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Vocal repertoire of the social giant otter
Caroline Leuchtenberger
a)
Wildlife Laboratory, Embrapa Pantanal, Corumb
a, Mato Grosso do Sul, Brazil
Renata Sousa-Lima
b)
Laboratory of Bioacoustics, Department of Physiology, Federal University of Rio Grande do Norte, Natal,
Rio Grande do Norte, Brazil
Nicole Duplaix
Fisheries and Wildlife Department, Oregon State University, Corvallis, Oregon 97331-3803
William E. Magnusson
Instituto Nacional de Pesquisas da Amaz^
onia–INPA, Manaus, Amazonas, Brazil
Guilherme Mour~
ao
Wildlife Laboratory, Embrapa Pantanal, Corumb
a, Mato Grosso do Sul, Brazil
(Received 14 October 2013; revised 8 September 2014; accepted 15 September 2014)
According to the “social intelligence hypothesis,” species with complex social interactions have
more sophisticated communication systems. Giant otters (Pteronura brasiliensis) live in groups
with complex social interactions. It is likely that the vocal communication of giant otters is more
sophisticated than previous studies suggest. The objectives of the current study were to describe the
airborne vocal repertoire of giant otters in the Pantanal area of Brazil, to analyze call types within
different behavioral contexts, and to correlate vocal complexity with level of sociability of mustel-
ids to verify whether or not the result supports the social intelligence hypothesis. The behavior of
nine giant otters groups was observed. Vocalizations recorded were acoustically and statistically
analyzed to describe the species’ repertoire. The repertoire was comprised by 15 sound types emit-
ted in different behavioral contexts. The main behavioral contexts of each sound type were signifi-
cantly associated with the acoustic variable ordination of different sound types. A strong
correlation between vocal complexity and sociability was found for different species, suggesting
that the communication systems observed in the family mustelidae support the social intelligence
hypothesis. V
C2014 Acoustical Society of America.[http://dx.doi.org/10.1121/1.4896518]
PACS number(s): 43.80.Ka, 43.80.Ev [AMS] Pages: 2861–2875
I. INTRODUCTION
Animals communicate through different kinds of sig-
nals, which presumably increases their fitness (Bradbury and
Vehrencamp, 1998;Wilson, 2000). The content of signals
may provide information about the status, motivation, and
identity of senders and may vary according to behavioral
contexts and the environment (Bradbury and Vehrencamp,
1998). Vocal signals are usually classified according to the
behavioral context in which they are used, and thus, their
function in communication (Bradbury and Vehrencamp,
1998). Although many mammal species present a continuous
repertoire of sounds, vocal repertoire analysis usually aims
to discriminate discrete sound types that are associated with
different behavioral contexts, as described in a wide range of
species, including otters (e.g., Schassburger, 1993;Sieber,
1984;McShane et al., 1995;Wong et al., 1999;Lemasson
et al., 2014).
Behavioral context and the motivational state of senders
influence the use of different signals as well as their structure
(Morton, 1977;August and Anderson, 1987). The “social
intelligence hypothesis” proposes that species living in more
complex social groups present a more sophisticated commu-
nication system (“large number of structurally and function-
ally distinct elements or a high amount of bits of
information,” Freeberg et al., 2012), which is necessary to
deal with a wider range of social interactions in different be-
havioral contexts. Moreover, the use of gradations and com-
binations of sounds may result in more complex repertoires
and increase the number of messages that can be transmitted
(Schassburger, 1993;Wilson, 2000). Therefore, large and
graded repertoires are expected to occur with greater fre-
quency in highly social species, compared to solitary or non-
social animals (Bradbury and Vehrencamp, 1998;McComb
and Semple, 2005).
Mustelid sociability has been categorized as a dichoto-
mous system (primarily solitary versus highly gregarious)
(Creel and Macdonald, 1995;Wong et al., 1999) or as dis-
crete degrees of sociality (solitary, pairs, variable groups,
groups) (Johnson et al., 2000). Mustelid social systems vary
greatly within species and may also be correlated with eco-
logical factors that change in space and time (Johnson et al.,
2000). According to the classification of sociability, as
a)
Author to whom correspondence should be addressed. Current address:
Instituto Federal Farroupilha, Rua Erechim, 860-Bairro Planalto-CEP
98280-000-Panambi-RS, Brazil. Electronic mail: caroleucht@gmail.com
b)
Also at: Bioacoustics Research Program, Laboratory of Ornithology,
Cornell University, Ithaca, NY 14850.
J. Acoust. Soc. Am. 136 (5), November 2014 V
C2014 Acoustical Society of America 28610001-4966/2014/136(5)/2861/15/$30.00
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suggested by Johnson et al. (2000), giant otters (Pteronura
brasiliensis) and small-clawed otters (Aonyx cinerea) show
the highest degrees of sociability within mustelids. These are
followed by species that form groups of variable sizes, such
as Zaire clawless otters (Aonyx congicus), sea otters
(Enhydra lutris), European river otters (Lutra lutra), spot-
necked otters (Lutra maculicollis), North American river
otters (Lontra Canadensis), and badgers (Meles meles).
Giant otters live in cohesive groups of two to 20 individ-
uals (Duplaix, 1980;Leuchtenberger and Mour~
ao, 2008),
including a dominant breeding pair and other individuals
that may or may not be genetically related (Ribas, 2012).
Group members help in caring for the offspring of the domi-
nant pair, whose reproductive period in nature is around
10 yr for females and 15 yr for males (Davenport, 2010).
Subadults usually leave their natal group when they achieve
sexual maturity at around 2 years of age (Duplaix, 1980).
Nonetheless, there are records of subadults leaving their
social groups earlier and also remaining long after reaching
sexual maturity (Leuchtenberger and Mour~
ao, 2008). Giant
otter social groups are mainly diurnal and engage in almost
all of their daily activities together, such as scent-marking to
delineate territories, resting on the shore, foraging, playing
and defending territories from intruders with aggressive
behaviors and loud vocal choruses (Duplaix, 1980;Ribas
and Mour~
ao, 2004;Leuchtenberger and Mour~
ao, 2009;
Leuchtenberger et al., 2014).
Although giant otters are highly social, previous studies
of their airborne vocal repertoire described only nine differ-
ent sound types. These sounds were associated with behav-
ioral contexts registered during observations of free-ranging
animals in the Guyanas and the Amazon Basin (Duplaix,
1980;Staib, 2005;Bezerra et al., 2010), observations of cap-
tive animals originating from the Amazon and Pantanal
regions (Machado, 2004), and a few spectrographic descrip-
tions of sounds emitted in specific contexts by free-ranging
animals in the Pantanal (Ribas and Mour~
ao, 2004;
Leuchtenberger and Mour~
ao, 2009;Ribas et al., 2012).
Additionally, other mustelids, such as badgers (M. meles)
and sea otters (E. lutris), although presenting a lower degree
of sociability (Johnson et al., 2000), show larger vocal reper-
toires containing complex graded signal structures compared
to giant otters (McShane et al., 1995;Wong et al. 1999).
Considering the prediction of the social intelligence hy-
pothesis (Freeberg et al., 2012) and the high degree of soci-
ability in giant otters among mustelid species (Johnson
et al., 2000), we hypothesized that the vocal communication
system of giant otters is likely to be more sophiticated than
the past studies suggest. Since the description of vocal reper-
toires can be highly subjective, our first aim was to quantita-
tively describe the airborne vocal repertoire of giant otters in
the Brazilian Pantanal and second, to associate the resultant
call types with different behavioral contexts, considering
that sounds vary according to the social context in which
they are emitted and according to the arousal of senders. We
also correlated the vocal complexity of 15 mustelid species
with their degree of sociability to assess whether or not the
complexity of vocal communication systems observed in the
family mustelidae support the social intelligence hypothesis.
