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Discrimination of chirp vocalizations in the cotton-top tamarin.

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American Journal of Primatology 2153-60 (1990)
Discrimination of Chirp Vocalizations in the
Cotton-Top Tamar in
Department of Psychology, University of Wisconsin, Madison
Natural exemplars of two types of chirp vocalizations were presented to
eight groups of cotton-top tamarins (Saguinus 0. oedipus) in a playback
paradigm. The two chirps share many acoustic features in common but are
used in entirely different circumstances. The tamarins gave different vocal
and behavioral responses to the playbacks of each chirp type, indicating
that a discrimination was made. The results suggest that tamarins can
discriminate subtle acoustic cues which have communicative significance.
In the absence of the nonvocal cues and social contexts that normally
co-occur with these vocalizations the tamarins responded with the same
vocal responses they would have given in normal social contexts. Significant differences in post-stimulus behavior to the two types of stimuli appeared in the first two blocks of trials, indicating that the playback paradigm can be an efficient means of testing discrimination between
different call types.
Key words: playback paradigm, vocal communication, natural response
A major question in vocal communication research is whether the various call
categories assigned by human investigators are isomorphic with the perceptual
classifications used by the animals [Snowdon, 19791. Only a few studies on primates have examined how animals perceive different call types: “coo” calls of
Japanese macaques (Macaca fuscata) [Petersen et al., 1978, 1984; Zoloth et al.,
19791; loud calls of gray-cheeked mangabeys (Cercocebus albigena) [Waser, 19771;
alarm calls of Goeldi’s monkey (Callimico goeldii) [Masataka, 19831; trills of
pygmy marmosets (Cebuella pygmaea) [Snowdon & Pola, 1978; Snowdon, 19871;
grunts of vervet monkeys (Cercopithecus aethiops) [Cheney & Seyfarth, 19821;
screams of rhesus macaque (Macaca mulatta) [Gouzoules et al., 19841.
Most of these studies have tested perceptual classification by using a playback
Received for publication October 13, 1989; revision accepted December 22, 1989.
Address reprint requests to Kim Bauers, Wisconsin Regional Primate Research Center, 1223 Capitol
Court, Madison, WI 53715; or Charles Snowdon, Department of Psychology, University of Wisconsin,
1202 West Johnson St., Madison, WI 53706.
0 1990 Wiley-Liss, Inc.
54 I Bauers and Snowdon
technique. The value of the playback paradigm lies in its ability to isolate the
information conveyed by a vocal signal from the nonvocal cues and social contexts
that co-occur with vocalizations in normal social interactions. If there are behavioral measures that differentiate between the two types of vocalizations in a playback paradigm, then one may conclude that the acoustic differences in the structure of the vocalizations are sufficient for discrimination. If the behavioral
responses are also appropriate to the situations in which these vocalizations are
normally given, then the structure of the call also conveys a semantic message
independent of other contextual cues.
Some studies have used a n operant paradigm, but the constraints of the operant environment may alter responsiveness to the stimuli, especially if animals
must perform tasks that are unrelated to the responses a n animal might exhibit in
a natural social environment. For example, Symmes & Newman [1974] used a n
avoidance learning task to show that squirrel monkeys could discriminate between
isolation peeps of different individuals, and Petersen et al. [1978, 19841 used a
lever-releasing paradigm to study discrimination of two different types of coo vocalizations in Japanese macaques and other species. In these studies discrimination was eventually shown, but the squirrel monkeys required several hundred
trials and the Japanese macaques appear to have been given upwards of 30,000
trials. Thus the operant technique requires lengthy training and testing of animals. Some primate species are less amenable to extensive handling for operant
testing than others, and these methods may be impractical or disruptive with
socially housed primate groups.
We have studied the discrimination of chirp vocalizations in captive cotton-top
tamarins by using playback techniques typically used in field studies. By housing
animals in normal social groups, we could observe and record spontaneous responses to stimuli. By studying captive animals we had control over which animals
were present for a test, and we could record lower-intensity vocalizations and
subtle behavioral changes.
