Journal of Comparative Psychology
2001, Vol. 115, No. 3, 258-271
Copyright 2001 by the American Psychological Association, Inc.
0735-7036/01/$5.00 DOI: 10.1037//0735-7036.115.3.258
The Production and Perception of Long Calls by Cotton-Top Tamarins
(Saguinus oedipus): Acoustic Analyses and Playback Experiments
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
Daniel J. Weiss, Brian T. Garibaldi, and Marc D. Mauser
Harvard University
The authors' goal was to provide a better understanding of the relationship between vocal production and
perception in nonhuman primate communication. To this end, the authors examined the cotton-top
tamarin's (Saguinus oedipus) combination long call (CLC). In Part 1 of this study, the authors carried out
a series of acoustic analyses designed to determine the kind of information potentially encoded in the
tamarin's CLC. Using factorial analyses of variance and multiple discriminant analyses, the authors
explored whether the CLC encodes 3 types of identity information: individual, sex, and social group.
Results revealed that exemplars could be reliably assigned to these 3 functional classes on the basis of
a suite of spectrotemporal features. In Part 2 of this study, the authors used a series of habituationdishabituation playback experiments to test whether tamarins attend to the encoded information about
individual identity. The authors 1st tested for individual discrimination when tamarins were habituated
to a series of calls from 1 tamarin and then played back a test call from a novel tamarin; both oppositeand same-sex pairings were tested. Results showed that tamarins dishabituated when caller identity
changed but transferred habituation when caller identity was held constant and a new exemplar was
played (control condition). Follow-up playback experiments revealed an asymmetry between the authors'
acoustic analyses of individual identity and the tamarins' capacity to discriminate among vocal signatures; whereas all colony members have distinctive vocal signatures, we found that not all tamarins were
equally discriminable based on the habituation—dishabituation paradigm.
Many species that dwell in dense environments develop a system of long-range vocalizations (Chapman & Weary, 1990;
Cheney & Seyfarth, 1996; Marten, Quine, & Marler, 1977; Mitani
& Nishida, 1993; Ryan & Sullivan, 1989; Wiley & Richards,
1978). In general, visually restrictive habitats promote greater
vocal communication between individual animals (Altmann, 1967;
Cheney & Seyfarth, 1996; Morton, 1986; Norcross & Newman,
1993; Romer & Bailey, 1986). Call morphology may become
increasingly differentiated in such habitats so that subtle variations
denote different contexts (Snowdon, Cleveland, & French, 1983).
The acoustic variation within these calls may convey information
about territorial status, group spacing, group location, or individual
identity (e.g., Beecher, 1982; Chapman & Weary, 1990; Cleveland
& Snowdon, 1982; Mitani, 1985). Therefore, to gain a better
understanding of the design of communication signals, researchers
must identify the sources of variation and attempt to discern the
types of information conveyed. To that effect, this study focuses
on the long call produced by cotton-top tamarins (Saguinus oedi-
pus), a species that inhabits dense tropical rainforest and has a
highly diversified vocal repertoire.
Cleveland and Snowdon (1982) identified three classes of long
calls produced by captive cotton-top tamarins. On the basis of their
analyses, the long calls we examined in the present study may be
classified as "combination long calls" (CLCs), vocalizations consisting of two syllable types: chirps and whistles. Cleveland and
Snowdon noted that the CLC has the greatest variability across
tamarins, perhaps due to individual tamarin differences. CLCs
appear to occur in a variety of circumstances involving social
excitement, disturbance, pairing with a new mate, play, and social
isolation (Cleveland & Snowdon, 1982). The most common context appears to be social isolation (Cleveland & Snowdon, 1982;
Thurwachter, 1980). Given the variability in acoustic parameters
noted (e.g., overall number of syllables and call duration) between
callers and the context in which the calls occur, the CLC provides
an excellent opportunity for investigating the relative contribution
of individual, sex, and group identity to call morphology. In fact,
the closely related phee call in marmosets, which seems to occur
in similar contexts, encodes information about both the sex and the
identity of the caller (Jorgensen & French, 1998; Norcross &
Newman, 1993).
Our research program represents an attempt to explore the
meaningful components of a communication system among tamarins by designing playback experiments that are informed by
detailed acoustic analyses. This integration of information from
studies of production and perception has been successfully carried
out with a number of species (e.g., birds: Brown, Dooling, &
O'Grady, 1988; Chaiken, 1992; Emlen, 1972; pikas: Conner,
1985; frogs: Burmeister, Wilczynski, & Ryan, 1999; Wilczynski,
Rand, & Ryan, 1999; and primates: Hauser, 1998b; May, Moody,
Daniel J. Weiss, Brian T. Garibaldi, and Marc D. Mauser, Department of
Psychology, Harvard University.
This work was supported by Harvard University's Mind Brain and
Behavior Grant 368422. We thank Douwe Yntema, Kristen Vickers, and
Eric Loken for their advice on analyzing the data; Kerry Jordan for her help
in running the experiments and scoring trials; Fritz Tsao and Joe Swingle
for their help in analyzing data; and Asif Ghazanfar for his comments on
an earlier version of this article.
Correspondence concerning this article should be addressed to Daniel J.
Weiss, who is now at Brain and Cognitive Sciences Department, Meliora
Hall, Office 494, University of Rochester, Rochester, New York 14627.
Electronic mail may be sent to dweiss@bcs.rochester.edu.
258
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
VOCAL PRODUCTION AND PERCEPTION BY TAMARINS
& Stebbins, 1988; Snowdon & Cleveland, 1980; Snowdon et al.,
1983). First, we report the findings from an acoustic analysis of the
CLC designed to assess the types of information encoded in this
call. Next, we report the results from a series of playback experiments designed to test whether tamarins can be discriminated by
voice alone, and more specifically, by the acoustic morphology of
their CLCs.
The goal of the acoustic analyses was to determine whether the
morphology of the tamarin's CLCs carries information about individual identity, sex, and group membership. Given previous
work with other closely related species, we anticipated finding
evidence of individual vocal signatures (e.g., common marmosets,
Jones, Harris, & Catchpole, 1993; black-tufted-ear marmosets:
Jorgensen & French, 1998) and sex-specific vocal signatures (e.g.,
red-chested moustached tamarins: Masataka, 1988; golden lion
tamarins: Benz, French, & Leger, 1990). Evidence of group-level
acoustic signatures has been weaker, coming primarily from chimpanzees (Mitani & Brandt, 1994) and the more closely related
pygmy marmosets (Elowson & Snowdon, 1994). Such withingroup acoustic convergence has been taken as evidence of vocal
learning. To date, there is no evidence showing that convergence
in call morphology occurs when multiple groups are housed in
close proximity, a situation that arose in our captive colony.
The playback experiments were designed to complement the
acoustic analysis of individual variation within CLCs. For a tamarin to
be recognized by voice alone, two conditions must be satisfied. First,
the sender must produce a signal that contains an individual signature.
Second, the receiver must be able to detect differences between
signals on the basis of the parameters that define the signature
(Beecher, 1982). On the basis of these conditions, individual recognition has been successfully demonstrated in a variety of species,
including pikas (Conner, 1985), tungara frogs (Wilczynski et al.,
1999), budgerigars (Brown et al., 1988), Cory's shearwaters (Bretagnolle & Lequette, 1990), and European starlings (Chaiken, 1992).
Because prior work (e.g., Snowdon et al., 1983) and the acoustic
analyses presented in Part 1 suggest that individual identity is encoded
in the tamarin's CLC, the playback experiments presented in Part 2
were designed to explore the perceptual component of individual
recognition, assessing whether tamarins actually perceive differences
in CLCs from different tamarins.
Our study is structured as follows. In Part 1, we present the
results of our acoustic analyses of individual, sex, and group
identity and then discuss these results in light of current thinking
about the sources of acoustic variation and their role in perceptual
classification. In Part 2, we report findings from several experiments designed to test the extent of individual discrimination using
a habituation-dishabituation paradigm; in the wild this technique
has been successfully used with primates (e.g., Cheney & Seyfarth,
1988; Hauser, 1998a; Zuberbuehler, Cheney, & Seyfarth, 1999),
but in captivity it has only been successfully used with speech
stimuli (Ramus, Hauser, Miller, Morris, & Mehler, 2000) as opposed to species-specific signals. We conclude by discussing the
benefits of integrating studies of production and perception as well
as some of the limits of our experimental approach.
Part 1: Call Production and Acoustic Morphology
The ability to convey and receive information regarding individual identity represents an important adaptation for social com-
259
munication (Beecher, 1982; Cheney & Seyfarth, 1990). Thus, it is
not surprising that this capacity is widespread across many species
(e.g., frogs, Davis, 1987; dolphins: Sayigh et al., 1999; passerine
birds: Stoddard, 1996). In nonhuman primates, the ability to recognize individuals on the basis of vocal signals alone has received
much attention. The focus of many of these studies has been on
calls that are able to convey identity over long distances (e.g.,
Chapman & Weary, 1990; Kajikawa & Hasegawa, 1996; Mitani,
Gros-Louis, & Macendonia, 1997; Snowdon & Cleveland, 1980).
The capacity of cotton-top tamarins to recognize other tamarins
on the basis of the acoustics of the CLC seems likely because
related species have demonstrated this capability (e.g., pygmy
marmosets: Snowdon & Cleveland, 1980; common marmosets:
Jones et al., 1993; black-tufted-ear marmosets: Jorgensen &
French, 1998). Given these studies, it seems likely that most, if not
all, Callitrichids will exhibit an individual signature system. This
includes cotton-top tamarins.
