The Production and Perception of Long Calls by Cotton-Top ... · 0735-7036/01/$5.00 DOI: 10.1037//0735-7036.115.3.258 The Production and Perception of Long Calls by Cotton-Top Tamarins

Journal of Comparative Psychology2001, 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

Daniel J. Weiss, Brian T. Garibaldi, and Marc D. MauserHarvard University

The authors' goal was to provide a better understanding of the relationship between vocal production andperception in nonhuman primate communication. To this end, the authors examined the cotton-toptamarin's (Saguinus oedipus) combination long call (CLC). In Part 1 of this study, the authors carried outa series of acoustic analyses designed to determine the kind of information potentially encoded in thetamarin's CLC. Using factorial analyses of variance and multiple discriminant analyses, the authorsexplored 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 ofa suite of spectrotemporal features. In Part 2 of this study, the authors used a series of habituation-dishabituation playback experiments to test whether tamarins attend to the encoded information aboutindividual identity. The authors 1st tested for individual discrimination when tamarins were habituatedto a series of calls from 1 tamarin and then played back a test call from a novel tamarin; both opposite-and same-sex pairings were tested. Results showed that tamarins dishabituated when caller identitychanged but transferred habituation when caller identity was held constant and a new exemplar wasplayed (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 signa-tures; whereas all colony members have distinctive vocal signatures, we found that not all tamarins wereequally discriminable based on the habituation—dishabituation paradigm.

Many species that dwell in dense environments develop a sys-tem 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 greatervocal communication between individual animals (Altmann, 1967;Cheney & Seyfarth, 1996; Morton, 1986; Norcross & Newman,1993; Romer & Bailey, 1986). Call morphology may becomeincreasingly differentiated in such habitats so that subtle variationsdenote different contexts (Snowdon, Cleveland, & French, 1983).The acoustic variation within these calls may convey informationabout territorial status, group spacing, group location, or individualidentity (e.g., Beecher, 1982; Chapman & Weary, 1990; Cleveland& Snowdon, 1982; Mitani, 1985). Therefore, to gain a betterunderstanding of the design of communication signals, researchersmust identify the sources of variation and attempt to discern thetypes of information conveyed. To that effect, this study focuseson the long call produced by cotton-top tamarins (Saguinus oedi-

Daniel J. Weiss, Brian T. Garibaldi, and Marc D. Mauser, Department ofPsychology, Harvard University.

This work was supported by Harvard University's Mind Brain andBehavior Grant 368422. We thank Douwe Yntema, Kristen Vickers, andEric Loken for their advice on analyzing the data; Kerry Jordan for her helpin running the experiments and scoring trials; Fritz Tsao and Joe Swinglefor their help in analyzing data; and Asif Ghazanfar for his comments onan 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, MelioraHall, Office 494, University of Rochester, Rochester, New York 14627.Electronic mail may be sent to [email protected].

pus), a species that inhabits dense tropical rainforest and has ahighly diversified vocal repertoire.

Cleveland and Snowdon (1982) identified three classes of longcalls produced by captive cotton-top tamarins. On the basis of theiranalyses, the long calls we examined in the present study may beclassified as "combination long calls" (CLCs), vocalizations con-sisting of two syllable types: chirps and whistles. Cleveland andSnowdon noted that the CLC has the greatest variability acrosstamarins, perhaps due to individual tamarin differences. CLCsappear to occur in a variety of circumstances involving socialexcitement, disturbance, pairing with a new mate, play, and socialisolation (Cleveland & Snowdon, 1982). The most common con-text appears to be social isolation (Cleveland & Snowdon, 1982;Thurwachter, 1980). Given the variability in acoustic parametersnoted (e.g., overall number of syllables and call duration) betweencallers and the context in which the calls occur, the CLC providesan excellent opportunity for investigating the relative contributionof individual, sex, and group identity to call morphology. In fact,the closely related phee call in marmosets, which seems to occurin similar contexts, encodes information about both the sex and theidentity of the caller (Jorgensen & French, 1998; Norcross &Newman, 1993).

Our research program represents an attempt to explore themeaningful components of a communication system among tama-rins by designing playback experiments that are informed bydetailed acoustic analyses. This integration of information fromstudies of production and perception has been successfully carriedout 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,

258

VOCAL PRODUCTION AND PERCEPTION BY TAMARINS 259

& Stebbins, 1988; Snowdon & Cleveland, 1980; Snowdon et al.,1983). First, we report the findings from an acoustic analysis of theCLC designed to assess the types of information encoded in thiscall. Next, we report the results from a series of playback exper-iments designed to test whether tamarins can be discriminated byvoice alone, and more specifically, by the acoustic morphology oftheir CLCs.

The goal of the acoustic analyses was to determine whether themorphology of the tamarin's CLCs carries information about in-dividual identity, sex, and group membership. Given previouswork with other closely related species, we anticipated findingevidence 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 liontamarins: Benz, French, & Leger, 1990). Evidence of group-levelacoustic signatures has been weaker, coming primarily from chim-panzees (Mitani & Brandt, 1994) and the more closely relatedpygmy marmosets (Elowson & Snowdon, 1994). Such within-group acoustic convergence has been taken as evidence of vocallearning. To date, there is no evidence showing that convergencein call morphology occurs when multiple groups are housed inclose proximity, a situation that arose in our captive colony.

The playback experiments were designed to complement theacoustic analysis of individual variation within CLCs. For a tamarin tobe 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 betweensignals on the basis of the parameters that define the signature(Beecher, 1982). On the basis of these conditions, individual recog-nition 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 (Bretag-nolle & Lequette, 1990), and European starlings (Chaiken, 1992).Because prior work (e.g., Snowdon et al., 1983) and the acousticanalyses presented in Part 1 suggest that individual identity is encodedin the tamarin's CLC, the playback experiments presented in Part 2were designed to explore the perceptual component of individualrecognition, assessing whether tamarins actually perceive differencesin CLCs from different tamarins.

Our study is structured as follows. In Part 1, we present theresults of our acoustic analyses of individual, sex, and groupidentity and then discuss these results in light of current thinkingabout the sources of acoustic variation and their role in perceptualclassification. In Part 2, we report findings from several experi-ments designed to test the extent of individual discrimination usinga habituation-dishabituation paradigm; in the wild this techniquehas 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 speechstimuli (Ramus, Hauser, Miller, Morris, & Mehler, 2000) as op-posed to species-specific signals. We conclude by discussing thebenefits of integrating studies of production and perception as wellas some of the limits of our experimental approach.

Part 1: Call Production and Acoustic Morphology

The ability to convey and receive information regarding indi-vidual identity represents an important adaptation for social com-

munication (Beecher, 1982; Cheney & Seyfarth, 1990). Thus, it isnot surprising that this capacity is widespread across many species(e.g., frogs, Davis, 1987; dolphins: Sayigh et al., 1999; passerinebirds: Stoddard, 1996). In nonhuman primates, the ability to rec-ognize individuals on the basis of vocal signals alone has receivedmuch attention. The focus of many of these studies has been oncalls 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 tamarinson the basis of the acoustics of the CLC seems likely becauserelated species have demonstrated this capability (e.g., pygmymarmosets: 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 notall, Callitrichids will exhibit an individual signature system. Thisincludes cotton-top tamarins.

