Interspecific and intraspecific responses to synthesized pygmy marmoset vocalizations

Anim. Behav., 1978, 26, 1 92-206

INTERSPECIFIC AND INTRASPECIFIC RESPONSES TO SYNTHESIZEDPYGMY MARMOSET VOCALIZATIONS

BY CHARLES T. SNOWDON & YVONNE V. POLADepartment of Psychology, University of Wisconsin, Madison, Wisconsin

Abstract . Four different types of trill vocalizations used by pygmy marmosets are acoustically similarto one another and occur in different contexts . Synthetic replicas of these vocalizations and variantsalong each of the acoustic continua separating them have been produced and played to both pygmymarmosets and humans. The marmosets responded to a broad range of variations as equivalent tonatural vocalizations, but responded quite differently to variants of some calls used in different contexts .This was analogous to the `categorical perception' that humans show with speech sounds . Humansmade finer discriminations among all of the synthesized marmoset sounds and showed no perceptualboundaries between them . Thus humans differ from marmosets in their perceptual responses to thesesounds. The tolerance of broad variations in vocalizations coupled with sharp boundaries betweenfunctionally different sounds is a mechanism that could ensure an accurate reception of a signal by arecipient despite variations due to specific individuals or environmental noise .

The sound patterns produced by many primatespecies appear to be intergraded rather thandiscrete calls (e .g . Rowell 1962 ; Marler 1965,1975 ; Green 1975). In the absence of cleardifferentiation between vocalizations, correlationof a given form of vocalization with specificbehavioural patterns or contexts is difficult .However, there have been some successfulattempts to make distinctions between rathersimilar vocalizations and to correlate thesewith specific contexts . Green (1975) distinguishedseven different forms of the `coo' vocalizationof the Japanese macaque (Macaca fuscata),and identified 10 different situations in whicha `coo' vocalization might be emitted . When thespecific form of a `coo' variation was plottedagainst specific situations, there was a signifi-cant correlation between situation and theparticular form of `coo' most likely to be used .

A similar correlation between form of avocalization and context has been found forthe pygmy marmoset (Cebuella pygmaea) byPola & Snowdon (1975) . They distinguished fourtypes of contact/location calls that were acous-tically similar to each other but which could bemapped onto specific situations. (These will bedescribed below along with an additional typeof call not found earlier.)

There is a serious problem with the researchprocedures described above . Whether a series ofvocalizations is labelled as discrete or gradedis a function of the perceptual system of thehuman observer, and not of the species understudy. Even when one can make fine distinctionsin the form of a vocalization type and can cor-

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relate this with specific contextual situations,one still does not know whether the speciesbeing observed makes distinctions between thecalls in the same way. As a solution to thisproblem, both Marler (1965) and Green (1975)have suggested an experimental method involv-ing the synthesis of the vocalizations and play-back to the species being observed . Throughsuch a procedure one can discover the propertiesof the vocalization that are perceptually impor-tant to the species being studied, and whetherthe human's perception corresponds to that ofthe animals .Two major studies in non-mammalian verte-

brates have used synthesized vocalizations todetermine the perceptually salient characteristicsof these vocalizations to that species . Capranicaand his colleagues (e .g . Capranica 1966, 1968 ;Frischkopf et al. 1968) have studied the responseof the bullfrog (Rana catesbeiana) to synthesizedversions of their mating calls. Their results haveshown a `fine-tuning' in both behaviouralresponse and the sensory receptors underlyingthat response. With rather minor variation in thepitch of a vocalization the response to thatvocalization is eliminated, and, in fact, thesensory receptors (Frishkopf et al . 1968) reflectthis fine tuning . Such intolerance of variationin signal form is adaptive to maintain reprod-uctive isolation among several sympatric speciesof frogs.

Falls & Brooks (Falls 1963, 1969 ; Brooks &Falls 1975a, b ; Falls & Brooks 1975) haveinvestigated playbacks of various variants ofwhite-throated sparrow (Zonotrichia albicollis)

SNOWDON & POLA : SYNTHESIZED MARMOSET VOCALIZATIONS

song. They found that white-throated sparrowswill tolerate a considerable variation in someparameters of their song (pitch, pattern ofpitch, and pattern of timing (Falls 1963, 1969)in identifying members of their species . However,rather minor variation (of the order of 10 %)in these same variables will affect the birds'abilities to discriminate particular individuals(Brooks & Falls 1975b) .