Sex differences in vocal morphology have also been reported in
a number of primate species (e.g., vervet monkeys, Cercopithecus
aethiops, Seyfarth, Cheney, & Marler, 1980), including several
Callitrichids (e.g., moustached tamarins, Saguinus mystax, Heymann, 1987; red-chested moustached tamarins, Saguinus I. Labiatus, Masataka, 1988; golden lion tamarins, Leontopithecus rosalia,
Benz et al., 1990; common marmosets, Callithrix jacchus,
Norcross & Newman, 1993). Indeed, there is some evidence suggesting that long calling in marmosets and some tamarin species
may play a role in mating (e.g., Yoneda, 1981; Masataka, 1988;
Norcross & Newman, 1993).
Our final acoustic analyses focus on the possibility of group
convergence in call morphology, and consequently, on the significant between-group differences in acoustic structure. Three factors make these analyses different from those reported to date.
First, all of our tamarin groups were housed in the same room, and
thus had continuous acoustic contact. Second, there were no obvious motivational differences that could explain acoustic convergence within groups. Third, there were no genetic or environmental factors that could account for within-group convergence. Thus,
if cage group identity is encoded in the CLC, it may indicate that
some level of vocal learning is taking place.
In one of the few laboratory studies conducted to find evidence
of vocal learning in nonhuman primates, Elowson and Snowdon
(1994) discovered that pygmy marmosets (Cebuella pygmaea) can
modify their trill vocalization in response to their social environment. In addition, experiments on an array of species have shown
that call structure may be modified as a result of changes in social
pairings (e.g., spear-nosed bats, Boughman, 1997; pygmy marmosets, Snowdon & Elowson, 1999; budgerigars: Hile, Plummer, &
Striedter, 2000). Our analyses may be more limited with respect to
vocal learning in that we did not manipulate the social context of
the colony. Nevertheless, if group identity is encoded in the CLCs
of cotton-top tamarins, then vocal learning is a possible mechanism, and future work can be designed to explore this possibility
and others.
General Method
Subjects. The subjects consisted of a colony of 13 cotton-top tamarins
(Saguinus oedipus). The members of the colony were born in captivity at
the New England Regional Primate Center (Southborough, MA) and then
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
260
WEISS, GARIBALDI, AND HAUSER
housed at the Primate Cognitive Neuroscience Laboratory at Harvard
University. Tamarins were housed in groups of 2 or 3 animals in
a 6.0 X 5.0 X 2.5 ft (1.8 X 1.5 x 0.76 m) home cage made of stainless
steel wire and Plexiglas. The cage contained tree branches, perches, and
wooden nest boxes. At the start of the experiment, there were four mated
pairs: one family group consisting of a mated pair and a female offspring
and one female pair. During the course of the experiment, 1 female tamarin
(MR) died and was replaced by a new male tamarin (RJ). The female
tamarin pair was divided and paired with males. Thus, the colony consisted
of five mated pairs and one family group. Their diet consisted of Purina
tamarin and marmoset chow, crickets, mealworms, supplemental vitamins,
and sunflower seeds. This completely balanced diet was supplemented by
food received during experiments (typically Noyes [Lancaster, NH] bananas and sweet pellets, fruit, occasionally Froot Loops, and marshmallows). They were fed once a day in the early evening. Tamarins had ad
libitum access to water.
The cage group membership was as follows (male-female): Cage 1, AC
and JG; Cage 2, DD, ES, and RB; Cage 3, RW and SH; Cage 4, SP and EN;
Cage 5, ID and EM; and Cage 6, RJ and UB. The females that were
separated (as mentioned above) were SH and UB. There were a number of
related tamarins within the colony: RB was the daughter of DD and ES, SP
was the daughter of UB, and RW and ID were twin brothers.
Call acquisition. The CLCs used as exemplars for the acoustic analyses were recorded from May 1998 through March 1999. The calls were
recorded in two contexts: either in isolation in an acoustic chamber or in an
experiment focusing on the social aspects of communication.
To obtain calls from the acoustic chamber (Model 400-A, Industrial
Acoustics, Lodi, NJ) we transported the tamarins to a test room that was
both visually and acoustically isolated from all other members of the
colony. Tamarins were placed in a cage (45 X 45 X 20 cm) within the
larger sound chamber for a period of up to 15 min. Sessions were recorded
onto a digital audiotape (DAT; DaPl digital audio tape recorder, Tascam,
Tokyo, Japan; sampling rate: 48 kHz) using a Sennheiser ME66 directional
microphone (Sennheiser, Old Lyme, CT; frequency response: 50-20,000
Hz) or a Sennheiser MKH60P48 microphone (frequency response: 5020,000 Hz). The tape was then acquired digitally onto a Power Macintosh
7100/80 (Apple Computer, Inc., Cupertino, CA) using Sound Designer II
software (1996) and an Audiomedia II card. Some sessions were recorded
directly into the computer by passing the signal through the DAT and
acquiring with Sound Designer II.
For the calls recorded in the social communication experiment, we
transported the tamarins into a test room that was visually and acoustically
isolated from the colony room. The tamarins were placed in the social
communication apparatus consisting of two runways separated by a Plexiglas barrier. Food troughs were placed out of sight at the end of the runway.
The experiment tested for audience effects (sensu, Marler, Dufty, & Pickert, 1986) in the presence of food or predators. The calls that were used
from these experiments were recorded while the tamarin was alone in the
apparatus with no predator or other tamarin present. Sessions were taped
with a Sennheiser ME66 directional microphone and the signal was passed
through a Tascam DAT (see above) into a Power Macintosh 7100/80. The
Sound Designer II software was used to acquire the sound onto the
Audiomedia U sound card.
All calls (regardless of origin) were hi-pass filtered just below the lowest
frequency (as determined by a 512 fft spectrogram generated in Canary
Version 1.2, 1995) and then normalized (using Sound Designer II). After
the sound files were edited, we listened to them in the acoustic chamber to
check for audible background noise or any distortion in the playback.
A total of 129 CLCs were recorded from 12 different tamarins over a
period of 1 year. A range of 3 to 21 exemplars per tamarin was examined.
The calls were selected at random from our catalog of high quality
recordings (obtained through the methods described above). By selecting
randomly, we ensured that these calls were representative of the natural
variation within our population. It should be noted that the number of
vocalizations selected for each tamarin differed because of the individual
differences in rates of production.
Of the 129 CLCs analyzed, 74 were five-syllable CLCs. In addition to
the multiple discriminant analyses (MDAs) reported on the overall call set,
separate sets of MDAs were reported for this subset of calls. It should also
be noted that the analyses performed for this study were repeated to ensure
that the results were replicable (though these analyses are not reported
here).
Acoustic analysis. All calls were analyzed using Canary (Version 1.2,
1995) for Macintosh computers. Table 1 outlines the parameters that were
measured for each acquired CLC (see Figure 1 for an example of a
spectrogram generated for the analysis). Two factors contributed to the
selection of spectral and temporal characteristics chosen for measurement.
The first was that previous studies of nonhuman primates have shown that
both temporal and spectral characteristics of vocalizations may be used in
order to process species-specific vocalizations (e.g., see Fischer, 1998;
May et al., 1988, 1989; Owren & Bernacki, 1988; Seyfarth & Cheney,
1984). In addition, in a previous study of the vocal repertoire of the
cotton-top tamarin, the authors used a number of these parameters in their
analysis (Cleveland & Snowdon, 1982; Snowdon et al., 1983). The use of
similar parameters may facilitate comparisons across these different
populations.
Bonferroni adjusted factorial analyses of variance (ANOVAs) and t tests
were initially performed to identify significant parameters for discriminating between individual tamarins and groups of tamarins. MDA was then
used to generate functions to reliably categorize calls across parameters of
interest. However, because sex is a dichotomous variable, a binary logistic
regression was used instead of the MDA. Because the data set consisted of
calls ranging from three to seven syllables, we focused many analyses on
the first syllable and the average of the final two syllables, as this statistical
approach helped avoid overfilling Ihe functions lo the data.
To determine whelher our resulls were statistically significant, we used
a highly conservative measure. Because there were unequal samples across
tamarins, we computed chance on the basis of the largest sample from any
one tamarin. For example, in Ihe individual identity analysis, the greatesl
contribution came from a tamarin lhal produced 21 oul of Ihe 129 calls lhal
were analyzed. Therefore, for lhal condition, chance was computed as
21/129 or 16% for all tamarins.
There were Iwo groups of vocalizations for each analysis. The first group
consisted of all CLCs recorded, regardless of how many syllables were
present To control for some of Ihe variability of the CLCs, we restticted
Ihe second group lo only five-syllable long calls. These calls were stereo-
Table 1
Parameters Measured
Parameter
Temporal
Call duration
Syllable duration
No. of syllables
Intersyllable pause
Duration to peak frequency of
syllable
Spectral
Syllable start frequency
Syllable end frequency
Frequency contour
Syllable peak frequency
Mean high frequency
Mean low frequency
a
fft size = 512.
b
fft size = 2,048.
Measuremenl
Waveform or spectrogram
Waveform or spectrogram
Spedrogram"
Waveform or spectrogram
From speclrogram
Power spectrum al start of syllable6
Power spectrum al end of syllable
Difference between peak frequency
al start and end of syllable
Speclrogram
Spectrum
Lowesl frequency in the syllable15
c
On the basis of power spectrum.
261
VOCAL PRODUCTION AND PERCEPTION BY TAMARINS
Time(s)
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
Figure 1. A spectrogram from a five-syllable long call. Note that temporal information such as syllable duration, overall duration, and intersyllable intervals may be easily extracted from this representation.
typed in that they always consisted of two chirps followed by three
whistles. The five-syllable CLCs were also used as stimuli in our perceptual studies.
Results
Individual identity. A Bonferroni adjusted factorial ANOVA
(p < .006) shows that there are a number of spectral and temporal
parameters that significantly differ across tamarins (see Tables 2
and 3). A pairwise comparison across all tamarins shows that
different pairs of tamarins vary with respect to the number of
significant spectral and temporal differences. This suggests that
individual tamarin callers differ from each other in a variety of
ways and that some tamarins may be more closely related to others
in their call morphology; this finding is clearly limited by the fact
that it is restricted to the parameters that we selected to measure.
