An Overview of the Vocal Repertoire of Indri Indri

JASs Reports

Journal of Anthropological Sciences
Vol. 88 (2010), pp. 151-165

Not just a pretty song: an overview of the vocal repertoire of Indri indri

Giovanna Maretti¹, Viviana Sorrentino¹, Andriamasitoly Finomana², Marco Gamba¹& Cristina Giacoma¹

1 ) D epartment of Animal and Human Biology, University of T o rino, Via Accademia Albertina 13, 10123 T o rino, Italy

e-mail: [email protected]

2) Faculté des Sciences, University of Mahajanga, Campus Ambondrona, BP 652, Mahajanga (401), Madagascar

Summary - e vocal behaviour of wild indris inhabiting the area near Andasibe was studied by means of all occurrence sampling. We provide a quantitative overview of the vocal repertoire of Indri indri, describing qualitative contextual information and quantitative acoustic analysis for all the utterances we recorded from adult individuals. Other than the song, the repertoire of Indri indri comprises 8 vocal types uttered by the adults. Future studies are necessary to explore whether vocalisations uttered in diﬀerent contexts have diﬀerent functions and how these functions relate to acoustic structure.

Keywords - Strepsirhine primates, V o cal behaviour, Acoustic structure, Ambient noise.

Introduction

The indri (Indri indri) is a particularly interesting species for the study of vocal communica-
To investigate the relationship between vocal tion for at least three reasons. It lives in small and non-vocal behaviour, it is crucial to analyse family groups in lowland to mid-altitude primary vocal signals making up the vocal repertoire of a and secondary rainforest of eastern Madagascar species, to describe vocal types and, where possi- (Garbutt, 1999; Pollock, 1979), spending most ble, provide information regarding the variation of its time in the dense canopy. Each group has of acoustic parameters between and within vocal a relatively stable home range and shows exclutypes. The study of vocal repertoires can provide sive territoriality. In order to regulate spacing information about the factors that affect signal- between neighbouring groups in the forest, all ling and how vocal signals influence the behav- group members emit a complex howling call, iour of receivers, thereby indicating the function which can be broadcast over several kilometres.

of the signals. Information concerning the acous-

In the present study, we aimed to provide a

tic structure and the context, or contexts, of comprehensive overview of the vocal repertoire vocal production can lay the foundation for fur- of the indri (Indri indri) with special attention ther studies on a species, and provide researchers to those utterances that do not occur during the with the basic knowledge necessary for design- indri song. Previous studies of the indri’s vocal ing detailed studies on the relationship between communication focussed their attention on the vocal communication and social behaviour, or to song (Pollock, 1975, 1986; Oliver & O’Connor, perform cross-specific comparisons (Owings & 1980; Haimoff, 1986; Thalmann et al., 1993;

Morton,1998; Owren & Rendall, 2001).

Geissmann & Mutschler, 2006; Sorrentino et al.,

the JASs is published by the Istituto Italiano di Antropologia

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Vocal repertoire of Indri indri

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in press).The indri song is a vocal display in which capital Antananarivo and the east coast, ca. 30 one or more individuals emit a sequence of notes km east of Moramanga. Previously covered with separated by short pauses (Pollock, 1986). Songs continuous forest, the region now has only fraglast 40-250 s and are usually introduced by three ments of forest (Dolch, 2003). We collected data or four “roars” uttered simultaneously by several in three different sites: the 810 ha Analamazaotra members of a group (Pollock, 1986); then, one at Reserve (18° 56’ S, 48° 25’ E); Mitsinjo Forest a time, or sometimes in pairs, the members of the Station (18° 56’ S, 48° 24’ E), a 250 ha area group produce a long “modulated howl” (Petter 200 m from the border of the Analamazaotra & Charles-Dominique, 1979), or “song proper” Reserve; and Mantadia National Park, 10,000 ha (Pollock, 1986). Previous investigators agreed situated 20 km from the other two sites (Powzyk that the main functions of indri songs are related & Mowry, 2003). The climate is humid with to territorial announcement and defence (Petter a mean annual rainfall of 1700 mm, a mean et al., 1977; Petter & Charles-Dominique, 1979; annual temperature of 18°C, and an atmospheric Pollock, 1986; Geissmann & Mutschler, 2006). humidity >70%; elevation ranges between 850- We aimed at improving knowledge of the indri 1220 metres and mean canopy cover is 87.6 repertoire, providing a robust classification of the 4.3% (Stephenson, 1994; Powzyk & Mowry, utterances based on quantitative acoustic descrip- 2003; Biebouw, 2009). tions as well as contextual information for each of the vocal types. Our hypothesis is that, as in Data collection

