Research Article |
Corresponding author: Iuri Ribeiro Dias ( iurirdias@hotmail.com ) Academic editor: Angelica Crottini
© 2017 Iuri Ribeiro Dias, Caio Vinicius de Mira-Mendes, Carlos Augusto Souza-Costa, Flora Acuña Juncá, Mirco Solé.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Dias IR, Mira-Mendes CV, Souza-Costa CA, Juncá FA, Solé M (2017) The advertisement call and comments on the distribution of Eleutherodactylus bilineatus Bokermann, 1975, an endemic frog of Bahia State, Brazil (Amphibia, Anura). ZooKeys 677: 151-159. https://doi.org/10.3897/zookeys.677.12309
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Advertisement calls can be used to aid solving taxonomic problems and understanding the evolution of certain groups. In this study, the advertisement call of Eleutherodactylus bilineatus is described. It is composed by two different notes with a total duration of 0.529–4.241 seconds and dominant frequency of 1.72–3.45 kHz. Additionally, new data is provided on the geographical distribution of Eleutherodactylus bilineatus and the most inland record for this species.
Atlantic Forest, bioacoustics, vocalization, Holoadeninae , range extension
A recent research on the phylogenetic relationships within the anuran clade Terrarana, from the Brazilian Atlantic rainforest frog genus Ischnocnema, included Eleutherodactylus bilineatus as incertae sedis, likely close to the genus Noblella and Barycholos within the Holoadeninae (
Eleutherodactylus bilineatus (Figure
Different individuals of Eleutherodactylus bilineatus showing some variation of the dorsal pattern of the species. A and B RPPN Mata do Passarinho, Macarani C Estação Ecológica Wenceslau Guimarães and D Serra do Corcovado, Almadina, Bahia, Brazil (photographs A, B and D Iuri R. Dias, C Rafael O. Abreu).
During the execution of the Project “Diversity and genetic structure of the amphibians of the Central Corridor of the Atlantic Forest of southern Bahia” supported by the Boticário Group Foundation for Nature Protection (Project n°.0991_20132), field expeditions were conducted lasting 7-8 days, using the same methodology and similar sampling efforts to nine different locations (Serra da Jibóia, Serra do Timbó, Wenceslau Guimarães, Serra do Corcovado, Pedra Lascada, Serra Bonita, Serra das Lontras, Macarani and PARNA Alto do Cariri), in the Atlantic Forest of Bahia. Specimens deposited in the Museum of Zoology of Universidade Estadual de Santa Cruz were also examined (Table
Distribution records of Eleutherodactylus bilineatus based on literature review, museum data (
Municipality | Localities | Latitude / Longitude | Reference | Voucher analyzed |
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Almadina | Serra do Corcovado | -14.7011, -39.6625 |
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Amargosa | Serra do Timbó | -13.0365, -39.6325 | Marciano-Jr et al. 2014 |
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Arataca | Serra das Lontras | -15.1624, -39.3437 | This study |
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Barro Preto | Serra da Pedra Lascada | -14.7723, -39.5408 | This study |
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Boa Nova | – | -14.3591, -40.2383 |
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- |
Cairu | Fazenda Subaúma | -13.5067, -38.9812 |
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- |
Camacan | RPPN Serra Bonita | -15.4413, -39.5189 |
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Canavieiras | – | -15.6750, -38.9469 |
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- |
Guaratinga | Fazenda Vista Bela | -16.4529, -40.0586 |
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Igrapiúna | Reserva Ecológica da Michelin | -13.8585, -39.1728 |
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Ilhéus | CEPLAC/UESC | -14.7867, -39.2249 |
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MUESC 8110 |
Jequié | – | -13.9654, -40.0002 | This study |
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Jussari | RPPN Serra do Teimoso | -15.1675, -39.5444 |
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- |
Macarani | RPPN Mata do Passarinho | -15.7907, -40.5192 | This study |
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Nilo Peçanha | Fazenda São João | -13.6585, -39.1884 |
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- |
Itarantim | Serra do Mandim | -15.6295, -39.9803 | This study |
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Santa Teresinha | Serra da Jibóia | -12.7283, -39.5694 |
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Uruçuca | Fazenda Provisão | -14.6512, -39.2232 | This study |
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Valença | RPPN Água Branca | -13.3791, -39.0916 | This study |
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Wenceslau Guimarães | Estação Ecológica de Wenceslau Guimarães | -13.6285, -39.6264 |
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The advertisement call of Eleutherodactylus bilineatus was recorded at two sites in Bahia state: Serra da Jibóia, Santa Terezinha municipality (-12.728397; -39.569476, 790 m a.s.l.) and RPPN (Private Natural Heritage Reserve) Mata do Passarinho, Macarani municipality (-15.79071; -40.51927, 850 m a.s.l.). In the Serra da Jibóia the recordings were made on three different occasions: December 04, 1995, total of 10 calls from two males (air temperature = 21°C, 19:40h); April 21, 1997, four calls from one male (air temperature 20°C, 20:50h); and March 03, 2015, total of 36 calls from three males (air temperature 21.4°C, 18:15h). The advertisement call (n = 4) of one male from RPPN Mata do Passarinho (encountered in November 27, 2014) is also included in our analysis, recorded after it was placed in a plastic bag. These calls showed the same acoustic patterns as the calls from the males recorded in their natural environment.