A series of MDAs were used to explore whether we could reliably
distinguish tamarins on the basis of the acoustic parameters of their
CLCs.
MDA: First syllable and average of two terminal syllables.
Sixty-five of the 129 CLCs were used in a discriminant function
analysis. A series of functions were generated that reliably predicted tamarin identity for 91% of the calls. When the 64 calls that
we withheld were entered into the function, they were correctly
classified 63% of the time. This result is significantly above
chance (binomial test, chance = 16%, p < .001). Overall, this
analysis was able to reliably predict individual identity 77% of the
time. Figure 2 shows the plot of the centroids (function averages)
of each tamarin for the first three canonical functions used in the
analysis. This plot displays a three-dimensional representation of
the relationship between the CLCs of each tamarin on the basis of
the most important canonical functions. The associated eigenvalues were greater than 10% of the sum of the eigenvalues of all
functions. This is a common criterion used in choosing which
functions should be included in an analysis (see Yntema, 1997).
Overall, several spectral and temporal parameters were important
for classification. Spectral parameters included the mean low frequency of the last two syllables and the mean high and mean low
frequencies of the first syllable. Temporal parameters included
total duration of the call and average duration to the peak frequency of the two terminal syllables.
MDA: First syllable and average of the last two syllables for
five-syllable calls. Forty of the 74 five-syllable CLCs were used
to create a MDA that was able to predict the identity of the caller
with an accuracy of 98%. When the remaining 34 calls were
entered into the analysis, we correctly classified them 56% of the
time (binomial test, chance = 19%, p < .001). In total, the discriminant analysis was able to predict the identity of the caller with an
accuracy of 78%.
There were a number of spectral and temporal parameters that
were important in classifying the data set. The temporal parameters
included overall call duration, average syllable duration (for the
two terminal whistles), and average duration to peak frequency
(for the two terminal whistles). The most significant spectral
parameters included the mean high frequency and the mean low
frequency of the first syllable as well as the average mean low
frequency of the two terminal syllables.
Sex differences.
We performed a series of / tests (Bonferroni
adjusted, p < .005) across each parameter of the call to determine
whether there were any significant differences based on the sex of
the caller. Table 2 shows the results of these tests using data from
Table 2
Significant Differences: All Calls
Syllable order
Parameter
Temporal
Duration
No. of syllables
Syllable duration
Intersyllable pause
Duration to peak frequency of syllable
Spectral
Syllable start frequency
Syllable pause frequency
Syllable end frequency
Frequency contour
Mean high frequency
Mean low frequency
Note.
1st syllable
, S, C
I, C
,C
,C
,C
,C
2nd to last
syllable
I, S, C
I, C
I, S, C
I, S
I, S, C
Last syllable
,S, C
,c
,S, C
,S
Syllable
average
I, S, C
I, C
I, S
I
I, S, C
I
C
I, S
I.C
,c
c
,C
I
I
I, C
I, c
I, c
I = individual identity; S = sex identity; C = cage group membership. For all values, p < .005.
262
WEISS, GARIBALDI, AND HAUSER
Table 3
Significant Differences: 5-Syllable Calls
Syllable order
Parameter
Temporal
Duration
Syllable duration
Intersyllable pause
Duration to peak frequency of syllable
Spectral
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
Syllable start frequency
Syllable pause frequency
Syllable end frequency
Frequency contour
Mean high frequency
Mean low frequency
Note.
1st
syllable
2nd
syllable
3rd
syllable
4th
syllable
5th
syllable
I, S, C
I, S, C
I, S, C
I
I, S, C
I, S, C
I, S, C
I, S, C
I, S
I
I
I
I, S
C
C
C
C
C
I, S
I, S, C
C
C
C
I, S
I
I = individual identity; S = sexual identity; C = cage group membership. For all values, p < .005.
the first syllable and the two terminal syllables in addition to the
averages across all syllables. Temporal parameters accounted for
most of the significant differences between sexes. Female calls
tended to be longer than male calls by an average of 437 ms. The
terminal syllables in female CLCs were also significantly longer in
duration (M difference = 159 ms, SD = 23.0 ms). The intersyllable latency before the second-to-last syllable was longer for
female calls (M difference = 10 ms, SD = 2.5 ms). The duration
to the peak frequency of the next-to-last syllable was longer for
4'
I
EN4
JG1
u.
U
CF1
Figure 2. This figure contains a plot of each tamarin's centroids (across
all long calls) for the first three canonical functions (CF) used in the
analysis of individual identity. Note that this type of plot represents an
acoustic space for the tamarin callers. The distances between the centroids
indicate how the tamarins differ with respect to each of these dimensions.
The superscript numbers show the cage group membership for each tamarin. Lowercase letters represent male tamarins, and uppercase letters represent female tamarins.
females than for males (M difference in duration = 176 ms,
SD = 26.0 ms).
Binary logistic regression: First syllable and average of the last
two syllables. Sixty-five calls were used in the binary logistic
regression. A linear function was created that classified the sex of
the caller with an accuracy of 85%. The generated function was
able to classify the remainder of the call set (64 calls) with an
accuracy of 70% for males (binomial test, chance = 43%, p =
.004) and 76% for females (binomial test, chance = 57%, p =
.017). Overall the classification average was 76% for males (binomial test, chance = 43%, p < .001) and 82% for females
(binomial test, chance = 57%, p < .001) across all CLCs.
Of further relevance, the parameters that were significant in the
t tests were also the most important in defining the function. These
included call duration, syllable duration, and duration to the peak
frequency of the call.
Sex differences in five-syllable calls. A total of 29 male and 45
female five-syllable CLCs were used in this analysis. Bonferroni
adjusted t tests were used to compare parameters across all syllables. The results from these tests were similar to those observed
with all CLCs included (see Table 3). Female calls were significantly longer than male calls (including longer whistles). Further,
the duration to the peak frequency of the last three syllables was
also significantly longer in female calls.
Binary logistic regression: First syllable and average of the two
terminal syllables in five-syllable long calls. There were not
enough five-syllable long calls from both sexes to generate a
reliable function with the first half of the calls and then check the
reliability with the remaining calls. We, therefore, entered all of
the calls into the regression and found that the calls could be
assigned to the correct sex with an accuracy of 85% (76% of
males, 91% of females). These results are significantly above
chance (binomial test: males, chance = 39%, p = .0001; females,
chance = 61%, p < .00001). Many of the parameters that were
important in determining the function when all calls were analyzed
were also important in this analysis. These included duration of the
entire call, syllable duration, and duration to the peak frequency.
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
VOCAL PRODUCTION AND PERCEPTION BY TAMARINS
Cage-group membership. In general, several temporal and
spectral parameters appeared to differ between cage groups (see
Table 2). Temporal parameters included duration of the entire call,
duration of the last two syllables, number of syllables in the call,
duration to the peak frequency of the fourth syllable, and the
intersyllable latency between the third and fourth syllables. Important spectral parameters included the start, peak, and end frequency of the first syllable as well as the mean high and mean low
frequencies of the first syllable. The temporal parameters that were
significant included the overall duration, the duration of the last
two syllables, duration to the peak frequency of the fourth syllable,
and the intersyllable latency between the fourth and fifth syllables.
MDA: First syllable and average of last two syllables. A series
of functions were created that predicted cage-group membership
with an accuracy of 77%. The remaining calls were classified by
these functions with an accuracy of 52% (binomial test: chance =
25%, p < .001). Using all calls, we reliably predicted the analysis
of cage-group membership with an accuracy of 64%. The results
across individual cages varied, ranging from 30% to 80%.
The first two canonical (discriminant) functions generated in the
analysis accounted for 74% of the variance in the data. Figure 3
shows the plot of the centroids for each cage group on the first 2
canonical functions. The parameters that were important for generating the functions were similar to the parameters that were
significant in the factorial ANOVAs. The important temporal
parameters included total duration of the call, the duration of the
first syllable, and the average duration of the last two syllables.
Important spectral parameters included the mean high and mean
low frequencies of the first syllable as well as the start and peak
frequencies of the first syllable.
Cage-group differences in five-syllable long calls. A series of
factorial ANOVAs (Bonferroni adjusted, p < .006) revealed significant differences across a number of parameters (see Table 3).
Significant temporal parameters included total call duration, duration of the two terminal syllables, and duration to the peak frequency of the fifth syllable. Significant spectral parameters included the mean high and mean low frequencies of the first three
syllables and the start, peak, and end frequencies of the first
syllable.
MDA: First syllable and the average of the last two syllables.
Forty of the 79 five-syllable CLCs were used in the initial analysis.
A series of functions were generated that predicted cage-group
membership with an accuracy of 80%. The remaining calls were
then correctly classified with an accuracy of 56% (binomial test:
2
1
5:
0
-1
4
3
-2
6
-
1
0
1
2
3
CF1
Figure 3. This figure contains a plot of each cage's centroids (across all
long calls) for the first two canonical functions (CF) generated in the
analysis of cage group membership.
263
chance = 34%, p = .004). The combined results yielded a classification average of 69%. Accuracy varied across cage group from
29% to 100%.
The first two functions accounted for 95% of the variance in the
data. The parameters that were most important for these functions
resembled the list of parameters that were significant in the factorial ANOVAs. Important temporal parameters included total
duration of the call, the average duration of the fourth and fifth
syllables, and the duration to the peak frequency in the first and
last two syllables. Important spectral parameters included the mean
high and mean low frequencies of the first syllable and the start,
peak, and end frequencies of the first syllable.
Discussion
The main findings from our analyses are that the CLCs of the
cotton-top tamarin can be categorized by individual, sex, and
group identity. For individual identity, both spectral and temporal
parameters were important for classification. For sexual identity,
temporal parameters seemed most important. For group identity,
temporal parameters were important as were some spectral parameters related to the first syllable. Although these findings do not
allow us to conclude that tamarins use the selected features to
identify the identity, sex, or group of the caller, or that they are
able to do so, they do reveal that within this call type, there is the
potential for such recognition.
