SALAMANDRA 52(4) 328–336 30 December 2M01a6rtin IJSaSnNse 0n0 3et6 –al3.375 Temporal variation, duty cycle, and absolute calling effort during sustained calling of Leptodactylus mystacinus (Anura: Leptodactylidae) Martin Jansen1, Anastasia Masurowa1 & R. Bob O’Hara2 1) Senckenberg Research Institute and Nature Museum, Senckenberganlage 25, 60325 Frankfurt a.M., Germany 2) Senckenberg Biodiversity and Climate Research Centre, Senckenberganlage 25, 60325 Frankfurt a.M., Germany Corresponding author: Martin Jansen, e-mail: [email protected] Manuscript received: 17 December 2014 Accepted: 3 July 2015 by Jörn Köhler Abstract. We studied the within-night temporal call variation of Leptodactylus mystacinus using automated bioacoustic survey and pattern recognition techniques. Based on ca 50,000 detected calls we report on large-scale variation of domi- nant frequency, call duration, peak power, call interval, call period, and call rate. The “absolute” calling effort (as absolute seconds per hour spent on calling calculated as the sum of all detected calls during one hour) was between 165 and 716 s/ hour (535 ± 191) with a peak at around 23:00 h, followed by a decrease until the end of the calling period. This might be due to vocal fatigue. In comparison with literature, the overall call production was higher than expected, but calling effort is comparable to estimates from the literature for other leptodactylid frogs. We hypothesize that species-specific mating tactics might be employed to achieve high calling effort during sustained calling. Further intra- and interspecific studies should aim at studying contest behaviour in mating frogs to test this hypothesis. Key words. Amphibia, advertisement call, amplitude detection, automated bioacoustic survey, Bolivia, contest behaviour, sustained calling, overall call production. Introduction der & Nevo 1972, Gerhardt 1991, Bee & Gerhardt 2001, Bee et al. 2001, 2010, 2013, Marquez & Bosch 2001, Bee By using automated survey methods, scientists have to an 2004, Gasser et al. 2009, Rodriguez et al. 2010), as well increasing extent demonstrated that bioacoustics can be as on temporal calling variation of anurans (e.g., Bridg- used as a key tool in assessing and measuring biodiversity es & Dorcas 2000, Brooke et al. 2000, Todd et al. 2003, (Pijanowski et al. 2011, Depraetere et al. 2012, Gasc et de Solla et al. 2006, Wogel et al. 2006, Benevides et al. 2013). In taxonomy, many scientists use species-specific al. 2009, Jansen 2009, Llusia et al. 2013a,b, Ospina et al. animal communication signals for species delimitation, and 2013, Steen et al. 2013, Akmentins et al. 2014, Willacy et especially in frogs, where no learning effect of the acoustic al. 2015), however, only few studies exist on the individu- signal is known, descriptions of species-specific frog calls al temporal variation during sustained calling. For exam- are commonly included in species descriptions as diagnos- ple, Brepson et al. (2013) analysed in a laboratory study tic characters (e.g., Schneider et al. 1993, Heyer et al. 1996, on average 11,500 calls per individual emitted in one night Angulo & Reichle 2008, Lemmon et al. 2008, Moravec (in total more than 4.5 million calls from 36 males of Hyla et al. 2008, Padial et al. 2008, de Carvalho & Giaretta arborea) to study the management of calling under ener- 2013; see Schneider & Sinsch 2007 for a review). Hereby, getic constraints. frog calls have recently been used in combination with other Knowledge of the temporal variation in call traits might lines of evidence, such as morphology and DNA taxonomy, be relevant for taxonomists (e.g., for the delimitation of to discover morphologically look-alike cryptic species (e.g., species based on call traits) on the one hand. On the other, Glaw et al. 2010, Jansen et al. 2011, Funk et al. 2012, Pan- calling is the most expensive behaviour in the lifespan of sonato et al. 2013, Fouquet et al. 2014, Wang et al. 2014). a male frog (e.g., Taigen & Wells 1985, Wells & Taigen Regarding large-scale variation of frog calls, however, 1986, 1989), and information on the individual calling ef- only limited information is available. Although there is