Research Article |
Corresponding author: Stefan Lötters ( loetters@uni-trier.de ) Academic editor: Eva Ringler
© 2019 Stefan Lötters, Dietrich Mebs, Gunther Köhler, Joseph Vargas, Enrique La Marca.
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:
Lötters S, Mebs D, Köhler G, Vargas J, La Marca E (2019) The voice from the hereafter: vocalisations in three species of Atelopus from the Venezuelan Andes, likely to be extinct. Herpetozoa 32: 267-275. https://doi.org/10.3897/herpetozoa.32.e39192
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Atelopus is a species-rich group of Neotropical bufonids. Present knowledge on bioacoustics in this genus is relatively poor, as vocalisations have been described in only about one fifth of the ca. 100 species known. All studied members of the genus produce vocalisations although, with a few exceptions, most species lack a middle ear. Nonetheless, hearing has been demonstrated even in earless Atelopus making bioacoustics in these toads an inspiring research field. So far, three structural call types have been identified in the genus. As sympatry is uncommon in Atelopus, calls of the same type often vary little between species. Based on recordings from the 1980s, we describe vocalisations of three Venezuelan species (A. carbonerensis, A. mucubajiensis, A. tamaense) from the Cordillera de Mérida, commonly known as the Andes of Venezuela and the Tamá Massif, a Venezuelan spur of the Colombian Cordillera Oriental. Vocalisations correspond, in part, to the previously identified call types in Atelopus. Evaluation of the vocalisations of the three species presented in this study leads us to recognise a fourth structural call type for the genus. With this new addition, the Atelopus acoustic repertoire now includes (1) pulsed calls, (2) pure tone calls, (3) pulsed short calls and (4) pure tone short calls. The call descriptions provided here are valuable contributions to the bioacoustics of these Venezuelan Atelopus species, since all of them have experienced dramatic population declines that limit possibilities of further studies.
Anura, Bufonidae, Atelopus carbonerensis, Atelopus mucubajiensis, Atelopus tamaense, bioacoustics
Atelopus Duméril & Bibron, 1841, is a monophyletic lineage of Neotropical bufonids of Cretaceous origin (
Over the last four decades, along with most species of the genus (see overview in
All Atelopus species lack a tympanum and most lack a columella (
Bioacoustics in the seven members of the genus from the Cordillera de Mérida and Tamá Massif are still unstudied. Back in the 1980s, two of the authors (DM and ELM) recorded calls of A. carbonerensis, A. mucubajiensis and A. tamaense (Fig.
As a milestone in bioacoustics of the genus, Cocroft et al. (1990) reviewed Atelopus vocalisations and defined three call types, emitted by males. They differ in structure and duration (this is why the term ‘call type’ is not meant in a functional way as in common literature; e.g.
All three call types may occur in a single species of Atelopus (Table
In addition to the 13 taxa in which vocalisations were known by the time of Cocroft et al. (1990), vocalisations in seven other Atelopus species have been described (Table
Reported structural call types in the genus Atelopus, an update and refinement of Cocroft et al. (1990: 640), who only distinguished pulsed calls, pure tone calls and short calls. Species, in which ‘other calls’ (see text) are known, are marked with an asterisk. Applied taxonomy, if different to original call description, is based on
Species | Pulsed call | Pure tone call | Short pulsed Call | Short pure tone call | Source(s) |
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A. barbotini | × |
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A. carbonerensis* | × | × | × | × | This paper |
A. chiriquiensis | × | × | × |
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A. cruciger* | × | × | × | Cocroft et al. 1990 | |
A. exiguus | × |
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A. flavescens | × |
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A. franciscus | × |
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A. hoogmoedi | × |
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A. limosus | × | × |
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A. minutulus* | × | × | × | Cocroft et al. 1990 | |
A. mucubajiensis | × | × | This paper | ||
A. nahumae | × |
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A. nicefori | × | Cocroft et al. 1990 | |||
A. pulcher | × | × |
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A. peruensis | × |
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A. reticulatus | × |
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A. senex | × | Cocroft et al. 1990 | |||
A. tamaense | × | This paper | |||
A. tricolor | × | × |
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A. varius | × | × | × |
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Atelopus sp. ‘Panama’ | × | Cocroft et al. 1990 (cf. A. limosus) | |||
Atelopus sp. ‘Itaya’ | × |
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Atelopus cf. loettersi | × | Cocroft et al. 1990 (as A. s. spumarius) |
Since only anecdotal descriptions of vocalisations from other Atelopus species exist (e.g. on A. arthuri and A. ignescens by
Details of recordings are provided in Table
Details of Atelopus call recordings studied in this paper. An asterisk means that one or more vouchers are available (see Materials and methods). For additional information see figure legends.