II. METHODS
A. Study site
The current study was conducted in the Nhecol^
andia
area of the Pantanal region, a large, seasonally flooded wet-
land covering approximately 160 000 km
2
and located at low
altitude (75–200 m a.s.l), near the geographic center of
South America. The Pantanal is subject to a strong annual
flood pulse, which affects the home range size of giant otter
groups and may cause shifts in territory boundaries and own-
ership (Leuchtenberger et al., 2013). The Paraguay river is
the main river draining the region from north to south, and
most of its tributaries flow from east to west, including the
Miranda and Negro rivers where the vocal recordings and
behavioral observations for this study were realized (Fig. 1).
B. Data collection and classification
We monitored five giant otter groups (G1, G2, G4, G10,
and G12) on a monthly basis, from September 2009 to June
FIG. 1. Map of the study area, present-
ing the Miranda, Vermelho, and Negro
rivers, located in the Southern Pantanal
in Brazil.
2862 J. Acoust. Soc. Am., Vol. 136, No. 5, November 2014 Leuchtenberger et al.: Vocal repertoire of giant otters
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2011, along a stretch of the Miranda river (19360S, 57
000W) and its tributary, the Vermelho river (19
o
340S;
57
o
010W). Four additional groups (G17–G20) were moni-
tored along the Negro river (19
o
350S; 56
o
110W) in
September 2009, June and September 2010, and June 2011.
Each monthly field campaign lasted from 7 to 10 days.
Groups were located by conducting systematic visual sur-
veys by boat during daylight hours (5:00–19:00 h). All data
collection and field observation activities were authorized
under license no. 12794/4 issued by ICMBio, the Federal
Environmental Agency of Brazil, and followed the guide-
lines of the American Society of Mammalogists for the use
of wild mammals in research (Sikes et al., 2011).
The locations of individuals, groups and signs of the
species, such as dens and latrines, were registered with a
global positioning system receptor (Garmin Etrex, Inc.,
Olathe, KS). Once located, a group was followed at a dis-
tance of 10–100 m, depending on the perceived shyness and
general reaction of the group to observer presence, to avoid
any unnecessary disturbance. Individuals were identified by
the naturally occurring unique whitish markings on their
throats. Whenever possible, the gender of each individual
was determined and their behavior recorded during the dura-
tion of the observation period using a high-definition cam-
corder (Canon HF-200). Video recordings were analyzed
afterward to describe behavior and identify individuals. We
also identified the social status of individuals within the
group based on their behaviors, such as defensive posturing
and frequency of scent-marking, or by signs of lactation (for
more details see Leuchtenberger and Mour~
ao, 2009) in order
to determine whether any particular sound types were attrib-
uted to dominant individuals only.
Airborne sounds were recorded with a directional
microphone (Sennheiser ME-66) connected to a digital
Marantaz PMD-660 recorder (AIFF format, 16-bit resolution
and 44.1 kHz sampling rate). Behavioral samples of visible
individuals vocalizing (senders) were filmed ad libitum
(Altmann, 1974), and the sounds were recorded concomi-
tantly, at a maximum distance of 50 m.
We classified the senders into three age categories
according to Groenendijk et al. (2005): adults and subadults
(>12 months), juveniles (6–12 months), and cubs (0–6
months). Since the giant otters inhabiting the study area have
been monitored since 2002 (Leuchtenberger and Mour~
ao,
2008), the exact birth month of some individuals was known.
When this was not the case, the approximate age of each
individual was estimated based on the behavioral features
described by Groenendijk et al. (2005). The nine giant otter
groups monitored here included a total of 43 adults (20
males, 16 females, and 7 unknown), 4 juveniles (2 male, 1
female, and 1 unknown), and 25 cubs (1 male, 1 female, and
23 unknown). During the study period, 8 cubs matured to
juvenile status, and 3 juveniles became adults. Group size
varied from 2 to 15 individuals, with an average of 6 individ-
uals per group.
The behavioral contexts observed for individuals or
giant otter groups during the study were classified in the fol-
lowing manner: (i) close contact (CC), when two or more
members of the same group displayed affiliative contact; (ii)
grooming (GR), when individuals displayed self-grooming
or groomed other members of the group; (iii) swimming
(SW), when moving through the water; (iv) within den
behavior (DE), when cubs vocalized from within the den; (v)
scent-marking (SM), when individuals were scent marking
and/or defecating; (vi) isolation (IS), when an individual was
distant from the other members of the group and started to
call looking around or toward the den; (vii) begging (BE),
when an individual solicited a prey item from another indi-
vidual; (viii), warning/defense (WD), when an individual
caught a fish and/or was eating, and it vocalized to keep
another individual away; (ix) inquiry (IN), when individuals
investigated something new in their environment, sometimes
adopting a periscoping posture; (x) alarmed (AL), when an
individual was startled and its behavior generated attention
or led other members of the group to escape; (xi) intraspe-
cific agonistic encounter (IA), when an individual or the
group engaged in conflict (physical or vocal) with a conspe-
cific intruder; and (xii) interspecific encounter (IE), when an
individual or the group faced a caiman (Caiman crocodilus
yacare). Note that caimans may represent a threat to giant
otter cubs (Duplaix, 1980), but are also a food resource for
adults (Ribas et al., 2012).
When the whole group was involved in the same behav-
ioral context and emitting similar sounds in a chorus (e.g.,
during agonistic encounters), the emission rate for the whole
group was estimated as the number of sounds emitted by all
group members combined during each sampling period. The
average emission rate per individual was subsequently
divided by the number of individuals observed vocalizing
during the recording period. The monitoring interval was
counted from the beginning of the visual detection of a group
or individual at a maximum distance of 50 m, until the end
of observations, when the subjects were lost from sight. The
monitoring interval restarted when the same or another indi-
vidual or group (with the same composition of individuals)
was re-located during the same day. The emission rate of
sounds given exclusively by a particular age category was
calculated based on the time that an individual of a certain
age was present during the sampling period. To determine
emission rates, we only considered sounds recorded from six
of the groups monitored (G1, G2, G10, G17, G18, and G20),
because the other three groups (G4, G12, and G19) were
very shy, which might have compromised our ability to
approach without disturbing their normal behavior. We did
not estimate the emission rates of individuals that reacted to
observer presence by drastically changing their behavior,
such as running away or inspecting the observer.
Nonetheless, no new call types were observed during these
particular situations.
