Acta Herpetologica 12(1): 95-101, 2017 ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah DOI: 10.13128/Acta_Herpetol-18731 The advertisement call of Pristimantis subsigillatus (Anura, Craugastoridae) Florina Stănescu1,4, Rafael Márquez2, Paul Székely3,4,*, Dan Cogălniceanu1,4,5 1 Ovidius University Constanţa, Faculty of Natural and Agricultural Sciences, Al. Universităţii 1, campus B, 900470 Constanţa, Roma- nia 2 Fonoteca Zoológica, Dept. de Biodiversidad y Biología Evolutiva. Museo Nacional de Ciencias Naturales (CSIC), José Gutiérrez Abas- cal 2, E-28006 Madrid, Spain 3 Universidad Técnica Particular de Loja, Departamento de Ciencias Biológicas, San Cayetano Alto, calle Marcelino Champagnat s/n, Loja, Ecuador 4 Asociación Chelonia, Str. Pașcani, nr. 5, București, 062082, Romania. *Corresponding author. E-mail: jpszekely@utpl.edu.ec 5 Universidad Nacional de Loja, CITIAB, Ciudadela universitaria La Argelia, EC 110101 Loja, Ecuador Submitted on 2016, 11th August; revised on 2016, 18th October; accepted on 2016, 26th October Editor: Adriana Bellati Abstract. We describe for the first time the advertisement call of Pristimantis subsigillatus from southern Ecuador. Our study provides a detailed quantitative characterization of the advertisement call of P. subsigillatus, filling a gap in our knowledge of this genus, the most speciose among vertebrates. Males called perched on vegetation 0.5-2.5 m above ground, always during mild rain. The advertisement call is composed of a single note with a duration of 63-80 ms, with an initial short pulse (3-10 ms) followed by a longer tonal component. Call rates ranged between 4-12 calls/ min. The dominant frequency varied between 2.02-2.82 kHz. Keywords. Advertisement call, Anura, Craugastoridae, acoustics. Vocalizations play an important role in the biology and evolution of anurans since acoustic parameters may encode information about species, sex, fitness, reproduc- tive availability, territoriality or distress (Gerhardt and Huber, 2002; Wells and Schwartz, 2006). Acoustic param- eters can be genetically and environmentally shaped, therefore deciphering the information within vocal reper- toires and analysing their variability in time and space is vital to tracing and understanding evolutionary patterns (Duellman and Trueb, 1994; Gerhardt, 1994; Cocroft and Ryan, 1995; Wells and Schwartz, 2006). Four main types of calls are currently described in anurans (Duellman and Trueb, 1994): advertisement, reciprocation, release and distress, and their functionality is relatively well known. Advertisement calls represent one of the most conspicu- ous and important components of anuran communica- tion, acting as a premating isolating mechanism and thus providing valuable data for phylogenetic studies (Cocroft and Ryan, 1995; Vences and Wake, 2007). With more than 470 species, direct-developing frogs of the genus Pristimantis make up for almost one third of the anuran species of Ecuador (Ron et al., 2011), and the genus is by far the most diverse among terrestrial verte- brates (Hedges et al., 2008; Frost, 2016). Species of the genus Pristimantis have a high phenotypic variability with- in populations and scant morphological differences among species (Crawford and Smith, 2005). This frequently causes misidentifications even in museum specimens (Padial et al., 2008). Advertisement calls can be a valuable tool in describing or distinguishing among species when morpho- logical characters are not sufficient in species identification (e.g., Köhler and Lötters, 1999; Reichle et al., 2001). 