HERPETOZOA 29 (314): 17s - l8l t75 Wien, 30. Jänner 2017
First evidence of sound production in the genus Iberolacerta ARRTBAS, 1997 (Squamata: Sauria: Lacertidae)
ErsterNachweis einer ti$äl3#ä: Annrees, Iee7 3;L*;i f:Hfuf;-tacerta
RoeeRro Gancie-Roe & Drpco Lrusm & Pnen Löpnz & JosE MARTIN
KURZFASST'NG
.I-aytäuße_ryp99 spielen eine Schlüsselrolle in einer Vielzahl von Interaktionen zuvischen artgleichen und -verschiedenen Individuen. Doch im Vergleich mit anderen Sinnesleistungen wird der Akustik bei Feptilien nur wenlg Aufinerksamkeit geschenkt. Innerhalb der Lacertidae wird Fehlen und Vorhandensein von Lautäußerungen als ein U-nterscheidungsmerkmal zwischen den Unterfamilien Gallotinae und Lacertinae angesehen, wobei letztäre, höchst diverse Unterfamilie als mehrheitlich nicht stimmbegabt betrachtet wird. Mit Hilfe von Bild- und lonaufzeichnungen berichten die Autoren erstmals über die Lautäußerungen bei Iberolacerta cyreni (Mürrrr. & HELLMIcH, 1937), einer europäischen Felseidechsenart. Tonaufnahmen eiies Ex- emplars.im Freiland geben kurze nasale quietschende Laute *ieder, die hinsichtlich des Mechanismus der Schall- qrgdyktlo1 und der,akustischen Merkmale Ahnlichkeit mit den Lauten nahe verwandter Lacertidenarten zeigen. Die funktionale Bedeutung derartiger Lautäußerungen ist unklar, doch weisen die akustischen Merkmale und'der Verhaltenskontext aufdie_Möglichkeit eines bei Gefahr abgegebenen Schreckrufs hin. Die vorliegenden Beobach- tungen lasserr vermuten, daß sich die Fähigkeit zur Lautproduktion bei verschiedenen systematisclen Gruppen der Halsbandeidechsen entwickelt hat und, auch wenn selten eingesetzt, weiter verbreitet ist als erwartet.
ABSTRACT
Sound_production plays a key role in a broad range ofanimal interactions among both conspecifics and het- 91ospe9ificg. Yet less attention has been paid to acoustic communication in reptiles thän to other iensorial modal- ities. WithinLacertidae,thepresenceorabsenceofvocalbehaviorhasbeenröfenedasadistinctivetraitbetween their two subfamilies Gallotinae and Lacertinae, being the latter the most diverse group of lacertid lizards and con- sidered to be mainly silent. _ Usingimage and sound recordings, the authors report for the first time the ability to sound production in a European rock lizard species. Recorded sounds of a free-ranging female of the Carpetan Rock L izird Iberolacerta cyreni (MisrrF]. & HBU-vrcr, 1937),were short nasal squeak-like sounds showing ä similar production mechanism and acoustic characteristics to_ sounds emitted by closely related lacertid speciesl Functionäl significance of such a sound activity is unclear, although its acoustic characteristics and behavibral context point ouithat these sounds might function as distress calls. The present findings suggest that the ability to sound production might have er'rolved at different systematic groups across lacertid lizards and, even if spoiadically usöd, is more wiäespread than previously expected.