Species | Site | Date, recorded by | Remark(s) |
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A. carbonerensis | La Carbonera, San Eusebio Forest (2,400 m a.s.l., Mérida State) | 25 May 1986 by ELM* | During daytime (~10 am), distance to recorder ca. 0.3 and ca. 0.7 m (two recordings) |
A. carbonerensis | La Carbonera, San Eusebio (2,330 m a.s.l., Mérida State) | 10 June 1987 by DM* | Shortly before noon, distance to recorder ca 1.5 m |
A. mucubajiensis | Páramo La Corcovada, cerca Laguna La Victoria (3,000 m a.s.l., Mérida State) | 23 June 1982 by ELM | During daytime (4:40 pm), distance to recorder ca. 0.3 m |
A. mucubajiensis | La Corcovada, ca. Laguna Mucubají (3,050 m a.s.l., Mérida State) | 7 June 1989 by ELM* | During daytime (12:45 am), distance to recorder ca. 2 m |
A. tamaense | Páramo de Tamá (2,950 m a.s.l., Apure State) | 12 August 1987 by ELM* | During daytime, distance to recorder < 2 m |
Calls were analysed using the software Raven pro 1.5 Beta version (44.1 kHz sample rate, 16-bit) (
Temporal measurements of calls such as repetition rates, duration of notes and number of pulses, were taken on the waveforms. Terminology of call descriptions follows
We recorded a series of typical pulsed calls from a male (Fig.
Characteristics of vocalisations in three Venezuelan Atelopus species. The mean is followed by the standard deviation and the range in parentheses. Frequency is abbreviated frequ. Pulsed, pure tone, pulsed short and pure tone short calls are as defined in the text.
Species | Call type | Call duration (ms) | Interval between calls (ms) | Pulse rate/sec | Pulse length (ms) | Lower frequ. range (Hz) | Higher frequ. range (Hz) | Dominant frequ. (Hz) | Amplitude (KU) |
Calls analysed | |||||||||
Figure reference | |||||||||
A. carbonerensis | Pulsed | 575 ± 38 (478–623) | 3601 ± 994 (1473–5389) | 0.48 | 14 ± 4 (4–32) | 2580 ± 110 (2380–2770) | 4020 ± 62 (3920–4100) | 3410 ± 21 (3380–3450) | 1.10 ± 0.504 (0.37–1.87) |
N = 6 | |||||||||
Fig. |
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A. carbonerensis | Pulsed short | 136 ± 25 (74–171) | 5181 ± 4172 (1041–13870) | 0.11 | 14 ± 1 (7–48) | 680 ± 81 (580–840) | 2110 ± 98 (1910–2260) | 1430 ± 44 (1380–1500) | 13.94 ± 7.319 (6.45–32.76) |
N = 8 | |||||||||
Fig. |
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A. carbonerensis | Pure tone | 273 ± 59 (202–347) | 3732 ± 2860 (872–6591) | n/a | n/a | 890 ± 37 (850–940) | 2000 ± 118 (1880–2160) | 1390 ± 37 (1360–1440) | 3.60 ± 0.679 (3.17–4.53) |
N = 11 | |||||||||
Fig. |
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A. carbonerensis | Pure tone short | 21 ± 10 (8–47) | 3059 ± 2884 (140–9379) | n/a | n/a | 730 ± 99 (600–1050) | 1840 ± 206 (1540–2260) | 1330 ± 151 (1160–1810) | 6.20 ± 3.848 (2.43–18.29) |
N = 13 | |||||||||
Fig. |
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A. mucubajiensis | Pure tone | 243 ± 48 (159–337) | 3704± 59 (3179–45605) | n/a | n/a | 1760 ± 138 (1550–2040) | 3170 ± 836 (2710–5350) | 2420 ± 763 (2340–2580) | 0.22 ± 0.255 (0.09–0.90) |
N = 8 | |||||||||
Fig. |
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A. mucubajiensis | Pure tone short | 41 ± 10 (22–57) | 2122 ± 2059 (50–8395) | n/a | n/a | 1030 ± 110 (860–1310) | 2240 ± 183 (1960–2460) | 1620 ± 1101 (2540–2640) | 0.73 ± 0.727 (0.13–2.74) |
N = 17 | |||||||||
Fig. |
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A. tamaense | Pure tone short | 22 ± 57 (13–30) | 1209 ± 897 (103–3802) | n/a | n/a | 2290 ± 48 (2210–2380) | 2850 ± 62 (2730–2970) | 2590 ± 36 (2540–2640) | 0.11 ± 0.033 (0.05–0.19) |
N = 15 | |||||||||
Fig. |
We further recorded typical short calls from the same specimen (Fig.
