Short Notes-Padial.Indd

Short Communication

SALAMANDRA 44 3 187-191 Rheinbach, 20 August 2008 ISSN 0036-3375

The complex distress call of Ptychadena pumilio (Boulenger, 1920) (Anura: Ptychadenidae)

José M. Padial, José M. Barea-Azcón, Luis García-Cardenete & Ignacio De la Riva

Abstract. We describe the previously unknown distress call of Ptychadena pumilio. The call is composed of three completely diﬀerent kinds of notes. The composite note is the most complex and longest note. It starts with a long series of pulses modulated in amplitude, continues with a region of complex harmonic structure modulated in amplitude and frequency and ends with a short series of pulses. The short modulated note is the shortest note and the only one that lacks pulses. It consists of a single, short sound modulated in frequency and amplitude and with harmonic structure. The pulsed note is intermediate in length relative to the other two kinds of notes, and is the only one that lacks harmonics and frequency modulation. We hypothesize that the high diversity of notes involved in the distress call of P. pumilio and the complexity and variability of distress calls in other species may be the result of the adaptation to attempt to “tune” these calls to the auditory sensitiveness of diﬀerent possible predators. Key words. Amphibia, vocalisation, evolution.

During fieldwork in Senegal, the previously 686) have been deposited in the amphibian unknown distress call of Ptychadena pumil- collection and Fonoteca Zoológica, respec- io (Boulenger, 920) (Fig. ) was recorded. tively, of the Museo Nacional de Ciencias This call is surprisingly complex and deserves Naturales, Madrid, Spain (MNCN). Termi- a detailed description that may be useful in nology of call characteristics follows Hödl & understanding the evolutionary origin and Gollmann (986) as modified by Padial et significance of distress calls in anurans. Calls al. (2006). were recorded on TDK SA60 cassettes using a Sony WM D6C tape recorder and a Sen- nheiser ME 80 directional microphone with K-3U power module. Calls were digitized at a sampling frequency of 44. KHz and 32-bit resolution with a Delta 66 digitizing board, and edited with Audacity .2.6 for MacOS X (Free Software Foundation Inc. 99). Praat 4.5.02 for MacOS X (Boersma & Weenink 2006) software was used to obtain numerical information and to generate audiospectrograms and oscillograms. Frequen- cy information was obtained through Fast Fourier Transformations (FFT) (width 024 Fig. 1. Adult male (one from MNCN 44065-6) of points). Two adult males (MNCN 44065–6; Ptychadena pumilio in life from Simenti, Niokolo snout-vent-length 24.2 and 24.6 mm, respec- Koba National Park, Senegal. Photo: J. Rodrí- tively) and digitized calls (FonoZoo number: guez-Osorio.

Rödel (2000) provided a comprehensive account for P. pumilio including a description of its advertisement call, but not its distress call. We recorded distress calls of P. pumilio at Simenti, Niokolo Koba National Park, Senegal (3º0’40.7’’ N, 3º7’37.9’’ W), on the night of 0 April 2006 (air temperature 3ºC). To record the distress calls, two specimens were held by their hind legs until they begun to vocalize (with the mouth closed or partial- ly opened) when shaken slightly. Call length, call rate, dominant frequency, amplitude and number of harmonics changed with the intensity of shaking (Table ). The distress call of P. pumilio is composed of three diﬀerent kinds of notes (Fig. 2): Composite note (Fig. 2A): this is the longest and most complex note. It starts with a long series of pulses modulated in amplitude, continues with a region of complex harmonic structure modulated in amplitude and frequency, and ends with a short series of pulses (Table ). This note is usually fol- lowed by one or two short, frequency-modulated notes without pulses (short modulated note, see below). The amount and range of energy invested, the dominant frequency and the number of harmonics of the call reach the highest values in this kind of note. Most energy is invested after the third harmonic; indeed, dominant frequency might correspond to any harmonic up to the third. Short modulated note (Fig. 2B): this is the shortest note and the only one that lacks pulses. It consists of a single, short sound modulated in frequency and amplitude, and with harmonic structure (Table ). These notes were emitted after composite notes, or after one pulsed note (see below), or on its own when the specimen was less stimulated. Most of the energy of the call is distributed between 400-6000 Hz into one to ﬁve dominant harmonics. The dominant frequency Fig. 2. Audiospectrograms and oscillograms of the distress calls of Ptychadena pumilio from Niokolo usually coincides with the second or third Koba National Park, Senegal: (A) Composite note; harmonic. (B) Short modulated note; (C) Pulsed note. Pulsed note (Fig. 2C): this note is intermediate in length relative to the other two kinds