other non-human primates, certain vocal types

We recorded the vocalisations of ten

occur in several behavioural contexts, while oth- groups of indris. Six groups were recorded in ers are strictly associated with particular contexts, Analamazaotra Special Reserve, one group in

or referential.

Mantadia National Park, and three groups

In the indri, as in most primates, phona- in Mitsinjo Forest Station. Of these groups tion is usually the result of an expiratory airflow, (Tab. 1), three were usually exposed to tourwhich causes oscillation of the vocal folds to pro- ist groups (contributing for 38% of the study duce sounds. The acoustic correlate of the rate of sample), and three more were seldom visited vocal fold vibration is the fundamental frequency by tourists (contributing for 23%). The other (F0) of the vocal signal. By changing the stiffness four groups were habituated by V. S. before the and length of the vocal folds, mammals (includ- beginning of the recording sessions (contributing humans) can modify the periodicity of vocal ing for 39%). The total number of individuals fold vibration and vary the F0 characteristics of a recorded was 28: 14 males, 13 females, and one

vocal sound over time.

infant of unknown sex (Tab. 1). We observed

Our second goal was to quantify the vocal and recorded only one group per day, for a total flexibility of this species, analysing F0 variation of 160 days. We usually followed the same group quantitatively across the vocal types. We expected for a minimum of four consecutive days, during that, as for many non-human primates, F0 vari- September-December of four consecutive years ation would be marked between different vocal (2005-2008). We carried out survey walks daily

types and limited within vocal type.

from 06.00 h to 13.00 h.

For the purpose of this research we obtained research permits from Direction des Eaux et Forêts in 2005 (N° 197 /MINENV.EF/SG/ DGEF/DPB/SCBLF/RECH), 2006 (N° 172/06 /MINENV.EF/SG/ DGEF/DPB/SCBLF), 2007

Materials and Methods

Study areas

We conducted the study in a mid-altitude (N° 0220/07 /MINENV.EF/SG/ DGEF/DPSAP/ montane rain forest near Andasibe, Madagascar. SSE) and 2008 (N° 258/08 /MEFT/SG/ DGEF/ The small village of Andasibe lies between the DSAP/SSE).

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153

Tab. 1 - Composition of the study groups (2005-2008).

Group

Fieldsite

Number of

recorded individuals

Composition

Number of

recording sessions
Number of vocalizations per group

1R§ 2R§ 3R#
5R
Analamazaotra SR Analamazaotra SR Analamazaotra SR Analamazaotra SR Analamazaotra SR Analamazaotra SR Station Forestière Station Forestière Station Forestière Mantadia NP

4

1AF; 2AM; [1SAF]*

2AM; 1JM

25

512

3

7

80

4

1AF; 2AM; [1AM]**

1AM; [1AF]**
1AF; 1SAF; 1AM
1AF

7

63

2

7

6R

3

11

596

XR# ASF§ YSF# WSF
1M

1

48

3

1AF; 1AM; 1JM

2AF; 1SAF; 1AM; 1I
1AF; 1AM
8

5

14

313

21
53
40

1SAF

10

TOT. 28

TOT. 82

TOT. 1670

§ usually visited by tourists, # seldom visited by tourists. Analamazaotra SR: Analamazaotra Special Reserve; Station Forestière: Station Forestière Mitsinjo; Mantadia NP: Mantadia National Park. * departed since 2008, ** departed since 2007. M = male, F = female, ? = sex unknown. Age classes according to Pollock 1986: A = adult (>6 years), SA = subadult (>3 years), J = juvenile (<3 years), I = infant (<1 year).