It is not surprising that we found acoustic information about
individual tamarin identity encoded in the CLCs. As mentioned
earlier, individual recognition is widespread among many different
species (see above) because it plays an important role in social
communication.
The finding that sexual identity may be contained within the
acoustics of the call suggests that long calling may play a role in
mating or group composition. This is consistent with findings from
closely related species (e.g., common marmosets: Norcross &
Newman, 1993). In fact, the importance of temporal factors in this
analysis resembles findings in red-chested moustached tamarins
(Masataka, 1988) as well as in the common marmosets' phee calls
(Norcross & Newman, 1993). It is also possible, of course, that sex
differences in call morphology are a by-product of differences in
vocal tract morphology that were selected for reasons other than
calling and mate choice. These findings need to be augmented with
both field studies as well as perceptual experiments in order to
verify that sexual identity can be discriminated and used in mate
choice.
We may look to the closely related phee call in marmosets to
gain some insight as to why sex differences in CLCs may be
important. It has been hypothesized that phee calls may function to
advertise reproductive status to conspecifics (Moynihan, 1970). In
addition, field studies have shown that solitary tamarins may use
long calls as a mechanism for vocally searching for mates. Young
female tamarins have been observed to approach unfamiliar male
callers (see Masataka, 1988; Norcross & Newman, 1993; Yoneda,
1981). In contrast, preliminary results from phonotaxis experiments, in which calls were played from known and unknown
individual tamarins, suggest that female tamarins approach known
males, whereas males approach unknown females (Miller, Hauser,
Miller, & Gilda Costa, 2001). More research is necessary to
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
264
WEISS, GARIBALDI, AND HAUSER
determine whether and how the CLC plays a role in attracting
potential mates.
Our finding that information about group identity is encoded in
the acoustics of the CLC suggests that some degree of vocal
learning may occur within each cage group. This finding is of
particular interest because there have been few examples of vocal
learning in primates (see Janik & Slater, 1997). In addition, although previous studies of vocal learning have found differences
between colonies (e.g., Elowson & Snowdon, 1994; Marshall,
Wrangham, & Arcadi, 1999), the tamarins used in our analyses
were housed within the same room, allowing for visual, olfactory,
and acoustic contact between members of different cages. However, further research is necessary in order to establish that vocal
learning occurs. This includes experiments designed to measure
the extent to which call matching occurs (during calling bouts) as
well as recordings from newly mated pairs.
The extent to which our findings will generalize to other species
or other call types within species must be tempered by a number of
factors. Norcross and Newman (1993) discovered differences in
call structure that depended on the context of the recordings. When
vocalizations were recorded from an isolated tamarin as opposed
to a group-housed tamarin, there were more syllables per call and
an overall increase in call duration. These modifications may have
made the callers easier to localize. Likewise, in our study, it is
important to bear in mind the context in which these calls were
recorded. The calls were taken from tamarins that were isolated
from their groups. Thus, these findings may not extend to CLCs
that are produced by tamarins that are not isolated.
Similarly, one must be careful in comparing the acoustics from
this set of recorded tamarin calls with other call sets. Given the
findings of Jorgensen and French (1998) that phee calls in marmosets may not be stable over time despite the persistence of
individual characteristics, it would be interesting to investigate the
stability of the tamarin CLC. It should be noted that the entire
tamarin call sample used in this study was recorded within a
12-month period to diminish the effects of longitudinal changes.
As mentioned earlier, in the study of communication it is important to consider aspects of production and perception. On the
basis of the fact that the cotton-top tamarin's CLC encodes acoustic information about tamarin caller identity, sex, and group membership, in the following playback experiments, we investigated
whether such acoustic differences are perceptually salient. Specifically, we asked whether cotton-top tamarins can discriminate
individual tamarins by their calls alone. If tamarins are able to
perceive differences between callers, then future experiments may
investigate which features are perceptually salient and underlie this
ability.
Part 2: Playback Experiments
Several studies, spanning a wide variety of primate species,
have shown that individual identity may be encoded in contact
calls (e.g., chimpanzees, Marler & Hobbett, 1975; squirrel monkeys, Symmes, Newman, Talmage-Riggs, & Lieblich, 1979; ringtailed macaques, Macedonia, 1986; common marmosets, Jones et
al., 1993; blue monkeys, Butynski, Chapman, & Chapman, 1992;
black-tufted-ear marmosets, Jorgensen & French, 1998). However,
these studies do not address whether individual animals use the
information encoded in the signal to identify other individual
animals by voice. Playback experiments are essential for addressing the problem of individual recognition from the perceptual
perspective.
Studies of several primate species have used playback experiments to explore the question of individual recognition (e.g.,
vervet monkeys: Cheney & Seyfarth, 1980, 1982; rhesus macaques: Hansen, 1976; Kendall, Rodman, & Edmond, 1996; barbary macaques: Hammerschmidt & Fischer, 1998; pygmy marmosets: Snowdon & Cleveland, 1980; chimpanzees: Kajikawa &
Hasegawa, 1996). Of these studies, few have been performed with
captive populations (e.g., Kajikawa & Hasegawa, 1996; Snowdon
& Cleveland, 1980) and none have made use of the habituationdishabituation paradigm that has proved effective in field studies
(e.g., Cheney & Seyfarth, 1988; Kendall et al., 1996; Seyfarth &
Cheney, 1990; Hauser, 1998a; Zuberbuehler et al., 1999). This
paradigm is powerful because it allows researchers to investigate
perceptual classification in animals without training.
There are several reasons to expect that tamarins can recognize
individuals on the basis of their CLCs. First, results from our
acoustic analyses (reported earlier) suggest that information about
individual tamarin identity is contained within the CLC. Second,
previous studies with related species (e.g., pygmy marmosets,
Snowdon & Cleveland, 1980), as well as one study with cotton-top
tamarins (Snowdon et al., 1983), provide evidence of individual
recognition; the latter study used a different kind of long call and
a different method. Finally, the function of the CLC has been
described as an affiliative signal (e.g., Cleveland & Snowdon,
1982), sometimes occurring when an individual animal is separated from its group. Therefore, one would expect CLCs to provide
sufficient information for individual recognition. These experiments represent only an initial step in our attempt to identify the
critical features mediating perceptual classification of vocalizations in cotton-top tamarins.
Because we anticipated finding evidence of individual recognition for the cotton-top tamarin's CLC, we generated the following
prediction: If we habituate our test subject to several CLC exemplars from one individual and then present this subject with a CLC
from a different individual, the test subject should dishabituate
(i.e., respond) to the new individual's call. However, if the subject
is habituated to CLCs from one individual and then presented with
a novel CLC from the same individual, the subject should transfer
habituation (i.e., not respond). Therefore, our first series of playbacks used this procedure to test for responses to changes in
tamarin caller identity for both opposite and same-sex pairings.
General Method
Apparatus. The test cage used for the playback experiments was
housed in an acoustic chamber. During experiments, we placed the tamarins in a wire and cloth test cage (45 X 45 X 20 cm) with a wire floor. A
thin black cotton sheet hung behind the cage. Behind the sheet, an Alesis
Monitor One speaker (Alesis Corporation, Santa Monica, CA; frequency
range, 45-18,000 Hz ± 3 dB) was mounted on a shelf above the box, either
directly behind, or to the left or right of center (location was changed
between experiments to prevent habituation to sounds emitted from one
location).
A video camera (Videolabs Flexcam Videolabs, Minneapolis, MN) was
used to record and monitor the sessions. An Alesis RA-100 amplifier drove
the speaker. Hie experimenters watched the session on a monitor outside
of the acoustic chamber. The experiment was run using a HyperCard (1996)
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
VOCAL PRODUCTION AND PERCEPTION BY TAMARINS
program on a Power Macintosh 7100/80 AV. We played back calls using
an Audiomedia n sound card (sampled at 48 kHz) outputting to an Alesis
Monitor 1 speaker. A log of each session was recorded in HyperCard. This
allowed the experimenters to enter data on-line and keep track of time
elapsed between trials. We recorded vocal responses during trials using a
Sennheiser MKH60P48 directional microphone (frequency response, 5020,000 Hz).
Stimuli. Calls used in this experiment were recorded during sessions of
another experiment. We recorded additional calls while the animals were in
the playback chamber. In both cases, the calls were recorded on a Tascam
DAT using a Sennheiser ME-60 microphone.
We hi-pass filtered the calls using Sound Designer n software. To
determine the frequency of the filter, we calculated a spectrogram (1024
fft) and measured the lowest frequency of the call. After filtering the call
at that frequency, all of the calls were normalized to 100% for amplitude.
Only high quality calls were selected for use in this experiment. We
screened each call by examining the spectrograms (1024 fft) as well as
listening to each exemplar to ensure that they were free of any artifacts
(e.g., cage noise, clipping, etc.).
Procedure. We placed a tamarin into the playback chamber and allowed it to acclimate for 1 min before we played back any recorded sounds.
After 1 min elapsed, we waited for the tamarin to face away from the
speaker before playing the first call of the habituation set. Habituation
stimuli were always randomly presented. If more than one cycle of the
habituation set was required during a session, we presented the second set
of stimuli in a different, randomized order than the first set.
For each of the experiments presented in this study, we played a series
of calls until the tamarin failed to respond on three consecutive trials. After
three no-response trials, we played the test call followed by a posttest if
necessary (see below). Responses were measured using the following
parameters: head turning toward speaker, body orienting toward speaker,
movement toward speaker, freezing response (if animal was moving and
then froze when the recorded call was played), and vocal responses
(producing vocalizations within 5 s of hearing the recorded call). A "no
response" was recorded in the absence of these responses. During sessions,
trials with ambiguous responses (as determined by the experimenters while
running a session) were treated functionally as "yes" responses. Ambiguous responses included trials in which the tamarin was facing the speaker
before any sound was played (because of either an errant press by the
experimenter or a slight latency between button press and sound) or when
experimenters were unable to determine the direction of the tamarin's gaze.
