The Influence of Internote-Interval Variation of the Advertisement Call

Amphibia-Reptilia 28 (2007): 227-234

The inﬂuence of internote-interval variation of the advertisement call on the phonotactic behaviour in male Allobates femoralis (Dendrobatidae)

Mario Göd, Alexander Franz, Walter Hödl*

Abstract. Acoustic conspecific recognition depends on spectral and temporal call properties, but not all of these are necessary for species identification. To test the importance of the advertisement call’s internote interval of the dendrobatid frog Allobates (=Epipedobates) femoralis, we conducted field playback experiments with modified conspecific calls and investigated phonotactic responses. Allobates femoralis males showed positive phonotaxis when calls with internote intervals varying up to ±60% of the population’s mean were presented. No phonotactic approach was observed in response to modified advertisement calls containing internote intervals of the syntopic heterospecific leptodactylid frog Adenomera hylaedactyla. However, 26.7% of the A. femoralis males tested showed positive phototoxic when altered advertisement calls with internote intervals of the syntopic heterospecific dendrobatid frog Epipedobates cf. hahneli were presented. Our results show that only a combination of different acoustic call parameters provides correct species-specific recognition.

Introduction Pyles, 1983; Schwartz and Wells, 1984; Garcia- Rutledge and Narins, 2001). Nevertheless, even Beside the attraction of conspecific females as when the means differ, the distributions of mating partners, the function of male anuran the properties of different species’ calls often communication is the recognition of conspe- overlap (Fouquette, 1960; Duellman and Pyles, cific males (Wells, 1977; Rand, 1988; Ryan, 1983; Schwartz and Wells, 1984). 1988). Matching between conspecific calls and Males of the territorial dendrobatid frog Al- the auditory system of the receiver depends lobates (=Epipedobates) femoralis (sensu Zim- on multiple acoustic criteria (Gerhardt and mermann and Zimmermann, 1988; Vences et Huber, 2002), such as spectral, temporal calling properties or a combination of both. Not al., 2003) are known to exhibit distinct behav- all of these features have the same relevance ioural reactions in response to acoustic play- for conspecific recognition (Loftus-Hills and backs of conspecific calls at suprathreshold lev- Littlejohn, 1971; Schwartz, 1987; Gerhardt, els. Acoustic playback of A. femoralis adver- 1988; Gerhardt and Doherty, 1988; Gerhardt tisement calls in a Peruvian population at inten- and Huber, 2002). For species communicat- sities above 68 dB sound pressure level (SPL) ing syntopically and synchronically, calling pat- (re 20 µPa) measured at the conspecific fo- terns should provide correct species-specific cal male showed head and body orientation to- identification (Ryan, 1988). Various studies ward the sound source, and a zigzag approach have shown that advertisement calls of co- toward the broadcasting speaker (Hödl, 1982, occurring anuran species differed significantly 1987; Narins et al., 2003). This behavioural re- in the mean values of their acoustic proper- action provides strong evidence for perception ties (Fouquette, 1960; Duellman, 1967; Hödl, and recognition of acoustic stimuli. Therefore, 1977; Drewry and Rand, 1983; Duellman and playback experiments using manipulated natural and artificial advertisement calls are a pow- erful tool to study the importance of calling fea- Department of Evolutionary Biology, University of Vi- enna, Althanstrasse 14, A-1090 Vienna, Austria tures in question. *Corresponding author; e-mail: The advertisement call of the A. femoralis [email protected] populations in the central and eastern Ama-