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Tab. 1. Summary of quantitative parameters of the diﬀerent notes of the distress calls of Ptychadena pumilio.

call dominant fundamen- intensity number domi- pulses be- pulses length frequency tal frequency Range (Hz) of har- nant fore har- after har- (ms) (Hz) (Hz) monics harmo- monics monics nics Composite note specimen  39 4444 56 3993-8753  3-6 0 3 (n = 2) 409 3626 690 2827-7393 7 3-8 5 3 specimen 2 378 383 949 3040-244 8 3-25 8 8 (3-3) (n = ) (4-70) (2773-095) (497-64) (2446-39) (2-25) (2-25) Short modulated note specimen  5 338 037 2706-5329 6 -5 0 - (n = 4) (23-25) (2270-4538) (079-2270) (904-6323) (2-0) specimen 2 38 2988 78 20-4590 5 -3 0 - (n = 6) (924-46) (594-3520) (05-332) (469-882) (3-9) Pulsed note specimen  52 5590 5590 4500-6000 0 - 20 - (n = ) specimen 2 74 308 308 2682-4479 0 - 4 - (n = 2) 84 2925 2926 2308-7055 0 - 6 - of notes, and is the only one that lacks har- ural selection (Laiolo et al. 2004). This may monics and frequency modulation. Ampli- be supported by the fact that females and ju- tude can be modulated, with the highest am- veniles are able to emit distress calls (Sazi- plitude reached in the middle of the call. The ma 975, Duellman & Trueb 986) and that, dominant frequency coincides with the fun- in contrast with advertisement calls, distress damental, and is higher than in the other call calls are very similar between different spe- types (Table ). cies of distant taxa (Duellman & Trueb The complexity of the distress call of Pty- 986, Hödl & Gollmann 986, Padial et chadena pumilio evidences that a single spec- al. 2006). Laiolo et al. (2004) provided evi- imen is able to emit completely different dence suggesting the transmission of infor- kinds of sounds within the same sound emis- mation from prey to predator through dis- sion. In contrast, advertisement calls of am- tress calls. Nevertheless, amphibians are sub- phibians are usually regular and constant and ject to predation by many different species most likely evolve in a single direction under of vertebrates and invertebrates (Duellman sexual selection (e.g. Blair 956, Ryan 980). & Trueb 986). Hence, we hypothesize that On the other hand, distress calls in frogs the high diversity of notes involved in the are emitted under dangerous circumstances distress call of P. pumilio and the complexity presumably to disturb or discourage preda- and variability of distress calls in other spe- tors (Hödl & Gollmann 986, Leary & Ra- cies (Bosch et al. 996, Martins & Haddad zafindratsita 998) and differ completely 998, De Souza & Haddad 2003, Padial et from advertisement calls of the correspond- al. 2006) may be the result of the adaptation ing species. Hence, the main evolutionary to attempt to “tune” the distress calls to the force acting upon distress calls should be nat- auditory sensitiveness of different kinds of