C. Acoustical analyses
Acoustic analyses were performed using Raven Pro 1.4
(Cornell Lab of Ornithology), applying the following set-
tings for spectrograms and power spectra: Hanning window;
FFT size ¼1024 and 50% overlap. Sound parameters were
measured from spectrograms, oscillograms, and power spec-
tra (Fig. 2) and used to describe and/or compare
J. Acoust. Soc. Am., Vol. 136, No. 5, November 2014 Leuchtenberger et al.: Vocal repertoire of giant otters 2863
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vocalizations. The call parameters measured include: (CD)
call duration, (LF) lowest frequency of the sound, (HF) high-
est frequency of the sound, (PF) peak frequency of the entire
sound, (Q3) 3rd quartile frequency, this value is computed
automatically by the software and represents the frequency
that divides the selection into two frequency intervals con-
taining 75% and 25% of the energy in the selection, (PU)
number of pulses (temporal units that repeat rhythmically) of
the sound, (FI) initial frequency of F0 (for harmonic sounds)
or of the peak frequency (for non-harmonic sounds), (FM)
maximum frequency of F0 or PF, (FF) final frequency of F0
or PF, (FD) difference between the highest and the lowest
frequency of F0 or PF, (D1) duration from the start of the
vocalization to the highest frequency value of F0 or PF, (D2)
duration from the highest frequency of F0 or PF to the end
of the vocalization, and (PD) plateau duration (when the fre-
quency of F0 or PF did not vary). The number of pulses was
measured using oscillograms for sounds that presented
stretches with regularly spaced pulses (e.g., coo-call, purr,
snort, adult and cub growls, scream, and scream-gurgle), and
for sounds that presented a large number (>10) of pulses, we
estimated the number of pulses by dividing the duration of
pulsed stretches by the inter-pulse interval within that
stretch. The sound parameters are presented as the mean and
standard deviation (SD) of the mean or median and its
respective ranges. Since we did not estimate the distance
from which the subjects were recorded, it was not possible to
measure amplitude parameters. However, we were able to
describe some sound characteristics, such as relative inten-
sity, by considering observer perceptions at the time of
sound acquisition in the field. Sound types that were already
known were named according to the first descriptions
elaborated by Duplaix (1980), while newly identified sounds
were named by considering the acoustic characteristics and
behavioral context in which they were emitted. Spectrogram
and oscillogram figures were produced with R software
using the spectro function in the seewave package (Sueur
et al., 2008).
D. Statistical analyses
All statistical analyses were performed using R 2.13
Software (R Foundation for Statistical Computing, 2011).
The vocal repertoire of giant otters was derived from a con-
tinuum, with transitions, gradations and combinations among
different sound types. Classifying the sounds occurring
within this kind of complex communication system is a
major challenge. Therefore, we used statistical methods to
test for significant differences among the 15 discrete sounds
types classified according to visual inspections of spectro-
grams and by measuring 13 structural characteristics
(Appendix), and the behavioral context in which the sounds
were emitted following studies of other mustelid species
(McShane et al., 1995;Wong et al., 1999;Lemasson et al.,
2014). We standardized the acoustic parameters by columns
and rows using the decostand function with the total method
in the Vegan package (Oksanen et al., 2013) and used a
nested nonparametric multivariate permutational analysis of
variance (PERMANOVA, age categories nested within
sound types) to identify differences among sound types. We
used the PERMANOVA analysis with 1000 permutations,
which permutes the distance matrix (Manhattan method) of
acoustic parameters, through the adonis function in the
Vegan package.
FIG. 2. Measurements of acoustic pa-
rameters of a giant-otter coo-hum call:
(a) Oscillogram used to measure the
total call duration (CD); the duration
(D1) from the start of the vocalization
to the highest value of fundamental
frequency (F0) or peak frequency (PF);
the duration (D2) from the highest fre-
quency of F0 or PF to the end of the
vocalization; and the plateau duration
(PD), when the frequency of F0 or PF
did not vary. (b) Zoom view of a
stretch of the oscillogram showing the
measurement of the inter-pulse interval
used to estimate the number of pulses
of the sound. (c) Spectrogram (window
size 512) used to measure the lowest
frequency (LF) of the sound; the high-
est frequency (HF) of the sound; the
difference (FD) between HF and LF;
the initial frequency (FI) of F0 or PF
of the sound; final frequency (FF) of
F0 or PF; and the maximum frequency
(FM) of the FO or PF. (d) Power spec-
trum used to measure of the PF of the
selection.
2864 J. Acoust. Soc. Am., Vol. 136, No. 5, November 2014 Leuchtenberger et al.: Vocal repertoire of giant otters
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A linear discriminant analysis (LDA) was carried out to
estimate the distinctiveness between sound types, using the
package MASS (Venables and Ripley, 2002). We applied
the first step of LDA with a sorted (training) subset of 50%
of the data. The remaining (validation) subset of data was
used to evaluate the accuracy of classification based on equa-
tions derived from the training subset. The percentage of
correctly classified cases indicates the effectiveness of dis-
criminant function in distinguishing groups (vocalization
type). We only used four variables to estimate the LDA
among sound types (PF, Q3, FD, PU), since the other varia-
bles did not conform to the linearity assumptions of the anal-
ysis (Venables and Ripley, 2002). These included variables
linked to the structure of the vocalizations and may reflect
the emotional state of mammals (Briefer, 2012).
Because some of the sound types were expected to be
subdivided between age categories, we applied a
PERMANOVA with 1000 permutations (adonis, Vegan pack-
age) to test for these differences. We then conducted a hier-
archical clustering analysis taking into account these
subdivisions. For this analysis, we used a Manhattan-distance
matrix of the median values of the variables extracted from
each sound type and the average linkage between groups
(UPGMA). This analysis results in a dendrogram representing
the similarity between sound clusters (Wong et al.,1999).
A principal-coordinate analysis (PCoA) was carried out
to ordinate the 13 acoustic variables of the 15 main sound
types from the Manhattan-distance matrix. To avoid distor-
tions of the configuration due to extreme points from the
PCoA, we corrected 53.3% of the distances using the
“extended” procedure available in the stepacross function
from the package Vegan. We used a PERMANOVA (1000
permutations, adonis, Vegan package) to test whether the
main context associated with the emissions of sounds was
statistically associated with the ordination of acoustic varia-
bles (i.e., the first three axis of the PCoA).
E. Relationship between mustelidae vocal complexity
and sociability
The vocal complexity of mustelids was estimated by the
number of vocal types used by each species. We assessed this
information in original articles found in the Web of Science
search engine (http://apps.webofknowledge.com), using the
arguments “vocalization” and “mustelidae,” vocalization and
“mustela,” vocalization and “otter,” and combined informa-
tion from the literature with the data on giant otters collected
for this study. Mustelid sociability level was estimated as the
mean number of individuals in a breeding group according to
Johnson et al. (2000). We applied a Spearman correlation
between vocal complexity and breeding group size to deter-
mine whether or not the communication systems of musteli-
dae species supports the social intelligence hypothesis.
III. RESULTS
We recorded 6246 vocalizations during 112 h of moni-
toring. The individual total emission rate was 11.4 sounds/h
(Table I), and the frequency of individual sound types varied
from the rarely emitted cub squeak (0.03 sounds/h) to the
most frequent cub call (3.4 sounds/h). We included only 458
of the total recorded sounds for the repertoire analysis (379
from adults/subadults, 9 from juveniles, and 70 from cubs),
TABLE I. Individual emission rates (number of sounds/h) and proportions of giant otter vocalizations given in different behavioral contexts (CC, close con-
tact; GR, grooming; SW, swimming; DE, within the den; SM, scent-marking; IS, isolation; BE, begging; WD, warning/defense; IN, inquiry; AL, alarm; IA,
intraspecific agonistic encounter; and IE, interspecific encounter by adults (A), subadults (S), juveniles (J), and cubs (C) from six groups. nis the number of
sounds recorded, (groups) refers to the number of groups that presented that particular sound type in its repertoire.