96 F. Stănescu et alii Pristimantis subsigillatus (Fig. 1) was described by Boulenger (1902) from Salidero, Esmeraldas Prov- ince, Ecuador and is considered a locally abundant spe- cies in western Ecuador and south-western Colombia at elevations of 100-930 m a.s.l. (Lynch, 1980; Lynch and Duellman, 1997; Frenkel et al., 2013). This species is encountered most frequently in forests, at night, perching on vegetation at heights of 0.6-10 m above the ground; males usually call during rainy nights from vegetation at 2-5 m height (Lynch and Duellman, 1997). The advertise- ment call was described by Lynch (1980) as a single sharp explosive ‘’tweet” or as “a single, clear, bell-like note”. However, to the best of our knowledge, there is no quan- titative characterization of these calls. Our paper provides the first quantitative description of the advertisement call in P. subsigillatus. DC recorded the advertisement calls of three P. sub- sigillatus males from Buenaventura Ecological Reserve, EL Oro Province, Ecuador (Table 1). Calls were record- ed with an Olympus LS-11 Linear PCM Recorder and a RØDE NTG2 condenser shotgun microphone, at 44.1 kHz sampling frequency and 16-bit resolution, in wav file format. Air temperature and humidity were measured with a data logger (Lascar Electronics, model EL-USB- 2-LCD, accuracy: ± 0.5°C; ± 5%). The three focal males were captured following the recording sessions after being photographed. The snout-vent length (SVL) was measured to the nearest 0.1 mm with dial callipers, and then the animals were anaesthetized with benzocaine, fixed with formalin 10% and preserved in 70% alcohol. The specimens were deposited in the amphibian collec- tion of Museum of Zoology of the Pontificia Universidad Católica del Ecuador (specimen ID is provided in Table 1). Following Toledo et al. (2015) recordings were depos- ited in Fonoteca Zoológica - www.fonozoo.com, at Museo Nacional de Ciencias Naturales (CSIC), Madrid, Spain (records ID are provided in Table 1). Individuals were identified as P. subsigillatus based on the characters described by Lynch and Duellman (1997), especially as having skin on dorsum finely shagreened, that of venter areolate, without dorsolateral folds, dis- coidal fold prominent, tympanic membrane and annu- lus evident, snout subacuminate in dorsal view, truncate or protruding in profile, snout bearing a small papilla at tip, canthus rostralis relatively sharp, upper eyelid lacking tubercles, outer fingers bearing broad discs, heel lacking or bearing very small tubercle and fifth toe much longer than the third (Lynch, 1980; Lynch and Duellman, 1997). Despite the fact that identification of Pristimantis species based only on morphological characters is challenging, we are confident that the recorded individuals belong to P. subsigillatus. We have conducted a thorough inventory of amphibians in the area and are familiar with the spe- cies found there (e.g., Székely et al. 2016), and P. subsig- illatus cannot be confounded with other species of the genus present based on morphological characters. At present, P. subsigillatus is not assigned to any spe- cies group after it was removed from the former, non- monophyletic, Pristimantis unistrigatus group (Padial et al., 2014). Pristimantis subsigillatus is most similar to P. nyctophylax from which it is distinguished by the absence Fig. 1. Male Pristimantis subsigillatus calling (Photo credit: José Seoane Rodríguez). Table 1. Information regarding the recordings used in this study. Air temperature = Temp; humidity = H; distance from the tip of the microphone and the focal male = Dist. Specimen ID/ FonoZoo ID SVL (mm) Coordinates Altitude (m) Date Time (h) Temp (°C) H (%) Dist (cm) QCAZ47284/ 9863-64 28.2 3°39’21.4”S 79°46’08.0”W 464 12 September 2014 23:00 - - 100 QCAZ62538/ 9865-66 26.1 3°39’16.9”S 79°46’34.8”W 453 08 September 2015 21:00 21 98 25 QCAZ62543/ 9867-69 - 3°39’07.0”S 79°45’43.6”W 600 14 September 2015 18:45 21 98 50 97Call of Pristimantis subsigillatus of observable tubercles on the eyelids and heels, presence of small terminal papilla at the tip of the snout, presence of numerous supernumerary plantar tubercles and of the inner tarsal tubercle. Additionally, the eye of P. nyc- tophylax is very distinctive in having orange or red sclera (Lynch and Duellman, 1997). Also, this species occurs usually at higher elevations (1140-2100 m a.s.l.) com- pared to P. subsigillatus. We used Raven Pro 1.4 software (http://www.birds. cornell.edu/raven) to analyse 54 advertisement calls. We measured the temporal parameters from the oscil- lograms and the spectral parameters from spectrograms obtained through Hanning function, at a window size of 1024 samples, and 50% overlap. We measured the dura- tion, rise time proportion, dominant frequency (Df ), and aggregate entropy (Entropy) of the calls and component parts. We computed rise time proportion, as the ratio between the period from the onset of the sound and the moment of maximum amplitude within the analysed call, and the call duration (Márquez et al., 2005). We also computed the dominant frequency modulation within a call (DfM) as the difference between the dominant fre- quencies of the two component parts (Márquez et al,. 1996). The aggregate entropy provides a measure of the overall disorder in the sound, by analysing the distribu- tion of energy in the spectrogram; zero entropy values characterize single pure tones, while higher entropy val- ues correspond to greater disorder in the acoustic spec- trum (Charif et al., 2010). Following Gerhardt (1991), we computed a coefficient of within-individual varia- tion (CV% = SD/mean X 100) in order to differentiate between static (CV% < 5) and dynamic (CV% > 12) call parameters. The three P. subsigillatus males were calling after sunset perched on leaves or branches up to 2.5 m above ground, during mild rain. In each case, several other males were calling in the background. The advertisement call was composed of a single note with two consecutive parts: an initial short pulsed part, followed by a longer tonal part with harmonics (Fig. 2). Call rates ranged Table 2. Quantitative description of P. subsigillatus advertisement calls. Mean ± SD (above the line) and min-Max values (below the line) are provided for all acoustic parameters analysed. n = call sample size, Df = Dominant frequency, DfM = Dominant frequency modulation. Specimen Measurement Duration (ms) Rise time (%) Df (Hz) DfM (Hz) Entropy (u) 47284 (n = 9) Call 80 ± 2.9 0.141 ± 0.177 2651.0 ± 19.9 435.5 ± 260.8 2.9 ± 0.3 77 - 85 0.01 - 0.43 2627.1 - 2691.7 -21.5 - 624.5 2.5 - 3.4 Part 1 7 ± 1.4 0.346 ± 0.186 2215.5 ± 273.9 5.0 ± 0.1 6 - 10 0.10 - 0.71 2024.1 - 2670.1 4.9 - 5.2 Part 2 73 ± 3.0 0.298 ± 0.097 2651.0 ± 19.9 2.6 ± 0.1 69 - 78 0.09 - 0.43 2627.1 - 2691.7 2.4 - 2.8 62538 (n = 15) Call 63 ± 0.9 0.025 ± 0.005 2584 ± 0 140.7 ± 124.5 2.4 ± 0.5 61 – 65 0.02 - 0.03 2584 0 - 430.7 1.5 - 3.1 Part 1 3 ± 0.5 0.443 ± 0.123 2433.3 ± 124.4 4.0 ± 0.1 3 - 4 0.33 - 0.67 2153.3 - 2584.0 3.6 - 4.2 Part 2 60 ± 0.8 0.073 ± 0.006 2584 ± 0 2.2 ± 0.5 58 - 61 0.07 - 0.09 2584 1.4 - 2.9 62543 (n = 30) Call 70 ± 3.0 0.016 ± 0.004 2822.3 ± 33.4 476.6 ± 202.3 2.6 ± 0.4 61 - 74 0.01 - 0.03 2756.2 - 2885.4 0 - 645.9 1.9 - 3.2 Part 1 7 ± 0.7 0.152 ± 0.046 2345.7 ± 201.9 3.8 ± 0.2 6 - 8 0.12 - 0.29 2239.5 - 2842.4 3.3 - 4.1 Part 2 63 ± 3.1 0.226 ± 0.163 2822.3 ± 33.4 1.9 ± 0.2 53 - 67 0.02 - 0.48 2756.2 - 2885.4 1.5 - 2.6 All (n = 54) Call 70 ± 6.1 0.378 ± 0.083 2727.5 ± 112.2 376.4 ± 242.4 2.6 ± 0.4 61 - 85 0.01 - 0.43 2584.0 - 2885.4 -21.5 - 645.9 1.5 - 3.4 Part 1 6 ± 1.9 0.265 ± 0.166 2351.1 ± 208.0 4.1 ± 0.5 3 - 10 0.10 - 0.71 2024.1 - 2842.4 3.3 - 5.2 Part 2 64 ± 5.2 0.198 ± 0.150 2727.5 ± 112.2 2.1 ± 0.4 53 - 78 0.02 - 0.48 2584.0 - 2885.4 1.4 - 2.9 98 F. Stănescu et alii between 4-6 calls/min (individual 47284) to 9-12 calls/ min (individuals 62538 and 62543). Descriptive statistics of the analysed acoustic parameters and their intra-indi- vidual variation are presented in detail in Tables 2 and 3. The first part of the note was composed of 2 to 4 pulse groups in individual 47284, while in the other two individuals it consisted of a single pulse group. In indi- vidual 62543, the pulse was bell-shaped (Fig. 2C). The second part of the note was always longer than the first, and had a harmonic structure, with the fundamental har- monic corresponding to the dominant frequency. The dominant frequency was higher in the second part and therefore