This conservative approach was adopted to minimize the number of trials
that needed to be rerun (and thereby minimize exposure to the test stimuli).
Intertrial interval was set at a minimum of 10 s and at a maximum of 30 s.
The session was aborted if we were unable to play back a call within this
30-s window. However, this did not occur during our experiments.
Trials started once the tamarin's face was visible and turned away from
the speaker. In addition, if the tamarin spontaneously produced a long call,
we waited at least 5 s before playing back a call.
When tamarins failed to respond to the test call, we played back a
posttest stimulus. The posttest stimulus, a tamarin scream, represented a
call that was both acoustically and functionally different from the habituation and test calls. Scream exemplars were recorded while the medical
staff caught the tamarins and administered tuberculosis shots and then
normalized for amplitude. The duration of the posttest screams was within
the range of the habituation stimuli. The purpose of the posttest was to
ensure that the tamarin had not habituated to the playback setup in general.
Failure to respond to the test stimulus could indicate that the tamarin had
either habituated to the playback setup in general or had perceptually
clustered the habituation and test stimuli into one category. If the tamarin
had habituated to the playback setup, then it should ignore the posttest
stimulus. In contrast, if failure to respond to the test call was due to the
tamarin's perception of similarity between the habituation series and the
test stimulus, then it should respond to the posttest stimulus. Sessions in
265
which the tamarins failed to respond to the posttest were rerun at a later
date.
Analyses. Because responses to playbacks can be difficult to score in
real time, we digitized (Adobe Premiere version 4.2; Adobe Systems Inc.,
San Jose, CA) the last 13 habituation trials (including the three no response
habituation trials), the test, and the posttest. This ensured that there would
be a distribution of both yes and no response trials, thereby reducing the
opportunity for biased scoring. These trials were assigned code file names
and then randomized to ensure that the scorers were naive to the condition.
Once scores were obtained, we consulted the master list to determine the
condition. Two scorers then analyzed each of the trials and recorded a yes,
no, or ambiguous response; the type of response (e.g., head turn, countercall, etc.) and the duration of response were recorded as well. Trials in
which it was not clear whether a tamarin had looked at the speaker were
deemed ambiguous. These responses were treated as yes responses if they
occurred in the habituation series. If a test trial was determined to be
ambiguous, then the trial was rerun. This occurred in less than 8% of all
sessions. Sessions were discarded if scorers assessed any of the three
habituation trials (the three trials preceding the test trial) as a yes response.
Likewise, sessions in which there was disagreement between scorers on
any of the three no response habituation trials, the test, or the posttest
stimuli were also discarded. Finally, sessions in which the tamarin did not
respond to both the test and the posttest were also discarded.
Condition 1: Individual recognition. In the first condition, we presented tamarins with a habituation set composed of eight different fivesyllable CLCs from male RW. The test stimulus was a five-syllable CLC
from female ES. RW and ES were from different groups. The posttest
stimulus was a scream from male SP matched in length and filtered in
accordance with the habituation and test stimuli. As a control for this
condition, we presented tamarins with the same habituation series from
RW and a novel five-syllable CLC from RW.
An additional test was conducted in which the habituation series and test
stimuli were produced by tamarins of the same sex. In this condition, the
habituation set consisted of eight different five-syllable CLCs from female
ES. The test stimulus was a five-syllable CLC from female JG. The posttest
stimulus consisted of a scream from either male SP or male ID.
Condition 2: Individual recognition of same sex cage mates. Because
the acoustic analyses revealed that cage mates sounded more similar to
each other in some dimensions than to noncage mates, it is possible that
tamarins tested in Condition 1 used those features that are salient for
distinguishing among cage groups rather than individuals. Therefore in
Condition 2 we also set out to test whether tamarins could discriminate
callers regardless of sex and cage group membership. Because of the
configuration of our colony, we had access to only a single group with two
tamarins of the same sex: the mother-daughter pair, ES and RB, respectively. If our colony of tamarins could discriminate between these callers,
then we could be fairly confident that they are able to recognize the
differences between any two tamarins on the basis of their calls. If the
tamarins failed to discriminate between these callers, however, then dishabituation in Condition 1 could be explained by the perceptual salience of
both sex and group membership. In other words, although tamarins may
fail to recognize individual tamarins on the basis of their five-syllable CLC,
they can recognize the sex of the caller or its group membership.
The habituation set for Condition 2 consisted of 8 five-syllable CLCs
produced by female ES. The test stimulus was a five-syllable CLC produced by female RB. The posttest stimulus was a scream from male ID. A
second habituation set was created in which RB exemplars were used for
habituation and an ES exemplar was used as the test stimulus. A number
of tamarins were inaccessible during the ES-RB condition, and thus, we
ran only 10 tamarins.
Condition 3: Discrimination of acoustically similar callers. One potential confound in Condition 2 was that the callers were more acoustically
similar than those used in Condition 1 (see Discussion). To begin exploring
this possibility, we designed a final series of playbacks to test whether
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
266
WEISS, GARIBALDI, AND HAUSER
tamarins would discriminate between two unrelated callers with acoustically similar CLCs. On the basis of the results from the MDA (reported
earlier), we chose CLCs from tamarins ID and RB as stimuli; the coordinates for ID and ES (the mother from the previous condition) were similar
in the three most important acoustical dimensions and differed from the
calls of RB along similar dimensions. Likewise, pairwise ANOVAs comparing the acoustics of CLCs from RB and ID revealed no significant
differences (Garibaldi, 1999).
The habituation set consisted of 8 five-syllable CLCs produced by
female RB. The test stimulus was a five-syllable CLC produced by male
ID. The posttest stimulus was a scream from ID. A second habituation set
was created in which five ID exemplars were used for habituation and an
RB exemplar was used as the test stimulus. The IDhab-RBtest condition was
run 12 months after the other conditions (see General Discussion) when the
colony expanded, allowing for 14 tamarins to be tested.
Results
Condition 1: Individual recognition. In the RWhab-EStes, condition, 12 out of 13 tamarins responded to the test call following
habituation (see Figure 4). Tamarins' responses for this condition
included 9 head turns, 1 approach, 5 long calls, and 2 chirps. Note
that four test trials had multiple responses (e.g., one trial contained
a head turn and a long call, etc.). The average number of calls
played back until habituation was 22.8 (SD = 15.60, range =
4-58). In the control condition involving RWhab-RWtest, 3 out
of 13 tamarins dishabituated to the novel RW call (see Figure 4).
All three tamarins responded with head turns. The average number
of calls played back until habituation was 19.8 (SD = 12.20,
range = 5-49). There was a statistically significant difference in
the number of tamarins responding to the test trial for these two
conditions (paired sign test, p < .02). There was, however, no
difference between conditions in the number of trials to habituation, paired t test, r(12) = 0.77, p < .46.
For the EShab-JGtest condition, 11 out of 13 tamarins responded
to the test call following habituation (see Figure 4). The responses
for this condition included 7 head turns, 2 approaches, 5 long calls,
and 1 trilled vocalization (consisting of multiple chirps). The
average number of calls played back until habituation was 25.18
RW-ES
RW-RW
ES-JG
ES-ES
• Response
Q No Response
Figure 4. Results from both the initial change of identity condition,
RWhab-ESt<:st including the control RWhab-RWtest, and from the same-sex
change of identity condition, ES^-JG,^, including the control EShab-
(SD = 27.59, range = 5-99). In the control condition involving
EShab-ES,,.st, 2 out 13 tamarins dishabituated to the novel ES call
(see Figure 4). One tamarin responded with a trilled vocalization
and the other responded with an antiphonal call. The average
number of trials until habituation was 12.84 (SD = 7.02, range =
4-27). There was a statistically significant difference in the number of individual tamarins responding to the test trial for these two
conditions (paired sign test, p < .004). There was no significant
difference between conditions in the number of trials until habituation, paired t test, f(12) = 1.69, p < .12.
Condition 2: Individual recognition of same-sex cage mates.
In the EShab-RBtest condition, 5 out of 10 tamarins dishabituated to
the RB test call. The observed responses included 4 head turns, 1
trilled response (chirps), and 1 antiphonal call. The average number of calls played back until habituation was 26.3 (SD = 20.60,
range = 5-57). The proportion of those responding was not
significant when compared with baseline results from EShab-ES,est
(paired sign test, p < .38).
In the RBhab-ESt(,st condition, 8 out of 13 tamarins dishabituated
to the ES test call (see Figure 5). The observed responses included 4 head turns, 2 approaches, and 4 antiphonal long calls (see
Figure 6). The average number of calls played back until habituation was 28.7 (SD = 21.00, range = 5-66). The proportion of
those responding was not significant when compared with the
baseline results (paired sign test, p < .13). There was no difference
in the number of trials until habituation in the EShab-RBtest and in
the RBhab-ESMS, conditions, paired t test, t(9) = 0.16, p < .88.
Condition 3: Discrimination of acoustically similar callers. In
the RBhab-IDKst condition, 9 out of 13 tamarins dishabituated to
the ID test call (see Figure 7). The responses included 4 head
turns, 2 approaches, 1 chirp, and 2 antiphonal long calls. The
average number of calls played back until habituation was 18.6
(SD = 14.30, range = 5-58). The proportion of those responding
was significant when compared with baseline results (paired sign
test, p < .04).
In the IDhab-RBtest condition, 11 out of 14 tamarins dishabituated to the RB test call. The responses included 5 head turns and 10
antiphonal calls. The average number of calls played back until
habituation was 17.5 (SD = 15.30, range = 5-50). The proportion
of those responding was significant when compared with the
baseline results (paired sign test, p < .02). There was no difference
in the number of trials until habituation in the RBhab-IDtest and in
the IDhab-RBtcst conditions, paired t test, f(12) = 0.66, p < .53.