KEYWORDS
__ _Reptilia: Squamata. Sauria: Lacertidae; Iberolacerta cyreni;behavior, acoustic communication; distress calls; lizard vocalization; Iberian Peninsula
INTRODUCTION
Sound enables animals to convey in- (Snancv & Nowrcrr 2005). In some condi- formation to conspecifics and heterospe- tions, acoustic cues are more efficiently cifics in a wide array of social interactions propagated and detected than those from and encounters, including mate choice, ter- other sensorial modalities (RosnNruar- & ritorial defense, or antipredator responses RvaN 2000). Moreover, they are also used R. GARciA-RoA & D. LLUSIA & P. L6pBz & J. MARTiN
together with other cues in multimodal sig- vocalizations in the subfamily Lacertinae, naling, particularly in agonistic or aggres- the most diverse group of lacertid lizards, sive behavior, to enhance receivers'respon- with 19 genera and approximately 100 siveness (NenrNs et al. 2003). species, have been scarcely recorded, and In reptiles, less attention has been correspond to only a few species (BöHIrln et paid to acoustic communication than in al. 1985; Ounoren 1990). other groups or to other sensorial modali- Here, the authors report the first evi- ties, such as visual and chemical communi- dence of sound production in the Archaeo- cation (FnaNKENBERG & WsnNen 1992; lacerta group sensu lato, one ofthe histori- ManriN & Löprz 20 14; Wrrr-rs er al. 2014). cal species groups within Lacertinae. Crocodiles, geckos, and some species of Image and sound recordings, provide a lizards are known to vocalize during repro- detailed acoustic characteization of sounds ductive season, aggressive interactions or emitted by a free-ranging Carpetan Rock distress behavior (FneNxrNnrnc & WEn- Lizard Iberolacerta cyreni (MünEn & Npn 1984; Hreerrrs et al.200l; VERGNE et Hprrvrrcn, 1937), as well as a description al. 2009). Within lacertid lizards (Lacer- of sound production mechanism, behavior, tidae), the ability to sound production has and context. The functional significance of traditionally been referred as one of the such a sound activity is discussed. To the behavioral traits separating its two subfam- best ofthe authors'knowledge, no record- ilies (Serveron & Pr-ecuEZUELos 2013). ings ofEuropean rock lizards (Iberolacerta Lizards belonging to the subfamily Gallo- spp.) nor lizards within the Archaeolacerta tiinae, which comprises two genera and 16 group s. lat. are available to date, despite of species (PvnoN etal.2013), are able to pro- the increasing interest aroused in their duce sounds in inter- and intra-specific behavioral ecology and evolution (ManriN interactions (Böhme et al. 1985). However, 20ts).
MATERIALS AND METHODS
Iberolacerta cyreni is a medium-sized ST23i, Tokyo, Japan) was obtained at a dis- lizard, endemic of Sistema Central, the cen- tance of around 1.5-2 m from the subject. tral mountain range of the Iberian Pen- Subsequently, an audio file (48 kHz, l6-bit) insula, where it inhabits rocky highlands was extracted from this recording with near the treeline (> 1,700 m a.s.l.). This YLC 2.0.6 (Video LAN, Paris, France) and species belongs to European rock lizards, analyzed with Raven 1.4 (Cornell Uni- which were historically included in Ar- versity, Ithaca, USA). For each sound, a chaeolacerta group ,r. /al. (CamaNzd. et al. total of 10 acoustic parameters were meas- 2004). ured using both oscillogram and spectro- In May to September 2014, adult indi- gram: 5 in the temporal domain and 5 in the viduals were captured in the "Cerro Del spectral domain (Table l). Spectral param- Tel6grafo" (23"10' 12"N, 102'53' 19"W Si- eters were calculated through a fast short- erra de Guadarrama, Spain) to gain behav- term Fourier transform (FFT) set at a length ior and morphology data. During subse- of 512 points with 90 oÄ overlap between quent release of individuals (August 7, successive Hanning windows, providing a 2014), a free-ranging female basking on a resolution of 135 Hz ar'd 10.6 ms. Band- rock immediately began to emit serial stop frequency filter (0-0.3 kHz) and peak sounds upon the observer's approach. After normalization (100 Yo) were applied with three series of sound production, the speci- Raven 1.4 to the audio recordings before men fled and hid in an underground refuge. parameter measurements. The R package During this activity, images of the focal "seewave" was used to create visual repre- individual were taken (Canon 450D, lens sentations of a characteristic sound (Sueun 18-55 mm) and a 22 second digital film re- et al. 2008). cording (MPG4 format, Sony Xperia Miro Sound production in lberolacerta cyreni t'77
Table 1: Description of acoustic parameters measwed in a vocalizing female of lberolacerta cyreni (MüLLER & Hnr-rurcH, 1937). Hz - Hefiz,s - seconds. Tab. 1: Beschreibung der bei den Lautäußenrngen eines Weibchens von lberolacerta cyreni (Mürrnn & Hru-rr.ricn, 1937) untersuchten akustischen Meßgrößen. Hz -Hertz, s - Sekunden.