Behavioral Context (%)
Sound n(Groups) Age class Sound/h CC GR SW DE SM IS BE WD IN AL IA IE
1. Cub call 1388 (6) J/C 3.4 10 59 31
2. Purr 1523 (6) A/S 3.0 52 15 12 21
3. Snort 781 (6) A/S/J/C 1.4 9 5 2
4. Coo 584 (6) A/S 1.1 51 9 14 26
5. Coo-hum 322 (6) A/S 0.7 72 9 12 5 2
6. Scream 310 (5) A/S 0.5 39 47 9 5
6.1. Cub scream 43 (5) C 0.2 1
7. Hum 235 (6) A/S 0.5 55 19 5 21
8. Coo-call 197 (6) A/S 0.3 64 8 12 16
9. Hah 174 (6) A/S 0.3 10
10. Begging scream 149 (4) A/S 0.3 10 58 3
10.1. Cub begging scream 155 (3) J/C 0.7 10
11. Growl 149 (5) A/S 0.3 74 2 2
11.1. Cub Growl 12 (1) C 0.1 1
12. Adult call 148 (6) A/S 0.2 74 5 2
13. Scream-gurgle 25 (3) C 0.1 1
14. High scream 25 (3) A/S 0.1 10
14.1. Cub high scream 11 (2) C 0.05 1
15. Squeak 15 (1) C 0.03 10
Total 6246 11.4
J. Acoust. Soc. Am., Vol. 136, No. 5, November 2014 Leuchtenberger et al.: Vocal repertoire of giant otters 2865
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because most of the recordings overlapped with sounds from
motor boats and/or vocalizations of other species or non-
focal giant otters.
The vocal repertoire of giant otters was classified as 15
discrete sound types (PERMANOVA: F
14,443
¼130.66,
R
2
¼0.81, P<0.001), of which seven were emitted only by
adults and subadults; one, by juveniles and cubs only; two,
exclusively by cubs; and five, by all age categories. Linear
discriminant analysis correctly classified 74% of the 15
sound types. The first two discriminant functions explained
92% of the variance in sound variables. The number of
pulses was the variable that contributed most to the first dis-
criminant function, while the difference between the highest
and the lowest frequency of F0 or PF (FD) was the most im-
portant variable in the second discriminant function.
Some of the main sound types could be subdivided
into two subtypes, depending on the age of the sender,
resulting in a total of 19 distinct sound subtypes (Fig. 3). The
begging scream of adults/subadults and cubs/juveniles differed
(PERMANOVA: F
1,19
¼3.35, P¼0.016), but accounted for
little of the variance in the data (R
2
¼0.15), so it was described
as a single type within the repertoire. The cub growl differed
from adult growls (PERMANOVA: F
1,25
¼14.53, P<0.001),
but the difference explained a relatively low proportion of the
variance in the data (R
2
¼0.37), and considering that the cub
sound was very similar aurally to the adult growl, we consid-
ered them to be the same sound type. The high scream of cubs
and adults (PERMANOVA: F
1,12
¼0.78, P¼0.536) did not
differ, although the high scream of some adults had nonlinear
components. The adult/subadult and cub screams also did not
differ statistically (PERMANOVA: F
1,27
¼1.35, P¼0.232).
A. Vocal repertoire and behavioral context
1. Coo
Thecooisadiscreteharmonicsound(Fig.4)producedby
adults and subadults with the mouth closed and was heard only
at close range (to approximately 10 m) at a rate of 1.1 sounds/h
(Table I). The average coo duration was 0.36 (SD ¼0.11 s), with
two harmonic parts or notes and visible pulses in part of or
throughout the entire harmonic segment (Appendix; Table II).
This chevron-shaped double-note sound was emitted mainly
during close-contact episodes (51%, n¼290), especially when
adults were caring for cubs, but also during scent-marking events
(26%, n¼148). Adults cooed when they met while swimming
(14%, n¼80), sometimes touching noses, and before changing
their activity or leaving the site. Coos were also emitted during
grooming sessions (9%, n¼51).
2. Coo-hum
This low frequency sound was emitted by adults and suba-
dults at a rate of 0.7 sounds/h (Table I) with the mouth closed,
and can be described as a combination of the coo and the hum
(Fig. 4) sounds. The coo-hum is a harmonic sound with at least
three visible harmonics and a mean call duration of 0.2s
(SD ¼0.09 s), with pulses (Appendix; Table II) during the entire
sequence or in segments of the sound. Individuals produced
coo-hums mainly during close-contact events (72%, n¼226),
when they were swimming together (12%, n¼38), grooming
(9%, n¼28) and scent marking (5%, n¼16), similar to the be-
havioral contexts in which coos were produced. However, this
sound was also emitted when an adult called other individuals,
independent of their ages, to come out of the den (2%, n¼6).
3. Coo-call
The coo-call is perceived as louder than coos and coo-
hums, with an average duration of 0.44 (SD¼0.13) s, and
was given by adults and subadults at a rate of 0.3 sounds/h
(Table I) with the mouth partially closed. This sound seems to
be a combination of the coo and adult calls (Fig. 4). It is char-
acterized by an abrupt transition from an ascendant low-pitch
harmonic and pulsed segment resembling a coo to a high-
pitched and bell-shaped frequency modulated harmonic sound
similar to the adult call and then reverts back to a descendant
pulsed sound at the end of the vocalization. The middle part of
this sound may have a plateau (median of 0.03 s, ranging from
0.01 to 0.2 s) with a constant frequency (Appendix; Table II).
Coo-calls were emitted when an animal appeared to be in a
state of high arousal, mainly during close-contact events (64%,
n¼124). This sound was also used for calling to other mem-
bers of the group (16%, n¼31), as well as during scent-
marking events (12%, n¼23), and swimming (8%, n¼15).
4. Hum
The hum is a low frequency sound emitted by adults and
subadults at a rate of 0.5 sounds/h (Table I)withthemouth
closed. This sound had at least five visible harmonics (Fig. 4),
lasting an average of 0.33 (SD ¼0.19) s, with some segments
of regular pulses (Appendix; Table II). Hums were heard more
FIG. 3. Dendrogram of the hierarchical-cluster relationship of the 19 sounds
(n¼458 vocalizations) emitted by giant otters distributed in nine groups in
the Southern Pantanal, from November 2009 to June 2011. *Height repre-
sents a vector of the distances between merging clusters at successive stages,
with shorter end branches indicating greater similarity of sound types.
2866 J. Acoust. Soc. Am., Vol. 136, No. 5, November 2014 Leuchtenberger et al.: Vocal repertoire of giant otters
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frequently during affiliative close contacts (55%, n¼123), fol-
lowed by scent-marking events (21%, n¼47) and grooming
(19%, n¼43). This type of sound was heard less often during
swimming (5%, n¼11). The hum was commonly produced in
combination with purrs [hum-purr, Fig. 5(a)] and growls.
5. Purr
The purr is a low frequency, harmonic and pulsed sound
that was given by adults and subadults at a rate of 3 sounds/h
(Table I) with the mouth closed and has a nasal quality
(Fig. 4). This sound had a call duration average of 0.54
(SD ¼0.27) s and an average of 11.65 (SD ¼5.25) pulses
(Appendix; Table II). Purrs were the most frequent vocaliza-
tions (Table I), emitted during behavioral contexts similar
those in which coos and hums were observed and were more
frequently observed during close contact events (52%,
n¼733). Gradations between the close contact coo, coo-
hum, and coo-call sounds were commonly combined with
hums and purrs [Fig. 5(b)]. Peters (2002) suggested that the
FIG. 4. Spectrograms (FFT: 512) and oscillograms (bottom) of vocalizations emitted by giant otters in the southern Pantanal of Brazil.