In another interaction in which multiple males were involved (and in physical contact) during mating in June 1987, pure tone calls were recorded (Figs
It is important to note that both pure tone calls and pure tone short calls were emitted in a series along with pulsed short calls. Little is known about the function of Atelopus pure tone calls, as these ‘whistles’ have been observed in a few species only (Table
The function of the pure tone short call remains even less clear, but in A. nahumae, it was interpreted as a release call (
With four structural call types recognised, A. carbonerensis is the member of the genus with the largest call repertoire known (Table
On different occasions, we were able to obtain pure tone and pure tone short calls (as defined above) from this species (Figs
The identity of the specimen emitting pure tone calls, however, remains tentative. It was neither seen nor collected. Indeed, no other anurans producing such ‘typical’ Atelopus pure tone calls are known from the site. Alternatively, it may be considered that a female A. mucubajiensis produces the pure tone calls recorded, as at least in one other member of the genus, females can emit calls while in physical interaction with other specimens (
The pure tone short call was emitted by a male in amplexus with a female in a collection bag; no other conspecifics were present. As afore-mentioned, the function of pure tone short calls is poorly understood but they may play a role in close-range intraspecific communication (see A. carbonerensis). However, the absence of conspecifics (other than the amplectant female) further complicates their interpretation in A. mucubajiensis.
When the type series of this species was collected, vocalisations of one male were recorded while handling. It is a pure tone short call and thus A. tamaense is the fifth Atelopus species (besides the two described above, plus A. nahumae and A. varius) from which this call type is known. It is similar in duration to that of A. carbonerensis (Table
Bioacoustics in the genus Atelopus remain poorly understood. One reason is that, including the present paper, vocalisations of only 23 of more than 100 species are known; a fact that is apparently linked to the dramatic declines which these amphibians have undergone. Moreover, the call repertoire is more complex in the genus than previously supposed and behavioural contexts are not entirely clear. We suggest that, instead of three, four call types emitted by males should be distinguished by structure and duration, which show some overlap in duration across the entire genus, but not within species (Table
We thank Alexander Kupfer and Günter Stephan from SMNS for providing data on A. carbonerensis material. The photograph of A. tamaense was kindly provided by Juan Manuel Renjifo. Roberto Ibáñez kindly shared information with us on the taxonomic status of Panamanian Atelopus for which calls are known. Philippe Kok and an anonymous reviewer made valuable comments on a previous version of the manuscript of this paper. The final manuscript was language-checked by Marius Burger before submission.
Atelopus carbonerensis various call recorded by DM
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Atelopus carbonerensis pulsed call recorded by ELM
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Atelopus carbonerensis short call recorded by ELM
Data type: WAV file
Atelopus mucubajiensis pure tone call recorded by ELM
Data type: WAV file
Atelopus mucubajiensis pure tone short call recorded by ELM
Data type: WAV file
Atelopus tamaense pure tone short call recorded by ELM
Data type: WAV file