The vocal repertoire of the cotton-top tamarin has eight chirp vocalizations
(short frequency-modulated calls). Chirps can be described in terms of four acoustic
variables, and each type is used in different contexts [Cleveland & Snowdon, 19821.
We chose to study the two chirp types most nearly similar in acoustic structure to
explore the limits of discriminability by tamarins. F-chirps and G-chirps differ
only in mean frequency and in the peak- to end-frequency range. The two calls are
given in different behavioral contexts and elicit different responses from cagemates when each is emitted spontaneously. The G-chirp is typically given by animals that appear to be relaxed and engaging in environmental exploration. The
F-chirp alerts other animals and is given in response to conspecific groups heard
from other rooms. In this study we monitored the behavioral and vocal responses
of tamarins to playbacks of each chirp.
Subjects and Housing
Eight pairs of adult cotton-top tamarins were tested. Three of these pairs had
one or more offspring. All but one of the animals were laboratory-born descendants
of a colony established before the species was designated as endangered. The animals were housed in large cages (0.9 x 1.5 x 2.3 m to 1.8 x 3.1 x 2.3 rn) fitted
with nest boxes and numerous branches and ropes to provide arboreal pathways.
Additional details of housing and husbandry are presented in McConnell & Snowdon [19861.
Chirp Vocalizations in Cotton-Top Tamarins / 55
TABLE I. Acoustic
Parameters of Chiru Vocalizations (kHz, Mean
Initial frequency
End frequency
Freauencv range
Initial frequency
End frequency
Frequency range
F-chirD all subiects
F-chin, stimulus
4.7 ? 0.6
3.6 & 0.4
1.5 ? 0.3
Single or first
of two G-chirps
Second G-chirp
G-chirp stimulus
8.9 & 0.5
5.8 ? 0.3
3.1 ? 0.4
6.9 ? 0.3
5.1 ? 0.5
1.8 ? 0.4
*The parameters are based on 12 individuals for the F-chirps and 14 individuals for the G-chirps.
Acquisition and Preparation of Stimuli
Chirp vocalizations were recorded from each adult in the study by using a JVC
KD 1636 cassette recorder with a Sennheiser ME 80 microphone with a K3U power
module. Several examples of each chirp that were recorded from each of the eight
pairs were measured to provide structural parameters for the population. For the
playback experiments we used chirps produced by a single animal living in a group
that was not tested. Thus, each subject was tested with identical stimuli, and each
animal was unfamiliar with the calls of the animal that provided the stimuli.
Table I presents the structural characteristics of the stimuli used in the experiment and of the population of calls recorded. We elected to use a G-chirp that
matched the parameters of the second G-chirp in a series to minimize the acoustic
differences in comparison with the F-chirp. Thus animals were presented with the
F-chirp and G-chirp stimuli that were most similar to each other. If a discrimination is made between these two stimuli, then more diverse exemplars of each class
of calls should be discriminable as well. Figure 1presents the sound spectrograms
of the stimuli used.
Stimuli were processed through a signal-processing software program
(VOCAL) to attenuate low-frequency noise and to adjust the peak amplitudes to
match those in spontaneously given calls. The stimuli consisted of a sequence of
two identical chirps separated by a 600 ms inter-chirp interval. This interval was
chosen based on inter-chirp intervals observed when chirps were produced in sequence spontaneously. Since the stimuli were very brief, we wanted to be certain
that if one stimulus were masked by cage noise or other vocalizations, the second
would be likely to be heard.
Experimental Procedure
The JVC recorder was connected via a Realistic amplifier to one of two speakers (Audax HD 13D34 with frequency response to 15 kHz) that were mounted in
each cage. A Sony TC-158SD cassette recorder and Sennheiser ME 80 microphone
were used to record the vocal activity of a pair. Each of the eight pairs was presented with four trials within each block, two with the F-chirp and two with the
G-chirp. Within each test session there were two playback trials using the same
stimuli separated by 15 min. The order of presentation of F-chirps and G-chirps
was alternated from one session to the next. Four blocks of trials were conducted
for a total of 128 trials. No pair was tested more often than twice a week.