J. Acoust. Soc. Am., Vol. 136, No. 5, November 2014 Leuchtenberger et al.: Vocal repertoire of giant otters 2867
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term purr is not adequate for similar sounds made by mustel-
ids because it is not homologous to felid purring. However,
considering the low intensity and rhythmic characteristics of
this sound and the behavioral context in which giant otters
emitted purrs, we maintained this term in describing the spe-
cies’ vocal repertoire.
6. Snort
The snort is an explosive, noisy, and pulsed sound, emit-
ted during strong exhalations of air with the mouth partially
open by all age classes, including 5-month-old cubs. While
snorting in water, the animals commonly raised their throat
out of the water (periscoping). The call duration of snorts
showed an average of 0.27 (SD ¼0.1) s, with a mean of 6.55
(SD ¼2.35) pulses (Appendix; Table II). Snorts can be emit-
ted as a single note or in double bursts. The snort burst was
often louder when the animal was startled and may serve to
alert other members of the group. Five formants were visible
along the spectrogram of the snorts (Fig. 4). The snort was
the second most often emitted sound type observed (1.4
sounds/h, Table I). This sound was usually given during
alarm situations (93%, n¼726). Snorts were also emitted
during intra-specific agonistic encounters (5%, n¼39)
between different groups and inter-specific events (2%,
n¼16) when the group faced caimans.
7. Hah
The hah is a noisy, atonal sound was produced by
adults and subadults through exhalation and/or inhalation
(Fig. 4). The hah is a short-lived sound with a mean dura-
tion of 0.16 (SD ¼0.07) s (Appendix; Table II). Hahs were
emitted mostly in low alarm situations within an inquiry
context (100%, n¼174). In conflict situations, groups may
emit sequential hahs combined with snorts. Hahs were
emitted at a rate of 0.3 sounds/h and can transition into ei-
ther alarm or affiliative sounds.
8. Adult call
The adult call is a harmonic, bell-shaped sound (Fig. 4),
given by adults and subadults with the mouth partially open
and at a rate of 0.2 calls/h (Table I). The mean call duration
was 0.3 (SD ¼0.1) s, with a plateau lasting from 0.01 to
0.26 s (median ¼0.05 s, Appendix; Table II). This sound was
emitted mainly when animals were calling to other group
members (74%, n¼120), which sometimes elicited a
response from another individual(s) that vocalized back with
either calls or screams. During intra-specific agonistic
encounters (21%, n¼33) adult calls were given in combina-
tion with screams and snorts. Adult calls were also emitted
when individuals were startled (5%, n¼8). The ending of
this sound became harsher and noisier or transitioned to a
scream as the senders became more excited.
9. Growl
The growl is a low frequency, harmonic and pulsed
sound given by adults and subadults. This sound is emitted
with the mouth totally or partially closed and may present
amplitude modulation along the signal, with increasing
energy toward the end of the sound (Fig. 4). The mean dura-
tion of this sound was 2.35 (SD ¼1.71) s, and a high number
of pulses and high values of the 3rd quartile frequency were
observed (Appendix; Table II). Adults and subadults
growled at a rate of 0.3 sounds/h (Table I). Growls were
emitted mainly in warning and defense contexts (74%,
n¼107), when the vocalizing individual was handling and
eating a fish or it was directed toward another individual try-
ing to steal it. While eating and growling, some individuals
opened their mouths, producing a more intense sound with a
slight increase in frequency. Startled individuals also
growled as an alarm call (24%, n¼35) and during inter-
specific encounters (2%, n¼3) with caimans (C. yacare).
a. Cub growl. The cub growl is similar to the growl
emitted by adults and subadults, and is a pulsed sound with a
harmonic interval (Appendix; Table II). The mean duration
was 0.46 s (SD ¼0.25), with no frequency modulation. This
sound was recorded from newborn cubs (1–3 months) inside
of the den at a rate of 0.1 sounds/h.
10. Scream
The scream is a harmonic sound, which may present
a wavering quality, and was emitted by adults and
subadults, with the mouth open, at a rate of 0.5 sounds/h
(Table I). This sound has some pulsed segments
(Appendix; Table II), a mean duration of 0.93 s
(SD ¼0.41) and at least 11 visible harmonics (Fig. 4).
Screams were emitted mainly during fishing events (47%,
n¼145), and apparently served as a warning call. An
individual that had caught a fish (especially if the fish
was large) usually screamed with the prey in its mouth or
in its forepaws. This sound was also emitted by giant
otters that were caught trying to steal a prey item from
another group member, and was usually answered with
growls. When the motivation of an individual sender
appeared to be more intense, screams showed chaotic
components toward the end of the signal [Fig. 5(c)] or the
scream merged into a begging scream. Screams were also
emitted when individuals called to each other (39%,
n¼121). For instance, individuals screamed to get cubs to
come out of the den, or if an individual was not keeping
up with the rest of the group during traveling events,
where the individual may scream as a signal for other
group members to wait up and may be answered with
screams by other individuals. Moreover, individuals
screamed (9%, n¼28) when startled, apparently as an
alarm call for others. Screams may also become harsher
in hostile situations, such as during intra-specific agonistic
encounters (5%, n¼16) when almost all members of the
group screamed in a chorus interspersed with abrupt calls.
a. Cub scream. The cub scream is a harmonic sound,
similar to the adult scream, and was emitted by young cubs
within the den at a rate of 0.2 sounds/h (Table I). Cub
screams presented pulsed segments with a mean duration of
0.81 (SD ¼0.44) s (Appendix; Table II).
2868 J. Acoust. Soc. Am., Vol. 136, No. 5, November 2014 Leuchtenberger et al.: Vocal repertoire of giant otters
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11. Begging scream
The begging scream was emitted by adults and suba-
dults and is similar to the scream, but with a highly modu-
lated tonal frequency component along parts of the signal or
throughout the entire sound. The begging scream was given
by opening and closing the mouth and during states of high-
intensity motivation. The mean begging scream duration was
1.21 s (SD ¼1.03) and presented a higher peak frequency
than that of a regular scream (Appendix; Table II). The beg-
ging scream was emitted at a rate of 0.3 sounds/h (Table I)
in a begging context during fishing events (58%, n¼86) and
during agonistic encounters (32%, n¼48). Individuals
sometimes screamed while scent marking (10%, n¼15),
probably in response to the scent of an intruder.
a. Cub begging scream. The cub begging scream
(Fig. 4) was emitted by both cubs and juveniles, at a rate of
0.7 sounds/h, when begging for fish (n¼155).
12. High scream
The high scream is a harmonic sound given by adults
and subadults, with the mouth open. The median call duration
of adult high screams was 0.94 s (ranging from 0.36 to 2.25 s,
Fig. 4). Unlike the regular scream (described in
Sec. III A 10), the peak frequency values of high screams
were found for the fundamental frequency (F0) (Appendix;
Table II). This sound showed nonlinear phenomena,
including subharmonics and biphonation at irregular time
intervals. High screams were heard only in the context of five
fishing events (emission rate ¼0.1 sounds/h, n¼25), when
an individual begged for a fish from another group member.