Sex differences in vocal morphology have also been reported ina number of primate species (e.g., vervet monkeys, Cercopithecusaethiops, Seyfarth, Cheney, & Marler, 1980), including severalCallitrichids (e.g., moustached tamarins, Saguinus mystax, Hey-mann, 1987; red-chested moustached tamarins, Saguinus I. Labia-tus, Masataka, 1988; golden lion tamarins, Leontopithecus rosalia,Benz et al., 1990; common marmosets, Callithrix jacchus,Norcross & Newman, 1993). Indeed, there is some evidence sug-gesting that long calling in marmosets and some tamarin speciesmay play a role in mating (e.g., Yoneda, 1981; Masataka, 1988;Norcross & Newman, 1993).

Our final acoustic analyses focus on the possibility of groupconvergence in call morphology, and consequently, on the signif-icant between-group differences in acoustic structure. Three fac-tors make these analyses different from those reported to date.First, all of our tamarin groups were housed in the same room, andthus had continuous acoustic contact. Second, there were no ob-vious motivational differences that could explain acoustic conver-gence within groups. Third, there were no genetic or environmen-tal factors that could account for within-group convergence. Thus,if cage group identity is encoded in the CLC, it may indicate thatsome level of vocal learning is taking place.

In one of the few laboratory studies conducted to find evidenceof vocal learning in nonhuman primates, Elowson and Snowdon(1994) discovered that pygmy marmosets (Cebuella pygmaea) canmodify their trill vocalization in response to their social environ-ment. In addition, experiments on an array of species have shownthat call structure may be modified as a result of changes in socialpairings (e.g., spear-nosed bats, Boughman, 1997; pygmy marmo-sets, Snowdon & Elowson, 1999; budgerigars: Hile, Plummer, &Striedter, 2000). Our analyses may be more limited with respect tovocal learning in that we did not manipulate the social context ofthe colony. Nevertheless, if group identity is encoded in the CLCsof cotton-top tamarins, then vocal learning is a possible mecha-nism, and future work can be designed to explore this possibilityand 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 atthe New England Regional Primate Center (Southborough, MA) and then

260 WEISS, GARIBALDI, AND HAUSER

housed at the Primate Cognitive Neuroscience Laboratory at HarvardUniversity. Tamarins were housed in groups of 2 or 3 animals ina 6.0 X 5.0 X 2.5 ft (1.8 X 1.5 x 0.76 m) home cage made of stainlesssteel wire and Plexiglas. The cage contained tree branches, perches, andwooden nest boxes. At the start of the experiment, there were four matedpairs: one family group consisting of a mated pair and a female offspringand one female pair. During the course of the experiment, 1 female tamarin(MR) died and was replaced by a new male tamarin (RJ). The femaletamarin pair was divided and paired with males. Thus, the colony consistedof five mated pairs and one family group. Their diet consisted of Purinatamarin and marmoset chow, crickets, mealworms, supplemental vitamins,and sunflower seeds. This completely balanced diet was supplemented byfood received during experiments (typically Noyes [Lancaster, NH] ba-nanas and sweet pellets, fruit, occasionally Froot Loops, and marshmal-lows). They were fed once a day in the early evening. Tamarins had adlibitum access to water.

The cage group membership was as follows (male-female): Cage 1, ACand 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 wereseparated (as mentioned above) were SH and UB. There were a number ofrelated tamarins within the colony: RB was the daughter of DD and ES, SPwas the daughter of UB, and RW and ID were twin brothers.

Call acquisition. The CLCs used as exemplars for the acoustic anal-yses were recorded from May 1998 through March 1999. The calls wererecorded in two contexts: either in isolation in an acoustic chamber or in anexperiment focusing on the social aspects of communication.

To obtain calls from the acoustic chamber (Model 400-A, IndustrialAcoustics, Lodi, NJ) we transported the tamarins to a test room that wasboth visually and acoustically isolated from all other members of thecolony. Tamarins were placed in a cage (45 X 45 X 20 cm) within thelarger sound chamber for a period of up to 15 min. Sessions were recordedonto a digital audiotape (DAT; DaPl digital audio tape recorder, Tascam,Tokyo, Japan; sampling rate: 48 kHz) using a Sennheiser ME66 directionalmicrophone (Sennheiser, Old Lyme, CT; frequency response: 50-20,000Hz) or a Sennheiser MKH60P48 microphone (frequency response: 50-20,000 Hz). The tape was then acquired digitally onto a Power Macintosh7100/80 (Apple Computer, Inc., Cupertino, CA) using Sound Designer IIsoftware (1996) and an Audiomedia II card. Some sessions were recordeddirectly into the computer by passing the signal through the DAT andacquiring with Sound Designer II.

For the calls recorded in the social communication experiment, wetransported the tamarins into a test room that was visually and acousticallyisolated from the colony room. The tamarins were placed in the socialcommunication apparatus consisting of two runways separated by a Plexi-glas barrier. Food troughs were placed out of sight at the end of the runway.The experiment tested for audience effects (sensu, Marler, Dufty, & Pick-ert, 1986) in the presence of food or predators. The calls that were usedfrom these experiments were recorded while the tamarin was alone in theapparatus with no predator or other tamarin present. Sessions were tapedwith a Sennheiser ME66 directional microphone and the signal was passedthrough a Tascam DAT (see above) into a Power Macintosh 7100/80. TheSound Designer II software was used to acquire the sound onto theAudiomedia U sound card.

All calls (regardless of origin) were hi-pass filtered just below the lowestfrequency (as determined by a 512 fft spectrogram generated in CanaryVersion 1.2, 1995) and then normalized (using Sound Designer II). Afterthe sound files were edited, we listened to them in the acoustic chamber tocheck for audible background noise or any distortion in the playback.

A total of 129 CLCs were recorded from 12 different tamarins over aperiod 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 qualityrecordings (obtained through the methods described above). By selectingrandomly, we ensured that these calls were representative of the naturalvariation within our population. It should be noted that the number of

vocalizations selected for each tamarin differed because of the individualdifferences in rates of production.

Of the 129 CLCs analyzed, 74 were five-syllable CLCs. In addition tothe multiple discriminant analyses (MDAs) reported on the overall call set,separate sets of MDAs were reported for this subset of calls. It should alsobe noted that the analyses performed for this study were repeated to ensurethat the results were replicable (though these analyses are not reportedhere).

Acoustic analysis. All calls were analyzed using Canary (Version 1.2,1995) for Macintosh computers. Table 1 outlines the parameters that weremeasured for each acquired CLC (see Figure 1 for an example of aspectrogram generated for the analysis). Two factors contributed to theselection of spectral and temporal characteristics chosen for measurement.The first was that previous studies of nonhuman primates have shown thatboth temporal and spectral characteristics of vocalizations may be used inorder 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 thecotton-top tamarin, the authors used a number of these parameters in theiranalysis (Cleveland & Snowdon, 1982; Snowdon et al., 1983). The use ofsimilar parameters may facilitate comparisons across these differentpopulations.