© Koninklijke Brill NV, Leiden, 2007. Also available online - www.brill.nl/amre 228 M. Göd, A. Franz, W. Hödl zonian basin consists of four frequency modu- hylaedactyla) call from similar sites and partially overlap in lated notes each sweeping up in frequency be- their calling activity with A. femoralis (Hödl et al., 2004). tween 2.5-4.1 kHz (Narins et al., 2003; Hödl et Experimental design and playback experiments al., 2004). Playback experiments with frequen- cies within the range of heterospecifics were In order to determine the influence of internote-interval vari- tested by Hödl et al. (2004) and Amézquita et ation of the advertisement call of A. femoralis in eliciting phonotactic response, playback experiments with internote al. (2005) and partly evoked positive phono- intervals beyond the range of the natural signal were car- tactic approach in A. femoralis males. This re- ried out. The temporal and spectral parameters of the syn- sult demonstrates that frequency is not suf- thetic (i.e. standard) male advertisement calls were derived from the mean values of 15 males from the Arataï popula- ficient for discrimination between conspecific tion (fig. 1A). Allobates femoralis advertisement calls con- and heterospecific signals in male A. femoralis. sist of four notes and the means of the three internote in- Schlüter (1980) mentioned the inflexibility of tervals for this population are 50.2 ms, 96.2 ms and 43.9 A. ms, respectively (Narins et al., 2003). For a description of the patterning of notes per call of male’s other essential call parameters of A. femoralis see Narins femoralis advertisement calls. Although 34 anu- et al. (2003). The advertisement call of E.cf.hahneli con- ran species have been identified at the study site tains a long series of single notes per call with an average = Arataï (Lescure and Marty, 2000; Gottsberger internote interval of 156.4 ms (SE 6.7 ms) (fig. 1D). Adenomera hylaedactyla advertisement calls consist of a and Gruber, 2004), only males of Epipedobates single note as well, but call intervals are long and irregu- cf. hahneli (sensu Vences et al., 2003) and lar (mean internote interval 752.3 ms, SE = 168.2ms). Adenomera hylaedactyla exhibit partial over- Preliminary statistical analysis of advertisement calls of A. femoralis males (Arataï population) showed a natural lap of their calling-activity periods with A. internote-interval variation of ±25% (H. Gasser, personal femoralis (Hödl et al., 2004). Calls of these het- communication). Therefore, internote intervals were mod- erospecifics have distinct temporal patterns. The ified with the software CANARY¨ 1.2.4 by copy-pasting − − advertisement call of E.cf.hahneli consists of silence intervals using deviations from 60% to 30% and +30% to +60% on the three internote intervals by steps of a long series of single-note calls and A. hy- 10%. The absolute values of the internote intervals 1, 2 and laedactyla transmits single-note calls with long 3for−60% are 20.1, 38.5 and 17.6 ms; for +60% 80.3, irregular intervals. The temporal pattern of four 153.9 and 70.2 ms. In a given stimulus all intervals were identical. Other parameters of the advertisement call of male notes per call in A. femoralis could therefore A. femoralis remained unchanged. be a critical parameter and may provide infor- To answer the question whether observable reactions mation for recognition of species-specific sig- depend on conspecific internote intervals in A. femoralis males, playback experiments using standard A. femoralis nals. This prediction was tested in two ways, calls modified with heterospecific internote intervals of 1) by modifying the advertisement call’s inter- A. hylaedactyla and E.cf.hahneli were undertaken. The note intervals beyond the limits of the natural means of 50 intervals of the advertisement call of 11 E.cf. signal and 2) by presenting advertisement calls hahneli (fig. 1B) and of 20 intervals of one A. hylaedactyla (fig. 1C) were utilized as modified A. femoralis internote in- with internote intervals of the two co-occurring tervals. Additionally, playbacks of the natural advertisement species. call of male E.cf.hahneli (fig. 1D) from the Arataï population were used. Following observable behavioural changes were documented: head-body orientation, calling, and positive phonotactic approach. Materials and methods Trials were conducted under rainless conditions during the two daily calling activity peaks of male A. femoralis in Study area and study animals the morning and in the afternoon (Hödl et al., 2004). Air Field playback experiments were undertaken with 15 males temperature was measured immediately after each trial in the vicinity of the tested male and ranged between 23.6◦C of the territorial dendrobatid frog A. femoralis in the pri- ◦ mary forest near the field station at Arataï, French Guiana and 27.5 C. Acoustic stimuli were broadcasted exclusively (3◦59N, 52◦35W) at the beginning of the rainy season in to vocally-active territorial males. Individuals were not han- January 2004. The study site is located in a lowland wet dled prior to, during or after any trial. Once a calling male tropical forest (23 m a.s.l.), in which the mean annual rain- was located, a battery powered loudspeaker (Sony SRS- fall and temperature are 3000-3250 mm and 26◦C, respec- A47) was placed on the forest floor at a distance of about 2 tively. Only males of two other anuran species, one den- m to the frog facing the male under test. Synthetic calls were drobatid and one leptodactylid frog (E.cf.hahneli and A. randomly broadcasted at SPLs of 80 dB (re 20 µPa) from a Temporal call feature for acoustic recognition in Allobates femoralis 229