High screams were often combined in a continuous sequence
with screams.
a. Cub high scream. The cub high scream was recorded
from young cubs (1–3 months) at a rate of 0.05 sounds/h
(Table I). This sound showed at least three visible harmonics
and presented a median duration of 0.46 s (ranging from 0.29
to 0.95 s, Appendix; Table II). It was recorded when cubs
were inside the den and sometimes displayed a gradation dis-
tinct from cub screams [Fig. 5(d)].
13. Cub call
The cub call is a high pitched and loud sound emitted by
individuals ranging from 2 to 9 months of age at a rate of 3.4
sounds/h, with the mouth open (Fig. 6). Cub calls were fre-
quency modulated with a mean duration of 0.35 s
(SD ¼0.15) and sometimes showed a flat frequency plateau
at variable intervals (median 0.03 s, ranging from 0 to 0.34 s,
Appendix; Table II). This sound was mainly given when
cubs were calling to other individuals (59%, n¼811), typi-
cally when they were separated from the group. Cubs also
used this type of sound to beg for fish (31%, n¼426) during
fishing sessions. These calls may have a harsher ending or
FIG. 5. Spectrograms and oscillograms
(bottom) of vocalizations emitted by
giant otters in the southern Pantanal of
Brazil: (a) combination of hum and
purr sounds (hum-purr, FFT ¼1024),
(b) gradation among affiliative sounds
(coo, coo-hum, and hum-purr,
FFT ¼1024), (c) adult scream with a
harsh, noisy ending (arrow indicates
the transition, FFT ¼512), (d) transi-
tion between cub high scream and cub
scream (arrow indicates the transition,
FFT ¼1024).
J. Acoust. Soc. Am., Vol. 136, No. 5, November 2014 Leuchtenberger et al.: Vocal repertoire of giant otters 2869
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merge into a longer and high-frequency modulated begging
scream when given by an individual in a more excited state.
Cubs also emitted this call when being cared for by adults
(10%, n¼137) in close-contact situations.
14. Scream-gurgle
The scream-gurgle was emitted by young cubs at a rate
of 0.1 sounds/h. This harmonic sound presented a mean du-
ration of 1.01 s (SD ¼0.1), begins with a pulsed scream
(Appendix; Table II) and ascends to a high-frequency inter-
val, comprising four to five bell-shaped frequency modulated
parts interspersed by short screams (Fig. 6). Scream-gurgles
were given by young cubs from inside the den, while other
cubs vocalized frequently with screams and high screams in
the background. All scream-gurgles were recorded when a
lactating female was in the den. On one occasion, cubs were
observed emitting scream-gurgles while suckling from the
female, which was lying near the den entrance.
15. Squeak
The squeak is a harmonic sound with an emission rate
of 0.03 sounds/h that was recorded only in 2-month-old cubs
from one group. The mean duration of squeaks was 0.44
(SD ¼0.1) s, with a peak frequency of 8.38 (SD ¼0.65) kHz
(Fig. 6, Appendix; Table II). This sound was given during
close contact events, while adults were caring for cubs, also
emitting purrs, coos, and hums in the background.
The PCoA analysis resulted in three axes that accounted
for 56% of the variation among sounds types, with 27.7% of
the variation represented by the first axis; 17.1%, by the sec-
ond axis; and 11.2%, by the third axis. Axis 1 had the highest
loadings for the D2 (0.686), D1 (0.573), and PU
(0.536), and axis 2 had the highest loadings for FD
(0.675), PU (0.388), and PD (0.328), while PU (0.377),
D1 (0.353), and FD (0.302) presented the highest loadings
on the third axis (Fig. 7).
Although there is some overlap between fearful and
friendly contexts (Fig. 7), the behavioral context of
sound types was significantly associated with the ordina-
tion of acoustic variables provided by the three axes of
the PCoA (PERMANOVA: F
6451
¼121.7, R
2
¼0.62,
P<0.001).
Digital audio files of all the sound types described above are
available at http://ppbio.inpa.gov.br/knb/metacat?action¼read
&qformat¼ppbio&sessionid¼0&docid¼naman.540.1.
B. Relationship between mustelidae vocal complexity
and sociability
We compiled published information on the repertoire
size of 15 species of mustelids (Appendix; Table III).
Adding our results to this list, we found a strong correla-
tion between the repertoire size and the mean breeding
group size of these mustelids (q¼0.67, P<0.01).
IV. DISCUSSION
The vocal repertoire of giant otter groups in this study
comprised 15 main sound types, usually emitted in different
behavioral contexts. Discrimination of sounds, including in-
formation about the age category of the sender, resulted in a
total of 19 sound subtypes. Although statistically and struc-
turally different, some sound types, such as coos could be
considered a single sound type because of similarity in the
contexts in which these sounds are emitted. Duplaix (1980)
described nine of these sounds qualitatively for giant otters
in Suriname. Bezerra et al. (2010) presented acoustic meas-
urements of five known sounds (snort, hah, scream, purr and
cub call) recorded from five individual giant otters in Ja
u
National Park, Amazonas, Brazil. Machado (2004) identified
nine sound types emitted by captive giant otters and free-
ranging groups in the Balbina Hydroelectric reservoir in the
Brazilian Amazon and described three new sound types
recorded in the captive animals (buck, humhum, and a sound
emitted by a resting adult female). The statistical methods
applied here allow for a more objective classification of call
types, resulting in a more robust means of measuring the
size of the giant otter vocal repertoire.
In our study, the purr was the most frequently emitted
sound in adults, followed by the snort, while the cub call was
the most frequently emitted vocalization by cubs. Purrs have
been described in the vocal repertoires of many mammals
FIG. 6. Spectrograms (FFT ¼512) and oscillograms (bottom) of vocalizations emitted by giant otters in the southern Pantanal of Brazil.
2870 J. Acoust. Soc. Am., Vol. 136, No. 5, November 2014 Leuchtenberger et al.: Vocal repertoire of giant otters
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(Peters, 2002) and are commonly classified as an affiliative
close-contact sound (Sieber, 1984;Wong et al., 1999). Giant
otters emitted purrs in intra-group close-contact events and
when individuals were engaged in group activities, such as
scent marking or swimming. The emission of purrs by giant
otter groups in Suriname was found to be rare, as Duplaix
(1980) recorded this sound only when adults were caring for
young cubs, and observed that purrs were replaced by hums
and coos as the cubs matured. However, Bezerra et al.
(2010) recorded purrs emitted by a giant otter group in the
Amazon but did not mention hums or coos, which were rela-
tively common in our study (emission rate, hum ¼0.5
sounds/h and coo ¼1.1 sounds/h). Snorts, hahs, screams and
cub calls seem to be common vocalizations in the repertoire
of giant otters and have been described by many authors
(Duplaix, 1980;Machado, 2004;Staib, 2005;Bezerra et al.,
2010). Call-emission rates may also change among giant
otters from different localities and could be a consequence
of differences in sampling effort and recording methodology,
as well as being influenced by environmental features, learn-
ing, or genetic variation among clades (Bradbury and
Vehrencamp, 1998;Wilson, 2000).
