the relationship between the behavioral activity and the underwater vocalization of the beluga whale...

ISSN 0001�4370, Oceanology, 2012, Vol. 52, No. 1, pp. 79–87. © Pleiades Publishing, Inc., 2012.Original Russian Text © E.M. Panova, R.A. Belikov, A.V. Agafonov, V.M. Bel’kovich, 2012, published in Okeanologiya, 2012, Vol. 52, No. 1, pp. 85–94.

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INTRODUCTION

Beluga whales have a rich vocal repertoire, whichincludes tens of different sound types of tonal andpulse nature [3, 7]. While the acoustic signals pro�duced by land mammals are classified first of all basedon their functions, such an approach is almost inappli�cable to cetaceans, as the greater part of their life ishidden from observers. Traditionally, the vocalizationsof toothed whales (Odontoceti) are classified based onthe physical (time–frequency) characteristics of thesounds. In this case, the classification can be based onthe auditory perception of the operator [1, 8, 19] or onthe comparative analysis of the signal spectrograms [3,4, 25]. However, the determination of the functionalload is a very difficult problem.

Revealing the function of the signals produced bytoothed whales is reduced in many cased to distin�guishing of so�called ethological�acoustic correlates,i.e., to revealing the relationship between the behav�ioral activity of the animals and the acoustic signalingaccompanying it [16, 18, 20, 25]. Such studies devotedto the acoustic activity of beluga whales were carriedout for the first time with the populations inhabitingCunningham Bay and the estuary of the St. LawrenceRiver [18, 25, 26]. The relationships between the keytypes of the behavioral activity (social interactions,resting, directional motion, anxiety situations, etc.)

and the large physical categories of the sounds (whis�tles, pulsed�tonal signals, and click series) were deter�mined.

The vocalization activity and behavior of the belugawhales inhabiting the White Sea have been studied forover 30 years [1]. However, till recently, the vocalizationbehavior of beluga whales has been investigated in detailonly in large�scale behavioral contexts, namely, duringhunting [8] and in stress situations [14].

The long�term experiments showed that, duringthe summer period, the females and calves of theWhite Sea beluga whales form eight groups, namely,local stocks [5], with each owning its section where theanimals gather every day, thus forming a “reproductivegathering.” For the first time, the vocalization activityof beluga whales in the context of reproductive gather�ings was studied in detail in the Solovetsky stock [3, 4,16]. The prevailing forms of the behavioral activity,namely, social interactions, sexual behavior, quietswimming, and the situations where the animals areannoyed by humans, were selected for the ethological�acoustic analysis.

This work is devoted to the investigation of thevocalization activity and the behavior of the Myagos�trovsky stock forming a reproductive gathering in thevicinity of the Roganka–Goly Sosnovets–Myagostovislands (Onega Bay). The following forms of the

The Relationship between the Behavioral Activity and the Underwater Vocalization of the Beluga Whale

(Delphinapterus leucas)E. M. Panovaa, R. A. Belikovb, A. V. Agafonovb, and V. M. Bel’kovichb

a Faculty of Biology, Moscow State University, Moscow, 119991 Russiab Shirshov Institute of Oceanology, Russian Academy of Sciences, Moscow, 117997 Russia

E�mail: [email protected] September 15, 2010; in final form, April 26, 2011

Abstract—The underwater vocalizations of the beluga whale summering in Onega Bay (64°24′N, 35°49′E)were recorded in June–July of 2008. The vocalizations were classified into five major whistle types, four typesof pulsed tones, click series, and noise vocalizations. To determine the relationship between the behavioralactivity and the underwater vocalizations, a total of fifty�one 2 minute�long samples of the audio records wereanalyzed in the next six behavioral contexts: directional movements, quiet swimming, resting, social interac�tions, individual hunting behavior, and the exploration of hydrophones by beluga whales. The overall vocal�ization rate and the percentage of the main types of signals depend on the behavior of the belugas. We suggestthat one of the whistle types (the “stereotype whistle”) is used by belugas for long�distance communications,while other whistle types (with the exception of “squeaks”) and three types of pulsed tones (with the excep�tion of “vowels”) are used for short distance communication. The percentage of “squeaks” and “vowels” wasequally high in all the behavioral situations. Thus, we assume that “squeaks” are contact signals. “Vowels”have a specific physical structure and probably play a role in identification signals. A high rate of the clickseries was observed in the process of social interactions.