189 Short Communication predators. Some birds are sensitive to specific quez for the critical reading of a previous draft of stimuli associated with changes in frequency the manuscript. modulation and number of harmonics (e.g. Charrier et al. 200), and bats show a be- References havioral response to constant frequencies in the sonic range of their frog prey (Ryan et al. Blair, W. F. (956): Call differences as an isola- 983). Indeed, these are parameters that are ting mechanism in southwestern toads. – Te- constantly changed in distress calls (e.g. Pa- xas Journal of Science, 8: 87-06. dial et al. 2006, this study). Furthermore, Boersma, P. & D. Weenick (2006): Praat: doing predators of frogs may also have the ability phonetics by computer. Version 4.5.02. – Ams- to reverse the evaluation of the cues that sig- terdam. nal preferred versus poisonous preys (Page Bosch, J., I. De la Riva & R. Márquez (996): & Ryan 2005). It would be interesting to test The calling behaviour of Lysapsus limellus and if the complexity of distress calls might be a Pseudis paradoxa (Amphibia: Anura: Pseudi- result of natural selection favouring the flexi- dae). – Folia Zoologica, 45: 49-55. bility of prey to vary cue signals interpretable Charrier, I., N. Mathevon, P. Jouventin & T. by predators. To our knowledge, there is no Aubin (200): Acoustic communication in a experimental study on amphibians that at- black-headed gull colony: how do chicks iden- tempts to address these questions. Moreover, tify their parents? – Ethology, 07: 96-974. there is no comparative phylogenetic study De Souza, M.B. & C.F.B. Haddad (2003): Rede- that attempts to study the pattern of evolu- scription and reevaluation of the generic sta- tion of distress calls in different taxa. Distress tus of Leptodactylus dantasi (Amphibia, Anura, calls could have evolved quickly in anurans Leptodactylidae) and description of its unusu- al advertisement call. – Journal of Herpetology, and been retained due to their putative effi- 37: 490-497. cacy in disturbing or discouraging predators, or could have evolved several times for the Duellman, W. E. & L. Trueb (986): The biology of amphibians. – New York (McGraw-Hill, same or other reasons. If this kind of analy- Inc.). sis were to be done, the results could be con- Free Software Foundation Inc. (99): Audacity: a trasted with the geographic patterns of diver- free, cross-platform digital audio editor. Versi- sity of putative predators, in order to identify on .2.6. – Boston. any relationship that may illustrate the pat- Hödl, W. & G. Gollmann (986): Distress calls tern of evolution of distress calls to specific in Neotropical frogs. – Amphibia-Reptilia, 7: predators. Nevertheless, all these initiatives -2. may be impeded by the limited number of Laiolo, P., J. L. Tella, M. Carrete, D. Serrano anuran distress calls described to date. & G. López (2004): Distress calls may honestly signal bird quality to predators. – Proceedings of the Royal Society of London B, 27: 53-55. Acknowledgements Leary, C. J. & V. R. Razafindratsita (998): Attempted predation on a hylid frog, Phryno- We are grateful to P. Bueno, M.A. Díaz, José M. hyas venulosa by an indigo snake, Drymarchon Gil-Sánchez, F. Molino, J. Rodríguez- Oso- corais, and the response of conspecific frogs rio, A. Ruiz and M. Tardio for their friendship to distress calls. – Amphibia-Reptilia, 9: 442- and help during the fieldwork; to R. Márquez, 446. M. Pérez, G. Solís and L. González (FonoZoo, MNCN) for their help with the digitization and Martins, M. & C. F. B. Haddad (998): Vocaliza- storage of the recordings; to J. Rodríguez-Os- tions and reproductive behaviour in the smith orio for providing the picture of P. pumilio. To frog, Hyla faber Wied (Amphibia: Hylidae). – the personnel of Simenti and our field guides Vie Amphibia-Reptilia, 9: 49-60. Tamba and Ndiñgñu Fall for their collabora- Padial, J. M., R. De Sà & I. De la Riva (2006): tion; to S. Castroviejo, S. Lötters and R. Már- The distress calls of Leptodactylus chaquen-

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sis Cei, 950 and Leptodactylus elenae Heyer, Ryan, M. J. (980): Female mate choice in a Neo- 978 (Anura: Leptodactylidae). – Salamandra, tropical frog. – Science, 209: 523-525. 42: 57-60. Ryan, M. J., M. D. Tuttle & R. M. R. Barclay Page, R. A. & M. J. Ryan (2005): Flexibility in as- (983): Behavioral responses of the frog-eating sessment of prey cues: frog-eating bats and bat, Trachops cirrhosus, to sonic frequencies. frog calls. – Proceedings of the Royal Society of – Journal of Comparative Physiology, 50: 43- London B, 272: 84-847. 48. Rödel, M.-O. (2000): Herpetofauna of West Af- Sazima, I. (975): Distress call in newly metamor- rica. Vol I. Amphibians of the West African phosed smith frog, Hyla faber Wied. – Herpe- Savanna. – Frankfurt am Main (Edition Chi- tologica, 3: 47-472. maira).

Manuscript received: 27 March 2007 Authors’ addresses: José M. Padial, Ignacio de la Riva, Department of Biodiversity and Evolutionary Biology, Museo Nacional de Ciencias Naturales-CSIC, C/ José Gutiérrez Abascal 2, 28006 Madrid, Spain, E-Mail: [email protected]; José M. Barea-Azcón, Empresa de Gestión Medio Ambiental, Consejería de Medio Ambiente, Junta de Andalucía, C/ Marqués de la Ensenada, 4, 1C-D, E-18004 Granada, Spain; Luis García-Cardenete, Carrera de San Agustín, 32 2A, 18300 Loja, Spain.

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