a fort is important for our understanding of sexual selection, huge body of literature on individual, intra- and interspecif- contest behaviour, or energetic trade-offs (Brepson et al. ic call variation (e.g., Schneider 1967, 1968, 1978, Schnei- 2013, Dyson et al. 2013). © 2016 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Mannheim, Germany A32ll 8articles available online at http://www.salamandra-journal.com Call variation in Leptodactylus mystacinus Here we use automated bioacoustic survey and pattern set up on the ground and connected to two omnidirection- detection methods to study sustained calling of the South al microphones, with one being about 1.5 m from the call- American frog Leptodactylus mystacinus. Besides testing ing frog. The recordings were automatically digitised at a techniques for the recording and analysis of large numbers sampling frequency of 22,050 Hz and 16 bit resolution. Re- of frog calls, the present study aims at providing informa- cordings were stored on 32 GB SD cards in .wav format. tion on individual and temporal call trait variation during We recorded from 22:00 to 6:00 h, resulting in a total of hours of sustained calling, and providing for the first time 480 minutes of recording. Temperature was recorded with data of the actual, i.e., calculated or “absolute”, calling effort the built-in temperature sensor and data logger of the Song per hour of a leptodactylid frog in the wild. Meter (measurements every 5 min). Leptodactylus mystacinus is a territorial frog that usually calls from entrances of small channels or caves in termite Material and methods mounds that are used for sheltering during the heat of the day (Jansen, own data). The advertisement call of Lepto­ Leptodactylus mystacinus (Fig. 1A), a frog of the L. fuscus dactylus mystacinus consists of a single note per call (see species group of the species-rich family Leptodactylidae, Fig. 2 for three typical calls) that are emitted continuously is distributed from southeastern Bolivia and eastern Bra- in long series, i.e., without being arranged in obvious call zil to Uruguay and through Paraguay to central Argentina bouts, at a call rate of 250–400 calls per minute (Heyer et (Frost 2014, de Sá et al. 2014). The advertisement call of al. 2003). Heyer et al. (2003) reported on a call duration Leptodactylus mystacinus was previously described from of 0.04–0.06 s and a dominant frequency (= fundamental populations in Argentina (Barrio 1965, de Sá et al. 2014), frequency) that ranged from 2050–2500 Hz. The focal spe- Paraguay (Heyer et al. 2003), and central Brazil (Oliveira cies is an ideal model system for studying the above men- Filho & Giaretta 2008). Jansen et al. (2011) stated that tioned questions, because the following reasons facilitate genetic and morphological data suggest that Bolivian pop- the automated detection of single signals by means of soft- ulations might be referable to an unnamed lineage, how- ware: (1) the frog has a rather simple call (unpulsed, simple ever, this could not be confirmed until now. structure), (2) it is a solitary, territorial species (and not a Our study site was near the Biological Station “Cen- chorusing frog), and 3) there is low ambient noise in its tro de Investigaciones Ecológicas Chiquitos” on the cattle preferred habitat (e.g., few or no other syntopic frog spe- ranch San Sebastián (-16.3622°, -62.00225°, 500 m a.s.l.), cies). Because the voucher was not collected, we identified 24 km south of the town of Concepción, Province of Ñuflo the species according to the call description given by (Hey- de Chávez, Santa Cruz Department, Bolivia. Currently, er et al. 2003). more than 40 species of frogs are known from this area Recordings were analysed on a personal computer using (Jansen 2009, Jansen et al. 2009, 2011, Schulze et al. the software Raven Pro v 1.4 (Bioacoustics Research Pro- 2009, 2011, own publ. data). gram 2011). Frequency information was obtained through Our recordings were made on 24 January 2012 with a Fast Fourier Transformation (FFT, width 256 points). Spec- weatherproof Song Meter SM2 digital audio field recorder trograms were obtained using the Hanning window func- (Wildlife Acoustics 2014) connected to a 12V car battery tion with 256 bands resolution. We filtered below 1,100 Hz as power source (Fig. 1B). After detecting a calling male and above 3,000 Hz to eliminate ambient noise. Using Lepto dactylus mystacinus in the field, the Song Meter was Ravens’ amplitude detectors (settings: amplitude threshold Figure 1. A) Male Leptodactylus mystacinus (not the specimen recorded herein) from the study area at San Sebastián, Department of Santa Cruz, Bolivia; B) call perch (termite mound) and recorder setup in the field. Photos: Martin Jansen. 