Recording methods

occurring concomitant with vocalisations were
We recorded calls using Marantz PMD671 recorded and coded into broad categories as folsolid-state recorders on compact flash memory lows: rest (remaining still or quietly monitoring cards. Recorders were equipped using Sennheiser the environment), foraging (searching, obtaining MKH-60 (with windscreen) and ME66 (with and eating food), travel (moving for a distance Sennheiser MZW66 windscreen) shotgun greater than 10 m), vigilance (looking into vegmicrophones. Sounds were digitised at 44.1 kHz etation, either quickly moving the head or with sampling rate, 16 bits amplitude resolution. No the head stationary), aggression (chasing or fightrecording was taken when tourists were near the ing between group members), agonistic (negative focal group, nor were vocalisations elicited by interaction without physical contact), territorial means of playbacks. We only recorded spontane- advertisement (sequential singing of the indri ously occurring vocalisations. Recording sessions song), anti-predatory [in presence of terrestrial or took place when researchers could directly see aerial predators or potential predators (e.g. dogs, the animals and follow them in the forest. The mongooses), or human observers]. Recording distance between the researcher and the focal sessions usually lasted 10 to 45 minutes, dependindri could range from 3 m to approximately ing on the animal movements. We analysed a 10 m. A recording session ended when the dis- total of 82 recording sessions (Tab. 1).

tance between the animal and the microphone

The software Praat 5.1.15 (Boersma &

exceeded 10 m or the animal fled away. For each Weenink, 2009) was used for visual inspection utterance, we noted the identity of the vocal- and selection of high quality vocalisations. These iser and the behavioural context. Behaviours utterances were identified on the basis of their

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intensity, the absence of overlapping vocalisa- emphasis: 6.0 dB/Oct; dynamic compression: tions, and the degree of background noise (e.g. 0.0). The actual variation of the fundamental insects, birds, rain). We analysed a total of 1670 frequency was measured by using the autocorrevocal signals, 1514 of which were used in the dis- lation method [“Sound: To pitch (ac)…”], after

criminant function analyses.

adjusting the analysis parameters according to

The recording equipment we used for noise the range of variation in each of the vocalisations recordings was the same as that used for vocalisa- (Gamba & Giacoma, 2005).

tions. We considered 455 sound files, the dura-

Formants (F1, F2, F3) were studied using

tion of which was a minimum of 2 s, recorded linear predictive coding (LPC, Markel & Gray, before and after indri vocalisations. All ambient 1976). Because the vocal signals usually vary noise recordings were made at heights rang- with time, this process was done all along the siging between 1.5 and 4 m, with the microphone nal frames and then average formants were calcuorientated at about 45° above the horizontal lated. Depending on the acoustic characteristics towards the canopy, in order to record at the of the vocalisation, we used a window length strata mainly used by the indris. Recordings were of 0.03-0.05. Because the number of formants

taken between 06.00 and 13.00 h.

varies with vocal tract length, we measured 3-6

formants depending on the vocal type. Two methods were used in order to check the form-

Acoustic analyses

Taking the perspective of the source-filter ants predicted by LPC. First, formant analyses theory (Fant, 1960), we analysed the vocalisations were superimposed over the signal spectrogram. in the light of their being the combined product Second, autocorrelation-based LPC spectra were of two independent mechanisms: vibration of the overlaid on independently-derived FFT spectra vocal folds and filtering of the supra-laryngeal of the same frames to validate the LPC analysis. vocal cavities. Several studies have demonstrated The typical setting for the dynamic range was 25 how non-human primate acoustic signals are Hz. The formant pattern fitting was inferred durshaped by both these events (Fitch, 1997; Rendall ing a step-by-step monitored process, where the

et al., 2005; Gamba & Giacoma, 2006).

operator could interrupt the analysis and modify

We carried out all acoustic analyses using a the analysis parameters. The final output file window length of 0.05 s. The time range of the was assembled within PRAAT and exported to operating screen window was usually set to 3 s a SPSS spreadsheet. We only included variables during the acoustic analyses. We set the frequency that could be measured from all vocal types.

range to 0-10 kHz and dynamic range to 35 dB.