Parameter Description of the measurement / Meßwertdefinition
Note duration (s) / Time (s) from the onset to the end of one sound, as shown in an oscillogram Rufdauer (s) Zeit (s) vom Beginn bis zum Ende des Rufs wie im Oszillogramm angezeigt Inter-note interval (s) / Time (s) from the end ofone sound to the onset oftle next sound Rufintervall (s) Zeit (s) vom Ende eines Rufs bis zum Beginn des folgenden Rufs Rise duration / Time (s) from the onset to the point of the maximum amplitude of one sound Anstiegszeit (s) Zeit (s) vom Rufbeginn bis zum Zeitpunkt der maximalen Rufamplitude Fall duration (s) i Time (s) from the point of the maximum amplitude to the end of one sound Abfallzeit (s) Zeit (s) vom Zeitpunkt der maximalen Rufamplitude bis zum Rufende Rise ratio (%) / Percentage (%) ofrise duration relative to note duration Anstiegsverhältnis (%) Anteil (%) der Anstiegszeit an der Rufdauer Dominant frequency (Hz) / Frequency (Hz) at which sound energy ofone sound is maximum Dominante Frequenz (Hz) Jene Frequenz (Hz) eines Rufs mit der maximalen Schallenergie Fundamental frequency (Hz) / Frequency (IIz) ofthe lowest harmonic ofone sound Grundfrequenz (Hz) Die tiefste Frequenz (Hz) im harmonischen Frequenzgemisch eines Rufs Maximum frequency (Hz) / Frequency (Hz) of the highest harmonic of one sound Ma.ximalfrequenz (Hz) Die höchste Frequenz (Hz) im harmonischen Frequenzgemisch eines Rufs Number of frequency bands / Total number of frequency bands in one sound Frequenzbandzahl Die Gesamtzahl der Frequenzb?inder eines Rufs Frequency modulation (Hz) / Difference in dominant frequency (Hz) between the first and the last 10 % Modulation der dominan- section of one sound / ten Frequenz (Hz) Differenz in der dominanten Frequenz der ersten und letzten 10 % des Rufs
RESULTS
The sound emitted by the I. cyreni ed of series of short nasal squeaks emitted in female was produced with open mouth and bouts of3-7 notes. These squeaks were sin- comprised two major phases, according to gle pulsed notes with a mean duration of video analysis: (i) abrupt air expiration by 122 ms that were repeated each 6.4 s on rapid thoracic compression of lungs at the average (Table 2 and Fig. 2). Most of the time of mouth opening, followed by an (ii) sound energy was produced at the very up and backward movement of the head at beginning ofthe note and then progressive- right angle to the ground, thorax relaxation, ly decreased across the emission. Thereby, and mouth closure (Fig. 1). Sounds consist- sound amplitude peaked after only an aver-
Table 2 : Descriptive statistics including mean a standard deviation, ranges and sample size of ten parame- ters of the sonnds produced by a female of lberolacerta cyreni (Mürrnn & IfurrvrcH, 1937).Hz-HerIz, s - ieconds. Tab. 2: Beschreibende Statistiken (Mean Mittelwert, SD - Standardabweichung, range - Spannweite, N Stichprobenumfang)vonl0KenngrößenjenerLaute,dievoneinemWeibchenvonlbirolacärtacyreni(Mür- I-Bn & Hru-utctt, 1937) prodliert wurden. Hz -Hertz, s - Sekunden.