Figure 1. Advertisement calls with different internote intervals used for playback experiments. Bandwidth of analysis filter: 133.29 Hz. A. Four mean advertisement calls of male A. femoralis used as control stimulus (=0% internote-interval deviation). Above: spectrogram, below: oscillogram. B. Oscillogram of three modified advertisement calls of A. femoralis using internote intervals of E.cf.hahneli (156.4 ms). C. Oscillogram of one modified advertisement call and one note of the second advertisement call of A. femoralis using internote intervals of A. hylaedactyla (752.3 ms). D. Natural advertisement call of E.cf.hahneli, taken from a commercial CD (Marty and Gaucher, 1999). Above: spectrogram, below: oscillogram. 230 M. Göd, A. Franz, W. Hödl

CD player (Panasonic S1-SX320), approximately represent- P = 0.346) (fig. 2A), temperature (F1,141 = ing the level of naturally-calling conspecifics at an equal 0.54, P = 0.464) and SPL (F1,141 = 1.12, distance (Hödl, 1987). Each trial or stimulus contained 10 = bouts (consisting of 40 notes per bout) and 9 interbout in- P 0.291) on the linear approach speed. tervals. In general, a single test was counted as successful and stopped as soon as a male approached a radius of at Internote intervals of E. cf. hahneli, A. hylae- least 30 cm around the loudspeaker during the time set for dactyla and the natural call of E. cf. hahneli one trial. Trials in which males failed to approach the loudspeaker within the experiment time were counted as nega- The Friedman test indicated significant dif- tive, if the individual under test exhibited a positive phonotactic approach in a subsequent control trial performed with ferences in the behavioural reactions of A. the mean parameters of the population’s call (=0% devia- femoralis males to the three different advertise- tion of internote interval, standard call). For each successful ment calls (χ 2 = 20.48, P<0.0001, n = 64, trial the linear approach speed was calculated by dividing the linear distance covered by the time required to the loud- 15 males tested). Accordingly, we used the two- speaker. In order to reduce a potential proximity effect of tailed Wilcoxon two-sample test for the three the loudspeaker, reaching a point 30 cm from the speaker different calls to specify the differences. The be- was counted as a positive approach. In all male dendrobatid frogs tested by the authors, the phonotactic approach was an havioural reactions to the natural call of E.cf. all-or-none reaction. Thus, we consider the linear approach hahneli differed significantly from the reactions speed as the most relevant quantifyable territorial response. to the presentation of the artificial call using in- Further details on measuring linear approach speed in A. ternote intervals of A. hylaedactyla (Z = 3.88, femoralis are published elsewhere (Hödl et al., 2004). To minimize potential habituation, each male was tested a max- P = 0.0005) and E.cf.hahneli (Z =−3.72, imum of three times a day. P = 0.0005). No significant differences were found between the presentation of modified A. Statistical methods femoralis advertisement calls with internote in- Statistical tests were performed using SAS¨ 8.2 for Win- tervals of A. hylaedactyla and E. cf. hahneli dows. To determine the differences in the linear approach (Z =−0.59, P = 0.5554). speed for each internote-interval deviation, we used a mixed model to consider repeated measurements on one frog with Presentation of the modified A. femoralis the variables temperature, SPL (re 20 µPa) (normalized for standard call with internote intervals of E.cf. 1 m) and internote-interval deviation. To compare the be- hahneli (n = 30, 15 males tested) caused posi- havioural reactions of the tested A. femoralis males to playbacks of the three different advertisement calls (A. femoralis tive phonotaxis in eight males (26.7%; fig. 3). advertisement call with internote intervals of E. cf. hahneli, Furthermore, a mixed model analysis showed A. hylaedactyla and natural call of E. cf. hahneli) for signif- no significant difference between the linear ap- icance, we used a Friedman test. The behavioural reactions proach speed of these trials (fig. 2B) and the to the different advertisement calls were coded as follows: 0, no observable behavioural change; 1, head-body orien- linear approach speed of the trials using the tation; 2, calling; 3, positive phonotactic approach. If the standard stimulus (F1,38 = 1.92, P = 0.172; Friedman test yielded significant differences, then a com- fig. 2A). Calling was observed in 13 (43.3%) parison was done with a two-tailed Wilcoxon two-sample test. A significance level of P<0.05 was applied to all and head-body orientation in three (10%) males, tests. respectively. Six individuals (20%) did not react to the presented call (fig. 3). Tests (17 trials, 15 males tested) using the Results standard A. femoralis call with internote intervals of A. hylaedactyla elicited calling in 14 Internote-interval deviations of the advertise- males (82.3%) and head-body orientation in one ment call of A. femoralis male (5.9%). Two individuals (11.8%) did not With the exception of six trials, we observed react to the call (fig. 3). positive phonotactic responses in all playback However, natural calls (17 trials, 15 males trials (n = 167, 15 males tested; fig. 2A). Mixed tested) of E.cf.hahneli did not cause any ob- model analysis revealed no significant influence servable reaction in 11 individuals (64.7%). In of internote-interval deviation (F8,141 = 1.13, only two males tested (11.8%) could calling Temporal call feature for acoustic recognition in Allobates femoralis 231