Bonferroni adjusted factorial analyses of variance (ANOVAs) and t testswere initially performed to identify significant parameters for discriminat-ing between individual tamarins and groups of tamarins. MDA was thenused to generate functions to reliably categorize calls across parameters ofinterest. However, because sex is a dichotomous variable, a binary logisticregression was used instead of the MDA. Because the data set consisted ofcalls ranging from three to seven syllables, we focused many analyses onthe first syllable and the average of the final two syllables, as this statisticalapproach helped avoid overfilling Ihe functions lo the data.

To determine whelher our resulls were statistically significant, we useda highly conservative measure. Because there were unequal samples acrosstamarins, we computed chance on the basis of the largest sample from anyone tamarin. For example, in Ihe individual identity analysis, the greateslcontribution came from a tamarin lhal produced 21 oul of Ihe 129 calls lhalwere analyzed. Therefore, for lhal condition, chance was computed as21/129 or 16% for all tamarins.

There were Iwo groups of vocalizations for each analysis. The first groupconsisted of all CLCs recorded, regardless of how many syllables werepresent To control for some of Ihe variability of the CLCs, we resttictedIhe second group lo only five-syllable long calls. These calls were stereo-

Table 1Parameters Measured

Parameter Measuremenl

TemporalCall durationSyllable durationNo. of syllablesIntersyllable pauseDuration to peak frequency of

syllableSpectral

Syllable start frequencySyllable end frequencyFrequency contour

Syllable peak frequencyMean high frequencyMean low frequency

Waveform or spectrogramWaveform or spectrogramSpedrogram"Waveform or spectrogramFrom speclrogram

Power spectrum al start of syllable6

Power spectrum al end of syllableDifference between peak frequency

al start and end of syllableSpeclrogramSpectrumLowesl frequency in the syllable15

a fft size = 512. b fft size = 2,048. c On the basis of power spectrum.


Time(s)

Figure 1. A spectrogram from a five-syllable long call. Note that tem-poral information such as syllable duration, overall duration, and intersyl-lable intervals may be easily extracted from this representation.

typed in that they always consisted of two chirps followed by threewhistles. The five-syllable CLCs were also used as stimuli in our percep-tual studies.

Results

Individual identity. A Bonferroni adjusted factorial ANOVA(p < .006) shows that there are a number of spectral and temporalparameters that significantly differ across tamarins (see Tables 2and 3). A pairwise comparison across all tamarins shows thatdifferent pairs of tamarins vary with respect to the number ofsignificant spectral and temporal differences. This suggests thatindividual tamarin callers differ from each other in a variety ofways and that some tamarins may be more closely related to othersin their call morphology; this finding is clearly limited by the factthat it is restricted to the parameters that we selected to measure.A series of MDAs were used to explore whether we could reliablydistinguish tamarins on the basis of the acoustic parameters of theirCLCs.

MDA: First syllable and average of two terminal syllables.Sixty-five of the 129 CLCs were used in a discriminant functionanalysis. A series of functions were generated that reliably pre-dicted tamarin identity for 91% of the calls. When the 64 calls thatwe withheld were entered into the function, they were correctly

classified 63% of the time. This result is significantly abovechance (binomial test, chance = 16%, p < .001). Overall, thisanalysis was able to reliably predict individual identity 77% of thetime. Figure 2 shows the plot of the centroids (function averages)of each tamarin for the first three canonical functions used in theanalysis. This plot displays a three-dimensional representation ofthe relationship between the CLCs of each tamarin on the basis ofthe most important canonical functions. The associated eigenval-ues were greater than 10% of the sum of the eigenvalues of allfunctions. This is a common criterion used in choosing whichfunctions should be included in an analysis (see Yntema, 1997).Overall, several spectral and temporal parameters were importantfor classification. Spectral parameters included the mean low fre-quency of the last two syllables and the mean high and mean lowfrequencies of the first syllable. Temporal parameters includedtotal duration of the call and average duration to the peak fre-quency of the two terminal syllables.

MDA: First syllable and average of the last two syllables forfive-syllable calls. Forty of the 74 five-syllable CLCs were usedto create a MDA that was able to predict the identity of the callerwith an accuracy of 98%. When the remaining 34 calls wereentered into the analysis, we correctly classified them 56% of thetime (binomial test, chance = 19%, p < .001). In total, the discrimi-nant analysis was able to predict the identity of the caller with anaccuracy of 78%.

There were a number of spectral and temporal parameters thatwere important in classifying the data set. The temporal parametersincluded overall call duration, average syllable duration (for thetwo terminal whistles), and average duration to peak frequency(for the two terminal whistles). The most significant spectralparameters included the mean high frequency and the mean lowfrequency of the first syllable as well as the average mean lowfrequency of the two terminal syllables.

Sex differences. We performed a series of / tests (Bonferroniadjusted, p < .005) across each parameter of the call to determinewhether there were any significant differences based on the sex ofthe caller. Table 2 shows the results of these tests using data from

Table 2Significant Differences: All Calls

Syllable order

2nd to lastParameter 1st syllable syllable

TemporalDuration , S, C I, S, CNo. of syllables I, C I, CSyllable durationIntersyllable pauseDuration to peak frequency of syllable

SpectralSyllable start frequencySyllable pause frequencySyllable end frequencyFrequency contourMean high frequencyMean low frequency

I, S, CI, SI, S, C

,C C,C I, S,C,C,c c,C I

Last syllable

,S, C,c,S, C

,S

I.CII, C

Syllableaverage

I,I,I,II,

I

I,I,

S, CCS

S, C

cc

Note. I = individual identity; S = sex identity; C = cage group membership. For all values, p < .005.


Table 3Significant Differences: 5-Syllable Calls

Syllable order

Parameter

TemporalDurationSyllable durationIntersyllable pauseDuration to peak frequency of syllable

SpectralSyllable start frequencySyllable pause frequencySyllable end frequencyFrequency contourMean high frequencyMean low frequency

1stsyllable

I, S, C

CCC

CC

2ndsyllable

I, S, CII, SI

C

3rdsyllable

I, S, CIII, S

C

4thsyllable

I, S, CI, S, CII, S

C

I, S

5thsyllable

I, S, CI, S, C

I, S, C

I

Note. 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 theaverages across all syllables. Temporal parameters accounted formost of the significant differences between sexes. Female callstended to be longer than male calls by an average of 437 ms. Theterminal syllables in female CLCs were also significantly longer induration (M difference = 159 ms, SD = 23.0 ms). The intersyl-lable latency before the second-to-last syllable was longer forfemale calls (M difference = 10 ms, SD = 2.5 ms). The durationto the peak frequency of the next-to-last syllable was longer for

4 ' EN4

JG1

u.U

CF1

Figure 2. This figure contains a plot of each tamarin's centroids (acrossall long calls) for the first three canonical functions (CF) used in theanalysis of individual identity. Note that this type of plot represents anacoustic space for the tamarin callers. The distances between the centroidsindicate how the tamarins differ with respect to each of these dimensions.The superscript numbers show the cage group membership for each tama-rin. Lowercase letters represent male tamarins, and uppercase letters rep-resent 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 lasttwo syllables. Sixty-five calls were used in the binary logisticregression. A linear function was created that classified the sex ofthe caller with an accuracy of 85%. The generated function wasable to classify the remainder of the call set (64 calls) with anaccuracy 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 (bi-nomial 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 thet tests were also the most important in defining the function. Theseincluded call duration, syllable duration, and duration to the peakfrequency of the call.