329 Martin Jansen et al. Table 1. Definitions and calculation formulae of temporal characters measured for this study. Character Definition respectively calculation formula Unit of measure call period interval between the beginning of call n to the beginning ms of call n+1 instantaneous call rate (inverse of the interval between the beginning of call n 1/hour to the beginning of call n+1 [ms]) × 3600 instantaneous calling effort or call duty cycle call rate × call duration s/hour or dimensionless or (percentage as ratio of call duration/call period sound to silence) absolute calling effort per hour sum of all durations of calls that were emitted during s/hour one hour = 2500 units; smoothing = 0.046 s; delay compensation = ally, all of them were less intense (usually at the beginning 0.005 s), we automatically detected a total of 50,092 calls. of a new series) and thus were not detected by the software, From those, we deleted ca 600 false positives by choosing leading to a total of 49,573 calls for analysis. We assigned all selections with (1) durations far below the minimum dura- the calls to one individual, because we found the possibil- tion of the call, (2) relative peak amplitudes below the min- ity of callers switching unlikely. Leptodactylus mystacinus is imum peak amplitude of the call in our recording. Every bound to particular calling sites near a shelter and a switch case of a putative deletion was carefully checked manually. in calling males would most probably result in some kind In addition, we checked the whole recording visually for of male–male combat. However, all calls in our recording false negatives and additionally selected ca 100 calls manu- were continuously emitted (larger breaks in the series were Figure 2. Spectrogram (above) and corresponding waveform (below) of a typical section of three calls of Leptodactylus mystacinus. Taken from the recording analysed herein (San Sebastián, Department of Santa Cruz, Bolivia, 24 January 2012, 25–26°C). 330 Call variation in Leptodactylus mystacinus Table 2. Call parameters of a 194-min calling period (n = 49,573 Statistical analysis was performed in R (R Development calls) of one individual of Leptodactylus mystacinus from Bolivia. Core Team 2010, version 3.0.2). For smoothening the data to means of 5 minutes, we used the R package “Openair” Mean (± SD) (Carslaw & Ropkins 2012). To visualize audiospecto- grams and waveforms, we used the R package “Seewave” dominant frequency 2024–2282 Hz (2136±36) (Sueur et al. 2008). call duration 0.014–0.053 s (0.043±0.004) peak power 70.8–107.3 dB (103 re 1±2) call interval 0.085–56.564 s (0.192±0.482) Results call period 0.127–56.603 s (0.235±0.482) instantaneous call rate 64–28,347/hour (18,438±4073) Within the 480 min of recording, the frog was active for call duty cycle 2–1282 s/hour (796±191) 194 min and 10.9 s. Temperature varied from 25.1 to 25.9°C absolute calling effort 165–716 s/h (535±250.7) (25.5 ± 0.2) during the calling period (Fig. 3). During this period, we detected 49,573 emitted calls. Three typical suc- cessive calls are shown in Figure 2, and a typical five-minute lacking), no emitted territorial calls could be found dur- section is shown in Figure 4. Call parameters of this 194- ing the recording session, and the relative amplitude of the min calling period are shown in Table 2: We found an over- calls was constant throughout the recording. all dominant frequency of 2,024 to 2,282 Hz, a call duration For each call, we measured the following call parame- of 0.014 to 0.053 s, a peak power of 70.8 to 107.3 dB-1, and ters with Raven: dominant frequency (Hz, the frequency a mean call interval of 0.192 s (Table 2). In addition, we at which the maximum power is seen, taken for the entire measured a mean call period of 0.235 s, a mean instantane- call), call duration (s, time from the beginning to the end of ous call rate of 18,438 calls per hour, a mean call duty cy- the vocalization), and peak power (dB re 1 dimensionless cle of 796 s/h, and an absolute calling effort of 535 s/hour sample unit; in a greyscale spectrogram, the peak power (Table 2). is the power at the darkest point). We calculated the call There was a high variation in all of these values during period (interval between the beginning of call n to the be- one night (Figs 5A–D), and all values seem to be affected ginning of call n+1). Based on this measurement, we esti- by the time of the night. In dominant frequency, call dura- mated the instantaneous call rate (calls per hour) ([inverse tion and call duty cycle, there was an increase from 22:00 h of the interval between the beginning of call n to the be- to around 23:00 h, followed by a decrease to around mid- ginning of call n+1] × 3600), and the instantaneous call ef- night, and then a smaller second peak around 01:00 h and fort or call duty cycle (sensu Klump & Gerhardt 1992) as a decrease towards the end of the night. The absolute call the product of call rate and call duration (e.g., Taigen & effort (as the sum of all call durations during one hour) Wells 1985, Tarano & Fuenmayor 2014), respectively the varied from 164.9 to 715.9 s/h between hours, had a peak ratio of call duration to call period (e.g., Gerhardt et al. of activity around 23:00 h, and was followed by an overall 2000). In addition, we calculated the “absolute call effort” decrease (Fig. 5D). per hour, which we define here as an absolute measure- ment of time spent calling or seconds per one hour called (sum of all durations of calls that were emitted during one Discussion hour). See Table 1 for the definition and calculation formu- lae of measured temporal characters within this study. The specific characters of the advertisement call of Lepto­ dactylus mystacinus of this study (Table 2) agree well with those revealed by previous studies. According to literature, the advertisement call consists of a single, unpulsed note emitted at rates of 213 (Oliveira Filho & Giaretta 2008) to 250 to 400 calls per minute (Barrio 1965, Heyer et al. 2003, de Sá et al. 2014) (these equal 12,780, respectively 15,000 to 24,000, calls per hour). The values of call dura- tion in the literature vary: Heyer et al. (2003, as well as de Sá et al. 2014) reported on a call duration of 0.04–0.06 s, Oliveira Filho & Giaretta (2008) measured a call dura- tion of 0.04 s (n = 18 calls, three males, SD = 0), and Bar- rio (1965) gave a value of 0.10 s (without providing sample size or SD). Heyer et al. (2003) suggested that the high values given by Barrio (1965) could be due to over-record- ing or microphone ringing. Heyer et al. (2003) measured a Figure 3. Temperature during calling activity measured with the dominant frequency (= fundamental frequency) that rang- built-in temperature sensor and data logger of the recording de- es from 2,050–2,500 Hz [Barrio (1965): 2,200–2,500 Hz], vice (see text for details). without harmonics. Oliveira Filho & Giaretta (2008) 331 Martin Jansen et al. stated 2,239 Hz as dominant frequency, and a mean call in- to avoid vocal fatigue, a phenomenon that might be wide- terval of 0.18 s (n = 18 calls, three males, SD = 0.12). How- spread among species with high vocal activity during mat- ever, it has to be mentioned that Barrio (1965) and Heyer ing (Humfeld 2013, Pitcher et al. 2014). Our study found et al. (2003) did not give the sample size of analysed calls, a peak of calling effort during one nightly activity period and no sample size for each individual is given by Olivei- and most probably, because it is related to this (see below), ra Filho & Giaretta (2008) either. a peak in the metabolic rate at the same time. The decrease Even though species-specific, advertisement calls may towards the end of the night might as well be due to vocal exhibit considerable variability due to ambient temperature