One study has focused on whether a primatespecies could distinguish between various formsof its own calls . Symes & Newman (1974) testedsquirrel monkeys (Saimiri sciureus) using ashock-avoidance procedure to determine if themonkeys could discriminate variants of theisolation peep vocalization . They found thatanimals successfully discriminated rather minorvariations, though several hundred shock-avoidance trials were necessary to establish aninitial differential response to call variants . Thefact that so many trials with shock-reinforcementwere needed indicates that the distinction bet-ween isolation `peep' variants may not becommon in nature, or that the unnaturalnessof the test procedure makes discriminationdifficult .

Reports of attempts to carry out playbackexperiments with primates in a more naturalsetting have indicated considerable difficulties(Green 1975). First, if the playback equipmentor speakers were visible to the animals, theyquickly ignored the sounds being produced .Green found that he was able to get a responseto calls only when he produced playbacks whilethe animals were out of sight of his equipment .However, Waser (1975) has reported thesuccessful use of playback techniques withforest-dwelling grey cheeked mangabeys (Cerco-cebus albigena) . A second difficulty is thatcomplexity in the acoustic form of most primatevocalizations makes them hard to synthesize .The pygmy marmoset, however, has two virtuesfor this type of study . It produces a contact/location call to which other marmosets respondantiphonally even when played back over aspeaker, and this contact/location call has arelatively simple acoustic structure which can beeasily synthesized.This paper presents the responses of pygmy

marmosets to synthetic versions of four of theircontact/location calls, as well as to systematicvariations of these calls along each of theacoustic parameters that define the calls. Inaddition, because most studies of animalcommunication are based on the perception of

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the human observers doing the study, themarmoset vocalizations and their variantshave been presented to human observers to seewhether human perception of these soundscorresponds to that of pygmy marmosets .Part 1 : Responses of Pygmy Marmosets toSynthesized Versions of Their Own VocalizationsPygmy marmosets emit five types of vocalizationsin contexts that could be described in terms ofthe animal either desiring contact with another,or communicating its location so that futurecontact could occur with speed and precision .All of these calls have as a basic acousticstructure a sinusoidal frequency modulation ofa centre frequency .

Representative samples of four of thesevocalizations are shown in Fig . 1 and the means,standard errors, and ranges for each of the fouracoustic parameters for each of the four types oftrills are presented in Table I . The closed mouthtrill (Fig. 1(a)) is the most common trill of thepygmy marmoset. It is emitted in a wide varietyof contexts where there is no sign of externaland intragroup disturbance. It is given onlyby adult animals and is generally responded toantiphonally by other animals . The open mouthtrill (Fig . 1(b)) is emitted in situations wherethere is a high probability of some agonisticevent occurring subsequent to the call (Pola &Snowdon 1975). This trill does not elicit anantiphonal vocal response. It differs from theclosed mouth trill by being of greater duration(mean 294 ms versus 175 ms). Note from Table Ithat the longest closed mouth trill and theshortest open mouth trill were each 250 ms .Therefore, whereas the mean durations of thetrills differ, there is a gradation of durationbetween the two .

The quiet trill (Fig. 1(c)) was not describedby Pola & Snowdon (1975). It is given in non-agonistic situations similar to those in which theclosed mouth trill would be given, but the quiettrill is emitted when animals are in close proxi-mity to one another (about 1 m) . Acousticallythe quiet trill is emitted with less energy thanthe closed mouth trill and it has a considerablyreduced range of frequency modulation (mean1 kHz bandwidth versus 3 .8 kHz bandwidthfor the closed mouth trill). There was no overlapof bandwidths between the quiet trills and closedmouth trills sampled for Table I .

The juvenile trill (Fig. 1(d)) was given byanimals between 5 and 12 months of age insituations identical to the adults' uses of theclosed mouth trills . The frequency modulation

t94 ANIMAL BEHAVIO-UR, 26, 1

Fig. 1. Representative trills from pygmy marmosets: A: closed mouth trill; B: open mouth trill; C: quiet trill; D: juvenile trill.