Figure 2. Box plots representing the medians of the linear approach speed of A. femoralis males during playback experiments. Boxes indicate the middle interquartile ranges (50%), horizontal lines represent median values, vertical lines extend to the smallest and largest values of the distribution. Open circles represent outliers and stars extremes. The number of executed tests for each stimulus is indicated above the box plots. A. Analysis of A. femoralis advertisement calls with internote-interval deviations from −60% to −30% and +30% to +60%. The light grey bar shows the distribution of the A. femoralis internote- interval variation at the study site. B. Modiﬁed A. femoralis calls using internote interval of E.cf.hahneli.

Figure 3. Proportion of A. femoralis males that responded to the playback of the three different call stimuli. The number of tests for each stimulus is indicated to the left of the bars. 232 M. Göd, A. Franz, W. Hödl be stimulated. Head-body orientation was ob- species. Responses at the upper end of possi- served in four individuals (23.5%; fig. 3). ble internote-interval variation might be limited by stabilizing selection of the occurrence of the nearest co-occurring heterospecific. Discussion Our results additionally corroborate the observations of other playback studies recently With the exception of six negative cases, pos- A. femoralis itive phonotaxis was observed in all tests per- undertaken on male in the field formed with internote-interval deviations be- (Amézquita et al., 2005; A. Vélez and A. yond the limits of the natural A. femoralis call. Amézquita, personal communication). For a Additionally, the linear approach speed as an in- population of A. femoralis at Leticia (Columbia) dicator of signal attractiveness and localization it could be shown that playback experiments us- efficiency did not differ significantly when calls ing a frequency range beyond the natural vari- with internote-interval variations up to ±60% ation but within the range of the co-occurring of the population’s mean were presented. Un- dendrobatid frog E. trivittatus evoked positive changed linear approach speeds under differ- phonotactic response (Amézquita et al., 2005). ent stimuli corroborates the all-or-none reaction The same was observed when calls with note of A. femoralis males towards both natural and duration or internote intervals beyond the nat- (frequency-) manipulated signals in the field ural range of A. femoralis and within the range (Hödl et al., 2004). However, positive phono- of E. trivittatus were offered (A. Vélez and A. tactic responses of male A. femoralis to modi- Amézquita, personal communication). Further- fied advertisement calls with internote intervals more, A. femoralis males also phonotactically of up to −60% were surprising, since responses approached the sound source, when pure tone at the lower end should be limited by the refrac- bursts or frequency modulated notes sweeping tory period of neurons in the auditory periphery, down in the range between 2.5-4.1 kHz were causing a lack of sound resolution at short inter- presented with the natural temporal call pat- vals (Gerhardt and Huber, 2002). tern (Hödl et al., 2004). Our results and those We also observed that temporally modified of other studies of the male A. femoralis call advertisement calls of A. femoralis with inter- indicate that manipulation of one acoustic fea- note intervals of E.cf.hahneli caused posi- ture up to the closest heterospecific value still tive phonotaxis in 26.7% of the cases. Again, may cause positive phonotaxis, suggesting that no significant difference in the linear approach only a combination of spectral and/or tempo- speed between positively reacting individuals ral call parameters allows correct discrimination to E. cf. hahneli internote intervals and indi- against heterospecifics. Both sexes of the three viduals reacting to the control stimulus was co-active species studied forage unhindered by detected. However, no phonotactic approach homo- and heterospecifics for food (ants, mites was observed using