Playbacks of own calls. Because of the design of our experiments, a number of tamarins heard their own calls played back
either during the habituation series or as the test call. This presented an interesting situation because the tamarins had never
heard their own calls broadcast from an external source. One
possible response is that tamarins perceived these calls as coming
from an unfamiliar caller. A second possibility is that tamarins
perceive such calls as familiar but not as their own call (e.g., from
a cage mate). Finally, tamarins may recognize the call as their own
and respond differently from how they respond to unfamiliar and
familiar callers.
Research conducted with birds has shown that when an individual bird's own song is played back, it responds with an intermediate response between that of a familiar neighbor and that of a
stranger (e.g., Brooks & Falls, 1975; Searcy, McArthur, Peters,
& Marler, 1981; Yasukawa, Bick, Wagman, & Mailer, 1982;
267
VOCAL PRODUCTION AND PERCEPTION BY TAMARINS
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
General Discussion
Figure 5. Results from the related female tamarins' change of identity
condition, RBhab-ESMst as well as the reverse EShab-RB,cst.
McArthur, 1986). Snowdon et al. (1983) studied quiet and normal
long calls in cotton-top tamarins and reported that tamarins responded to their own calls in the same way that they responded to
a cage mate's calls.
We did not run experiments involving unknown tamarins. Consequently, we cannot contrast the tamarin's response to its own call
as opposed to calls produced by unfamiliar tamarins. We can,
however, explore differences in response to self-call trials and
other call categories.
Summary. Across all conditions, tamarins that heard their own
calls during the habituation series took an average of 11.9 trials
(SD = 7.04) to habituate. This is not significantly different from
the number of trials those same tamarins required to habituate to
other call sets (M = 9.9, SD = 5.30), paired t test, f(5) = 0.52, p <
.62.
For conditions involving a change in caller identity, tamarins
whose calls were played as the habituation series responded to the
test call in three out of six trials. This is not significantly different
from how the rest of the sample performed on change of identity
conditions, unpaired t test, f(57) = 0.976, p < .34. For tamarins
whose calls were played as the test call, 5 out of 6 tamarins
responded. This is not significantly different from how the rest of
the sample performed on change of identity conditions, unpaired t
test, ?(51) = 0.66, p < .52.
In control conditions in which tamarin caller identity remained
constant (i.e., RWhab-RWtest, ES^-ES^, both tamarins transferred habituation to the novel exemplar from their own repertoire.
Results from Condition 1 provide support for the hypothesis that
cotton-top tamarins can discriminate between individual tamarins
on the basis of their five-syllable CLC. Of the 26 trials involving
a change in caller identity, tamarins responded 23 times. In addition, the results from the control conditions indicate that the
methodology is well suited for identifying which aspects of the
CLC may be meaningful to the perceiver. Of the 26 control trials
involving novel calls from the same caller, only 5 tamarins dishabituated. This finding is critical in that it indicates that the tamarins
were not simply responding to a novel acoustic change in the test
condition. Rather, tamarins responded to changes that were meaningful—in this case, a change in caller identity. These results also
show that the habituation-dishabituation procedure can be successfully used with captive nonhuman primates to test for perceptual classification of species-specific calls. Additional evidence for
the effectiveness of this procedure comes from studies testing
speech perception with cotton-top tamarins (Ramus et al., 2000).
The results from this first condition suggest that antiphonal
calling may be another assay that indicates whether tamarins find
the change in caller identity meaningful. This assay has been used
before in studies with pygmy marmosets (Snowdon & Cleveland,
1980) and cotton-top tamarins (Snowdon et al., 1983). Overall,
in 11 out of 26 trials, tamarins called back to the test call when
identity changed, whereas only 1 out of 26 control trials yielded a
similar response (see Figure 6 for a diagram of antiphonal calling
responses by condition). It should be noted that in tests of speech
perception, tamarins never respond with antiphonal calling (Ramus
et al., 2000), suggesting that this behavior may be restricted to
conspecific vocalizations. The implications of the antiphonal calling data are discussed below.
Results from Condition 2 suggest that tamarins fail to discriminate between two same-sex, related tamarins from the same
group. The results of this condition underscore the importance of
considering aspects of both production and perception in the study
of communication. On the basis of the acoustic analyses alone, one
might have predicted that these 2 tamarins could be discriminated.
Both ES and RB have discrete points on the plot of individual
centroids on the canonical functions generated by the MDA (see
Figure 2). By performing perceptual experiments in conjunction
with these analyses, we obtained a more complete understanding
of how tamarins recognize individual tamarins on the basis of
acoustics alone.
12
•s
6
I. I
RW-ES
RW-RW
ES-JG
ES-ES
RB-ES
I
ES-RB
Figure 6. Antiphonal calling data across all conditions.
ID-RB
RB-ID
268
WEISS, GARIBALDI, AND HAUSER
12
RB-ID
ID-RB
H Response
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
171 No Response
Figure 7. Results from the acoustically similar tamarin callers' change of
identity condition, RBhab-IDttst as well as the reverse
This conclusion, however, is limited to our methodological
assay. In contrast to a psychophysical task that asks whether Signal
A is discriminable from Signal B, the habituation-dishabituation
procedure asks whether Signal A is meaningfully different from
Signal B (see Nelson & Marler, 1990). Thus, although the tamarins
apparently did not perceive a meaningful difference between the
CLCs of ES and RB, a psychophysical task may well show that
their calls are discriminable.
An open question is whether tamarins can discriminate individual tamarins of the same sex and the same group. Recall that the
relationship between the 2 tamarins whose calls were played in
Condition 2 was that of parent-offspring. It may be that unrelated
tamarins within a group can be discriminated. Although our laboratory is not currently set up to allow for us to answer this
question, tamarin groups in the wild often contain unrelated tamarins of the same sex (Neyman, 1977). In addition, it would also be
interesting to test whether members of the same group have an
advantage in discriminating related tamarins from their own group.
One limitation to Condition 2 was that when the motherdaughter pair were plotted using MDA, the centroids were closer
than those of the other tamarins used in Condition 1 (see Figure 2).
In addition, pairwise ANOVAs revealed that there was only one
parameter that significantly differed between these 2 tamarins (the
starting frequency for some of the syllables in their calls). In
contrast, the tamarins from the first condition differed along more
dimensions. In particular, the CLCs of RW and ES differed in call
duration, in duration of the individual syllables, and in duration to
the peak frequency of the call. The CLCs of ES and JG differed in
the duration of the syllables and the intersyllable interval
(Garibaldi, 1999). Overall, this suggests that the calls produced by
these 2 tamarins have greater overlap in call morphology than the
exemplars used for previous test conditions. Therefore, there are
multiple interpretations for the playback results. Condition 3 examined whether results from the first two conditions could be
explained solely on the basis of acoustic similarity and, thus,
degree of discriminability. Specifically, if ES and RB could not be
discriminated because of acoustic similarity, then ID and ES
should also prove difficult to discriminate.
Results from Condition 3 indicate that tamarins can discriminate
the CLCs of two unrelated tamarins even though the degree of
acoustic similarity is high. The findings from this condition again
underscore the importance of considering both production and
perception when studying communication. On the basis of the
relative acoustic proximity of ID and ES (used in Condition 2), one
could not have predicted the results from these experiments—
specifically, that RB and ES were difficult to discriminate between
whereas ID and RB were not. Although studies of production help
establish the kinds of information encoded in the signal (e.g.,
individual identity, sexual identity, etc.), it is only through perceptual experiments that we can identify which acoustic features are
actually meaningful to the tamarins.
It should be noted that our acoustic analyses created only one of
many possible renditions of the acoustic space for tamarin CLCs.
Even the results from pairwise ANOVAs may be limited by
sample size. It is possible that there is one parameter, or even a
constellation of parameters, that distinguishes the ID calls from the
ES calls and that underlies the perceptual playback results. One
approach to solving this issue is to run playback experiments with
calls that have individual parameters manipulated. For example,
since ID and RB are of opposite sex, whereas ES and RB are of the
same sex, we could manipulate temporal parameters of the call
because these have been shown to be important in our acoustic
analyses of sexual identity. This kind of manipulation would
determine which parameters meaningfully contribute to individual
tamarin recognition and, in turn, would help explain why the
related females were more difficult to discriminate between than
ID and RB were. Thus, part of our overall research program
focuses on manipulating individual features and determining
which parameters are meaningful in the perception of the CLC.
The antiphonal calling data from this condition were somewhat
surprising. In the RBhab-IDtest condition, only 2 out of 9 responding tamarins produced antiphonal calls. It is unclear why this test
exemplar elicited few antiphonal responses and still was detected
by most tamarins as a change in speaker identity (see Discussion).
In contrast, 10 out of 11 responding tamarins called antiphonally to
the test stimulus in the IDhab-RBtest condition. This represents a
higher level of response than in other conditions (see Figure 6).
One factor that may have contributed to this effect is that this
condition was run 12 months after the initial individual tamarin
recognition conditions. It is possible that because the test call had
been recorded 12 months earlier, it sounded less familiar. Previous
research has shown that the phee call in marmosets changes over
a 12-month period (Jorgensen & French, 1998), and it is unknown
whether this occurs in tamarin contact calls as well.
One possibility not addressed in our study is that tamarins
cannot distinguish between the calls of their cage mates, regardless
of sex. However, this does not seem likely because Condition 3
showed that the tamarins are able to discriminate between acoustically similar callers of the opposite sex. It is likely that they
would respond to the acoustic differences known to exist between
the sexes. Future studies may address this issue further.
One finding from the analysis of self-call perception is that
tamarins are likely to dishabituate when their own calls are used as
the test stimulus in conditions involving change of identity. However, because most of our tamarins responded to changes in
speaker identity, further research is necessary to determine
whether tamarins are particularly sensitive to the acoustics of their
own call when it is played as a test.