Table I. Mean, Standard Error and Range of Acoustic Parameters of Four Trills

Trill Centre

N Duration (ms) frequency @Hz) Bandwidth (kHz) Modulating

frequency (Hz)

Closed mouth 26 175.2 f 5.8 $855 $13 35.3 f 0.77 (m-250) .-. (25-40)

Open mouth 15 294.0 f 12.9 9.5 i 0.23 33.3 * 1.07 (250-410) (7.2-10.7)

;;9,", $29 .-. w49

Quiet 25 173.2 f 9.8 10.4 f 0.22 1.0 f 0.1 33.1 * 0.51 (100-250) (8.5-l 1.7) (0.5-2.0) (30-40)

Juvenile 8 220.0 i- 17.4 10.8 f 0.35 3.1 f 0.5 31.9 f 0.5 (150-300) (10-2-12.2) (1.5-5.0) (30-35)

was less regular than that of the adults, and the centre frequencies were greater initially, descen- ding toward adult centre frequencies as the animals became older and larger. We found no evidence of amplitude modulation in any of these trills and, therefore in our syntheses we held amplitude constant.

A remaining contact/location call, the J-call (Pola & Snowdon 1975), was given by adult animals when isolated from the rest of the group. Structurally, it is an interrupted frequency modulated call with only the ascending portion

of the sine wave being produced. Because it has been more difficult to synthesize adequately, it was not included in the present series of experiments.

Method Colony. A small colony of eight pygmy

marmosets were housed in family groups within a larger room. Adjacent family groups could communicate with each other through the wire mesh screening separating their living areas. Details of the environment and the husbandry

SNOWDON & POLA: SYNTHESIZED MARMOSET VOCALlZATIONS 19.5

Fig. 2. Synthesized trills varying in duration. The mean duration of a natural closed mouth trill is 0.176 s.

of the animals have been presented previously (Pola & Snowdon 1975).

Synthesis of vocalizations. Vocalizations were synthesized through the use of two Wavetek generators. The sinusoidal modulating frequency was generated by a Model 130 Oscillator which had a variable voltage output. This output was supplied to the voltage-controll.ed input of a Model 131 A Oscillator which was set at the centre frequency. The resulting output was passed through a Lafayette Model 50012 electronic timer and an Iconix Model 0137 Electronic Switch set for a 50-ms rise and fall time which minimized onset and offset tran- sients. The signal was then passed through a Herrod amplifier to the speakers (Quam QClO PAXK, these speakers had a flat frequency response to 14 kHz). All signals used in the study were generated directly at the time of testing.

The signals used in the experiments are shown in Figs. 2 to 5. Because the closed mouth trill was the most common call of the animals and because it elicited the clearest behavioural response, it was used as the standard call. The closed mouth trill was generated with the following parameters based on the means of a large sample of natural trills : duration = 176 ms ; frequency range = 7.4 to 11 a4 kHz ; centre-

frequency = 9.4 kHz; modulating frequency = 36 Hz. Each of these four parameters (duration, frequency range, centre frequency, and modulating frequency) were varied separately. Figure 2 shows the duration-stimuli which varied from 176 to 338 ms. In addition to the six stimuli shown here, three additional duration-stimuli were added at a later time (249,257 and 265 ms). Figure 3 shows the frequency range stimuli which varied from a range of 8.9 to 9.9 kHz mimicking the quiet trill) to a range of 5.7 to 13.1 kHz. Figure 4 shows the centre-frequency stimuli which ranged from 7 to 12 kHz with 9.4 kHz representing the closed mouth trill. Figure 5 shows the modulating-frequency stimuli which ranged from 15 to 45 Hz with 36 Hz representing the rate of the closed mouth trill.

A number of modifications were directed toward overcoming the previously reported difficulties of doing playback experiments. First, to avoid the possibility of the animals’ localizing and subsequently ignoring the playbacks, five separate speakers were hidden in the light fixtures of the room. Playbacks could be directed through any one of the speakers, and the speaker location used for presenting stimuli was changed frequently. Secondly, in order to minimize the possible disrupting effects of playing what might

196 ANIMAL BEHAVIOUR, 26, 1

Fig. 3. Synthesized trills varying in frequency range. The mean frequency range of a natural closed mouth trill is 7.4 to 11.4 kHz.

