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RESEARCH ARTICLE
Acoustic Structure and Contextual Use of
Calls by Captive Male and Female Cheetahs
(Acinonyx jubatus)
Darya S. Smirnova
1
, Ilya A. Volodin
2,3
*, Tatyana S. Demina
3
, Elena V. Volodina
3
1Department of Animal Science, Russian State Agrarian University—Moscow Timiryazev Agricultural
Academy, Moscow, Russia, 2Department of Vertebrate Zoology, Faculty of Biology, Lomonosov Moscow
State University, Moscow, Russia, 3Scientific Research Department, Moscow Zoo, Moscow, Russia
*volodinsvoc@gmail.com
Abstract
The vocal repertoire of captive cheetahs (Acinonyx jubatus) and the specific role of meow
vocalizations in communication of this species attract research interest about two dozen
years. Here, we expand this research focus for the contextual use of call types, sex differ-
ences and individual differences at short and long terms. During 457 trials of acoustic
recordings, we collected calls (n = 8120) and data on their contextual use for 13 adult chee-
tahs (6 males and 7 females) in four Russian zoos. The cheetah vocal repertoire comprised
7 call types produced in 8 behavioural contexts. Context-specific call types (chirr, growl,
howl and hiss) were related to courting behaviour (chirr) or to aggressive behaviour (growl,
howl and hiss). Other call types (chirp, purr and meow) were not context-specific. The val-
ues of acoustic variables differed between call types. The meow was the most often call
type. Discriminant function analysis revealed a high potential of meows to encode individual
identity and sex at short terms, however, the vocal individuality was unstable over years.
We discuss the contextual use and acoustic variables of call types, the ratios of individual
and sex differences in calls and the pathways of vocal ontogeny in the cheetah with relevant
data on vocalization of other animals.
Introduction
Cheetahs (Acinonyx jubatus) are among animals that are most attractive for people due to their
nice appearance and interesting communicative behaviour with conspecifics and humans [1,2].
The cheetahs were intensely studied in relation to their wildlife ecology [3–7], conservation [8–
10], diseases [11], morphology [12–14] and genetics [15–17]. At the same time, the acoustic
communication is rather poorly investigated for the cheetah.
Previously, based on the acoustic structure, call types of the vocal repertoire have been
described for cheetah cubs [18] and for cheetah adults [19]. The vocal repertoire of adult chee-
tahs comprises eight call types: purr, hiss, growl, chirr, meow, chirp, howl and gurgle [19](Fig
1and S1 Audio). In cheetah cubs younger three months, the vocal repertoire comprised of the
same seven call types as in adults, for the exclusion of the gurgle [18]. For assessing the
PLOS ONE | DOI:10.1371/journal.pone.0158546 June 30, 2016 1/20
a11111
OPEN ACCESS
Citation: Smirnova DS, Volodin IA, Demina TS,
Volodina EV (2016) Acoustic Structure and
Contextual Use of Calls by Captive Male and Female
Cheetahs (Acinonyx jubatus). PLoS ONE 11(6):
e0158546. doi:10.1371/journal.pone.0158546
Editor: Gianni Pavan, University of Pavia, ITALY
Received: April 1, 2016
Accepted: June 19, 2016
Published: June 30, 2016
Copyright: © 2016 Smirnova et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are
credited.
Data Availability Statement: All data and
measurements are available without restrictions from
the paper, figures and Supporting Information. S1
Table contains acoustic measurements (10 acoustic
variables) of cheetah seven call types for describing
the acoustics of call types, in total 194 calls. S2 Table
contains acoustic measurements (9 acoustic
variables) of cheetah meows for estimating the
effects of sex and individuality on the acoustic
variables of meows and for estimating the stability of
vocal individuality in meows, in total 221 calls. Data
from S1 and S2 Tables are sufficient for calculation all
results and statistical comparisons, which are
provided in this paper.
functional role of different call types in the cheetah, a hypothetical scheme relating the acoustic
structure with emotional states of confidence/diffidence and aggressiveness/non-aggres-
siveness, has been proposed [19]. However, this scheme has not yet been confirmed with quan-
titative material on the contextual use of calls.
Whereas the study by Volodina [19] was related to the entire vocal repertoire of adult chee-
tahs, all other studies of cheetah vocalizations were related to particular call types within the
cheetah vocal repertoire. On example of cheetah purr and chirr vocalizations, the mechanism of
vocal vibration, representing an uninterrupted emission of pulsed vocalization for the duration
of both inspiration and expiration phases of breathing, has been investigated [20]. Purring is
caused by rapid twitching of the vocalis muscle, whereas the chirr vocalization is caused with
interaction between the purr and the tonal vocalization produced by the normal vibration of the
vocal folds [20,21]. The acoustics of cheetah purr vocalizations, produced continuously during
the inspiration and expiration phases, were also examined in a few studies [19,22–24]. The acous-
tics of agonistic vocalizations of the cheetah have been considered by Eklund with coauthors
[25]. Frustrative meows of captive adult male and female cheetahs and of cheetah cubs, were pre-
liminary described in [26]. The studies focused on searching the vocal indicators of reproductive
state in the cheetah [27,28] revealed that males produce a specific “courting”series of chirrs inter-
spersed with chirps when exposed to urine samples taken from receptive females.
While the bark represents the most characteristic vocalization of canids [29–36], the meow
represents the most characteristic vocalization of felids, either wild [37–39] or domesticated
[38–43]. Consistently, the meow represents a prominent vocalization in their vocal repertoire
of the cheetah [18,19,26]. Cheetah meows occur in different contexts but primarily in the con-
texts related to frustration and discomfort (solicitation, anticipation and separation)
[26,44,45]. Previously, vocal individuality of meow calls was shown in the isolation context for
domestic kittens (Felis catus)[42] and for four adult male cheetahs [44]. At the same time, sex-
specific variation of vocalizations was not yet studied for any felid species, although some vocal
sex dimorphism is expected given the sexual dimorphism in body size. For example, approxi-
mately 20% difference in body mass exists between male and female domestic cats [46], 15%
between male and female captive cheetahs [8] and 22% between male and female wild cheetahs
[14]. Therefore, the vocal apparatus and the sound-producing structures are also expected to
be larger for the larger sex [47,48] and their acoustics (the fundamental and formant frequen-
cies) are expected to be lower in the larger sex [49,50]. However, very close or indistinguishable
acoustics between vocalizations of the larger and smaller sex were reported for some subspecies
of red deer (Cervus elaphus hispanicus [51] and C.e.sibiricus [52]).