Sex differences in five-syllable calls. A total of 29 male and 45female five-syllable CLCs were used in this analysis. Bonferroniadjusted t tests were used to compare parameters across all sylla-bles. The results from these tests were similar to those observedwith all CLCs included (see Table 3). Female calls were signifi-cantly longer than male calls (including longer whistles). Further,the duration to the peak frequency of the last three syllables wasalso significantly longer in female calls.

Binary logistic regression: First syllable and average of the twoterminal syllables in five-syllable long calls. There were notenough five-syllable long calls from both sexes to generate areliable function with the first half of the calls and then check thereliability with the remaining calls. We, therefore, entered all ofthe calls into the regression and found that the calls could beassigned to the correct sex with an accuracy of 85% (76% ofmales, 91% of females). These results are significantly abovechance (binomial test: males, chance = 39%, p = .0001; females,chance = 61%, p < .00001). Many of the parameters that wereimportant in determining the function when all calls were analyzedwere also important in this analysis. These included duration of theentire call, syllable duration, and duration to the peak frequency.


Cage-group membership. In general, several temporal andspectral parameters appeared to differ between cage groups (seeTable 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 theintersyllable latency between the third and fourth syllables. Im-portant spectral parameters included the start, peak, and end fre-quency of the first syllable as well as the mean high and mean lowfrequencies of the first syllable. The temporal parameters that weresignificant included the overall duration, the duration of the lasttwo 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 seriesof functions were created that predicted cage-group membershipwith an accuracy of 77%. The remaining calls were classified bythese functions with an accuracy of 52% (binomial test: chance =25%, p < .001). Using all calls, we reliably predicted the analysisof cage-group membership with an accuracy of 64%. The resultsacross individual cages varied, ranging from 30% to 80%.

The first two canonical (discriminant) functions generated in theanalysis accounted for 74% of the variance in the data. Figure 3shows the plot of the centroids for each cage group on the first 2canonical functions. The parameters that were important for gen-erating the functions were similar to the parameters that weresignificant in the factorial ANOVAs. The important temporalparameters included total duration of the call, the duration of thefirst syllable, and the average duration of the last two syllables.Important spectral parameters included the mean high and meanlow frequencies of the first syllable as well as the start and peakfrequencies of the first syllable.

Cage-group differences in five-syllable long calls. A series offactorial ANOVAs (Bonferroni adjusted, p < .006) revealed sig-nificant differences across a number of parameters (see Table 3).Significant temporal parameters included total call duration, dura-tion of the two terminal syllables, and duration to the peak fre-quency of the fifth syllable. Significant spectral parameters in-cluded the mean high and mean low frequencies of the first threesyllables and the start, peak, and end frequencies of the firstsyllable.

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-groupmembership with an accuracy of 80%. The remaining calls werethen correctly classified with an accuracy of 56% (binomial test:

1

0

-1

-2

3

2

5:

6

4

- 1 0 1 2 3

CF1

Figure 3. This figure contains a plot of each cage's centroids (across alllong calls) for the first two canonical functions (CF) generated in theanalysis of cage group membership.

chance = 34%, p = .004). The combined results yielded a clas-sification average of 69%. Accuracy varied across cage group from29% to 100%.

The first two functions accounted for 95% of the variance in thedata. The parameters that were most important for these functionsresembled the list of parameters that were significant in the fac-torial ANOVAs. Important temporal parameters included totalduration of the call, the average duration of the fourth and fifthsyllables, and the duration to the peak frequency in the first andlast two syllables. Important spectral parameters included the meanhigh 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 thecotton-top tamarin can be categorized by individual, sex, andgroup identity. For individual identity, both spectral and temporalparameters were important for classification. For sexual identity,temporal parameters seemed most important. For group identity,temporal parameters were important as were some spectral param-eters related to the first syllable. Although these findings do notallow us to conclude that tamarins use the selected features toidentify the identity, sex, or group of the caller, or that they areable to do so, they do reveal that within this call type, there is thepotential for such recognition.

It is not surprising that we found acoustic information aboutindividual tamarin identity encoded in the CLCs. As mentionedearlier, individual recognition is widespread among many differentspecies (see above) because it plays an important role in socialcommunication.

The finding that sexual identity may be contained within theacoustics of the call suggests that long calling may play a role inmating or group composition. This is consistent with findings fromclosely related species (e.g., common marmosets: Norcross &Newman, 1993). In fact, the importance of temporal factors in thisanalysis 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 sexdifferences in call morphology are a by-product of differences invocal tract morphology that were selected for reasons other thancalling and mate choice. These findings need to be augmented withboth field studies as well as perceptual experiments in order toverify that sexual identity can be discriminated and used in matechoice.

We may look to the closely related phee call in marmosets togain some insight as to why sex differences in CLCs may beimportant. It has been hypothesized that phee calls may function toadvertise reproductive status to conspecifics (Moynihan, 1970). Inaddition, field studies have shown that solitary tamarins may uselong calls as a mechanism for vocally searching for mates. Youngfemale tamarins have been observed to approach unfamiliar malecallers (see Masataka, 1988; Norcross & Newman, 1993; Yoneda,1981). In contrast, preliminary results from phonotaxis experi-ments, in which calls were played from known and unknownindividual tamarins, suggest that female tamarins approach knownmales, whereas males approach unknown females (Miller, Hauser,Miller, & Gilda Costa, 2001). More research is necessary to


determine whether and how the CLC plays a role in attractingpotential mates.

Our finding that information about group identity is encoded inthe acoustics of the CLC suggests that some degree of vocallearning may occur within each cage group. This finding is ofparticular interest because there have been few examples of vocallearning in primates (see Janik & Slater, 1997). In addition, al-though previous studies of vocal learning have found differencesbetween colonies (e.g., Elowson & Snowdon, 1994; Marshall,Wrangham, & Arcadi, 1999), the tamarins used in our analyseswere housed within the same room, allowing for visual, olfactory,and acoustic contact between members of different cages. How-ever, further research is necessary in order to establish that vocallearning occurs. This includes experiments designed to measurethe extent to which call matching occurs (during calling bouts) aswell as recordings from newly mated pairs.