DOI: 10.1134/S000143701201016X

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behavior of the Myagostrovsky beluga whales wereobserved in the Goly Sosnovets–Myagostrov waterarea: social, sexual, parental, exploratory, resting,group motion of the animals, and a behavior similar tothe hunting one [2].

The aim of this study was to investigate the pecu�liarities of the acoustic signaling of the beluga whalesfrom the Myagostrovsky stock in different behavioralcontexts.

MATERIAL AND METHODS

Collection of ethological�acoustic material. Thevisual observations and the recording of acoustic sig�nals were performed in June–July of 2008 in the vicin�ity of Goly Sosnovets island (64°24′ N, 35°49′ E;Onega Bay, the While Sea). The total number of thisstock was approximately 50 mature (white) animalsand 30 calves of different ages. As a rule, the animalsare in the water area in the vicinity of the Roganka–Goly Sosnovets islands almost all the day.

The observation post was about 10 m above the sealevel. The observations revealed the distribution of thebeluga whales in the visible water area, the number andthe age composition of the animal groups, the type oftheir activity, and the meteorological conditions andsuch factors as the existing of vessels in the water area.The animals were filmed with a digital video camerawith synchronous recording of their vocalizationactivity.

The hydroacoustic complex consisted of two longhydroacoustic paths. One of the undirected spherical(50 mm in diameter) hydrophones was fixed 70 maway from the shore in the northwest part of the island.Another undirected spherical (50 mm) hydrophonewas fixed 100 m away from the shore in the eastern partof the island. Different sections of the water area nearGoly Sosnovets island actively used by the belugawhales were acoustically isolated due to the peculiarpositioning of the islands and, thus, the two hydroa�coustic paths made it possible to control almost theentire water area. The hydrophones were equippedwith preamplifiers and they were connected to the on�shore units of a phantom power supply with the help of acoaxial cable. The acoustic data were fixed with a digitalvideo camera (the frequency band of 0.02–24 kHz; non�uniformity of the amplitude–frequency characteristicof ± 10 dB). More than 22 hours of video and audiomaterial was obtained.

Processing of the ethological material. Behavioralsituations of six main types were selected for the anal�ysis:

1. Directional motion: the animals move in a densegroup in one direction. The group moves with a suffi�ciently high speed usually near the water’s surfacemaking shallow dives.

2. Quiet swimming: the animals move in a loosegroup with a low speed, while often changing thedirection of their motion.

3. Sleeping/resting: the animals lie almost motion�less near the water’s surface.

4. Social interactions: the animals move in a densegroup and actively communicate.

5. Feeding (individual exploratory–hunting behav�ior): this type of behavior includes the situations whenindividual animals or small groups of animals are scat�tered over a large water area, remain almost at one andthe same place, and periodically make deep dives. It isassumed that, in such situations, the beluga whaleswere in search of fish and were busy catching it.

6. Exploration of hydrophones: the situation whenthe beluga whales demonstrated exploratory behaviorwhen coming close to the massif of hydrophones.

Two minute�long videorecording fragments whereall or the overwhelming majority of the beluga whalesdemonstrated similar activity were selected for each ofthe distinguished types of behavior. All in all, 51 frag�ments lasting 1 h 42 min were chosen: 12 fragmentsduring directional motion, 13 fragments of quiteswimming, 8 fragments during sleeping/resting,10 fragments during social interaction, 6 fragmentsduring feeding, and 2 fragments during exploration ofthe hydrophones by the beluga whales.

Processing of the acoustic material. The vocaliza�tions were processed using Adobe Audition 1.5 soft�ware at the following fixed parameters: an FFT size of256 points and a Hamming window. The classificationof the vocalizations based on the time–frequencyparameters was performed by us earlier [7]. The vocal�izations were subdivided into the following basic phys�ical categories:

—Tonal signals or whistles: 26 types: 17 types ofhigh�frequency signals (with the pitch frequencyhigher than 5 kHz), 7 types of low�frequency signals(the pitch frequency lower than 5 kHz), and 2 types ofhybrid tonal signals (it being a stable combination ofhigh�frequency and low�frequency tonal signals).Such a grouping is related to the fact that the distribu�tion of the total signal frequencies is bimodal: the sig�nals in the frequency band of 4.5–5.5 kHz are met lessfrequently than the signals with the pitch frequencieshigher or lower than the boundary of this range.