The contextual use of different call types represents the powerful tool for examining the
functions of these calls [53]. For the cheetah, the occurrence of different call types across beha-
vioural contexts in captivity was examined only preliminary [45]. The focus of this study is to
integrate the structural and contextual analysis of cheetah vocalizations for more precise assess-
ment of the functional role of different call types in this species. The purposes of this study
were: 1) to estimate quantitatively the contextual use of different call types by adult captive
cheetahs across behavioural contexts, 2) to estimate quantitatively the identity and sex-related
differences in meows at short terms and 3) to estimate the stability of vocal individual traits in
cheetah meows over years.
Material and Methods
Ethics statement
Three authors (IAV, EVV and TSD) are zoo staff members, so no special permission was
required for them and for their Master’s student (DSS) to work with animals in Moscow Zoo
Cheetah Vocal Repertoire
PLOS ONE | DOI:10.1371/journal.pone.0158546 June 30, 2016 2/20
Funding: This work was supported by Russian
Science Foundation (http://www.rscf.ru/) funding to
IAV, DSS and EVV, grant number 14-14-00237. This
research received no additional funding from any
public, commercial or not-for-profit sectors. The
funder had no role in study design, data collection
and analysis, decision to publish, or preparation of
the manuscript.
Competing Interests: The authors have declared
that no competing interests exist.
Fig 1. Spectrogram illustrating seven call types produced by adult (male and female) cheetahs (Acinonyx jubatus)in
captivity. A–purr, B–hiss, C–growl, D–chirr, E–meow, F–chirp, G–howl (S1 Audio). The spectrogram was created at 11025
Hz sampling frequency, Fast Fourier Transform (FFT) 1024, Hamming window, frame 50%, overlap 93.75%.
doi:10.1371/journal.pone.0158546.g001
Cheetah Vocal Repertoire
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and Volokolamsk Zoo Breeding Station. For access to the cheetahs kept in Yaroslavl and Novo-
sibirsk zoos, the specific permissions were obtained from administration of these zoos by the
request from the President Director of Moscow Zoo V.V. Spitsin for the period of data collec-
tion. Vocalizations were recorded from inside and outside the animal enclosures during zoo
working hours under supervision of zoo staff. Call collector (DSS) did not manipulate the ani-
mals for the purpose of this study. Disturbance of animals was kept to a minimum. No animal
has suffered somehow due to the data collection. The research protocol # 2011–36 has been
approved by the Committee of Bio-ethics of Lomonosov Moscow State University. We adhered
to the ‘Guidelines for the treatment of animals in behavioural research and teaching’(Anim.
Behav., 2006, 71, 245–253) and to the laws on animal welfare for scientific research of the Rus-
sian Federation, where the study was conducted.
Study subjects
Spontaneously produced calls of 13 (6 male and 7 female) adult (older 2 years) captive-born
cheetahs of the African subspecies (A.j.jubatus) were recorded in 2012–2014 in zoos of Russia.
In particular, six animals (Male 1 “Seva”, Male 2 “Adam”, Male 3 “Kay”, Female 7 “Eva”,
Female 8 “Sindi”, Female 9 “Kimi”) were recorded at Volokolamsk Zoo Breeding Station of
Moscow Zoo (Moscow region, Volokolamsk district) in May-August 2012. Five of these ani-
mals (Males 1, 2 and Females 7, 8, 9) were then repeatedly recorded in June-July 2014 and their
calls served for analysis of the stability of the individual acoustic characteristics with time.
Two animals (Male 4 “Adday”, Female 10 “Nayla”) were recorded in Yaroslavl Zoo (Jaro-
slavl city) in June 2013. Two animals (Male 5 “Kidjan”, Female 11 “Annay”) were recorded in
Novosibirsk Zoo (Novosibirsk city) in July 2013. Three animals (Male 6 “Frank”, Female 12
“Zygota”, Female 13 "Winda") were recorded in Moscow Zoo (Moscow city) in October-
November 2014.
Animal housing
Animals were kept in outdoor enclosures (sizes varied from 240 to 500 m
2
depending on the
zoo) containing the indoor enclosures (warm houses subdivided inside into four departments
4x4 m, individual for each animal). During the day, animals were released into the outdoor
enclosure (together or singly, depending on the zoo), whereas during the night they stayed
inside their individual indoor enclosures. The walls of the indoor enclosures were made of
wire-mesh, so the animals could see the conspecifics in the indoor enclosures. The feeding
occurred twice a day in the individual indoor enclosures, the first one in the morning before
the releasing to the outdoor enclosures and the second one in the evening, before the locking
the exit for the night.
Call collection
Calls were recorded indoor and outdoor. The call collector (DSS) was in the same indoor or
outdoor enclosure as animals, but was separated from them with wire-mesh and not entered
into contact with animals. Calls were collected by the focal animal sampling method [54]. For
sound recordings (sampling rate 48 kHz, 16 bit resolution) we used a Zoom-H4n professional
digital recorder (Zoom Corporation, Tokyo, Japan) with built-in microphones. All acoustic
recordings were conducted during daytime in periods of maximal activity of the animals dur-
ing routine procedures (feeding, releasing from indoor to outdoor enclosures, communication
of animals with their keepers and with other cheetahs through the wire-mesh).