fatigue or body condition, or to a change in motivation for and individual body size (e.g., Zweifel 1959, 1968, Ger- some or other reason, however, this hypothesis needs to be hardt & Mudry 1980, Rodriguez et al. 2015; see reviews tested. As to how far such temporal variation or plasticity in Gerhardt & Huber 2001, Schneider & Sinsch 2007). of call traits (Castellano & Gamba 2011, present study) However, the influence of temperature and individual body might actually affect the practical use of frog calls by taxo- size on call traits can be ignored in our data set, because nomists for species delimitation has to be tested in future temperature hardly varied during that night (Fig. 3) and studies and should be analysed based on more data from body size of the studied individual was constant as well. different individuals and species. Instead, our results showed a significant influence of time Several studies have demonstrated that calling effort is on the variation in call traits. For example, the dominant a determinant of oxygen consumption in frogs (e.g., Hyla frequency deviated by about 12% from the mean during arborea: Brepson et al. 2013; Hyla versicolor: Taigen & the night, and call duration by 90% from the mean. Simi- Wells 1985, Wells & Taigen 1986; Dendropsophus micro­ lar to our results, Castellano & Gamba (2011) found that cephalus: Wells & Taigen 1989, Schwartz et al. 1995; call duration and pulse rate, both of which are commonly Engyostomops pustulosus: e.g., Bucher et al. 1982, Pough used as diagnostic characters in species descriptions, were et al. 1992; Pseudacris crucifer: Wells et al. 1996). How- variable during sustained calling of Hyla intermedia. They ever, although these studies suggest that calling is probably hypothesized that this might be due to different strategies the energetically most expensive activity in the lifetime of Figure 4. Spectrogram (above) and corresponding waveform (below) of a 5-minute section of calls of Leptodactylus mystacinus. Taken from the recording analysed herein (San Sebastián, Department of Santa Cruz, Bolivia, 24 January 2012, 25–26°C). 332 Call variation in Leptodactylus mystacinus a male frog (see also Pough et al. 1992, Prestwich 1994, unpulsed and single notes, with “note” being synonymous Wells 2001), practically nothing is known about the in- with “call”). The duty cycle of L. mystacinus found herein fluencing external (e.g., climate, social context) and inter- is slightly higher (mean 796 s/hour), and the absolute call- nal (e.g., metabolic rate, energy reserves, body condition) ing effort per hour is slightly lower (mean 535 s/h). Regard- factors of the absolute, i.e., not estimated, individual call- ing the absolute number of emitted calls (or notes) emitted ing effort in the wild (e.g., Schwartz et al. 1995, Dyson et during one night, our results are limited. Recording only al. 2013). For example, no absolute measurements of call started when the frog was detected (at 22:00 h), but this production or calling effort of other Leptodactylus spe- species usually already starts calling ca three hours earlier, cies in the wild have been recorded until now. However, namely approximately one hour after sunset (M. Jansen, Wells (2007, Table 5.2) compiled some estimates of the own data; in the present case around 19:00 h). Extrapola- duty cycle of selected frog species based on calling rates tion from the results of the present study (i.e., the detected and call duration from the literature, including one conge- 50,000 calls in ca three hours plus ca three hours of calling ner, Lepto dactylus fragilis (original data from Bevier 1995). with another 50,000) gives an estimate of around 100,000 According to Wells (2007), the duty cycle (estimated call- calls per night for this individual. Preliminary studies on ing effort per hour) of L. fragilis is 690 s/h, and the esti- another leptodactylid frog from Bolivia, L. syphax, revealed mated number of “notes” per night is 16,450 (as the call a mean absolute calling effort of 800–1100 s/h with 10,300 of L. fragilis is like the call of L. mystacinus composed of to 11,550 calls per night of one single male (M. Jansen, own Figure 