—Pulsed tones: 2 types of pulsed tones with a highpulse repetition rate (1000–1400 pulse/s) and 4 typesof pulsed tones with a low pulse repetition rate (200–400 pulse/s).

—Click series (4 types).—Noise signals (4 types).We selected the following signal groups for the

ethological�acoustic analysis (Fig. 1):1. Stereotype high�frequency tonal signals: they are

characterized by rather stable time–frequency param�eters and the shape of the frequency contour.


THE RELATIONSHIP BETWEEN THE BEHAVIORAL ACTIVITY 81

2. Variable high�frequency tonal signals: they arecharacterized by the frequency contour variabilitywithin the limits of one type.

3. Low�frequency tonal signals.4. Pulsed�tonal signals with a high pulse repetition

rate (pulsed�tonal calls).5. Pulsed�tonal signals with a low pulse repetition

rate (perceived by the ear as “moans” and “groans”).6. Click series.7. Noise signals.In addition, the most numerous signals tradition�

ally classified by Russian researchers into separategroups [8] were considered:

8. Relatively short low�frequency tonal signals withflattened, ascending, descending, or U�like shapes ofthe frequency contour (“squeaks”).

9. Low�frequency tonal signals represented in asonogram (at the above�mentioned parameters) as asequence of short U�shaped elements (“chirping”).

10. Short pulsed�tonal signals with a low pulse rep�etition rate (“vowels”).

11. Pulsed�tonal signals of medium duration withfrequency and amplitude modulation. During the sig�nal, the pulse repetition rate changes in a wavelikemanner (“bleating”).

The number of signals in each group was calculatedin each 2�minute�long fragment. All in all, 1 h and42 min of audio records were analyzed and 2727 sig�nals were logged.

The overall vocalization rates (signals/min) and therelative (signals/individual/min) were calculated foreach type of the behavioral activity and its percentagein the total vocal production was computed for eachsignal group.

The Analysis of the Acoustic Signaling Dependenceon the Behavioral Context. The obtained results werestatistically analyzed using Statistics 6.0 software(StatSoft Inc. 1984–2001). The statistical significanceof the differences between the overall vocalizationrates of the signaling and the relative vocalization rates

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Fig. 1. Spectrograms of the principal groups of signals produced by beluga whales from the Myagostrovsky stock. (1) Stereotypehigh�frequency tonal signals; (2) variable high�frequency tonal signals; (3) low�frequency tonal signals; (4) pulsed tones with ahigh pulse repetition rate; (5) pulsed tones with a low pulse repetition rate (“moans,” “groans”); (6) click series; (7) noise signals;(8) “squeaks”; (9) “chirping”; (10) “vowels”; (11) “bleating”.

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(signal/individual/min) for the different behavior typeswas estimated using the Kruskal–Wallis criterion [13]:

where N is the total number of observations in all thesamplings, n is the number of observations in eachsampling, and R is the sum of the ranks in each sam�pling.

The relative frequency of the signaling in the pairsof behavioral situations was compared with the help ofthe Mann–Whitney U�test [13]:

where n1 and n2 are the number of observations in thefirst and the second sampling, respectively, and Tx isthe largest of the two rank sums corresponding to thesampling with nx observations.

The percentage of the signals for each behaviortype was compared to that for the five remaining typesof behavior with the help of the two�proportion test.Thus, for each behavioral type, it was possible todetermine how often or how rarely this or that group ofsignals is used.

The relationship between the vocalization activityand the behavioral context was analyzed using the per�centage of the signals rather than the frequency of theoccurrence as was done in other works [18, 26]. Thevariations of the frequency of a signal’s occurrence inthis or that type of behavior can be explained by thechanges in the overall rate of the vocalizations, sincethe percentage of the signals in this case can remainunchanged. We can judge whether the significance ofthe signals from different groups changes with thechange in the behavioral activity based on the degreeof disproportion of the variations of the frequency ofthe signal’s occurrence with respect to the overallvocalization rate.