The extent to which our findings will generalize to other speciesor other call types within species must be tempered by a number offactors. Norcross and Newman (1993) discovered differences incall structure that depended on the context of the recordings. Whenvocalizations were recorded from an isolated tamarin as opposedto a group-housed tamarin, there were more syllables per call andan overall increase in call duration. These modifications may havemade the callers easier to localize. Likewise, in our study, it isimportant to bear in mind the context in which these calls wererecorded. The calls were taken from tamarins that were isolatedfrom their groups. Thus, these findings may not extend to CLCsthat are produced by tamarins that are not isolated.

Similarly, one must be careful in comparing the acoustics fromthis set of recorded tamarin calls with other call sets. Given thefindings of Jorgensen and French (1998) that phee calls in mar-mosets may not be stable over time despite the persistence ofindividual characteristics, it would be interesting to investigate thestability of the tamarin CLC. It should be noted that the entiretamarin call sample used in this study was recorded within a12-month period to diminish the effects of longitudinal changes.

As mentioned earlier, in the study of communication it is im-portant to consider aspects of production and perception. On thebasis of the fact that the cotton-top tamarin's CLC encodes acous-tic information about tamarin caller identity, sex, and group mem-bership, in the following playback experiments, we investigatedwhether such acoustic differences are perceptually salient. Specif-ically, we asked whether cotton-top tamarins can discriminateindividual tamarins by their calls alone. If tamarins are able toperceive differences between callers, then future experiments mayinvestigate which features are perceptually salient and underlie thisability.

Part 2: Playback Experiments

Several studies, spanning a wide variety of primate species,have shown that individual identity may be encoded in contactcalls (e.g., chimpanzees, Marler & Hobbett, 1975; squirrel mon-keys, Symmes, Newman, Talmage-Riggs, & Lieblich, 1979; ring-tailed macaques, Macedonia, 1986; common marmosets, Jones etal., 1993; blue monkeys, Butynski, Chapman, & Chapman, 1992;black-tufted-ear marmosets, Jorgensen & French, 1998). However,these studies do not address whether individual animals use theinformation encoded in the signal to identify other individual

animals by voice. Playback experiments are essential for address-ing the problem of individual recognition from the perceptualperspective.

Studies of several primate species have used playback experi-ments to explore the question of individual recognition (e.g.,vervet monkeys: Cheney & Seyfarth, 1980, 1982; rhesus ma-caques: Hansen, 1976; Kendall, Rodman, & Edmond, 1996; bar-bary macaques: Hammerschmidt & Fischer, 1998; pygmy marmo-sets: Snowdon & Cleveland, 1980; chimpanzees: Kajikawa &Hasegawa, 1996). Of these studies, few have been performed withcaptive populations (e.g., Kajikawa & Hasegawa, 1996; Snowdon& Cleveland, 1980) and none have made use of the habituation-dishabituation 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). Thisparadigm is powerful because it allows researchers to investigateperceptual classification in animals without training.

There are several reasons to expect that tamarins can recognizeindividuals on the basis of their CLCs. First, results from ouracoustic analyses (reported earlier) suggest that information aboutindividual 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-toptamarins (Snowdon et al., 1983), provide evidence of individualrecognition; the latter study used a different kind of long call anda different method. Finally, the function of the CLC has beendescribed as an affiliative signal (e.g., Cleveland & Snowdon,1982), sometimes occurring when an individual animal is sepa-rated from its group. Therefore, one would expect CLCs to providesufficient information for individual recognition. These experi-ments represent only an initial step in our attempt to identify thecritical features mediating perceptual classification of vocaliza-tions in cotton-top tamarins.

Because we anticipated finding evidence of individual recogni-tion for the cotton-top tamarin's CLC, we generated the followingprediction: If we habituate our test subject to several CLC exem-plars from one individual and then present this subject with a CLCfrom a different individual, the test subject should dishabituate(i.e., respond) to the new individual's call. However, if the subjectis habituated to CLCs from one individual and then presented witha novel CLC from the same individual, the subject should transferhabituation (i.e., not respond). Therefore, our first series of play-backs used this procedure to test for responses to changes intamarin caller identity for both opposite and same-sex pairings.

General Method

Apparatus. The test cage used for the playback experiments washoused in an acoustic chamber. During experiments, we placed the tama-rins in a wire and cloth test cage (45 X 45 X 20 cm) with a wire floor. Athin black cotton sheet hung behind the cage. Behind the sheet, an AlesisMonitor One speaker (Alesis Corporation, Santa Monica, CA; frequencyrange, 45-18,000 Hz ± 3 dB) was mounted on a shelf above the box, eitherdirectly behind, or to the left or right of center (location was changedbetween experiments to prevent habituation to sounds emitted from onelocation).

A video camera (Videolabs Flexcam Videolabs, Minneapolis, MN) wasused to record and monitor the sessions. An Alesis RA-100 amplifier drovethe speaker. Hie experimenters watched the session on a monitor outsideof the acoustic chamber. The experiment was run using a HyperCard (1996)


program on a Power Macintosh 7100/80 AV. We played back calls usingan Audiomedia n sound card (sampled at 48 kHz) outputting to an AlesisMonitor 1 speaker. A log of each session was recorded in HyperCard. Thisallowed the experimenters to enter data on-line and keep track of timeelapsed between trials. We recorded vocal responses during trials using aSennheiser MKH60P48 directional microphone (frequency response, 50-20,000 Hz).

Stimuli. Calls used in this experiment were recorded during sessions ofanother experiment. We recorded additional calls while the animals were inthe playback chamber. In both cases, the calls were recorded on a TascamDAT using a Sennheiser ME-60 microphone.

We hi-pass filtered the calls using Sound Designer n software. Todetermine the frequency of the filter, we calculated a spectrogram (1024fft) and measured the lowest frequency of the call. After filtering the callat that frequency, all of the calls were normalized to 100% for amplitude.

Only high quality calls were selected for use in this experiment. Wescreened each call by examining the spectrograms (1024 fft) as well aslistening 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 al-lowed 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 thespeaker before playing the first call of the habituation set. Habituationstimuli were always randomly presented. If more than one cycle of thehabituation set was required during a session, we presented the second setof stimuli in a different, randomized order than the first set.

For each of the experiments presented in this study, we played a seriesof calls until the tamarin failed to respond on three consecutive trials. Afterthree no-response trials, we played the test call followed by a posttest ifnecessary (see below). Responses were measured using the followingparameters: head turning toward speaker, body orienting toward speaker,movement toward speaker, freezing response (if animal was moving andthen froze when the recorded call was played), and vocal responses(producing vocalizations within 5 s of hearing the recorded call). A "noresponse" was recorded in the absence of these responses. During sessions,trials with ambiguous responses (as determined by the experimenters whilerunning a session) were treated functionally as "yes" responses. Ambigu-ous responses included trials in which the tamarin was facing the speakerbefore any sound was played (because of either an errant press by theexperimenter or a slight latency between button press and sound) or whenexperimenters were unable to determine the direction of the tamarin's gaze.This conservative approach was adopted to minimize the number of trialsthat 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 this30-s window. However, this did not occur during our experiments.