We established eight mutually exclusive behavioural contexts in which calls were produced:
1) "Offensive" context (attack or threat aggression toward a human, researcher or keeper, or
Cheetah Vocal Repertoire
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toward a conspecific); 2) "Defensive" context (defensive aggression toward a human or conspe-
cific); 3) "Conspecific-Contact" context (friendly close-range communication between conspe-
cifics); 4) "Call-Over" context (distant communication with a conspecific, commonly without
visual contact); 5) "Human-Contact" context (friendly close-range communication with a
human, researcher or keeper); 6) "Release-Soliciting" context (keeper-directed soliciting to
release the animal outdoor or back; 7) "Food-Anticipating" context (feeding anticipation and
arousal when seeing the food and feeding the neighbor animals; 8) "Courting" context (male
courting female as a component of sexual behaviour). Calls were not used as markers for iden-
tifying the contexts. During the recording, the researcher labeled the context by voice. Individ-
uals could be distinguished by their coloration pattern. The distance from microphones to the
animals was 0.5–10 m. Each recording trial (457 trials in total) lasted 1–10 minutes, contained
calls from a single individual cheetah and was stored as a wav-file. The number of trials per
cheetah individual was from 6 to 86, on average 35.2 ± 23.7 trials per individual.
Call samples
We tried to collect material maximally balanced by individuals and contexts. However, as vocal
activity of different individuals was unequal, call samples were unevenly distributed by differ-
ent animals. Most indoor recordings contained echo; this did not interfere determining call
types but limited the number of calls potentially applicable for analysis of the acoustic struc-
ture. We prepared four different call samples: 1) for analysis of the occurrence of call types in
different behavioural contexts, 2) for describing the acoustics of call types, 3) for estimating the
effects of sex and individual identity on the acoustics of meows and 4) for estimating the stabil-
ity of the acoustic individuality in meows with time.
For analysis of the occurrence of call types in different behavioural contexts, we analysed a
total of 8120 cheetah calls for their call type using the Avisoft SASLab Pro software (Avisoft
Bioacoustics, Berlin, Germany). Based on frequency and temporal acoustic structure, we subdi-
vided calls into seven types: purr, hiss, growl, chirr, meow, chirp and howl (Fig 1), following
the early classification [19]. In cases when calls had a transitional acoustic structure [19], e.g.
from meow to purr or from howl to growl, each call part was treated as a separate call. For each
call, we determined the behavioural context (among the eight contexts) in which it was pro-
duced. Then we examined the contexts in which the 8120 calls were used, following the criteria
previously adopted by Salmi et al. [53]. We classified a call type as context-specific if it was
given in the same behavioral context more than 65% of cases. Because multiple call types can
be used in the same context, we then examined whether this was the primary call type for this
context, classifying it as signal-specific if it accounted for more than 65% of all calls given dur-
ing that context [53].
For describing the acoustics of call types, occurring in cheetahs in captivity, we selected
from the total massive of recordings from 6 to 60 calls per each of the 7 call types, 183 calls in
total. For each call type, calls were taken from 3 to 12 animals. We took calls of best quality, not
superimposed with other calls and background noise.
For estimating the effects of sex and individuality on the acoustic variables of meows, we
selected 10–15 calls per individual from 12 individuals, for the exclusion of Female 13, which
did not produce meows, 151 meows in total. To decrease the effect of pseudoreplication, we
selected calls from different recording trials and within recording trials calls from different
parts of the trial, avoiding taking calls following one after other.
For estimating the stability of vocal individuality in meows with time (over 2 years), we
selected 10–15 meows per individual from 5 individuals (Males 1, 3 and Females 7, 8, 9)
recorded in 2012 (69 meows) and in 2014 (70 meows), 139 meows in total.
Cheetah Vocal Repertoire
PLOS ONE | DOI:10.1371/journal.pone.0158546 June 30, 2016 5/20
Call analysis
Only calls with high call-to-noise ratio, non-overlapped with background noise or calls of
other individuals, non-disrupted by wind, and clearly identified as belonging to focal individu-
als were included in the analysis. For call analysis, we used Avisoft, with 48 kHz sampling fre-
quency, the Hamming window, FFT length 1024 points, frame 50% and overlap 93.75%. These
settings allowed frequency resolution 46 Hz and time resolution 1.3 ms. All measurements
were made manually and have been exported to Microsoft Excel (Microsoft Corp., Redmond,
WA, USA).
For calls of all types, we measured the duration from the screen with the standard marker
cursor in the spectrogram window (Fig 2), for the exclusion of purr, whose duration could last
many minutes. In addition, for all calls of all types, we measured the maximum amplitude fre-
quency (f peak) and three quartiles (q25, q50 and q75), covering respectively 25, 50 and 75% of
call energy (hereafter the lower, medium and upper quartiles) from the mean power spectrum
of each call. For purr, produced continuously at both respiratory phases, the acoustic variables
were measured separately for the inspiration and the expiration call phases. In calls with rhyth-
mic pulsation (chirr, growl and purr call types) we also measured with the standard marker
cursor the pulse rate. For each purr vocalization, three subsequent phases of expiration-inspira-
tion were included in analyses for calculating power variables and pulse rate. In growl, meow,
chirp and howl calls we additionally measured, with the reticule cursor, the initial (f0 beg),
end (f0 end), maximum (f0 max) and minimum (f0 min) fundamental frequencies of each call
(Fig 2).
The acoustic measurements for describing the acoustics of call types are presented in S1
Table. The acoustic measurements for estimating the effects of sex and individuality on the
Fig 2. Measured variables for cheetah meows. Spectrogram (right) and mean power spectrum of the entire call (left). Designations: duration–call duration;
f0 beg–the fundamental frequency at the onset of a call; f0 end–the fundamental frequency at the endof a call; f0 max–the maximum fundamental frequency;
f0 min–the minimum fundamental frequency; f peak–the frequency of maximum amplitude within a call; q25, q50 q75 –the lower, the medium and the upper
quartiles, covering respectively 25%, 50% and 75% energy of a call spectrum. The spectrogram was created at 11025 Hz sampling frequency, Fast Fourier
Transform (FFT) 512, Hamming window, frame 50%, overlap 96.87%.
doi:10.1371/journal.pone.0158546.g002
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acoustic variables of meows and for estimating the stability of vocal individuality in meows
with time are presented in S2 Table.