the calls presented an upward frequency modu- lation pattern. Call duration, part 2 duration and domi- nant frequency showed low within individual variability (CV < 5%), and therefore can be considered static acous- tic parameters, useful in distinguishing among individu- als of the population. The first part of the call presented the highest acoustic variability. Our study provides the first detailed characterization of the advertisement call of P. subsigillatus, filling a gap in our knowledge of this poorly studied group. The calls described in this study are markedly different from the calls of Pristimantis eugeniae, P. nyctophylax and P. phoxo- cephalus which are considered similar species by Lynch and Duellman (1997). P. eugeniae has calls with a much higher dominant frequency (3400-3800 Hz) and lack the pulsed initial part of the call, P. nyctophylax has calls with lower dominant frequencies, around 2100 Hz. As for P. phoxocephalus, the recordings posted in Amphibia- WebEcuador show a high variation of dominant frequencies, from 1900 Hz to more than 3000 Hz, suggesting that maybe more than one taxon was included in these recordings. Advertisement calls are an important tool in describ- ing and characterizing anuran species, since they act as a premating isolating mechanism (Ryan, 1988). Based on detailed acoustic analyses, taxonomic relationships can be elucidated (e.g., Padial et al., 2008). As the most speciose vertebrate genus, Pristimantis species have been subject to taxonomic debates for a long time (e.g., Hedges et al., 2008; Padial et al., 2014). In August 2016, the total num- ber of Pristimantis species recognized was 480, of which 121 new species were described during the last decade only (Frost, 2016). Most descriptions do not include calls and are often based only on museum specimens. Recent reviews based only on molecular data could not shed light on the systematics of this genus (e.g., Hedges et al., 2008; Padial et al., 2014). In order to facilitate taxonomic work, this large genus has been subdivided into several species groups (Lynch and Duellman, 1997). There is a huge variation in the call parameters of the frogs within the genus Pristimantis (Padial et al., 2007), and acoustic parameters could prove to be an important tool in the revision of this genus. ACKNOWLEDGEMENTS The Secretaría de Educación Superior, Ciencia, Tec- nología e Innovación, Republic of Ecuador (SENESCYT) provided funding for Paul Székely and Dan Cogălniceanu through the Prometeo Project. The Jocotoco Foundation provided access to Buenaventura Forest Reserve. Florina Stănescu, Paul Székely and Dan Cogălniceanu received additional support from the SYNTHESYS Project. The SYNTHESYS Project is financed by the European–Com- munity–Research Infrastructure Action under the FP7 “Capacities” Specific Programme. Partial call analy- ses and call deposit were funded by project TATANKA (CGL2011-25062), Ministerio de Ciencia e Innovación, Table 3. Within-individual coefficient of variation of the analyzed acoustic parameters. n = call sample size, Df = Dominant frequency, DfM = Dominant frequency modulation. CV values < 5% are highlighted in grey (static parameters sensu Gerhardt, 1991). Specimen Measurement Duration Rise time Df DfM Entropy 47284 (n = 9) Call 3.6 125.5 0.8 59.9 10.3 Part 1 20.0 53.8 12.4 2.0 Part 2 4.9 32.6 0.8 3.8 62538 (n = 15) Call 1.4 20.0 0.0 88.5 20.8 Part 1 16.7 27.8 5.1 2.5 Part 2 1.3 8.2 0.0 22.7 62543 (n = 30) Call 4.3 26.6 1.2 42.4 15.4 Part 1 10.0 30.3 8.6 5.3 Part 2 4.9 72.1 1.2 10.5 99Call of Pristimantis subsigillatus Fig. 2. Oscillogram and spectrogram views of the advertisement calls of the three males of Pristimantis subsigillatus: specimen 47284 (A), 62538 (B), and 62543 (C). Spectrogram window size: 256 samples, 50% overlap, hop size 128 samples. 100 F. Stănescu et alii FCW (CGL2011-16159-E). We are grateful to Dr. Santi- ago Ron, Pontificia Universidad Católica de Ecuador for his support. 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