Trials started once the tamarin's face was visible and turned away fromthe 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 aposttest stimulus. The posttest stimulus, a tamarin scream, represented acall that was both acoustically and functionally different from the habitu-ation and test calls. Scream exemplars were recorded while the medicalstaff caught the tamarins and administered tuberculosis shots and thennormalized for amplitude. The duration of the posttest screams was withinthe range of the habituation stimuli. The purpose of the posttest was toensure that the tamarin had not habituated to the playback setup in general.Failure to respond to the test stimulus could indicate that the tamarin hadeither habituated to the playback setup in general or had perceptuallyclustered the habituation and test stimuli into one category. If the tamarinhad habituated to the playback setup, then it should ignore the postteststimulus. In contrast, if failure to respond to the test call was due to thetamarin's perception of similarity between the habituation series and thetest stimulus, then it should respond to the posttest stimulus. Sessions in

which the tamarins failed to respond to the posttest were rerun at a laterdate.

Analyses. Because responses to playbacks can be difficult to score inreal time, we digitized (Adobe Premiere version 4.2; Adobe Systems Inc.,San Jose, CA) the last 13 habituation trials (including the three no responsehabituation trials), the test, and the posttest. This ensured that there wouldbe a distribution of both yes and no response trials, thereby reducing theopportunity for biased scoring. These trials were assigned code file namesand then randomized to ensure that the scorers were naive to the condition.Once scores were obtained, we consulted the master list to determine thecondition. Two scorers then analyzed each of the trials and recorded a yes,no, or ambiguous response; the type of response (e.g., head turn, counter-call, etc.) and the duration of response were recorded as well. Trials inwhich it was not clear whether a tamarin had looked at the speaker weredeemed ambiguous. These responses were treated as yes responses if theyoccurred in the habituation series. If a test trial was determined to beambiguous, then the trial was rerun. This occurred in less than 8% of allsessions. Sessions were discarded if scorers assessed any of the threehabituation trials (the three trials preceding the test trial) as a yes response.Likewise, sessions in which there was disagreement between scorers onany of the three no response habituation trials, the test, or the postteststimuli were also discarded. Finally, sessions in which the tamarin did notrespond to both the test and the posttest were also discarded.

Condition 1: Individual recognition. In the first condition, we pre-sented tamarins with a habituation set composed of eight different five-syllable CLCs from male RW. The test stimulus was a five-syllable CLCfrom female ES. RW and ES were from different groups. The postteststimulus was a scream from male SP matched in length and filtered inaccordance with the habituation and test stimuli. As a control for thiscondition, we presented tamarins with the same habituation series fromRW and a novel five-syllable CLC from RW.

An additional test was conducted in which the habituation series and teststimuli were produced by tamarins of the same sex. In this condition, thehabituation set consisted of eight different five-syllable CLCs from femaleES. The test stimulus was a five-syllable CLC from female JG. The postteststimulus consisted of a scream from either male SP or male ID.

Condition 2: Individual recognition of same sex cage mates. Becausethe acoustic analyses revealed that cage mates sounded more similar toeach other in some dimensions than to noncage mates, it is possible thattamarins tested in Condition 1 used those features that are salient fordistinguishing among cage groups rather than individuals. Therefore inCondition 2 we also set out to test whether tamarins could discriminatecallers regardless of sex and cage group membership. Because of theconfiguration of our colony, we had access to only a single group with twotamarins of the same sex: the mother-daughter pair, ES and RB, respec-tively. If our colony of tamarins could discriminate between these callers,then we could be fairly confident that they are able to recognize thedifferences between any two tamarins on the basis of their calls. If thetamarins failed to discriminate between these callers, however, then dis-habituation in Condition 1 could be explained by the perceptual salience ofboth sex and group membership. In other words, although tamarins mayfail 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 CLCsproduced by female ES. The test stimulus was a five-syllable CLC pro-duced by female RB. The posttest stimulus was a scream from male ID. Asecond habituation set was created in which RB exemplars were used forhabituation and an ES exemplar was used as the test stimulus. A numberof tamarins were inaccessible during the ES-RB condition, and thus, weran only 10 tamarins.

Condition 3: Discrimination of acoustically similar callers. One po-tential confound in Condition 2 was that the callers were more acousticallysimilar than those used in Condition 1 (see Discussion). To begin exploringthis possibility, we designed a final series of playbacks to test whether


tamarins would discriminate between two unrelated callers with acousti-cally similar CLCs. On the basis of the results from the MDA (reportedearlier), we chose CLCs from tamarins ID and RB as stimuli; the coordi-nates for ID and ES (the mother from the previous condition) were similarin the three most important acoustical dimensions and differed from thecalls of RB along similar dimensions. Likewise, pairwise ANOVAs com-paring the acoustics of CLCs from RB and ID revealed no significantdifferences (Garibaldi, 1999).

The habituation set consisted of 8 five-syllable CLCs produced byfemale RB. The test stimulus was a five-syllable CLC produced by maleID. The posttest stimulus was a scream from ID. A second habituation setwas created in which five ID exemplars were used for habituation and anRB exemplar was used as the test stimulus. The IDhab-RBtest condition wasrun 12 months after the other conditions (see General Discussion) when thecolony expanded, allowing for 14 tamarins to be tested.

Results

Condition 1: Individual recognition. In the RWhab-EStes, con-dition, 12 out of 13 tamarins responded to the test call followinghabituation (see Figure 4). Tamarins' responses for this conditionincluded 9 head turns, 1 approach, 5 long calls, and 2 chirps. Notethat four test trials had multiple responses (e.g., one trial containeda head turn and a long call, etc.). The average number of callsplayed back until habituation was 22.8 (SD = 15.60, range =4-58). In the control condition involving RWhab-RWtest, 3 outof 13 tamarins dishabituated to the novel RW call (see Figure 4).All three tamarins responded with head turns. The average numberof calls played back until habituation was 19.8 (SD = 12.20,range = 5-49). There was a statistically significant difference inthe number of tamarins responding to the test trial for these twoconditions (paired sign test, p < .02). There was, however, nodifference between conditions in the number of trials to habitua-tion, paired t test, r(12) = 0.77, p < .46.

For the EShab-JGtest condition, 11 out of 13 tamarins respondedto the test call following habituation (see Figure 4). The responsesfor this condition included 7 head turns, 2 approaches, 5 long calls,and 1 trilled vocalization (consisting of multiple chirps). Theaverage 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-sexchange of identity condition, ES^-JG,̂ , including the control EShab-

(SD = 27.59, range = 5-99). In the control condition involvingEShab-ES,,.st, 2 out 13 tamarins dishabituated to the novel ES call(see Figure 4). One tamarin responded with a trilled vocalizationand the other responded with an antiphonal call. The averagenumber of trials until habituation was 12.84 (SD = 7.02, range =4-27). There was a statistically significant difference in the num-ber of individual tamarins responding to the test trial for these twoconditions (paired sign test, p < .004). There was no significantdifference between conditions in the number of trials until habit-uation, 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 tothe RB test call. The observed responses included 4 head turns, 1trilled response (chirps), and 1 antiphonal call. The average num-ber of calls played back until habituation was 26.3 (SD = 20.60,range = 5-57). The proportion of those responding was notsignificant 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 in-cluded 4 head turns, 2 approaches, and 4 antiphonal long calls (seeFigure 6). The average number of calls played back until habitu-ation was 28.7 (SD = 21.00, range = 5-66). The proportion ofthose responding was not significant when compared with thebaseline results (paired sign test, p < .13). There was no differencein the number of trials until habituation in the EShab-RBtest and inthe RBhab-ESMS, conditions, paired t test, t(9) = 0.16, p < .88.