For tamarins that heard their own calls in the habituation series,
half did not respond to the change of identity. However, because of
the small sample, this finding is not statistically significant. In
269
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
VOCAL PRODUCTION AND PERCEPTION BY TAMARINS
addition, the number of exemplars prior to habituation did not
change for tamarins that habituated to a series of their own calls.
This result supports Snowdon et al.'s (1983) position that self-calls
may be perceived as comparable with calls produced by known
tamarins. Of further relevance, results from experiments designed
to elicit antiphonal calling have found that there is no significant
difference between the tamarins' rate of antiphonal calling to their
own calls and the tamarins' rate of antiphonal calling to those of
other tamarins (Ghazanfar, Flombaum, Miller, & Hauser, 2001); in
these experiments as well, however, tamarins have not been tested
in a condition involving their own calls versus foreign tamarins'
calls.
As mentioned earlier, results from studies on bird songs have
found that birds respond to self-song with an intermediate response
between that of a familiar neighbor and that of a stranger (e.g.,
Brooks & Falls, 1975; McArthur, 1986; Searcy et al., 1981;
Yasukawa et al., 1982). One interpretation of these results is that
self-song production provides a template to which other songs are
compared as a criterion for species recognition (see McArthur,
1986; Searcy et al., 1981). Our data suggest that there is no
distinction between hearing one's own calls and hearing a familiar
individual's calls. Additional research is necessary to determine
whether an individual primate's own calls play a special role in
primates' vocal perception.
When hearing a long call, conspecifics often respond with their
own antiphonal long calls (Cleveland & Snowdon, 1982). Thus,
antiphonal calling may provide the most natural assay for gauging
responses. In our experiments, the first and third test conditions
had more antiphonal calling than the second condition (in which
discrimination was difficult; see Figure 6) or the control conditions. However, there were still some anomalous findings (see
Condition 3) with respect to the number of antiphonal calls elicited
by the different test stimuli. Further research is necessary to
determine which components of the call are critical to eliciting
these responses. For example, research on gorilla double grunts
has found that there are specific acoustic cues that tend to elicit
antiphonal calling (Seyfarth, Cheney, Harcourt, & Stewart, 1994).
Studies by Ghazanfar et al. (2001) suggest that tamarins are more
likely to produce antiphonal calls in response to complete CLCs
when contrasted with playbacks of chirps alone, whistles alone, or
white-noise bursts that mimic the temporal patterning of the CLC
without the species-typical amplitude envelope.
One goal of these experiments was to determine whether the
habituation-dishabituation paradigm could be effectively implemented in captivity to address issues pertaining to meaningful
differences in vocalizations. The results from these experiments
suggest that this paradigm is effective. In fact, it should be noted
that the IDhab-RBtest condition was run more than 12 months after
the first condition of this study. The responses in this condition
(which included a high proportion of antiphonal calling) suggest
that the effect is robust and that the paradigm is consistent across
time.
The overall goals for the analyses and experiments reported in
this study were met. Future research may determine which features
of the CLC are considered meaningful by perceivers. This can be
accomplished by habituating tamarins to a series of CLCs and then
presenting a test call in which one acoustic parameter has been
manipulated. The acoustic analyses reported in this study can be
used to guide the creation of these test calls.
References
Adobe premiere [computer software]. (1998). San Jose, CA: Adobe Systems Inc.
Altmann, S. A. (1967). The structure of primate social communication. In
S. A. Altmann (Ed.), Social communication among primates (pp. 325362). Chicago: University of Chicago Press.
Beecher, M. D. (1982). Signature systems and kin recognition. American
Zoologist, 22, 477-490.
Benz, J. J., French, J. A., & Leger, D. W. (1990). Sex differences in vocal
structure in a callitrichid primate (Leontopithecus rosalia). American
Journal of Primatology, 21, 257-264.
Boughman, J. W. (1997). Greater spear-nosed bats give group-distinctive
calls. Behavioral Ecology and Sociobiology, 40, 61—70.
Bretagnolle, V., & Lequette, B. (1990). Structural variation in the call of
the Cory's shearwater (Calonectris diomedea, aves, Procellariidae).
Ethology, 85, 313-323.
Brooks, R. J., & Falls, J. B. (1975). Individual recognition in whitethroated sparrows: I. Discrimination of songs of neighbors and strangers.
Canadian Journal of Zoology, 53, 879-888.
Brown, S. D., Dooling, R. J., & O'Grady, K. E. (1988). Perceptual
organization of acoustic stimuli by budgerigars (Melopsittacus undulatus): in. Contact calls. Journal of Comparative Psychology, 102, 236247.
Burmeister, S., Wilczynski, W., & Ryan, M. J. (1999). Temporal call
changes and prior experience affect graded signalling in the cricket frog.
Animal Behaviour, 57, 611-618.
Butynski, T. M., Chapman, C. A., & Chapman, L. J. (1992). Use of male
blue monkey "pyow" calls for long-term individual identification. American Journal of Primatology, 28, 279-284.
Canary (Version 1.2) [computer software]. (1995). Ithaca, NY: Cornell
Bioacoustics Workstation.
Chaiken, M. (1992). Individual recognition of nestling distress screams by
European starlings (Stumus vulgaris). Behaviour, 120, 139-150.
Chapman, C. A., & Weary, D. M. (1990). Variability in spider monkeys'
vocalizations may provide basis for individual recognition. American
Journal of Primatology, 22, 279-284.
Cheney, D. L., & Seyfarth, R. M. (1980). Vocal recognition in free-ranging
vervet monkeys. Animal Behaviour, 28, 362-367.
Cheney, D. L., & Seyfarth, R. M. (1982). How vervet monkeys perceive
their grunts: Field playback experiments. Animal Behaviour, 30, 739751.
Cheney, D. L., & Seyfarth, R. M. (1988). Assessment of meaning and the
detection of unreliable signals by vervet monkeys. Animal Behaviour, 36, 477-486.
Cheney, D. L., & Seyfarth, R. M. (1990). How monkeys see the world:
Inside the mind of another species. Chicago: University of Chicago
Press.
Cheney, D. L., & Seyfarth, R. M. (1996). The function and mechanisms
underlying baboon contact barks. Animal Behaviour, 52, 507-518.
Cleveland, J., & Snowdon, C. T. (1982). The complex vocal repertoire of
the adult cotton-top tamarin, Saguinus oedipus oedipus. Zeitschrift fur
Tierpsychologie, 58, 231-270.
Conner, D. A. (1985). The function of the pika short call in individual
recognition. Zeitschrift fur Tierpsychologie, 67, 131-143.
Davis, M. S. (1987). Acoustically mediated neighbor recognition hi the
North American bullfrog, Rana catesbeiana. Behavioral Ecology and
Sociobiology, 21, 185-190.
Elowson, A. M., & Snowdon, C. T. (1994). Pygmy marmosets, Cebuella
pygmaea, modify vocal structure in response to changed social environment. Animal Behaviour, 47, 1267-1277.
Emlen, S. T. (1972). An experimental analysis of the parameters of bud
song eliciting species recognition. Behaviour, 41, 130-171.
Fischer, J. (1998). Barbary macaques categorize shrill barks into two call
types. Animal Behaviour, 55, 799-807.
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
270
WEISS, GARIBALDI, AND HAUSER
Garibaldi, B. T. (1999). Lang calling in cotton-top tamarins. Unpublished
bachelor's thesis, Harvard University.
Ghazanfar, A. A., Flombaum, J. I., Miller, C. T., & Hauser, M. D. (2001).
The units of perception in the antiphonal calling behavior of cotton-top
tamarins (Saguinus oedipus): Playback experiments with long calls.
Journal of Comparative Physiology A., 187, 27-35.
Hammerschmidt, K., & Fischer, J. (1998). Maternal discrimination of
offspring vocalizations in barbary macaques (Macaco sylvanus). Primates, 39, 231-236.
Hansen, E. W. (1976). Selective responding by recently separated juvenile
rhesus monkeys to the calls of their mother. Developmental Psychobiology, 9, 83-88.
Hauser, M. D. (1998a). Functional referents and acoustic similarity: Field
playback experiments with rhesus monkeys. Animal Behaviour, 55,
1647-1658.
Hauser, M. D. (1998b). Orienting asymmetries in rhesus monkeys: The
effect of time-domain changes on acoustic perception. Animal Behaviour, 56, 41-47.
Heymann, E. W. (1987). Behavior and communication of moustached
tamarins, Saguinus mystax mystax (Primates: Calitrichidae), in an outdoor enclosure: I. The physical structure of long calls of the moustached
tamarin. Primate Report, 17, 45-52.
Hile, A. G., Plummer, T. K., & Striedter, G. F. (2000). Male vocal
imitation produces call convergence during pair bonding in budgerigars,
Melopsittacus undulatus. Animal Behaviour, 59, 1209-1218.
HyperCard Player (Version 2.3.5) [Computer software]. (1996). Cupertino,
CA: Apple Computer, Inc.
Janik, V. M., & Slater, P. J. B. (1997). Vocal learning in mammals.
Advances in the Study of Behavior, 26, 59—99.
Jones, B. S., Harris, D. H., & Catchpole, C. K. (1993). The stability of the
vocal signature in phee calls of the common marmoset, Callithrix
jacchus. American Journal of Primatology, 31, 67-75.
Jorgensen, D. D., & French, J. A. (1998). Individuality but not stability in
marmoset long calls. Ethology, 104, 729-742.
Kajikawa, S., & Hasegawa, T. (1996). How chimpanzees exchange information by pant-hoots: A playback experiment. The Emergence of Human Cognition and Language, 3, 123—128.
Macedonia, J. M. (1986). Individuality in the contact call of the ring-tailed
lemur (Lemur catta). American Journal of Primatology, 11, 163-179.