advertisement calls of A. and collembola) on the ground in the leaf lit- femoralis modified with internote intervals of ter. Thus, territoriality between heterospecifics A. hylaedactyla, even though in 82.5 % of is not based on competition for food, but justi- the tested individuals calling could be stimu- fied in competition for acoustic space and most lated. Ryan (1988) hypothesized the stabiliz- likely oviposition sites. ing effect of the presence of heterospecifics on The behavioural reactions of A. femoralis the evolution of the advertisement calls in a males to the natural calls of E. cf. hahneli dif- given species. With a mean internote interval fered significantly to all other tests performed. of 2.4 times that of A. femoralis, E. cf. hah- The frequency of all A. femoralis advertisement neli exhibits internote intervals that are closest calls modified by internote intervals of A. hy- to A. femoralis among the acoustically co-active laedactyla and E. cf. hahneli ranged within the Temporal call feature for acoustic recognition in Allobates femoralis 233 average of the A. femoralis population. Thus, be minimized by clear discrimination against the modified broadcasted calls differed exclu- heterospecifics. Under natural conditions we sively in their temporal structures. In the tests could not observe calling inhibition in male A. with modified calls playing back heterospecific femoralis induced by E.cf.hahneli calls. De- internote intervals, A. femoralis males contin- spite the fact that the three anuran species at ued calling after the onset of modified call trials. our study site live syntopically and are partially This behaviour, however, changed significantly calling synchronically they show different activ- when the natural call of E.cf.hahneli,i.e. ity peaks and use different microhabitats. These adding the spectral component of this species to observations suggest that in addition to the vari- its temporal pattern, was presented. In most of ation in spectral and temporal call patterns dif- the cases, playbacks of unmodified calls of E. ferent activity peaks as well as microhabitat dif- cf. hahneli caused no observable reaction in A. ferences may serve to minimize potential het- femoralis males. erospecific interference. Playback experiments with unmodified E. cf. hahneli calls were intentionally performed on the ground, the microhabitat of A. femoralis. Acknowledgements. We thank the Association Arataï and especially P. Gaucher for the generous assistance with this Male A. femoralis call from slight elevations project. H. Gasser provided data for synthesizing the play- above ground or in the leaf litter, whereas E. back signals. We are grateful to F. König for statistical as- cf. hahneli males were often found hidden in sistance. We thank A. Amézquita, P.M. Narins, A. Penkner, C. Zierhut, M. Denoël and two anonymous reviewers for the centres of palm trees (Astrocaryum para- helpful comments on earlier versions of the manuscript. Fi- maca) or on adjacent structures up to 2 meters in nancial support was granted from the Bureau of Interna- height. Therefore, performing the experiments tional Affairs, University of Vienna and the Austrian Sci- on the ground by-passes the natural microhabi- ence Foundation (FWF-15345). tat differences of the two species. Calling inhibition under these circumstances indicates that the References heterospecific background noise of E. cf. hahneli interferes with conspecific communication Amézquita, A., Castellanos, L., Hödl, W. (2005): Auditory of A. femoralis males in spite of the fact that matching of male Epipedobates femoralis (Anura: Den- drobatidae) under field conditions. Anim. Behav. 70: there is no overlap in spectral characteristics. 1377-1386. Our observations are in accordance with Drewry, G.E., Rand, A.S. (1983): Characteristics of an other published studies for which heterospecific acoustic community: Puerto Rican frogs of the genus Eleutherodactylus. Copeia 1983: 941-953. call playback causes calling suppression. For Duellman, W.E. 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