Condition 3: Discrimination of acoustically similar callers. Inthe RBhab-IDKst condition, 9 out of 13 tamarins dishabituated tothe ID test call (see Figure 7). The responses included 4 headturns, 2 approaches, 1 chirp, and 2 antiphonal long calls. Theaverage number of calls played back until habituation was 18.6(SD = 14.30, range = 5-58). The proportion of those respondingwas significant when compared with baseline results (paired signtest, p < .04).

In the IDhab-RBtest condition, 11 out of 14 tamarins dishabitu-ated to the RB test call. The responses included 5 head turns and 10antiphonal calls. The average number of calls played back untilhabituation was 17.5 (SD = 15.30, range = 5-50). The proportionof those responding was significant when compared with thebaseline results (paired sign test, p < .02). There was no differencein the number of trials until habituation in the RBhab-IDtest and inthe IDhab-RBtcst conditions, paired t test, f(12) = 0.66, p < .53.

Playbacks of own calls. Because of the design of our experi-ments, a number of tamarins heard their own calls played backeither during the habituation series or as the test call. This pre-sented an interesting situation because the tamarins had neverheard their own calls broadcast from an external source. Onepossible response is that tamarins perceived these calls as comingfrom an unfamiliar caller. A second possibility is that tamarinsperceive such calls as familiar but not as their own call (e.g., froma cage mate). Finally, tamarins may recognize the call as their ownand respond differently from how they respond to unfamiliar andfamiliar callers.

Research conducted with birds has shown that when an individ-ual bird's own song is played back, it responds with an interme-diate response between that of a familiar neighbor and that of astranger (e.g., Brooks & Falls, 1975; Searcy, McArthur, Peters,& Marler, 1981; Yasukawa, Bick, Wagman, & Mailer, 1982;


Figure 5. Results from the related female tamarins' change of identitycondition, RBhab-ESMst as well as the reverse EShab-RB,cst.

McArthur, 1986). Snowdon et al. (1983) studied quiet and normallong calls in cotton-top tamarins and reported that tamarins re-sponded to their own calls in the same way that they responded toa cage mate's calls.

We did not run experiments involving unknown tamarins. Con-sequently, we cannot contrast the tamarin's response to its own callas opposed to calls produced by unfamiliar tamarins. We can,however, explore differences in response to self-call trials andother call categories.

Summary. Across all conditions, tamarins that heard their owncalls during the habituation series took an average of 11.9 trials(SD = 7.04) to habituate. This is not significantly different fromthe number of trials those same tamarins required to habituate toother 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, tamarinswhose calls were played as the habituation series responded to thetest call in three out of six trials. This is not significantly differentfrom how the rest of the sample performed on change of identityconditions, unpaired t test, f(57) = 0.976, p < .34. For tamarinswhose calls were played as the test call, 5 out of 6 tamarinsresponded. This is not significantly different from how the rest ofthe sample performed on change of identity conditions, unpaired ttest, ?(51) = 0.66, p < .52.

In control conditions in which tamarin caller identity remainedconstant (i.e., RWhab-RWtest, ES^-ES ,̂ both tamarins trans-ferred habituation to the novel exemplar from their own repertoire.

General Discussion

Results from Condition 1 provide support for the hypothesis thatcotton-top tamarins can discriminate between individual tamarinson the basis of their five-syllable CLC. Of the 26 trials involvinga change in caller identity, tamarins responded 23 times. In addi-tion, the results from the control conditions indicate that themethodology is well suited for identifying which aspects of theCLC may be meaningful to the perceiver. Of the 26 control trialsinvolving novel calls from the same caller, only 5 tamarins disha-bituated. This finding is critical in that it indicates that the tamarinswere not simply responding to a novel acoustic change in the testcondition. Rather, tamarins responded to changes that were mean-ingful—in this case, a change in caller identity. These results alsoshow that the habituation-dishabituation procedure can be suc-cessfully used with captive nonhuman primates to test for percep-tual classification of species-specific calls. Additional evidence forthe effectiveness of this procedure comes from studies testingspeech perception with cotton-top tamarins (Ramus et al., 2000).

The results from this first condition suggest that antiphonalcalling may be another assay that indicates whether tamarins findthe change in caller identity meaningful. This assay has been usedbefore 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 whenidentity changed, whereas only 1 out of 26 control trials yielded asimilar response (see Figure 6 for a diagram of antiphonal callingresponses by condition). It should be noted that in tests of speechperception, tamarins never respond with antiphonal calling (Ramuset al., 2000), suggesting that this behavior may be restricted toconspecific vocalizations. The implications of the antiphonal call-ing data are discussed below.

Results from Condition 2 suggest that tamarins fail to discrim-inate between two same-sex, related tamarins from the samegroup. The results of this condition underscore the importance ofconsidering aspects of both production and perception in the studyof communication. On the basis of the acoustic analyses alone, onemight have predicted that these 2 tamarins could be discriminated.Both ES and RB have discrete points on the plot of individualcentroids on the canonical functions generated by the MDA (seeFigure 2). By performing perceptual experiments in conjunctionwith these analyses, we obtained a more complete understandingof how tamarins recognize individual tamarins on the basis ofacoustics alone.

12

•s 6

I. I IRW-ES RW-RW ES-JG ES-ES RB-ES ES-RB ID-RB RB-ID

Figure 6. Antiphonal calling data across all conditions.


12

RB-ID ID-RB

H Response

171 No Response

Figure 7. Results from the acoustically similar tamarin callers' change ofidentity condition, RBhab-IDttst as well as the reverse

This conclusion, however, is limited to our methodologicalassay. In contrast to a psychophysical task that asks whether SignalA is discriminable from Signal B, the habituation-dishabituationprocedure asks whether Signal A is meaningfully different fromSignal B (see Nelson & Marler, 1990). Thus, although the tamarinsapparently did not perceive a meaningful difference between theCLCs of ES and RB, a psychophysical task may well show thattheir calls are discriminable.

An open question is whether tamarins can discriminate individ-ual tamarins of the same sex and the same group. Recall that therelationship between the 2 tamarins whose calls were played inCondition 2 was that of parent-offspring. It may be that unrelatedtamarins within a group can be discriminated. Although our lab-oratory is not currently set up to allow for us to answer thisquestion, tamarin groups in the wild often contain unrelated tama-rins of the same sex (Neyman, 1977). In addition, it would also beinteresting to test whether members of the same group have anadvantage in discriminating related tamarins from their own group.