5. Graphs showing variation in calls and calling activity of the recorded individual of Leptodactylus mystacinus during one night (A–C smoothened data, see text): A) dominant frequency [Hz]; B) call duration [ms]; C) call duty cycle or instantaneous calling effort [s/h]; D) absolute call effort per hour [s/h], shown for every hour. 333 Martin Jansen et al. data). Even higher absolute numbers of calls per night are tion system. – Journal of the Acoustic Society of America, 116: expected from a close relative of L. mystacinus: Cassini et 3770–3781. al. (2014) reported the call rate of L. cupreus as amounting Bee, M. A., J. M. Cook, E. K. Love, L. R. O’Brian, B. A. Pettitt, to 14 calls/s, which would result in 50,400 calls per hour, K. Schrode & A. Vélez (2010): Assessing acoustic signal vari- and – given that the frog calls continuously throughout 4 ability and the potential for sexual selection and social recog- to 6 hours – which amounts to an impressive number of nition in Boreal Chorus Frogs (Pseudacris maculata). – Etho- lo gy, 116: 564–576. 200,000 to 300,000 calls per night. However, all-night re- cordings of this and other species are needed to prove such Bee, M. A. & H. C. Gerhardt (2001): Neighbour-stranger dis- extremely high calling performances. Further, it can be hy- crimination by territorial male bullfrogs (Rana catesbeiana): I. Acoustic basis. – Animal Behaviour, 62: 1129–1140. pothesized that there might be species-specific mating tac- tics to achieve a high calling effort during sustained calling Bee, M. A., C. E. Kozich, K. J. Blackwell & H. C. Gerhardt (e.g., many short calls like in L. mystacinus versus fewer (2001): Individual variation in advertisement calls of territo- rial male green frogs, Rana clamitans: Implications for indi- but longer calls in L. syphax, own data). Nevertheless, far vidual discrimination. – Ethology, 107: 65–84. more data are needed to comprehensively rank and com- pare absolute calling efforts and mating tactics in selected Bee, M. A., R. Suyesh & S. D. Biju (2013): The vocal repertoire of Pseudophilautus kani, a shrub frog (Anura: Rhacophoridae) frog species (M. Jansen, in prep.). from the Western Ghats of India. – Bioacoustics, 22: 67–85. Data on the variation in the hourly, daily, or seasonal calling effort of individual frogs are important, because, Benevides, F. Jr., W. J. Mautz & M. Warrington (2009): A piece-wise linear model of sound pressure level of male Eleu­ e.g., “until such information is available, it will be impos- therodactylus coqui overnight chorus. – Herpetological Re- sible to construct reliable annual energy budgets” for frogs view, 40: 162– 65 (Wells 2007: 229). Field measurements of the absolute Bevier, C. R. (1995): Biochemical correlates of calling activity in calling effort are an indirect measurement of the metabolic Neotropical frogs. – Physiological Zoology, 68: 1118–1142. rate, and therefore could shed some light on the manage- ment and strategy of calling, their underlying principles Bioacoustics Research Program (2011): Raven Pro: Interactive Sound Analysis Software (Version 1.4). – The Cornell Lab of of physiological constraints and consequences for fitness, Ornithology, Ithaca, New York. Available at http://www.birds. as well as different evolutionary scenarios. Future studies cornell.edu/raven. should include long-term studies of individual frogs (e.g., Brepson, L., Y. Voituron & T. Lengagne (2013): Condition-de- from one year to another as suggested by Dyson et al. 2015) pendent ways to manage acoustic signals under energetic con- to study contest behaviour during mating season in the straint in a tree frog. – Behavioral Ecology, 24: 488–496. context of evolution and sexual and natural selection. Bridges, A. S. & M. E. Dorcas (2000): Temporal variation in an- uran calling behavior: Implications for surveys and monitor- ing programs. – Copeia, 2000: 587–592. Acknowledgements Brooke, P. N., R. A. Alford & L. Schwarzkopf (2000): Envi- Raffael de Sá provided additional information on call data of ronmental and social factors influence chorusing behavior in other populations of Leptodactylus mystacinus. 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