Statistical analyses
Statistical analyses were made with STATISTICA, v. 6.0 (StatSoft, Tulsa, OK, USA) and R
v.3.0.1 [55]; all means are given as mean ± SD. Significance levels were set at 0.05, and two-
tailed probability values are reported. Only 20 of 224 distributions of measured parameter val-
ues did depart from normality (Kolmogorov-Smirnov test, p>0.05) what allowed us to apply
parametric tests.
We used a two-way ANOVA with Tukey HSD test to compare the acoustics among call
types, with call type as fixed factor and individual as random factor. We used a two-way
ANOVA with Tukey HSD test to compare the acoustics between purr inspiration and expira-
tion phases, with phase as fixed factor and individual as random factor. We used a nested
design of ANOVA with an individual nested within sex to estimate effects of factors “individu-
ality”and “sex”, on the acoustic variables of meows, with sex as fixed factor and individual as
random factor.
We used standard procedure of discriminant function analysis (DFA) to calculate the prob-
ability of the assignment of meows to the correct individual. Nine variables, used for the DFA,
showed very low Pearson correlation values to each other. Among the total of 36 pairwise cor-
relations, the R
2
values were lower 0.2 for 23 comparisons; between 0.2 and 0.4 for 3 compari-
sons; between 0.4 and 0.6 for 4 comparisons; between 0.6 and 0.8 for 5 comparisons, and only
for 1 comparison (f0 end with f0 min) the R
2
value was 0.91. Then we investigated the stability
of acoustic individuality of meows between years for cheetahs that provided calls in two years.
We classified meows from 2014 with DFA functions derived from 2012, considering the value
of the correct cross-validation as a measure of the retention of individuality over time [56–58].
With a 2x2 Yates' chi-squared test, we compared the values of correct assignment of meows to
the correct caller between years.
We used Wilks’Lambda values to estimate how strongly acoustic variables of calls contrib-
ute to discrimination of individuals. To validate our DFA results, we calculated the random val-
ues of correct assignment of calls to individual by applying randomization procedure with
macros, created in R. The random values were averaged from DFAs performed on 1000 ran-
domized permutations on the data sets as described by [59]. Using a distribution obtained by
the permutations, we noted whether the observed value exceeded 95%, 99% or 99.9% of the val-
ues within the distribution [59]. If the observed value exceeded 95%, 99% or 99.9% of values
within this distribution, we established that the observed value did differ significantly from the
random one with a probability p<0.05, p<0.01 or p<0.001 respectively [57–60].
Results
Acoustic structure of cheetah calls
From the total sample of cheetah calls, 7228 calls could be classified to distinctive call types,
whereas 446 calls (5.81%, N = 7674 calls) were transitional from one call type to another (thus
including two different call types, one after another without time space between them). In
these cases each call part of the transitional call was treated as a separate call, what resulted in
the total sample of 8120 calls analysed for call type. Most often transitional calls occurred
between purr and meow (267 calls), growl and howl (86 calls) and growl and meow (60 calls).
Based on ANOVA results, we found that all acoustic variables were significantly related to
call type (Table 1). The duration did not differ between the growl and howl, being significantly
higher than in all other call types for the exclusion of purr, the continuous vocalization whose
Cheetah Vocal Repertoire
PLOS ONE | DOI:10.1371/journal.pone.0158546 June 30, 2016 7/20
duration could not be measured. The duration did not differ significantly between the chirr,
meow, chirp and hiss call types (Table 1 and Fig 1).
The pulse rate was minimal in the chirr, intermediate in the purr and maximal in the growl
call type; all differences were found significant. All fundamental frequency variables did not
differ between the growl and howl call types, being significantly lower than for the meow and
chirp call types and for the meow significantly lower than for the chirp (Table 1,Fig 1).
The values of the peak frequency and of the three power quartiles were the highest for the
chirp, lower for the meow and more prominently lower for the chirr. For the purr, growl, howl
and hiss, the values of the peak frequency and of the three power quartiles were the lowest ones
and differed significantly from the three other call types (for the exclusion of q50 and q75 for
the hiss) (Table 1).
For the purr, we also compared the values of acoustic variables between the inspiration and
expiration phases (Table 2). The values of the pulse rate, the peak frequency, and the lower and
medium quartiles were significantly higher for the inspiration phase than for the expiration
phase, whereas the values of the upper quartile did not differ between the inspiration and expi-
ration phases of the purr call type (Table 2).
Context and signal-specific call types
Four of 7 call types were context-specific (i.e., given mostly in one specific context), including
growl, howl and hiss (during Offensive context) and chirr (during Courting context) (Table 3).
All context-specific calls were given in a single context more than in 80% cases, except for
Table 1. Values (mean±SD) of acoustic variables for the cheetah call types.