One limitation to Condition 2 was that when the mother-daughter pair were plotted using MDA, the centroids were closerthan those of the other tamarins used in Condition 1 (see Figure 2).In addition, pairwise ANOVAs revealed that there was only oneparameter that significantly differed between these 2 tamarins (thestarting frequency for some of the syllables in their calls). Incontrast, the tamarins from the first condition differed along moredimensions. In particular, the CLCs of RW and ES differed in callduration, in duration of the individual syllables, and in duration tothe peak frequency of the call. The CLCs of ES and JG differed inthe duration of the syllables and the intersyllable interval(Garibaldi, 1999). Overall, this suggests that the calls produced bythese 2 tamarins have greater overlap in call morphology than theexemplars used for previous test conditions. Therefore, there aremultiple interpretations for the playback results. Condition 3 ex-amined whether results from the first two conditions could beexplained solely on the basis of acoustic similarity and, thus,degree of discriminability. Specifically, if ES and RB could not bediscriminated because of acoustic similarity, then ID and ESshould also prove difficult to discriminate.

Results from Condition 3 indicate that tamarins can discriminatethe CLCs of two unrelated tamarins even though the degree ofacoustic similarity is high. The findings from this condition againunderscore the importance of considering both production and

perception when studying communication. On the basis of therelative acoustic proximity of ID and ES (used in Condition 2), onecould not have predicted the results from these experiments—specifically, that RB and ES were difficult to discriminate betweenwhereas ID and RB were not. Although studies of production helpestablish the kinds of information encoded in the signal (e.g.,individual identity, sexual identity, etc.), it is only through percep-tual experiments that we can identify which acoustic features areactually meaningful to the tamarins.

It should be noted that our acoustic analyses created only one ofmany possible renditions of the acoustic space for tamarin CLCs.Even the results from pairwise ANOVAs may be limited bysample size. It is possible that there is one parameter, or even aconstellation of parameters, that distinguishes the ID calls from theES calls and that underlies the perceptual playback results. Oneapproach to solving this issue is to run playback experiments withcalls that have individual parameters manipulated. For example,since ID and RB are of opposite sex, whereas ES and RB are of thesame sex, we could manipulate temporal parameters of the callbecause these have been shown to be important in our acousticanalyses of sexual identity. This kind of manipulation woulddetermine which parameters meaningfully contribute to individualtamarin recognition and, in turn, would help explain why therelated females were more difficult to discriminate between thanID and RB were. Thus, part of our overall research programfocuses on manipulating individual features and determiningwhich parameters are meaningful in the perception of the CLC.

The antiphonal calling data from this condition were somewhatsurprising. In the RBhab-IDtest condition, only 2 out of 9 respond-ing tamarins produced antiphonal calls. It is unclear why this testexemplar elicited few antiphonal responses and still was detectedby most tamarins as a change in speaker identity (see Discussion).In contrast, 10 out of 11 responding tamarins called antiphonally tothe test stimulus in the IDhab-RBtest condition. This represents ahigher level of response than in other conditions (see Figure 6).One factor that may have contributed to this effect is that thiscondition was run 12 months after the initial individual tamarinrecognition conditions. It is possible that because the test call hadbeen recorded 12 months earlier, it sounded less familiar. Previousresearch has shown that the phee call in marmosets changes overa 12-month period (Jorgensen & French, 1998), and it is unknownwhether this occurs in tamarin contact calls as well.

One possibility not addressed in our study is that tamarinscannot distinguish between the calls of their cage mates, regardlessof sex. However, this does not seem likely because Condition 3showed that the tamarins are able to discriminate between acous-tically similar callers of the opposite sex. It is likely that theywould respond to the acoustic differences known to exist betweenthe sexes. Future studies may address this issue further.

One finding from the analysis of self-call perception is thattamarins are likely to dishabituate when their own calls are used asthe test stimulus in conditions involving change of identity. How-ever, because most of our tamarins responded to changes inspeaker identity, further research is necessary to determinewhether tamarins are particularly sensitive to the acoustics of theirown 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 ofthe small sample, this finding is not statistically significant. In


addition, the number of exemplars prior to habituation did notchange for tamarins that habituated to a series of their own calls.This result supports Snowdon et al.'s (1983) position that self-callsmay be perceived as comparable with calls produced by knowntamarins. Of further relevance, results from experiments designedto elicit antiphonal calling have found that there is no significantdifference between the tamarins' rate of antiphonal calling to theirown calls and the tamarins' rate of antiphonal calling to those ofother tamarins (Ghazanfar, Flombaum, Miller, & Hauser, 2001); inthese experiments as well, however, tamarins have not been testedin a condition involving their own calls versus foreign tamarins'calls.

As mentioned earlier, results from studies on bird songs havefound that birds respond to self-song with an intermediate responsebetween 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 thatself-song production provides a template to which other songs arecompared as a criterion for species recognition (see McArthur,1986; Searcy et al., 1981). Our data suggest that there is nodistinction between hearing one's own calls and hearing a familiarindividual's calls. Additional research is necessary to determinewhether an individual primate's own calls play a special role inprimates' vocal perception.

When hearing a long call, conspecifics often respond with theirown antiphonal long calls (Cleveland & Snowdon, 1982). Thus,antiphonal calling may provide the most natural assay for gaugingresponses. In our experiments, the first and third test conditionshad more antiphonal calling than the second condition (in whichdiscrimination was difficult; see Figure 6) or the control condi-tions. However, there were still some anomalous findings (seeCondition 3) with respect to the number of antiphonal calls elicitedby the different test stimuli. Further research is necessary todetermine which components of the call are critical to elicitingthese responses. For example, research on gorilla double gruntshas found that there are specific acoustic cues that tend to elicitantiphonal calling (Seyfarth, Cheney, Harcourt, & Stewart, 1994).Studies by Ghazanfar et al. (2001) suggest that tamarins are morelikely to produce antiphonal calls in response to complete CLCswhen contrasted with playbacks of chirps alone, whistles alone, orwhite-noise bursts that mimic the temporal patterning of the CLCwithout the species-typical amplitude envelope.

One goal of these experiments was to determine whether thehabituation-dishabituation paradigm could be effectively imple-mented in captivity to address issues pertaining to meaningfuldifferences in vocalizations. The results from these experimentssuggest that this paradigm is effective. In fact, it should be notedthat the IDhab-RBtest condition was run more than 12 months afterthe first condition of this study. The responses in this condition(which included a high proportion of antiphonal calling) suggestthat the effect is robust and that the paradigm is consistent acrosstime.

The overall goals for the analyses and experiments reported inthis study were met. Future research may determine which featuresof the CLC are considered meaningful by perceivers. This can beaccomplished by habituating tamarins to a series of CLCs and thenpresenting a test call in which one acoustic parameter has beenmanipulated. The acoustic analyses reported in this study can beused to guide the creation of these test calls.

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The Production and Perception of Long Calls by Cotton-Top ... · 0735-7036/01/$5.00 DOI: 10.1037//0735-7036.115.3.258 The Production and Perception of Long Calls by Cotton-Top Tamarins