All of the subjects were habituated to the observer. They ceased to attend
visibly to the observer within 5-6 min of her entry to the room. Five minutes of
56 I Bauers and Snowdon
500 MS
Fig. 1. F-chirp and G-chirp stimuli (Kay Sonagraph Model 6061 B, 160-16,000 Hz frequency range, narrowband filter).
blank tape ran prior t o the auditory stimulus. A variety of behavior and all vocalizations of the animals were recorded for 5 min before and 5 min after the test
stimulus. Vocal activity was recorded continuously. Because it was not always
possible to determine unequivocally which animal produced a call, the pair was
considered as a unit in evaluating vocal response. A focal animal point-sampling
system in which the male and female alternated as focal animals was used t o score
non-vocal behavior at 30 s intervals.
Behavior Analysis
The 30 s point samples from the 2.5 min preceding and following the stimulus
presentation were used for analysis. An immediate change in visual orientation
was expected to occur immediately after presentation of either stimulus. Based on
prior observations we expected the behavioral categories of “freezing, visual scanning, and piloerection”; “scent marking and nose rubbing”; and “visual orientation
to other groups” to increase after an F-chirp playback. The combined categories of
“eating, drinking, and foraging” and of “grooming, huddling, and sitting” indicate
relaxed and affiliative contexts and were not expected to change following an
F-chirp. Other than a brief change in orienting response, no change in the frequency of any behavior or vocalization was expected in response to the G-chirp
stimulus. The proportion of scan samples in which an animal moved was used as
an index of activity.
Vocal Analyses
The frequency of emission of all major classes of calls in the adult repertoire
was analyzed for the 2.5 min before and after stimulus presentation. The record-
Chirp Vocalizations in Cotton-TopTamarins I 57
ings from each session were input to a Spectral Dynamics Real Time Analyzer
(Model SD301D-C) with an analysis range of 0-20,000 Hz at a sampling rate of
60,000 Hz. The output of the analyzer was displayed on an oscilloscope screen and
filmed on a Grass CR4 Kymograph Oscilloscope Camera. From the continuous
strip of film it was possible to identify all calls by using the vocal categories defined
by Cleveland & Snowdon [19821.
Based on observations of vocal activity after spontaneous F-chirps, we predicted increases in F-chirps and in the combined category of “squeaks and flat
whistles.” Increases were also expected in “normal and quiet long calls.” Three
types of calls were predicted to remain at the same level after both stimuli: “modulated multi-level calls,” “initially modulated whistles,” and G-chirps. These are
locational or contact calls to which no response is given. Because the G-chirps of
juveniles could not be discriminated from those of adults, all G-chirps were
counted. The total number of vocalizations given in the 30 s before and after the
stimulus was analyzed to detect any change in the animals’ overall rate of vocalizing following a playback. The Wilcoxon Test was used to evaluate differences in
response to F-chirp and G-chirp stimuli.
The results from each of the four blocks were evaluated separately. By the
third block there was habituation to the test stimuli. Thus, the data analyses are
based on Blocks I and 11, the mean of four trials with each stimulus for each subject
There was a significant change in orienting responses to both stimuli at the
stimulus playbacks in comparison to both 30 s pre-stimulus and post-stimulus
levels (P‘s < 0.005 for each, Wilcoxon Test). The orienting response rarely occurred
except immediately following stimulus presentation. The orientation response was
greater to an F-chirp stimulus than to a G-chirp stimulus (82% of trials vs. 47% of
trials, P < 0.005).
The combined category of “freezing, scanning, and piloerection” indicative of
arousal and vigilance occurred significantly more often after an F-chirp than a
G-chirp stimulus (P < 0.01; Wilcoxon Test, 71% vs. 22% of trials). Visual orientation toward the hallway or ceiling also increased significantly following an F-chirp
stimulus (P < 0.025; 10% to 18%),and there was an increase in movement following an F-chirp (P < 0.02, 8% to 17%).There were no differences to the two stimuli
in the remaining behavioral measures.
