have ill-defined portions, resulting from different pulse grouping arrangements. Dominant frequency of the long squawk-like note ranges between 3000–4125 Hz (3693 ± 258 Hz). Click-like notes (n = 27 notes) are also pulsed and resemble a squawk-like note, but are shorter and with irregular pulse organization (last pulses generally more juxtaposed than pulses at the beginning of the note), resulting in lower pulse emission rates. Click-like notes can be emitted alone (n = 15 cases) or in groups (n = 8 cases) of 2-3 notes, shortly after or before a long squawklike note. Notes have durations of 26–74 ms (35 ± 8 ms) with 3–12 pulses (6.3 ± 2.3 pulses) that are emitted at rates of 83.3–290.3 pulses/s (178.0 ± 57.7 pulses/s). Dominant frequency of the click-like note ranges between 2765–4125 Hz (3548 ± 447 Hz). Specimens collected at the type locality presented variation in dorsum color pattern, not previously reported in the original description (Lourenço et al. 2013). Distinct patterns such as blotches without bordering or less contrasting blotches were observed. Therefore, this trait should be used with caution and in combination with other traits (e.g., the lack of a hypertrophied inguinal gland, lack of a distinct nuptial pad, presence of an elliptical small spot between eyes and nostril, tadpole morphology) when diagnosing Ololygon pombali from other congeners. The vocal repertoire of O. pombali is formed by complex acoustic arrangements, as previously reported for other congeners. Call type A is assumed to operate as an advertisement call (Bastos & Haddad 2002; Bastos et al. 2011; Hepp et al. 2017; Bang & Giaretta 2017) and is herein used for qualitative interspecific comparisons. Advertisement calls of O. pombali differ from those of O. agilis (Cruz & Peixoto, 1983) (calls resembling the acoustic pattern of Scinax, by being composed of longer notes with lower pulse rates; Nunes et al. 2007; Hepp et al. 2017), O. angrensis (Lutz, 1973) (call type A composed of short squawk-like notes and click-like notes; Garey et al. 2012), O. aromothyella (Faivovich, 2005), O. berthae (Barrio, 1962) (extensive emission of short squawk-like notes with regular amplitude modulation with intermingled long squawk-like notes; Pereyra et al. 2012), O. caissara (Lourenço,
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Zina, Catroli, Kasahara, Faivovich & Haddad, 2016) (calls with a single note; Lourenço et al. 2016), O. heyeri Peixoto & Weygoldt, 1986 (call type A composed of a series of click-like notes; Hepp et al. 2017), O. humilis (Lutz & Lutz, 1954), and O. littoralis (Pombal & Gordo, 1991) (call type A composed of short squawk-like notes and click-like notes; Garey et al. 2012, Hepp et al. 2017), O. luizotavioi Caramaschi & Kisteumacher, 1989 (call type A composed of a series of click-like notes; Lourenço et al. 2009), O. rizibilis (Bokermann, 1964) (each short squawk-like notes within a call with a preceding discrete group of more spaced pulses; Bastos & Haddad 2002), and O. strigilata (Spix, 1824) (calls with a single note; Mendes et al. 2013), by having the call type A composed of a series of short squawk-like notes with note-bynote increase in amplitude and only one group of pulses within notes.
FIGURE 1. (A–C): Adult male topotypes of Ololygon pombali from Parque Nacional da Serra da Canastra, Capitólio (MG). (A) AAG-UFU 5591 (SVL 21.2 mm); (B) AAG-UFU 5590 (SVL 21.1 mm); (C) AAG-UFU 5598 (SVL 22.7 mm). (D–G): Vocal repertoire of Ololygon pombali: (D) Spectrogram (upper graph) and oscillogram (lower graph) of a call type A (assumed to be the advertisement call); (E) Oscillogram detailing the last three short squawk-like notes in the red brackets of (D); (F) Oscillogram depicting an extensive call; (G) Spectrogram (upper graph) and oscillogram (lower graph) of the other two note types: a click-like note (in red brackets) followed by a long squawk-like note.
Acoustic data seems to be taxonomically uninformative regarding some species of Ololygon (Bang & Giaretta 2017) and should be employed carefully for quantitative comparisons. For instance, several species which have acoustic data available (e.g., O. albicans (Bokermann, 1967), O. argyreornata (Miranda-Ribeiro, 1926), O. catharinae (Boulenger, 1888), O. canastrensis (Cardoso & Haddad, 1982), O. centralis (Pombal & Bastos, 1996), O. hiemalis (Haddad & Pombal, 1987), O. longilinea (Lutz, 1968), O. machadoi (Bokermann & Sazima, 1973), O. ranki (Andrade & Cardoso, 1987), O. skaios (Pombal, Carvalho, Canelas & Bastos, 2010), and O. trapicheiroi (Lutz, 1954)) share a stereotyped structure regarding call type A (a series of short squawk-like notes with increase in amplitude along call duration; Bastos & Haddad 2002; Bastos et al. 2011; Hepp et al. 2017; Bang & Giaretta 2017), and considering only quantitative data
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obtained from calls may bring subjectivities and inconsistencies in comparisons as some traits may greatly vary (e.g., note duration and pulse rate). Variation in these traits could also be related to behavioral and physiological responses to temperature or social interactions (Wells 2007), and these should be accounted for in more comprehensive interspecific comparisons in future studies. Long squawk-like, click-like notes and extensive calls are probably aggressive signals. This assumption could be made based on similarities with aggressive notes reported for other species of Ololygon (Bastos & Haddad 2002; Bastos et al. 2011). Particularly, extensive calls were emitted in close-range interactions between males, which increased call duration when neighboring males emitted the same call. Experimental assessments focused on male-male interactions and female preferences are still needed to clarify the behavioral role of different call types in Ololygon.
Acknowledgements Pedro Marinho helped in fieldwork. Financial support was granted by CNPq and FAPEMIG to AAG team. A grant was provided by CNPq to AAG. A master’s fellowship was provided by CNPq to DLB (process #159817/2015–3). ICMBio/ SISBIO conceded collection permits (#30059-7). Pedro I. Simões and an anonymous reviewer provided valuable suggestions that improved drafts of this work.
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