Parameter Mean + SD (range, /y')
Note duration (s) / Rufdauer (s) 0.122 + 0.035 (0.163-0.096, 3) Inter-note interval (s) / Rufintewall (s) 6.415 + 1.022 (7.138-5.692,2) Rise duration (s) /Anstiegszeit (s) 0.011 + 0.007 (0.02-0.005,3) Fall duratior (s) i Abfallzeit (s) 0.111 + 0.029 (0.143-0.036, 3) Rise ratio (%) / Anstiegsverhältnis (%) 9.091 + 4.009 (12.269-4.587,3) Dominant frequency (Hz) / Dominante Frequenz (Hz) 2937 .5 + 47 I .864 (337 5 .0-2437 .5 , 3) Fundamental frequency (Hz) / Grundfrequem (Hz) 1000 + 286.410 (1312.5-750.0,3) Maximum frequency (Hz) / Maximalfrequenz (Hz) 9563.9 + 879.958 (10435.0-5732.4,3) Number offrequency bands /Anzahl der Frequenzbänder 5 Frequency modulation (Hz) / Modulation der dominanten Frequenz (Hz) 1000 + 943.729 (1875.0-0.0, 3) R. GARciA-RoA & D. Lruslc & P.Löpez & J. MARTfN
age of ll ms (< l0 oÄ of rise ratio). The o spectral structure of the vocal sound is char- acteized by the presence of several fre- 8! quency bands, starting at 1.0 kHz, a discrete Elo otr frequency modulation, and 3.0 kHz of dom- Sound activity lasted oeoo.i inant frequency. around two min during which three series of 6o squeaks were uttered. Inter-series interval .d 806 was longer than duration of the series and ae6o.J: the subject allocated such pauses to change its position before restarting sound produc- toE tion. iEisad dox DISCUSSION !'- ! 6bE This study provides the first evidence o€-E !-e of sound production in a species belonging s'äd to the genus lberolacerta. Image and sound .EEI female L oa >H recordings of a free-ranging of €59os 60 cyreni suggest that the ability to sound pro- cEe duction might have evolved at different tax- :9iö ,Ji äo onomic groups across lacertid lizards and is ddE more widespread than previously expected. o.= 6 6€e Vocal behavior had hitherto been observed -oö0 and reported in four genera of the subfami- idk ly Lacertinae, namely Meroles, Zootoca, Lacerta, and Podarcis (Bötttrln et al. 1985; OusorBn 1990), in addition to Gallotia and oö.,tro o€ Psammodromzs within the subfamily Gallo- *g\ i=v tiinae. Nevertheless, acoustic cornmunica- tion seems to be sporadic in Lacertinae, ':ob C =Ev= o while it is a well-established behavioral trait .-l> Gallotiinae. $-,cs90 in b.EE Sounds emitted by L cyreni were t53B..-i d squeakJike sounds showing similar acoustic N oi{ features to sounds emitted by several closely söF related lacertid species. For instance, Pod- !Ar e56 arcis siculus (RerrNesqur-Scrnraarrz, I 8 I 0) o9r has been found to also produce brief o6l squeaks, slightly shorter (0.07 t and lower E 9O in frequency (0.2-2.2ffi2kL{z) than those -olY o{ d EES ;98.9go =A-ögE Abb. I (linke Spalte): Schallproduktion bei einem o.a I Weibchen von 1öerolacerta cyreni (Mürtlr. & Ed! Hnlurcn, 1937) aus der Sierra de Guadanama, io=a Madrid, Spanien. Drei aufeinanderfolgende Phasen ad sind dargestellt: A- Entspannungsphase vor der ..o Lautabgabe; B - plötzlicher Luftausstoß aus den rasche des bö Lungen durch Kontraktion Brustkorbs bei ü geöffiretem Maul; C -Aufivärts- und Rückwärts- bewegung des Kopfes, rechtwinkelig zur Unterlage, Entspannung des Brustkorbs, Schließen des Maules. Sound production in Iberolacerta cyreni 179
.oca 30 €15 E 30 .E -1s Cd 6ü -30
10 +N I o () ()d t! 0 0.00 0.10 0.15 0.25 0.30 Time (s) ca 20 () 10 0 q -10 E -20 -30 -40 üo -50
Frequency (kHz)
Fig. 2: A Oscillogram (above) and sound spectrogram (below), and B - power spectrum (512 points of FFT size, 135 Hz bandwidrh,90% overlap, and Hanning window) ofa sound uttered by a female of lberolacerta cyreni (Mürtrn & HELLMTcH, 1937). Abb. 2: A - Oszillogramm (oben) und Audiospektrogramm (unten) sowie C Energie.spektrum (Länge der schnellen Fourier-Transformation: 512 Sttitzstellen, Bandbreite 135 H2,90 % [,herlappung, Hanning Fenster) der Lautäußerung eines Weibchensvon Iberolacerta cyreni (MüLLER & Hrllvtcu, 1937).