RESULTS

Dependence of the overall vocalization rate of thebeluga whale activity on the type of behavioral activity.The overall vocalization rates and the relative vocaliza�tion rates (i.e., per individual) at different types ofbehavioral activity is listed in Table 1. The statisticalanalysis showed that the overall vocalization rate and

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the relative vocalization rate depend on the type ofactivity (H = 26.9, p < 0.01; Н = 24.5, p < 0.01). Thepairwise comparison of the relative vocalization rate atdifferent types of behavior yielded the followingresults. The statistical significance of the relativevocalization rate at social interactions is substantiallylarger as compared to quiet swimming (U = 18, p <0.01), “sleeping/resting” (U = 4, p < 0.01), and feed�ing (U = 2, p < 0.01). In the case of directional motion,the relative vocalization rate is higher than that at quietswimming (U = 26, p < 0.01), “sleeping/resting” (U =11, p < 0.01), and feeding (U = 10, p < 0.01). As for thesituation with the exploration of the hydrophones, therelative vocalization rate is higher than that at thesocial interactions (U = 0.00; p = 0.03) and “sleep�ing/resting” (U = 0.00; p = 0.04). The “exploration”and “feeding” contexts were not compared due to thesmall size of the sampling.

Changes in the percentage of the different signalgroups depending on the type of behavior. The compar�ison of the percentage of the signals at each type ofbehavior with the rest showed that there are differ�ences in using the signals of different groups depend�ing on the behavioral context (Table 2, Fig. 2).

Directional motion. As compared to the othertypes of behavior, the animals during directionalmotion through the water area used stereotype high�frequency tonal signals, “squeaks,” and “vowels”more often (p < 0.01). The percentage of such signalsas “chirping,” low�frequency tonal signals, pulsed�tonal calls, pulsed tones with a low pulse repetitionrate, click series, and noise signals are smaller in thisbehavioral context than that in other the types ofactivity (p < 0.01).

Quiet swimming. During quiet swimming, suchsignals as those of the “chirping” group, pulsed toneswith a low pulse repetition rate, and noise signals wereused more often as compared to the other types ofbehavior (p < 0.05). The percentage of low�frequencytonal signals, “bleating,” and click series at this type ofactivity turned out to be smaller (p < 0.05).

Sleeping/resting. For this type of behavior, the per�centage of the majority types of signals (except for“squeaks,” “bleating,” and pulsed tones with a lowpulse repetition rate, for which p < 0.03) did not differfrom that observed at the other types of behavior.

Social interactions. Variable high�frequency tonalsignals, “squeaks” and “bleating,” pulsed tones with alow pulse repetition rate, and pulsed�tonal calls were

Table 1. Overall rate of the acoustic signaling of beluga whales in different behavioral contexts (arithmetical mean ± standard deviation)

Type of behavior Directionalmotion

Quietswimming

Sleep�ing/resting

Socialinteractions Feeding Exploration

Overall vocalization rates, sig�nals/min

23.3 ± 12.5 24.6 ± 16.7 9.3 ± 7.0 58.9 ± 20.6 8.2 ± 11.3 31.5 ± 2.1

Relative vocalization rates,signal/individual/min

3.4 ± 2.4 1.5 ± 1.4 1.0 ± 0.8 3.1 ± 0.9 0.9 ± 0.9 4.5 ± 0.3



Table 2. Proportion of signals during a given type of behavior (the column marked with #) compared to the average proportionof signals for the five remaining behavioral types (the column marked with ##)

Types of behaviorGroups of acoustic signals

Directional motion

Quiet swim�ming

Sleeping/rest�ing

Socialinteractions Feeding Exploration

# ## # ## # ## # ## # ## # ##

Stereotype high�frequency tonal signals

0.07 0.02 0.04 0.03 0.01 0.03 0.01 0.04 0.07 0.03 0.02 0.03

p= 0.00 n.s.* n.s. 0.00 0.03 n.s.