Following an F-chirp presentation there was a significant increase in the number of F-chirps (P < 0.005, Fig. 2). The rate of F-chirps following an F-chirp
stimulus increased 358%in contrast t o the pattern following a G-chirp stimulus (P
< 0.01). There was also an increase in the number of “squeaks and flat whistles”
following an F-chirp playback (P < 0.0051, and in the total number of vocalizations
(P < 0.01). “Normal long calls and quiet long calls” occurred too infrequently
during test sessions to evaluate statistically.
The three categories of calls that were not predicted to change as a function of
stimulus presentation (“modulated multilevel calls,” “initially modulated whistles,” and G-chirps) were produced a t constant rates throughout the tests.
The cotton-top tamarins discriminated between exemplars of F-chirp and Gchirp stimuli in a playback paradigm. The responses agreed with our prior observations of the behavior associated with spontaneous production of these calls.
These brief stimuli differed in initial frequency and peak- to end-frequency range
58 I Bauers and Snowdon
4 1
Fig, 2. Vocal responses to chirp stimuli. A. F-chirp responses. B. "Squeaks and flat whistle" responses.
C: Overall frequency of vocalization. Histograms represent the mean number of calls in the pre-stimulus
interval (left),and post-stimulus interval (center).The right histogram in each set presents the pre-stimulus
to post-stimulus difference scores.
but shared many other acoustic features (Fig. 1).The acoustic stimuli alone, in the
absence of contextual cues which might otherwise elicit these responses, appear t o
provide sufficient information for animals to discriminate between chirps and to
make semantically appropriate responses. Natural response measures, appropriately documented, can be an effective means of assessing the validity of categories
that the human observer recognizes.
Chirp Vocalizations in Cotton-Top Tamarins I 59
The tamarins produced increased F-chirps and “squeaks and flat whistles” and
the total number of calls increased following the F-chirp stimulus. Tamarins also
showed more orientation and more vigilant behavior such as “scanning, freezing,
and piloerection” as well as greater locomotor activity after a n F-chirp stimulus.
The fact that orientation a t the stimulus was significantly increased to both Fchirps and G-chirps indicates that G-chirps were perceived by the tamarins even
though there were no other changes in behavior or vocal activity after a G-chirp
While it was possible to show a significant discrimination of call types with
only four trials per stimulus, there was also a rapid habituation of response to the
playback trials. By the third block of trials, there was a reduced tendency to orient
to the test stimuli. Thus, while a playback technique is efficient compared with
traditional operant techniques, there are potential drawbacks with playback techniques.
Nonetheless, the playback procedures used here allow the evaluation of behavioral responses to biologically relevant sounds by unrestrained captive primates in a normal social environment. This technique is very useful for understanding how other species partition their communicative sounds and helps human
observers validate their understanding of the contexts in which various sounds are
1. Two forms of chirp vocalizations with few acoustic differences (F-chirps and
G-chirps) were presented in a playback paradigm to eight pairs of cotton-top tamarins.
2. The tamarins oriented to both types of stimuli but showed predicted increases in specific vocalizations (F-chirps and “flat whistles”) and increased vigilant behavior following playbacks of F-chirps. These behavioral changes did not
occur following G-chirp playbacks.
3. The behavioral and vocal responses to the playbacks of each chirp type were
similar to the behavior and vocalizations following production of spontaneous
chirps. This indicates that the acoustic information in each chirp may be sufficient
to elicit appropriate responses in the absence of other contextual cues.
This research was supported by a National Science Foundation Graduate Fellowship to K.B. and by USPHS Research Grant MH 29,775 and Research Scientist
Award MH 00,177 to C.T.S. We are grateful for Jayne Cleveland’s long-term observations and analyses of the cotton-top tamarin vocal repertoire. We thank
Kevin Colwell for electronic assistance and Jack P. Hailman and anonymous reviewers for critical reading of the manuscript.
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