Acoustic Call type ANOVA
variable Chirr (N = 11) Purr (N = 11) Growl (N = 33) Meow (N = 60) Chirp (N = 6) Howl (N = 19) Hiss (N = 43)
Duration (s) 0.74±0.73
a
2.34±1.31
b
0.32±0.14
a
0.11±0.04
a
2.11±1.28
b
0.62±0.20
a
F
5,154
= 38.01; p<0.001
Pulse rate (Hz) 16.59±1.03
a
22.68±2.67
b
37.40±4.28
c
----F
2,44
= 98.46; p<0.001
f0 beg (kHz) - - 0.16±0.09
a
0.81±0.31
b
1.81±0.65
c
0.26±0.10
a
-F
3,102
= 69.85; p<0.001
f0 end (kHz) - - 0.15±0.03
a
0.69±0.24
b
0.89±0.39
c
0.25±0.09
a
-F
3,102
= 67.76; p<0.001
f0 max (kHz) - - 0.19±0.08
a
0.94±0.35
b
1.81±0.65
c
0.31±0.14
a
-F
3,102
= 74.29; p<0.001
f0 min (kHz) - - 0.14±0.04
a
0.68±0.23
b
0.89±0.39
c
0.21±0.06
a
-F
3,102
= 77.18; p<0.001
f peak (kHz) 0.59±0.33
a
0.16±0.14
b
0.21±0.11
b
1.07±0.40
c
1.76±0.60
d
0.27±0.10
b
0.32±0.11
b
F
6,157
= 77.58; p<0.001
q25 (kHz) 0.68±0.26
a
0.14±0.11
b
0.19±0.08
b
1.01±0.32
c
1.63±0.61
d
0.24±0.10
b,e
0.42±0.25
e
F
6,164
= 80.26; p<0.001
q50 (kHz) 1.19±0.36
a,d
0.32±0.14
b
0.34±0.16
b
1.52±0.42
a,c
1.88±0.61
c
0.44±0.31
b
1.01±0.72
d
F
6,164
= 40.18; p<0.001
q75 (kHz) 2.03±0.44
a
0.88±0.50
b
0.88±0.77
b
2.14±0.73
a
2.44±0.42
a
0.99±0.91
b
2.30±1.01
a
F
6,164
= 24.88; p<0.001
Results for comparison of acoustics between call types (two-way ANOVA with Tukey HSD test with call type as fixed factor and individual identity as random
factor) are given with letters; means sharing the same letter are not significantly different. N = total number of calls of each type.
doi:10.1371/journal.pone.0158546.t001
Table 2. Values (mean±SD) of acoustic variables for the cheetah purr inspiration and expiration phases.
Acoustic variable Inspiration (N = 11) Expiration (N = 11) ANOVA
Pulse rate (Hz) 24.57±2.05 20.80±1.74 F
1,18
= 64.65; p<0.001
f peak (kHz) 0.25±0.15 0.08±0.03 F
1,14
= 18.129; p<0.001
q25 (kHz) 0.21±0.11 0.08±0.03 F
1,18
= 22.58; p<0.001
q50 (kHz) 0.43±0.05 0.21±0.11 F
1,18
= 40.68; p<0.001
q75 (kHz) 0.91±0.22 0.84±0.69 F
1,18
= 0.09; p=0.77
Note: Three subsequent phases of expiration-inspiration measured for each poor vocalization (N = 11) served for calculating the acoustic variables.
doi:10.1371/journal.pone.0158546.t002
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howl, which were given in a context-specific way in 72.2% cases. The three remaining call types
(meow, chirp and purr) were not found context-specific. The meow was the single call type
occurring in all behavioural contexts (Table 3).
For each of the 8 behavioural contexts we found the signal-specific call types (i.e., the most
common call type used in a specific context) (Table 4). The chirr was given primarily during
the Courting context; the purr was given primarily during the Human-Contact context. The
growl was given primarily during two aggressive contexts: the Offensive and the Defensive.
The meow usage was specific during four contexts: the Conspecific-Contact, the Call-Over, the
Release-Soliciting and the Food-Anticipation. The remaining three call types (chirp, howl and
hiss) were not signal-specific (Table 4).
Effects of identity and sex on meow acoustics
Two-way ANOVA revealed effects of individual identity on all variables of meows, whereas
effects of sex were found only on variables of fundamental frequency (Table 5). Values of all fun-
damental frequency variables were substantially and significantly lower in males than in females
(for instance, the f0 max was 0.85±0.40 kHz in males and 1.07±0.25 kHz in females, Table 5).
We conducted two DFAs (for sex and for individual identity), each DFA based on all the 9
measured variables of meows. The DFA showed the average values of correct assignment to sex
Table 3. Call context-specificity: the percent of calls given in each of context, context-specific calls (i.e., for which >65%) are indicated in bold.
Call Context
type N
VOC
Offensive Defensive Conspecific-Contact Call-Over Human-Contact Release-Soliciting Food-Anticipating Courting
Chirr 978 0 0.2 0 0 2.2 0 0.1 97.4
Purr 1045 0 0 1.1 0.5 48.0 2.8 47.7 0
Growl 1485 81.1 9.6 0 0 0 1.9 7.3 0.2
Meow 3867 0.6 0.1 1.3 5.7 1.9 37.1 45.6 7.8
Chirp 73 1.4 2.7 0 26.0 1.4 52.1 8.2 8.2
Howl 212 72.2 6.6 0 0 0 8.0 13.2 0
Hiss 460 87.8 8.9 0 0 0 0 3.3 0
N
BC
8120 1786 204 60 243 598 1548 2418 1263
N
VOC
= total number of calls of each type recorded in all contexts; N
BC
= total number of calls given in each behavioral context.
doi:10.1371/journal.pone.0158546.t003
Table 4. Call signal-specificity: the percent of 7 call types given in each context, signal-specific calls (i.e., those for which >65% are given in a sin-
gle context) are indicated in bold.
Context Call type
N
BC
Chirr Purr Growl Meow Chirp Howl Hiss
Offensive 1786 0 0 67.4 1.3 0.1 8.6 22.6
Defensive 204 1.0 0 69.6 1.5 1.0 6.9 20.1
Conspecific-Contact 60 0 18.3 0 81.7 000
Call-Over 243 0 2.1 0 90.1 7.8 0 0
Human-Contact 598 3.7 83.9 0 12.2 0.2 0 0
Release-Soliciting 1548 0 1.9 1.8 92.8 2.5 1.1 0
Food-Anticipating 2418 0.1 20.6 4.5 72.9 0.2 1.2 0.6
Courting 1263 75.5 0 0.2 23.8 0.5 0 0
N
VOC
8120 978 1045 1485 3867 73 212 460
N
VOC
= total number of calls of each type recorded in all contexts; N
BC
= total number of calls given in each behavioral context.
doi:10.1371/journal.pone.0158546.t004
Cheetah Vocal Repertoire
PLOS ONE | DOI:10.1371/journal.pone.0158546 June 30, 2016 9/20
of 78.1%, what was significantly higher than the random value 59.4 ± 3.3% (permutation test,
1000 permutations, p<0.001) (Fig 3). In order of decreasing importance, the f0 beg, duration
and q50 were mainly responsible for discrimination of sex for the meows.