Variable high�frequency tonal signals

0.03 0.04 0.03 0.04 0.05 0.04 0.07 0.02 0.02 0.04 0.01 0.05

p= n.s. n.s. n.s. 0.00 n.s. 0.04

“Squeaks” 0.45 0.29 0.35 0.31 0.48 0.31 0.23 0.37 0.57 0.30 0.24 0.34

p= 0.00 n.s. 0.00 0.00 0.00 0.00

“Chirping” 0.08 0.12 0.14 0.10 0.09 0.11 0.16 0.08 0.06 0.11 0.04 0.13

p= 0.01 0.00 n.s. 0.00 n.s. 0.00

Low�frequency tonal sig�nals

0.04 0.09 0.03 0.09 0.05 0.09 0.04 0.11 0.02 0.09 0.26 0.04

p= 0.00 0.00 n.s. 0.00 0.02 0.00

Pulsed�tonal calls 0.01 0.04 0.03 0.04 0.01 0.04 0.07 0.02 0.01 0.04 0.02 0.04

p= 0.00 n.s. n.s. 0.00 n.s. n.s.

“Vowels” 0.18 0.12 0.13 0.13 0.09 0.13 0.12 0.13 0.12 0.13 0.12 0.13

p= 0.00 n.s. n.s. n.s. n.s. n.s.

“Bleating” 0.05 0.05 0.03 0.06 0.01 0.05 0.09 0.03 0.00 0.05 0.04 0.06

p= n.s. 0.00 0.03 0.00 0.02 n.s.

“Moans”; “groans” 0.03 0.06 0.07 0.05 0.01 0.05 0.08 0.04 0.01 0.05 0.02 0.06

p= 0.00 0.05 0.03 0.00 n.s. n.s.

Click series 0.04 0.10 0.06 0.10 0.09 0.09 0.08 0.09 0.01 0.09 0.18 0.07

p= 0.00 0.00 n.s. n.s. 0.00 0.00

Noise signals 0.01 0.04 0.08 0.03 0.06 0.04 0.03 0.04 0.06 0.04 0.02 0.04

p= 0.00 0.00 n.s. n.s. n.s. n.s.

Notes: Italics mark the percentage of signals that are more statistically significant, while bold, those which are less statistically significant forthe remaining types of behavior.

* n.s.—no significant.

used more often during social interactions than in thecase of other types of activity (p < 0.01), while stereo�type tonal signals, “squeaks,” and low�frequencytonal signals were, on the contrary, used more rarely (p< 0.01). During social interactions, only the percent�age of the noise signals and click series did not differfrom that observed at other types of behavior.

Feeding. In the “feeding” context, the signals ofthe “bleating” type were not recorded at all. Thus, thepercentage of these signals, as well as that of the low�frequency tonal signals and click series, turned out tobe smaller (p < 0.05) than that at the other types ofbehavior. During feeding, the statistical significance ofthe stereotypical high�frequency signals and“squeaks” was much higher (p < 0.05).

Exploration of hydrophones. Low�frequency tonalsignals and click series were produced much moreoften in the process of the hydrophones’ exploration(p < 0.01) as compared to the other behavioral con�

texts. The percentage of the variable high�frequencysignals and “squeaks” and “chirping” was lower in thiscase (p < 0.05) than that at other types of activity.

DISCUSSION

Overall vocalization rate of the beluga whale activ�ity. The data on the signaling frequency of the Mya�gostrovsky beluga whales in different behavioral situa�tions are in good agreement with the data obtained forthe beluga whales of the Solovetsky stock [16]. Theacoustic activity of the animals was maximal duringsocial interactions.

Function of tonal signals. Our investigation (as wellas other works [3, 18, 22]) showed that tonal signalsmake up the larger part of the vocalizations of belugawhales of different populations, which points to theimportant role of the signals belonging to this very cat�egory in the acoustic communication of beluga

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Stereotypical high�frequencytonal signals

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Noise signals “Squeaks” “Chirping”

“Vowels” “Bleating”

Pro

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Type of behavioral activity

Fig. 2. Percentage of signals of different groups depending on the type of behavior: (DM) directional motion; (QS) quiet swim�ming; (S/R) sleeping/resting; (SI) social interactions; (F) feeding; (EH) exploration of hydrophones.

whales. However, there is no consensus of opinionsabout the function of tonal signals. Tonal signals arecapable of propagating over long distances and, thus,they can be used by toothed whales for long�rangecommunication and coordination [28]. Nevertheless,the study of the beluga whales inhabiting the CanadianArctic [25] did not reveal the dependence of the usageof whistles on behavioral contexts. At the same time,the results obtained in another work [18] confirmedthe fact that whistles can be used by beluga whales aslong�range signals; however, the hypothesis abouttheir coordination role was not verified. Someresearchers also think that whistles play the role of“emotional” signals in the process of short�rangeinteractions [8].