Marler, P., Dufty, A., & Pickert, R. (1986). Vocal communication in the
domestic chicken: II. Is a sender sensitive to the presence and nature of
a receiver? Animal Behaviour, 34, 194-198.
Marler, P., & Hobbett, L. (1975). Individuality in a long-range vocalization
of wild chimpanzees. Zeitschrift fur Tierpsychologie, 38, 97-109.
Marshall, A. J., Wrangham, R. W., & Arcadi, A. C. (1999). Does learning
affect the structure of vocalizations in chimpanzees? Animal Behaviour, 58, 825-830.
Marten, K., Quine, D. B., & Marler, P. (1977). Sound transmission and its
significance for animal vocalization: n. Tropical habitats. Behavioral
Ecology and Sociobiology, 2, 291-302.
Masataka, N. (1988). The response of red-chested moustached tamarins to
long calls from their natal and alien populations. Animal Behaviour, 36,
55-61.
May, B. J., Moody, D. B., & Stebbins, W. C. (1988). The significant
features of Japanese monkey coo sounds: A psychophysical study.
Animal Behaviour, 36, 1432-1444.
May, B. J., Moody, D. B., & Stebbins, W. C. (1989). Categorical perception of conspecific communication sounds by Japanese macaques, Macacafuscata. Journal of the Acoustical Society of America, 85, 837-847.
McArthur, P. (1986). Similarity of playback songs to self song as a
determinant of response strength in song sparrows (Melospiz/a melodia).
Animal Behaviour, 34, 199-207.
Mitfer, C. T., Hauser, M. D., Miller, J., & Gilda Costa, R. (2001). Patterns
of selective phonotaxis in cotton-top tamarins. Manuscript in preparation.
Mitani, J. C. (1985). Responses of gibbons (Hylobates muelleri) to self,
neighbor, and stranger duets. International Journal of Primatology, 6,
193-200.
Mitani, J. C., & Brandt, K. L. (1994). Social factors influence the acoustic
variability in the long-distance calls of male chimpanzees. Ethology, 96,
233-252.
Mitani, J. C., Gros-Louis, J., & Macendonia, J. M. (1997). Selection for
acoustic individuality within the vocal repertoire of wild chimpanzees.
International Journal of Primatology, 17, 569-583.
Mitani, J. C., & Nishida, T. (1993). Contexts and social correlates of
long-distance calling by male chimpanzees. Animal Behaviour, 45, 735746.
Morton, E. S. (1986). Predictions from the ranging hypothesis for the
evolution of long-distance signals in birds. Behaviour, 83, 66-86.
Moynihan, M. (1970). The control, suppression, decay, disappearance, and
replacement of displays. Journal of Theoretical Biology, 29, 85-112.
Nelson, D. A., & Marler, P. (1990). The perception of birdsong and an
ecological concept of signal space. In W. C. Stebbins & M. A. Berkley
(Eds.), Comparative perception: Vol. II. Complex signals (pp. 443-478).
New York: Wiley.
Neyman, P. F. (1977). Aspects of the ecology and social organization of
free-ranging cotton-top tamarins (Saguinus oedipus) and the conservation status of the species. In D. G. KJeiman (Ed.), The biology and
conservation of the Callitrichidae (pp. 39-71). Washington, DC: Smithsonian Institution Press.
Norcross, J. L., & Newman, J. D. (1993). Context and gender-specific
differences in the acoustic structure of common marmoset (Callithrix
jacchus) phee calls. American Journal of Primatology, 30, 37-54.
Owren, M. J., & Bernacki, R. (1988). The acoustic features of vervet
monkey (Cercopithecus aethiops) alarm calls. Journal of the Acoustical
Society of America, 83, 1927-1935.
Ramus, F., Hauser, M. D., Miller, C. T., Morris, D., & Mehler, J. (2000,
April 14). Language discrimination by human newboms and cotton-top
tamarin monkeys. Science, 288, 349-351.
Rendall, D., Rodman, P. S., & Edmond, R. E. (1996). Vocal recognition of
individuals and kin in free-ranging rhesus monkeys. Animal Behaviour, 51, 1007-1015.
Romer, H., & Bailey, W. J. (1986). Insect hearing in the field: H. Male
spacing behaviour and correlated acoustic cues in the bushcricket Mygalopsis marki. Journal of Comparative Physiology, 159, 627-638.
Ryan, M. J., & Sullivan, B. K. (1989). Transmission effects on temporal
structure in the advertisement calls of two toads, Bufo woodhousii and
Bufo valliceps. Ethology, 80, 182-189.
Sayigh, L. S., Tyack, P. L., Wells, R. S., Solow, A. R., Scott, M. D., &
Irvine, A. B. (1999). Individual recognition in wild bottlenose dolphins:
A field test using playback experiments. Animal Behaviour, 57, 41-50.
Searcy, W. A., McArthur, P., Peters, S. S., & Marler, P. (1981). Response
of male song and swamp sparrows to neighbour, stranger, and self songs.
Behaviour, 77, 152-163.
Seyfarth, R. M., & Cheney, D. L. (1984). The acoustic features of vervet
monkey grunts. Journal of the Acoustical Society of America, 75, 129134.
Seyfarth, R. M., & Cheney, D. L. (1990). The assessment by vervet
monkeys of their own and another species' alarm calls. Animal Behaviour, 40, 754-764.
Seyfarth, R. M., Cheney, D. L., Harcourt, A. H., & Stewart, K. J. (1994).
The acoustic features of gorilla double grunts and their relation to
behavior. American Journal of Primatology, 33, 31—50.
Seyfarth, R. M., Cheney, D. L., & Marler, P. (1980). Vervet monkey alarm
calls: Semantic communication in a free-ranging primate. Animal Behaviour, 28, 1070-1094.
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
VOCAL PRODUCTION AND PERCEPTION BY TAMARINS
Snowdon, C. T., & Cleveland, J. (1980). Individual recognition of contact
calls by pygmy marmosets. Animal Behaviour, 28, 717-727.
Snowdon, C. T., Cleveland, J., & French, J. A. (1983). Responses to
context- and individual-specific cues in cotton-top tamarin long calls.
Animal Behaviour, 31, 91-101.
Snowdon, C. T., & Elowson, M. A. (1999). Pygmy marmosets modify call
structure when paired. Ethology, 105, 893-908.
Sound Designer II [Computer software]. (1996). Palo Alto, CA: Digidesign.
Stoddard, P. K. (1996). Vocal recognition of neighbors by territorial
passerines. In D. E. Kroodsma & E. H. Miller (Eds.), Ecology and
evolution of acoustic communication in birds (pp. 356-374). Ithaca,
NY: Cornell University Press.
Symmes, D., Newman, J. D., Talmage-Riggs, G., & Lieblich, A. K. (1979).
Individuality and stability of isolation peepes in squirrel monkeys.
Animal Behaviour, 27, 1142-1152.
Thurwachter, W. (1980). Einzel- und gruppenverhalten des Krallenaffchens Saguinus oedipus oedipus (Wollkopftamarin). Gefangenschaft
unter besonderer Berucksichtigung der LautauBerung "Long Call." Zulassungsarbeit: Univ. Freiburg i. Br.
Wilczynski, W., Rand, A. S., & Ryan, M. J. (1999). Female preferences for
temporal order of call components in the tungara frong: A Bayesian
analysis. Animal Behaviour, 58, 841-851.
Wiley, R. H., & Richards, D. G. (1978). Physical constraints on acoustic
communication in the atmosphere: Implications for the evolution of
animal vocalizations. Behavioral Ecology and Sociobiology, 3, 69-94.
Yasukawa, K., Bick, E. I., Wagman, D. W., & Marler, P. (1982). Playback
and speaker-replacement experiments on song-based neighbor, stranger,
and self-discrimination in male red-winged blackbirds. Behavioral Ecology and Sociobiology, 10, 211-215.
Yntema, D. (1997). Psychology 1952 course materials. Unpublished course
notes, Harvard University.
Yoneda, M. (1981). Ecological studies of Saguinus fuscicollis and Saguinus labiatus with reference to habitat segregation and height preference.
Kyoto University Overseas Research Report New World Monkeys, 2,
43-50.
Zuberbuehler, K., Cheney, D. L., & Seyfarth, R. M. (1999). Conceptual
semantics in a nonhuman primate. Journal of Comparative Psychology,
113, 33-42.
Received July 21, 2000
Revision received February 22, 2001
Accepted February 24, 2001
Members of Underrepresented Groups:
Reviewers for Journal Manuscripts Wanted
If you are interested in reviewing manuscripts for APA journals, the APA Publications
and Communications Board would like to invite your participation. Manuscript reviewers are vital to the publications process. As a reviewer, you would gain valuable
experience in publishing. The P&C Board is particularly interested in encouraging
members of underrepresented groups to participate more in this process.
If you are interested in reviewing manuscripts, please write to Demarie Jackson at the
address below. Please note the following important points:
•
•
•
•
271
To be selected as a reviewer, you must have published articles in peer-reviewed
journals. The experience of publishing provides a reviewer with the basis for
preparing a thorough, objective review.
To be selected, it is critical to be a regular reader of the five to six empirical journals that are most central to the area or journal for which you would like to review.
Current knowledge of recently published research provides a reviewer with the
knowledge base to evaluate a new submission within the context of existing research.
To select the appropriate reviewers for each manuscript, the editor needs detailed
information. Please include with your letter your vita. In your letter, please identify which APA journal(s) you are interested in, and describe your area of expertise. Be as specific as possible. For example, "social psychology" is not sufficient—you would need to specify "social cognition" or "attitude change" as well.
Reviewing a manuscript takes time (1-4 hours per manuscript reviewed). If you
are selected to review a manuscript, be prepared to invest the necessary time to
evaluate the manuscript thoroughly.
Write to Demarie Jackson, Journals Office, American Psychological Association, 750
First Street, NE, Washington, DC 20002-4242.