At the same time, DFA showed the average values of correct assignment to individual of
59.6%, what was significantly higher than the random value 25.5 ± 3.0% (permutation test,
1000 permutations, p<0.001) (Fig 3). In order of decreasing importance, the f0 max, q75 and
q25 were mainly responsible for discrimination of individuals for the meows. However, the
value of correct assignment varied among individuals from 20% to 73.3%, and for one of 12 indi-
viduals did not differ from the random value. Thus, meows had reliable individual-specific traits
Table 5. Values (meanSD) of the cheetah meow variables and results of nested ANOVA for individual and sex differences.
Acoustic ANOVA Variable values for each sex
variable Individual differences Sex differences Male calls (N = 71) Female calls (N = 80)
Duration (s) F
10,139
= 5.43; p<0.001 F
1,139
= 0.54; p= 0.46 0.31±0.17 0.34±0.14
f0 beg (kHz) F
10,139
= 4.79; p<0.001 F
1,139
= 40.19; p<0.001 0.68±0.29 0.92±0.22
f0 end (kHz) F
10,139
= 12.01; p<0.001 F
1,139
= 33.54; p<0.001 0.62±0.25 0.77±0.16
f0 max (kHz) F
10,139
= 13.18; p<0.001 F
1,139
= 29.30; p<0.001 0.85±0.40 1.07±0.25
f0 min (kHz) F
10,139
= 9.90; p<0.001 F
1,139
= 40.83; p<0.001 0.59±0.22 0.76±0.16
f peak (kHz) F
10,139
= 11.52; p<0.001 F
1,139
= 0.28; p= 0.60 1.22±0.74 1.11±0.35
q25 (kHz) F
10,139
= 20.27; p<0.001 F
1,139
= 0.01; p= 0.91 1.04±0.51 1.00±0.20
q50 (kHz) F
10,139
= 9.32; p<0.001 F
1,139
= 1.62; p= 0.21 1.58±0.63 1.43±0.38
q75 (kHz) F
10,139
= 4.35; p<0.001 F
1,139
= 0.0; p= 0.98 2.38±0.79 2.31±0.64
Note: Individual nested within sex (with sex as fixed factor, and individual as random factor); N = 12 cheetahs (6 males and 6 females).
doi:10.1371/journal.pone.0158546.t005
Fig 3. Sex and individual discrimination of the cheetah meows. Green bars indicate values of
discriminant function analysis and yellow bars indicate random values, calculated with the randomization
procedure. Comparisons between observed and random values with permutation tests are shown above the
bars.
doi:10.1371/journal.pone.0158546.g003
Cheetah Vocal Repertoire
PLOS ONE | DOI:10.1371/journal.pone.0158546 June 30, 2016 10 / 20
not in all individuals. Therefore, cheetah meows bear reliable cues to sex (higher fundamental fre-
quency in females compared to males) and have a potential to encode individual identity.
Between-year stability of meows
For 5 animals (2 males and 3 females) that provided sufficient number of meows in both 2012
and 2014, we compared the stability of vocal individuality in meows between years (Fig 4).
Within years, DFA showed high values of correct classification of meows to individual (75.4%
in 2012 and 78.6% in 2014) significantly exceeding the random value (44.4 ± 5.1% in 2012 and
44.8 ± 5.3% in 2014, permutation test, p<0.001 in both cases), and did not differ between
years (χ
21
= 0.06, p= 0.80).
However, cross-validation of meows recorded in 2014 using discriminant functions created
for meows recorded in 2012, revealed a strong decrease in the correct classification of individu-
als (Fig 4). The average value of correct classification dropped to the level expected by chance
alone (42.9%), and became significantly lower compared to call samples from either 2012
(χ
21
= 13.86, p= 0.002) or from 2014 (χ
21
= 17.25, p<0.001). Thus, in the cheetah, individual
identity of meows was unstable between years.
Discussion
Vocal repertoire of adult cheetahs
We found that values of acoustic variables were substantially different between call types in the
cheetah. In this sense, the cheetah vocal repertoire can be considered as “discrete”vocal
Fig 4. Discrimination of individual cheetahs by meows in two years (2012 and 2014). Green bars indicate values
of discriminant function analysis and yellow bars indicate random values, calculated with a randomization procedure.
Comparisons between observed and random values with permutation tests and comparisons between 2012 and 2014
meows with χ
2
tests are shown by brackets above the bars. The red bar indicates the classification value of 2014
meows with discriminant functions created for meows recorded in 2012.
doi:10.1371/journal.pone.0158546.g004
Cheetah Vocal Repertoire
PLOS ONE | DOI:10.1371/journal.pone.0158546 June 30, 2016 11 / 20
repertoire, similar to the more or less “discrete”vocal repertoires of other felids [37] and some
ungulates, e.g. red deer [52]. This is distinctive to the more “continual”vocal repertoires, e.g.,
in red fox (Vulpes vulpes)[36] and in the wild boar (Sus scrofa)[61], in which a noticeable
number of intermediate vocalizations occurred along to distinctive call types. Transitional
forms from one call type to another occurred only in 5.8% cases, similar to [19]. No complicat-
ing features such as nonlinear phenomena or articulation effects [36,62] have been detected in
the cheetah vocalizations by this or previous studies.
The values of acoustic variables were close to those found in the previous study of the cheetah
vocal repertoire [19]. For instance, the average pulse rate of the chirr was 16.6 Hz in this study and
18.4 Hz in [19]; the pulse rate of the purr was 22.7 Hz in this study and 23.5 Hz in [19]; and the
pulserateofthegrowlwas37.4Hzinthisstudyand36.4Hzin[19], although the samples of ani-
mals, the animal housing and the staff were entirely different compared to the former study [19].