The abundance of tonal signals among the belugawhale vocalizations and their high versatility speaks infavor of the fact that the signals of this category are

polyfunctional. Thus, when performing the ethologi�cal�acoustic analysis, we subdivided the vast categoryof tonal signals into several groups with different phys�ical characteristics and, probably, different functions.

The signals adapted for long�range communicationhave to be long, stereotypical, intensive, and spectrallysimple [29]. The tonal signals singled out by us in thegroup of stereotypical high�frequency tonal signals arecharacterized by such properties. The statistical anal�ysis showed that the percentage of signals from thisgroup is larger in the case of the directional motion ofthe beluga whales in a group and during feeding ascompared to other types of behavior. It can be assumedthat these signals provide for the coordination of theanimals moving in a group and, probably, can serve aslong�range signals when beluga whales are distributed(singly or in small groups) over a large water area. Inspite of the fact that high�frequency signals damp



faster when propagating through the medium thanlow�frequency ones [21], the beluga whales are likelyto use high�frequency whistles (with a dominant fre�quency of 7–9 kHz) for long�range communication.This can be explained by the fact that the low�fre�quency auditory threshold of beluga whales is very high:at 1 kHz, it makes up 102 dB with respect to 1 μPa,while, at 8 kHz, it decreases down to 65 dB with respectto 1 μP [15].

The signals intended for short�range communica�tion and, thus, weakly subjected to degradation cancarry more information decoded in minor variationsof their physical structure [29]. This is also confirmedby the data obtained by us: the percentage of variablehigh�frequency tonal signals characterized by a com�plex and varied physical structure was larger in thecontext of short�range communications.

The assumption that one type of high�frequencytonal signals can be used for short�range communica�tion, while the other ones are used for long�rangecommunication was made when investigating theWhite Sea beluga whales of the Solovetsky stock [4].

One more group of signals that can play an impor�tant role in the short�range communication due totheir physical characteristics includes low�frequencytonal signals. However, the statistical analysis revealeda sharp increase in the percentage of the signalsbelonging to this group only in the context of the bel�uga whales’ exploration of the hydrophones. This isrelated to the fact that the beluga whales in this casestarted producing long series of signals of one of thetypes. Probably, they have a specific function related tothe increased anxiety of the animals in the process ofthe exploration of an unknown object.

Squeaks are the most widely spread type of vocal�ization of the White Sea beluga whales belonging tothe Myagostrovsky and Solovetsky stocks [3].“Squeaks” and other signals with a similar physicalstructure are thought to play an emotional role [8, 18].However, the fact that equal percentages of “squeaks”are produced by the beluga whales from the Solovetskystock in different behavioral contexts shows that thesesignals are “background” ones and do not have anyemotional coloring [16]. In our study, the percentageof “squeaks” varied depending on the behavioral con�text. The fact that “squeaks” are produced more oftenin the process of directional motion, as well as in the“sleeping/resting” and “feeding” contexts, shows thatthis signal has a contact function. Such contact signalsintended for communication between the members ofthe group in conditions of restricted visibility weredescribed for different animal species, namely, fromschooling sparrows (e.g., [10]) to red wolves [29]. Thesimple shape of the contour, the transfer of the energyto higher harmonics, and the serial manner vocaliza�tion make the signals of this group well adapted topropagating in the conditions of noise.

The Myagostrovsky beluga whales, as well as theSolovetsky ones [16], produce “chirping�type” signals

more often during social interactions and quiet swim�ming; however, their functions remains unclear.

Functional significance of pulsed and noise signals.Pulsed�tonal signals are mainly produced duringshort�range interactions, and they are thought to playthe role of “emotional signals” [18, 26, 30]. Accordingto our results, the percentage of the majority of thepulsed�tonal signals increases during social interac�tions, which confirms the significance of these signalsfor short�range communication.