Recordings from 1995 and 1997 were made with a SONY WM-D6 Digital Audio Track (DAT) with a directional SONY microphone. For the recordings from 2014 and 2015 a Sennheiser ME45 microphone with a K6 power module connected to a Tascam DR1 digital recorder was used. All recordings were made from a distance of about 40 cm from the frogs. Calls were recorded at a resolution of 16 bit and 48 kHz sampling rate. Waveform and spectrogram were made using Raven Pro 1.4 and analyzed with a Fast Fourier Transformation of 256 points, 50% overlap for an entire call and Window Hamming. For all other configurations the “default” settings of Raven were used. Terminology follows
During field expeditions, 151 individuals of Eleutherodactylus bilineatus were registered in all locations sampled, except in PARNA do Alto do Cariri, municipality of Guaratinga, where the species was not found. The areas located more northwards revealed the largest abundances of this species: Serra do Timbó (n = 44), Serra da Jibóia (n = 43) and Wenceslau Guimarães (n = 35). In Macarani, located in the southeastern portion of Bahia we also encountered a high abundance with 24 individuals. At the other localities, records were limited to only one or two individuals.
Four new distribution records of specimens deposited in the Museum of Zoology of Universidade Estadual de Santa Cruz were found. Thus, the distribution map for the species is updated (Table
Distribution map of known localities for Eleutherodactylus bilineatus. Key: black star = type locality; red circle = new records; black circles = literature records. Municipalities = 1 Santa Teresinha 2 Amargosa 3 Wenceslau Guimarães 4 Valença 5 Cairu 6 Nilo Peçanha 7 Igrapiúna 8 Jequié 9 Boa Nova 10 Almadina 11 Barro Preto 12 Uruçuca 13 Ilhéus (Type Locality) 14 Jussari 15 Arataca, 16 Camacan 17 Canavieiras 18 Itarantim 19 Macarani and 20 Guaratinga. BA = state of Bahia; MG = state of Minas Gerais and ES = state of Espírito Santo. More details of the records are present in Table
Males began calling in the early evening, at places with dense leaf litter on the forest floor, near fallen trunks and tabular roots. During our observations (March 03, 2015) several individuals (n = 5–10) were calling together at the sites of recording, and calling activity decreased after 8:00 pm. In the RPPN Mata do Passarinho the advertisement call was heard sporadically, especially during the early evening. However, after one night of heavy rain, several males could be heard calling between 15:00–16:00 h.
The advertisement call (Figure
Intervals of 0.07–0.116 s (0.09 ± 0.01, n = 45) separated the two different note types. “Type II” was emitted in a sequence of 6–31 notes (13.98 ± 4.89, n = 54) with duration of 0.001–0.02 s (0.004 ± 0.003, n = 664) each with an interval between notes ranging from 0.07 to 0.21 s (0.13 ± 0.015, n = 660). The dominant frequency of “Type II” notes was 1.72–3.96 kHz (2.91 ± 423) and oscillated between the first (n = 9) and second (n = 31) harmonic. Four harmonic bands could be discerned, with peaks between 1.57–2.07 kHz; the second peak between 2.76–3.45 kHz; the third peak between 4.24–5.02 kHz and the fourth peak between 5.75–614 kHz.
The recordings from Macarani lasted longer and had a higher number of “Type II” notes (more than twice the average) than the recordings from Serra da Jibóia. In Macarani individuals were recorded inside a plastic bag, where they had been placed together with other individuals of Eleutherodactylus bilineatus, as well as individuals from other species as Ischnocnema verrucosa and Dendrophryniscus proboscideus. The observed difference in acoustic parameters could be associated to some kind of social context (e.g. agonistic interactions) and should be further investigated.
The uncertain taxonomic position of this species hampers the comparison of the acoustic parameters with other closely related species. Following
Acoustic parameters of advertisement call of Noblella and Barycholos, genera more closely related with Eleutherodactylus bilineatus according to
Barycholos ternetzi | Noblella carrascoicola | Noblella lochites | Noblella personina | |
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Number of Note | 1 | 5–8 (6.0 ± 1.2) | 6–8 | 5–11 |
Duration of Call | 30–79 (49 ± 8) |
254–436 (332.3 ± 62.6) |
369–537 (428.53 ± 53.60) |
570–1524 (1052 ± 307) |
Duration of each note | – | 12–20 | 6–17 (11.50 ± 2.90) |
13–20 (16 ± 2) |
Interval between notes | – | – | 51–95 (60.39 ± 5.77) |
103–166 (128 ± 14) |
Pulses per call | 4–12 (7.16 ± 1.47) |
– | – | – |
Dominant Frequency | 3.35–4.31 (3.77 ± 1.75) |
3.3–4.0 | 3.51–3.93 (3.73 ± 0.11) |
3.91–4.39 (4.10 ± 0.13) |
Reference |
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Batalla and Brito 2014† |
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The relationships within this clade (E. bilineatus, Noblella, Barycholos) require a more extensive approach, including morphological information in order to determine the taxonomic position of E. bilineatus, as well as the inclusion of molecular data into the phylogenetic analyses of other species of Holoadeninae (
We are grateful to the Fundação Biodiversitas and manager Alexandre Enout of RPPN Mata do Passarinho and GAMBA (Grupo Ambientalista da Bahia) for allowing us access to research areas (Macarani and Serra da Jibóia, respectively) under their care and for logistical assistance. We thank the Fundação Grupo Boticario de Proteção à Natureza (0991_20132), FAPESB (5154/2014), PROTAX-CNPq (440615/2015-1) and Rede Baiana de Pesquisa sobre Anfíbios (RBPA) - “Padrões e processos da diversidade de anfíbios na Bahia: influência das mudanças climáticas e propostas de conservação”, supported by FAPESB and the “Secretaria do Meio Ambiente da Bahia” (PAM0005/2014) for funding the project. Scholarships were provided by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq–Project: 404417/2015–9, Process: 150372/2016–7) to IRD and by the Fundação de Amparo à Pesquisa do Estado da Bahia (BOL0853/2012) to CVMM.