The vocal repertoire of a species that includes a variety
of sounds, may serve to transmit a corresponding number of
messages (Bradbury and Vehrencamp, 1998). The giant otter
snort is a sound type also found in the repertoire of other
mammals (Sieber, 1984;Wong et al., 1999) and that is com-
monly emitted in alarm situations. In giant otters, more ener-
getic snorts (with increasing amplitude) cause an immediate
response from group members, which usually run to the
water and submerge. The atonal hah has been suggested to
signify some sort of inquisitive behavior (Duplaix, 1980),
and is similar to the hiss sound commonly given in aggres-
sive and fearful contexts by sea otters (McShane et al.,
1995) and other mustelids (Huff and Price, 1968;Farley
et al., 1987;Wong et al., 1999). Screams and harmonic
sounds are common in the repertoires of many species
(McShane et al., 1995;Wong et al., 1999;Fitch et al., 2002)
and may provide identity information, as was recently docu-
mented for contact calls in giant otters (Mumm et al., 2014)
and Aonyx cinerea (Lemasson et al., 2013), and have an im-
portant function for group cohesion. Additionally, some
physical features of sounds, such as the presence of formants
in the snorts and the fundamental frequency of harmonic
sounds, may be considered an honest indication of body size
and individual identity (McShane et al., 1995;Sousa-Lima
et al., 2002;Fitch et al., 2002), and should also be consid-
ered in studies of acoustic individuality in the species.
Nonlinear phenomena, such as chaotic structures, bipho-
nations and subharmonics, were observed in adult screams
and high screams. These acoustic phenomena originate from
the intrinsic properties of the vibrating components of the
larynx (Fitch et al., 2002), but may also be produced as a
result of systemic infection or diseases in the vocal tract
(Riede et al., 1997). The presence of nonlinear components
has been observed in many other mammalian vocalizations
(Fitch et al., 2002;Sousa-Lima et al., 2002;Blumstein et al.,
2008) and may be another means of achieving individual
recognition. However, in some mammals, the presence of
non-linearity in sounds may indicate the arousal state of indi-
viduals (Marmota flaviventris,Blumstein et al., 2008;
Ailuropoda melanoleuca,Briefer, 2012).
The main behavioral contexts of sound types were sig-
nificantly associated with acoustic variables. The main vari-
ables of the three axes of the PCoA were related to the
duration and shape of the sound (D1, D2, FD) and the num-
ber of pulses (PU). According to Briefer (2012),thereisa
positive relationship between arousal level and some acous-
tic variables, especially source-filter parameters (e.g., F0
range, F0 contour) that reflect the structure of the vocaliza-
tion and the mode of production. This observation is con-
sistent with the motivational structure (MS) model, which
hypothesizes that vocalizations given in aggressive and hos-
tile situations are low frequency and noisy, and that sounds
given in fearful or friendly contexts are high frequency and
tonal (Morton, 1977;August and Anderson, 1987). In the
giant otter vocal repertoire, alarm, inquiry and warning
sounds were noisier and occurred at lower frequencies,
while calls and some scream types were harmonic and had
higher frequencies. In more excited motivational states, the
endpoint of adult calls and screams becomes harsher and
noisier, indicating a high degree of individual hostility, as
suggested by Morton (1977). The harmonic coo sounds,
given mainly in close contact situations, changed from a
lower intensity coo with a silent interval to a combination
coo-hum and, in a more excited state, to a coo-call with a
high frequency interval, which may elicit proximity in affili-
ative contexts. Although there is much overlap between
fearful and friendly contexts (August and Anderson, 1987),
the vocal repertoire of giant otters seems to be consistent
with the MS hypothesis and may reflect the arousal state of
individuals.
Transitions and gradations may increase the variability
of sound combinations and convey more information than
discrete signals (Wilson, 2000). The vocal repertoire of giant
otters can be classified as a continuum, presenting graded
sounds that were common during affiliative close contact
and in more excited and agonistic events, as also observed in
the repertoire other social mustelids (McShane et al., 1995;
Wong et al., 1999;Lemasson et al., 2014). The combination
of sounds, as in the hum with the affiliative purr, or the hum
with the aggressive growl, probably increases the amount of
information to be decoded (Crockford and Boesch, 2005).
During agonistic encounters, screams became modulated
and turned into abrupt calls, generating a long, harsh chorus
(Ribas and Mour~
ao, 2004; this study). During some excited
fishing events, as well as during suckling, screams and cub
calls graded into begging screams or high screams, which
may reflect the arousal state of those individuals, as it does
in sea otters (McShane et al., 1995). This high correlation
between vocal complexity and sociability in mustelids sug-
gests that the information compiled for this group supports
the social intelligence hypothesis of Freeberg et al. (2012).
Mustelids present a diverse and flexible social organization,
with both interspecific and interpopulation variation
(Johnson et al., 2000). Scent-marking is believed to be the
primary form of communication in mustelids and is highly
related to their social organization (Hutchings and White,
J. Acoust. Soc. Am., Vol. 136, No. 5, November 2014 Leuchtenberger et al.: Vocal repertoire of giant otters 2871
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2000). However, the details of vocal communication in most
species is still unknown and may be useful to understand the
social complexity of the group.
Giant otter vocal repertoires represent a good example
of how communication is intrinsically linked with sociality
(Freeberg et al., 2012). The large size (15 sound types) and
the presence of gradations, transitions and combinations in
the vocal repertoire of giant otters reflects their high degree
of sociality, as previously suggested (Duplaix, 1980, 1982)
and observed in mustelids and other social mammals (Canis
lupus, Schassburger, 1993;E. lutris,McShane et al. 1995;
M. meles, Wong et al., 1999;Pan troglodytes, Crockford
and Boesch, 2005;A. cinerea,Lemasson et al., 2014). The
variety of sound types and possible combinations, as well as
the function of nonlinear components in giant otter vocaliza-
tions, should be considered in future acoustic studies, as
these components may indicate an important mechanism in
the communication system of the species.
ACKNOWLEDGMENTS
We thank CNPq (Grant No. 476939/2008-9), the Rufford
Small Grants Foundation (Grant No. 88.08.09), the Mohamed
bin Zayed Species Conservation Fund (project no. 10051040),
and IDEA Wild for their financial support. We are also
indebted to Embrapa Pantanal, Barranco Alto Farm, and the
Federal University of Mato Grosso do Sul for their logistic
support. C.L. was the recipient of a CNPq scholarship. Paulo
dos Santos, Waldomiro de Lima e Silva, Sidnei Ben
ıcio,
Proc
opio de Almeida, and Jos
e Augusto da Silva assisted us
in the field. Carlos Andr
e Zucco and Victor Landeiro helped
us with some of the data analysis. We thank Victor S
abato,
Luciana Erdtman, and Jason Alan Mobley for helpful
suggestions. We are grateful to Ubiratan Piovezan for lending
equipment during field work.
APPENDIX
FIG. 7. Biplots of the relationship
between the first and second axes (a)
and the first and third axes (b) of the
principal coordinate analysis (PCoA) of
19 sounds (see legend beside the
graphs) vocalized by giant otters in dif-
ferent behavioral context (AL, alarm;
IN, inquiry; WD, warning/defense; BE,
begging; IS, isolation; DE, within den;
CC, close contact) represented by differ-
ent colors (see legend above the
graphs). The capital letters (in black)
indicate the sound features analyzed
(CD ¼call duration, LF ¼lowest, and
HF ¼highest frequencies of the sound,
PF ¼peak frequency of the entire
sound, Q3 ¼3rd quartile frequency,
PU ¼number of pulses of the sound,
FI ¼initial value of F0 (for harmonic
sounds)orofthepeakfrequency(for
non-harmonic sounds), FM ¼maximum
value of F0 o r PF, FF ¼final F0 or PF,
FM ¼maximum frequency of F0 or PF,
FD ¼difference between the highest
and the lowest frequency of F0 or PF,
D1 ¼duration from the start of the
vocalization to the highest frequency
value of F0 or PF, D2 ¼duration from
the highest F0 or PF to the end of the
vocalization, and PD ¼plateau duration
(when F0 or PF did not vary).