However, one type of pulsed tones (namely, “vow�els”) is likely to have quite another function. The per�centage of “vowels” for each specific type of behaviordoes not differ from the other types of behavioralactivity, and only in the case of directional motion is itlarger than that in other contexts. It can be assumedthat “vowels” are individual identifying contact sig�nals. The role of such signals in the repertoire of bottlenose dolphins (Tursiops truncates) is played by signa�ture whistles, i.e., tonal signals with a frequency con�tour individual for each dolphins [17]. For belugawhales, short low�frequency whistles [8], “vocal” sig�nals (i.e., pulsed�tonal signals with a low pulse repeti�tion rate) [6, 8, 11], high�frequency tonal signals withstereotypical multiloop structures [4], and low�fre�quency tonal signals with a flat�ascending contourshape [12] were considered to play an individual iden�tification function. However, “vowels” have a numberof structural peculiarities that also make them suitableas individual identification signals. The greater part(73%) of “vowels” is produced simultaneously with a“squeak�type” tonal signal; i.e., they are biphonic,which allows imparting high individual specificity to thesounds [9] and, probably, makes it possible to estimatethe approximate distance to the vocalizing animal [23].

It is thought that a series of individual clicks areused by toothed whales for echolocation during orien�tation, navigation, and in a searching–hunting con�text [24, 27]. Actually, our investigation revealed thatthe percentage of click series was maximal in the con�text of the exploration of the hydrophone massif by thebeluga whales, but, during directional motion andfeeding (when echolocation is necessary for orienta�tion and searching for prey), no intensification in theecholocation activity was observed. On the contrary,the percentage of click series in such contexts turnedout to be minimal. The almost complete absence ofecholocation series during directional motion wasrevealed for the populations of beluga whales inhabit�ing the Canadian Arctic and the St. Lawrence Estuary[18, 25]. Sjare and Smith [25] assumed that a decreasein the vocalization activity, including the echolocationone, can provide masking of the moving animals frompredators (killer whales). In our case, the reduced per�centage of the click series in this behavioral contextcan be explained by the fact that the beluga whalesmove over a well�known water area and, thus, do notneed echolocation for orientation. The fact that thepercentage of click series in the “feeding” context

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turned out to be smaller as compared to the otherbehavioral types can be explained as follows. Firstly,echolocation clicks have energy that is mainly concen�trated in the range of high frequencies and, thus, theyare more narrowly directed and more strongly sub�jected to degradation than low�frequency signals.During “feeding,” the beluga whales were hundreds ofmeters away from the hydrophone massif (while, dur�ing the exploration of the hydrophones, they wereright against it) and, therefore, due to the peculiaritiesof the propagation of the echolocation clicks and,probably, those of the bottom profile, we could notrecord echolocation click series. Secondly, we couldhave misinterpreted the “feeding” context. During thesearching–hunting activity, the beluga whales are sin�gly dispersed over a large water area and periodicallycome to the surface [8]. Such behavior was demon�strated by the Myagostrovsky beluga whales in thecontexts identified by us as “feeding”; however, wecannot assert with certainty that they were actuallyhunting.

As compared to the other types of behavior, theclick series were produced most often during socialinteractions. The intensification of the echolocationduring the activation of the beluga whales in the con�text of social interactions was observed in otherresearches as well [16, 18, 25]. It seems that belugawhales turn to echolocation not only for exploringtheir environment but also for “keeping an eye” onone another [16, 18]; in addition, it cannot be ruledout that the click series can play a communicativefunction.

The data on using noise signals are difficult toexplain. Noise signals is a very nonuniform category ofsounds likely to play a broad spectrum of roles.

CONCLUSIONS

We have revealed that the overall vocalization rateof beluga whales and the percentage of acoustic signalsin each group depend on the type of behavioral activ�ity. On the whole, variable tonal signals and the greaterpart of the pulsed�tonal signals are used for short�range communication, while stereotypical tonal sig�nals, for long�range communication. The percentageof click series increases during social interactions,which can point to the fact that beluga whales useecholocation to follow one another. The percentage ofpulsed�tonal signals of the “vowels” type turned out tobe high in different behavioral contexts. Along withthe peculiarities of their physical structure, this allowsassuming that they play a role in individual identifica�tion.

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the relationship between the behavioral activity and the underwater vocalization of the beluga whale...

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