of I. cyreni (Ounornn 1990). In contrast, recorded squeaks of I. cyreni (Böuvr et al. most of the species of the subfamily Gal- 1985). Among the variety of sounds uttered lotiinae, e.9., Psammodromus algirus (LtN- by lizards, these from I. cyreni and other NAEUS, 1758), P. hispanicus FItzrNGtR, squeak-like sounds, such as those of some 1826, and several Gallotia species exhibit Ano lis species (CuzusrrNseN-Dalscnann & markedly longer notes (0.1-1.8 s), often MeNrpy 2005; MrrroN & JENssEw 1979), reaching high and broad-banded frequen- largely converge in acoustic properties. cies (up to 16 kHz), in comparison to the Moreover, the sound production mechanism R. GARciA-RoA & D. Lrusn & P.LbpBz & J. MenriN
in L cyreni seems to be closely associated groups (ManriN 2015) and hence these with that described in other lizards (GaNs & iounds were unlikely alarm calls addressed MarnnsoN 1973). to off-guard conspecifics. Many sounds Specific investigations are required to produced by other lacertids have been inter- conclusively determine the functional sig- preted as antipredator responses aimed at nificance of the observed sound activity, deterring aggression or warning risk. Pod- although some insights may be gained by arcis siculus emits squeaks when handled, examining its characteristics and behavioral although also in free-ranging conditions context. On the one hand, sounds produced (Ounorrn 1990). Moreover, species of the by I. cyreni might correspond to vocaliza- subfamily Gallotiinae have been observed tions or communication signals directed to, to produce acoustic signals in agonistic for instance, a potential predator. Their encounters with both conspecif,rcs and het- temporal and spectral structure, character- erospecifics, even though their functions are ized by short rise time and one-way fre- poorly known. On the other hand, sounds quency modulation, is consistent with a produced by L cyreni might also correspond widespread acoustic pattem of animal alarm io non-communicative airborne sounds and distress calls (Wu-l-ts et al. 2014). Since emitted as by-products of other biophysical they were recorded in close proximity of a phenomena. It cannot be excluded that a human observer after animal manipulation, pathological condition in the respiratory these sounds might be ascribed to dishess tract was responsible for the sound activity calls. Individuals of the study species are in the observed Carpetan Rock Lizard. typically solitary and rarely form into social
ACKNOWLEDGMENTS
Roberto Garcia-Roa benefited from an FPI (Tor- 20ll -241 50 IBOS and CGL20 1 4-5 3523 -P/BOS). Diego maciön Personal Investigador) grant from the Ministerio Llusia was supported by the Fondation Fyssen (Post- de Ciencia e Innovaciön (research projects MICIINCGL doctoml Study Grant, 2014-2016, France).
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DATE OF SUBMISSION: Apm20,2016 Corresponding editor: Heinz Grillitsch
AUTHORS: Roberto G.mcie-Roa (Conesponding author < [email protected] >) l), Diego Lrusn 2, 3), Pilar Löpnz t) & Jos6 MenriN l)
l) Department ofEvolutionary Ecology. National Museum ofNatural Sciences - Spanish Research Council (MNCN-CSIC). Jos6 Guti6rrez Abascal, 2, 28006, Madrid, Spain. 2) Department of Biodiversity and Evolutionary Biology, Fonoteca Zoolögica. National Museum of Natural Sciences - Spanish Research Council (MNCN-CSIC). Jos6 Guti6rrezAbascal,2,28006, Madrid, Spain. 3) Institut de Syst6matique, Evolution, Biodiversitö, ISYEB - UMR 7205 - CNRS, MNHN, UltUC, efUe; Mus6um national d'Histoire naturelle, Sorbonne Universit6s, 57 rue Cuvieq CP 50, F-75005, Paris, France.