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TABLE II. Descriptive statistics [X6SD or median (minimum–maximum ranges)] of sound types emitted by giant otters from six groups monitored from September 2009 to June 2011 in the Southern Pantanal, Brazil.
Nrepresents the number of sounds used for acoustic measurements, and the number of giant otters groups included in analyses of each sound type is given in parentheses. (Sound: Co ¼coo, Cc ¼coo-call, Ch ¼coo-
hum, Hu ¼hum, Pu ¼purr, Gr ¼growl, Gr2 ¼cub growl, So ¼snort, Ha ¼hah, Ac ¼adult call, Sc ¼scream, Sc2 ¼cub scream, Be ¼begging scream, Be2 ¼cub begging scream, Hs ¼high-scream, Hs2 ¼cub high-
scream, Cu ¼cub call, Sk ¼scream-gurgle, Sq ¼squeak; Variables: CD ¼call duration, LF ¼lowest and HF ¼highest frequencies of the sound, PF ¼peak frequency of the entire sound, Q3 ¼3rd quartile frequency,
PU ¼number of pulses of the sound, FI ¼initial value of F0 (for harmonic sounds) or of the peak frequency (for non-harmonic sounds), FM ¼maximum value of F0 or PF, FF ¼final F0 or PF, FM ¼maximum frequency
of F0 or PF, FD ¼difference between the highest and the lowest frequency of F0 or PF, D1 ¼duration from the start of the vocalization to the highest frequency value of F0 or PF, D2 ¼duration from the highest F0 or
PF to the end of the vocalization, and PD ¼plateau duration (when F0 or PF did not varied), *temporal units in seconds (s), frequency units in kHz).
Call NCD LF HF PF Q3 PU FI FF FM FD D1 D2 PD
Co 15 0.36 60.11 0.18 60.05 5.29 60.94 0.45 60.05 0.61 60.26 109.67 629.19 0.27 60.06 0.33 60.05 0.52 60.06 0.25 60.06 0.15 60.06 0.07 60.03 0.16 60.09
Cc 18 0.44 60.13 0.16 60.04 4.98 61.43 0.5 (0.3–4.09) 2.89 61.38 77.22 633.55 0.26 60.1 0.34 60.1 4.32 61.14 4.06 61.14 0.26 60.12 0.13 60.07 0.03 (0.01–0.2)
Ch 20 0.2 60.09 0.17 60.03 4.75 61.31 0.44 60.08 0.51 (0.39– 3.66) 98.7 645.88 0.25 60.04 0.27 60.06 0.43 60.08 0.18 60.08 0.11 60.07 0.08 60.04 0
Hu 20 0.33 60.19 0.09 60.07 4.84 61.18 0.43 60.08 0.62 (0.43–4.1) 80.4 648.2 0.23 60.04 0.26 60.06 0.27 60.07 0.04 60.07 0.26 60.14 0 0
Pu 23 0.54 60.27 0.09 60.07 2.35 61.76 0.42 60.07 0.52 (0.39–3.19) 11.65 65.25 0.21 60.01 0.21 60.01 0.21 60.01 0 0.54 60.27 0 0
Gr 17 2.35 61.71 0.12 60.04 3.75 60.8 0.39 (0.17–2.63) 2.16 60.77 516.94 6339.27 0.2 60.03 0.2 60.04 0.22 60.04 0.02(0–0.1) 0.1 (0–1.97) 0.13 (0–4.23) 1.05 (0 to 3.22)
Gr2 10 0.46 60.25 0.07 (0– 0.15) 1.29 60.17 0.44 60.02 0.47 60.01 115.8 663.62 0.22 60.01 0.22 60.01 0.22 60.01 0 0.00 0.00 0.37 (0.17–0.93)
So 197 0.27 60.1 0.16 60.04 8.70 61.29 1.47 60.74 2.63 60.67 6.55 62.35 1.47 60.75 1.77 60.81 1.47 60.74 0 0 0 0.27 60.1
Ha 11 0.16 60.07 0 4.38 60.55 1.56 60.63 2.31 60.54 1 1.43 60.49 1.03 60.67 2.07 60.23 0 0.16 60.07 0 0
Ac 15 0.3 60.1 0.75 60.86 5.94 61.47 4.42 61.51 4.96 60.86 160 0.56 (0.27–4.15) 1.87 61.32 5.94 61.42 4.33 61.95 0.14 60.04 0.09 60.05 0.05 (0.01–0.26)
Sc 20 0.93 60.41 0.22 60.09 6.57 62.22 1.56 60.64 2.60 60.95 466.35 6202.72 0.35 60.06 0.43 60.07 0.48 60.08 0.12 60.09 0.27 60.22 0.29 60.26 0.23 (0–1.42)
Sc2 9 0.81 60.44 0.19 60.09 5.64 62.34 1.18 60.71 2.24 60.87 268.22 6146.67 0.32 60.07 0.34 60.05 0.37 60.05 0.05 (0–0.22) 0.09 (0–1.1) 0.31 60.3 0.22 60.09
Be 12 1.21 61.03 0.13 60.11 6.91 61.52 3.13 61.82 4.15 61.1 1 60 0.39 60.1 0.36 60.09 0.49 60.09 0.1 (0–0.34) 0.25 60.19 0.96 60.92 0
Be2 9 2.65 61.39 0.17 60.08 7.76 61.67 2.67 60.87 3.69 61.04 1 60 0.33 60.03 0.37 60.04 0.48 (0.35–3.22) 0.43 (0.07–2.9) 0.43 60.34 2.22 61.38 0
Hs 4 0.94 (0.36–2.25) 1.41 61.26 6.61 61.17 4.04 61.91 4.68 61.33 1 60 3.15 (0.39–6.09) 3.02 61.88 6.31 61.05 3.12 62.69 0.22 60.13 0.63 (0.2–2.13) 0 (0–0.07)
Hs2 10 0.46 (0.29–0.95) 1.72 60.81 6.3 62.29 3.29 61.07 4.29 60.77 1 60 3.03 61.71 2.83 60.98 5.19 61.96 2.16 62.06 0.17 (0–0.64) 0.33 60.19 0
Cu 27 0.35 60.15 1.41 60.46 9.95 (7.7–13.92) 8.02 61.46 8.64 60.99 1 60 3.17 62.12 5.54 62.82 8.83 61.92 5.66 62.43 0.13 60.06 0.14 60.09 0.03(0–0.34)
Sk 6 1.01 60.1 0.15 60.02 8.73 61.18 0.75 60.26 0.85 60.16 227.17 633.89 0.24 60.03 0.33 60.04 7.83 60.9 7.59 60.91 0.61 60.15 0.40 60.06 0
Sq 15 0.44 60.1 0 18.3 61.23 8.38 60.65 8.74 60.68 1 60 0.52 60.06 0.57 60.06 0.72 60.07 0.21 (0.06–0.8) 0.08 (0.06–0.1) 0.06 (0–0.24) 0.26 (0.2–0.5)
J. Acoust. Soc. Am., Vol. 136, No. 5, November 2014 Leuchtenberger et al.: Vocal repertoire of giant otters 2873
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