We generated a series of frequency spectra to

For each call, independent of the vocal cat- compare frequency distributions of the vocalisaegory to which it was assigned, we measured the tions emitted by the indris with those of the forest duration of the whole vocal emission (DUR); noise. We then visually inspected all the noise files three larynx-related features — average funda- by means of the spectrograms. Visual inspection mental frequency (MeF0), minimum fundamen- and the grouping techniques available in Praat tal frequency (MiF0), maximum fundamental (dynamic time warping) allowed us to select the frequency (MaF0); and four vocal tract-related typical frequency patterns, taking into account the acoustic features — average first formant (F1), most prominent bands and the background noise average second formant (F2) and average third (flies, birds, insects…). We then generated spectra formant (F3, see Fig. 2 in Gamba & Giacoma, from the vocalisation sound files for comparison. 2008 for details).
To detect source features (MeF0, MiF0, Statistical analysis

MaF0), Fast Fourier transforms were generated

We conducted stepwise cross-validation discri-

for all calls (frequency range: 0-12000 Hz; maxi- minant function analysis using SPSS 17.0 (SPSS mum: 50 dB/Hz; dynamic range: 30 dB; pre- Inc., USA) to classify vocalisations based on the

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155

vocal type and to verify which parameters were most important in the classification. To reduce the possible effect of pseudo-replication (as in some Description of the vocal repertoire cases inter-dependence of the data could not be Besides the proper song notes, adult indris

Results

excluded, e.g. because of indris fleeing when they possess eight different vocal types, all of which emitted terrestrial alarm calls), we used two dif- are distinguishable by visual inspection of the ferent resampling methods: Jackknife cross-valida- spectrograms (Fig. 1) and by ear: roar (Fig. 1a), tion and a permutation resampling strategy. The honk (Fig. 1b), hum (Fig. 1c), short tonal call Jackknife was performed using the SPSS function (Fig. 1d), long tonal call (Fig. 1e), kiss (Fig. 1f), in the discriminant analysis. The permutation wheeze (Fig. 1g), grunt (Fig. 1h). To complete was performed by resampling the most numerous the description of the vocal repertoire, we provocal types, which were then subjected to both vide a spectrogram of infant calls (Fig. 1i) and of original and cross-validated discriminant analyses. the song (Fig. 1j).

This method reduced both the potential influence

A schematic overview of call usage is provided

of pseudo-replication and the influence of the in Table 2, including information concerning the different sample sizes across the vocal types. We nomenclature used for the same vocal types in randomly generated 70 data sets (total N ranging previous studies, the general context in which the between 511 and 591) in which the most numer- sound is usually uttered, a short description of ous vocal types, hums and grunts, were down- the overall acoustic structure, and a description

sampled to 10% of the original sets.

of the phonation mechanisms.

Fig. 1 - Sound spectrograms of Indri indri vocal types: Roar (a), honk (b, anticipated by voiced inhalation), hum (c), short tonal call (d), long tonal call (e), kiss (f), wheeze (g), grunt (h), infant calls (hum, iI; contact-seeking call, iII; grunt, iIII) and the indri song (j, showing introductory roars). All spectrograms were generated in Praat 5.1.15 (www.praat.org) with the following parameters: window length: 0.02 sec, time range as shown (max. 0-62 sec); frequency range: 0-12000 Hz; maximum: 100 dB/Hz; dynamic range: 30-55 dB; dynamic compression: 0.0.

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Tab. 2 - Deﬁnition of the vocal types including synonyms used in previous works, context of emis-

sion, description of the call usage and phonation mechanics. References as follows: Petter, 1962 (1); Pollock, 1975 (2); Petter & Charles-Dominique, 1979 (3); Pollock, 1986 (4); Thalmann et al., 1991 (5); Macedonia & Stanger, 1994 (6); Sorrentino et al., (in press) (7); Giacoma et al., (in press) (8).

Call Type Synonyms

Context

Description

Phonation

Roar

Roar (4, 6),

bark (3),
Antipredatory
Loud and harsh vocalization used as a standalone vocal signal in the presence of aerial predators.
Mouth open waa note (5), aboiement (1)

Honk

Honk (3, 6),

klaxon (1), exhaled hoot (2), honk note (5)
Antipredatory
Alone, or together with other group individuals, indris produce rhythmic, rapid alerting calls given in series of short loud notes. These calls are given when terrestrial predators (e.g. fossa) or potential predators (e.g. mongoose, dog) are present. Nonhabituated indris emitted this also in presence of human observers. Inhalation before the uttering of honks is sometimes visible from the spectrograms.
Mouth open