For the two phases (expiration and inspiration) of the purr vocalization, we found the differ-
ences in the pulse rate, the peak frequency, and in the lower and medium quartiles (all were sig-
nificantly higher for the inspiration phase than for the expiration phase). The differences in the
pulse rate (24.6 Hz during the expiration phase and 20.8 Hz during the inspiration phase) were
similar with those reported by [20] (26 Hz and 21 Hz respectively), by [24] (20.9 Hz and 18.3
Hz respectively) and by [63] (21.9–23.4 Hz and 19.3–20.9 Hz respectively). The average value
of pulse rate for the cheetah purr of 17.5 Hz [23] probable represents the value of pulse rate for
the cheetah chirr, as in another study of this author [22] the average value of pulse rate for the
cheetah chirr (termed the gurgle by [22]) was 16 Hz (ranging from 11 to 20.8 Hz).
Contextual use of call types in the cheetah
Context-specific call types were either related to aggressive behaviour in the Offensive context
(growl, howl and hiss) or to sexual behaviour in the Courting context (chirr). Consistently, ear-
lier studies report that male cheetahs produce the chirrs when courting receptive females,
whereas females use the chirrs for communication with cubs [19,64]. Towards urine samples of
non-receptive (not ready to mate) females, male cheetahs remain silent [27,28]. This helps to
select appropriate time for joining pairs for mating [27,28], as in zoos, males and female chee-
tahs are kept separately [65], otherwise they do not breed. Chirr vocalizations given towards
female urine sample in the heat indicates male competence as a breeder, whereas male silence
in this situation indicates its incapability to mate [27,28].
Among call types that were not context-specific (chirp, purr and meow) the meow takes an
especial place in the vocal repertoire of captive cheetahs. In this study, the meow was the most
often produced call type (47.6% of all calls, Table 3) presented in both sexes and in 12 of 13
individuals. In four of the 8 behavioural contexts, the meow was the most often call type, being
therefore in terminology of [53] the signal-specific call type for these four contexts. Two of
these contexts (Conspecific-Contact and Call-Over) are related to communication between
conspecifics, therefore they might correspond to the natural usage of meows in the wild. Two
remaining contexts (Release-Soliciting and Food-Anticipation) are specific for the captive con-
ditions, as meows given in these contexts were frustration calls directed toward a keeper and
appealing to human help. The regular use of meows for cheetah-human interactions may indi-
cate manipulating the keeper behaviour by the animals. Similarly, domestic cats use meows for
manipulating their owners [38,40,41]. Consistently, domestic dogs (Canis familiaris) exposed
to insoluble tasks, appeal for help to humans, staring on them and producing specific move-
ments [66] and frustrative whining vocalizations [67].
In contrast to the meow, the chirp was the rarest call type comprising only 0.9% of all calls,
and half of them (52%, Table 3) was given in the Release-Soliciting context. In other studies,
Cheetah Vocal Repertoire
PLOS ONE | DOI:10.1371/journal.pone.0158546 June 30, 2016 12 / 20
the cheetahs used chirps for calling towards cubs, mothers, potential mates or group mates
[44,64]. At experimental separations of coalitions of adult males in captivity, the chirps com-
prised 90% of the total of 196 calls [44]. In addition, consistently to this study, both chirps and
meows were used by cheetahs in contexts of food or stroll soliciting [26]. The found in this
study signal-specificity of the purr for the context of friendly close-range communication with
humans (Human-Contact) is consistent to reported data for the cheetah [2,19,24] and for the
domestic cat [23,24].
In this study, cheetahs more often vocalized in discomfort-related contexts: the Offensive,
Defensive, Release-Soliciting and Food-Anticipating contexts comprised 73.3% of calls,
whereas contexts of friendly interactions between animals (Conspecific-Contact, Call-Over
and Courting) or animals and humans (Human-Contact) comprised only 26.7% of all calls
(Table 4). This agrees well with findings that mammals primarily use calls in contexts related
to the negative emotional arousal and vocalize much more rarely when experience positive or
neutral emotions [68–70].
For analysis of contextual use of call types, we used a pooled sample of calls from all chee-
tahs. This is the single possible approach for analysis of the contextual use of different vocaliza-
tions in either captivity or in the wild [53]. In captivity, each cheetah is situated in unique
conditions that limit the potential number of possible behavioural contexts. For instance, if an
animal is kept with mates, it can display towards them aggressive, friendly or sexual attitudes.
Otherwise, if an animal is kept singly, any interactive contexts are impossible. Furthermore,
high-ranking individuals may initiate aggressive interactions more often compared to the low-
ranking individuals; some cheetahs intended to interact with people whereas others intended
to avoid them. As the result, in our study different individuals participated in different sets of
situations. In nature, equal time of observations for focal animals also did not help to balance
call sets from different individuals by behavioural contexts [53].
Sex and individuality in meows
We found a strong influence of sex on cheetah meow vocalizations. Sexual differences were
well-expressed and mainly were determined by the values of fundamental frequency (lower in
males than in females), whereas the values of all other vocal variables were indistinguishable
between sexes. The found differences in fundamental frequency of about 20% (Table 5) are
comparable with 15% body mass differences between males and females in captive cheetahs [8]
and with 22% body mass differences between males and females in wild cheetahs [14].
However, the values of call fundamental frequency depend primarily on the length of vocal
folds in the larynx [71,72], which are related in most mammals with linear body dimensions.
In the cheetah, differences in linear body dimensions between males and females in the skull
length, the foreleg length and the hind leg length range between 4.2 to 7.3% depending on the
measure [14]. Therefore, we may expect that differences in size of the larynx between male and
female cheetahs exceed the overall differences of linear body size between sexes. Earlier, sex-
specific dimorphism in size of the larynx exceeding body size between males and females was
reported for humans [73], Mongolian gazelles (Procapra gutturosa)[47], and goitred gazelles
(Gazella subgutturosa)[48]. In humans, this dimorphism results from sexual selection for the
lower-pitched male voices as a component of apparent body size exaggeration for attracting
females and competing with males [74,75]. Nevertheless, in the cheetah, voice pitch differences
reliably reflect the differences in body size between sexes, as in most mammalian and bird spe-
cies with sex dimorphism of body size [76,77], but see [51,52].
In cheetah meows, sex differences were higher whereas individual differences were compa-
rable to other mammals, in which DFAs to identity and sex were applied to the same samples
Cheetah Vocal Repertoire
PLOS ONE | DOI:10.1371/journal.pone.0158546 June 30, 2016 13 / 20
of calls and animals. Sex discrimination higher than random was reported for alarm calls of
adult yellow-bellied marmots (Marmota flaviventris)[78], for contact calls of young goitred
gazelles [79] and for alarm calls of giant otters (Pteronura brasiliensis)[80]. At the same time,
in alarm calls of speckled ground squirrels (Spermophilus suslicus)[78], yellow ground squirrels
(S.fulvous)[78] and chinchillas (Chinchilla lanigera)[81] and in barks of two borzoi breeds of
the domestic dog [35], discrimination to sex was found on the level expected by chance alone,
whereas individual differences were comparable to those in cheetah meows in our study.
Although vocal individuality was well-expressed in cheetah meows, these individualistic fea-
tures were unstable over years. Indeed, all studied species of mammals display poor stability of
individual vocal traits with time: speckled and yellow ground squirrels [56,60,82], domestic
dogs [35], red deer [58,83], fallow deer (Dama dama)[57] and common marmosets (Callithrix
jacchus)[84]. In contrast, stable individual and pair duet vocal signatures were found for the
periods up to five years in some birds: red-breasted geese (Branta ruficollis)[85], red-crowned
cranes (Grus japonensis)[86] and crested auklets (Aethia cristatella)[87]. It seems that bird
calls retain better the individualistic traits compared to calls of mammals, however further
study with more species and call types is necessary to confirm this.
Vocal repertoires of adult and cub cheetahs
The vocal repertoire of the cheetah is primarily stated at birth, as all seven call types (chirr,
growl, meow, chirp, howl, purr and hiss) described in adults in this study and in [19] were pre-
viously described in 15 cheetah cubs aged from 2 days to 3 months [18]. However, whereas the
entire set of call types is already presented in cubs, the acoustic variables changed strongly with
age [18,19]. In vocal repertoire of 1.5–3 months-old cubs [18], the average duration of the chirr
was 0.42 s (n = 19 chirrs), that is much shorter than 0.74 s in adults in this study (Table 1); the
average duration of the growl was 0.93 s (n = 24 growls), that is much shorter than 2.34 s in
adults in this study (Table 1), and the average duration of the howl was 0.70 s (n = 6), that is
much shorter than 2.11 s in adults in this study (Table 1). At the same time, the average dura-
tion of cub meow was 0.56 s (n = 38 meows), that is substantially longer than 0.32 s in adults in
this study (Table 1). Consistently, the average duration of cub chirp was 0.32 s (n = 139 calls),
that is much longer than 0.11 s in adults in this study (Table 1).
The fundamental frequency variables also differed between the 1.5–3 months-old cheetah
cubs [18] and adults in this study. The average maximum fundamental frequency of cub
meows was 3.89 kHz (n = 38 meows) that is much higher than 0.94 kHz in adults in this study
(Table 1). The average maximum fundamental frequency of cub chirps was 5.85 kHz (n = 142
chirps) that is much higher than 1.81 kHz in adults in this study (Table 1). The average maxi-
mum fundamental frequency of cub howls was 2.58 kHz (n = 6) that is much higher than 0.31
kHz in adults in this study (Table 1).
For the cheetah, the substantially higher values of maximum fundamental frequency in cubs
than in adults indicate the descending ontogeny of fundamental frequency with age that is
usual for mammals [76,88], some birds [89–91] and reptiles [92]. The distinctive ontogenetic
pathways with same-frequency or even lower-frequency calls in the young than in adults were
reported for the Siberian red deer (Cervus elaphus sibiricus)[52], four species of ground squir-
rels [88,93–95] and two species of shrews [96–98].
Conclusion
All studies of cheetah vocalizations including the present study have been conducted in captiv-
ity. Captive conditions hardly affect the acoustic variables given that cheetah vocal repertoire is
stated at birth. However, the captive conditions might affect somehow the contextual use of
Cheetah Vocal Repertoire
PLOS ONE | DOI:10.1371/journal.pone.0158546 June 30, 2016 14 / 20
vocalization by these animals. Captive conditions include some behavioural contexts that do
not occur in nature (e.g, the contexts involving animal-human communication). At the same
time, some natural contexts may lack in captivity. Further research of vocal behaviour of free-
ranging cheetahs should reveal the natural use of each call type in different ages and sexes of
cheetahs.
Supporting Information
S1 Audio. Calls of adult cheetahs. Purr, hiss, growl, chirr, meow, chirp, howl.
(WAV)
S1 Table. Acoustic measurements of cheetah seven call types for describing the acoustics of
call types.
(XLS)
S2 Table. Acoustic measurements of cheetah meows for estimating the effects of sex and
individuality on the acoustic variables of meows and for estimating the stability of vocal
individuality in meows.
(XLS)
Acknowledgments
We thank the staff of Moscow Zoo, Jaroslavl Zoo, Novosibirsk Zoo and Volokolamsk Zoo
Breeding Station and personally T. Nemtsova and I. Egorov, for their help and support. We
thank the President of Eurasian Regional Association of Zoos and Aquariums (EARAZA), V.
Spitsin, for his administrative help in arrangement of this research in zoos of Russia. We thank
Livio Favaro and the anonymous reviewer for their valuable comments to the manuscript.
Author Contributions
Conceived and designed the experiments: IAV EVV. Performed the experiments: DSS TSD.
Analyzed the data: DSS IAV EVV. Contributed reagents/materials/analysis tools: DSS TSD
IAV EVV. Wrote the paper: DSS IAV EVV.
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