Fig. 4. Synthesized trills varying in centre frequency. The mean centre frequency of a natural closed mouth trill is 9.4 kHz.

SNOWDON & POLA: SYNTHESIZED MARMOSET VOCALIZATIONS 197

Fig. 5. Synthesized trills varying in modulating frequency. The mean modulating frequency of a natural closed mouth trill is 36 Hz.

be ‘abnormal’ stimuli, there were as many synthesized closed mouth trills presented as there were of each variant. This procedure was adopted to keep the density of possible ‘abnormal stimuli relatively low. Thirdly, to prevent habituation to specific synthesized stimuli, the number of presentations on a given day was limited to 10 to 15 stimuli, half of which were of one variant and half of which were closed mouth trills. In addition one or more days of no testing intervened between test days. Pilot testing with natural stimuli indicated that this schedule minimized habituation. The entire experiment was carried out over an 18-month period.

Pola & Snowdon (1975) observed that the closed mouth trill vocalization elicited an antiphonal response from other animals. This antiphonal trill was noted to be the most consistent behavioural response following naturally emitted closed mouth trills. Therefore, the production of this antiphonal trill was used to indicate whether or not the animals perceived a synthesized call as equivalent to a closed mouth trill. A positive response to a playback stimulus was scored if a trill was produced by an animal within 5 s of the presentation of the stimulus.

Given that individual responses could not be discriminated and the stimuli were audible to the

entire colony, the results are based on the response of the colony rather than its individual members. This procedure is somewhat unusual, but valid for several reasons: First, since the calls are emitted in a social setting, it seemed quite likely that removing individuals for separate testing would produce a highly abnormal response pattern. Indeed animals which were separated from the group for various periods of time did not respond to natural closed mouth trills in a normal way. Second, the commonly used technique of studying discrimination through selective reinforcement of an operant response to one stimulus did not work with pygmy marmosets. Pigmy marmosets tested in a discrimination paradigm within their social grouping would initially respond with quite good performance for 3 to 4 weeks, but would subsequently ignore the task regardless of the reinforcement used. Therefore, for both etho- logical and practical reasons the technique of playing back sounds to the entire colony seemed the best available.

The rate of production of closed mouth trills was scored at times when no playback stimuli were presented (null stimulus). The responses to each of the synthesized stimuli were evaluated relative both to the rates of response to a

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closed mouth trill stimulus and to the nullstimulus, respectively .

Over the 18-month testing period there were472 presentations of stimuli on the duration-continuum, 475 presentations on the frequency-range continuum, 376 presentations on thecentre-frequency continuum, and 526 presenta-tions on the rate-of-modulation continuum .Approximately half of the presentations oneach continuum were synthesized closed mouthtrills . The remaining stimulus presentations weredistributed approximately equally over thevariant sounds .

Differences between response rates to stimuliwere evaluated in comparison to both the closedmouth trill and the null stimulus conditionsusing the test for significance between proportionsdescribed by Ferguson (1959) .

ResultsThe antiphonal response of the pygmy

marmosets to variations in the duration of thetrill stimulus are presented in Fig . 6 . In this andsubsequent figures per cent response refers tothe proportion of trials with a stimulus where anantiphonal closed mouth trill was produced by amarmoset within 5 s of the presentation of thesynthesized stimulus. The 0 . 176-s point repre-sents the response to the synthesized closedmouth trill ; the 0 . 338-s point represents theresponse to the open mouth trill duration .

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ANIMAL BEHAVIOUR, 26, 1

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Fig. 6 . Responses of pygmy marmosets to trills varyingin duration . In this and subsequent figures CMT repre-sents the response to a closed mouth trill and null repre-sents the response when no auditory stimulus waspresented . Per cent response refers to the proportion ofstimulus presentations which were followed by amarmoset emitting a closed mouth trill within 5 s of thestimulus .

The responses to 0 .208, 0 .241 and 0 .249-sstimuli did not differ significantly from theresponse to the synthesized closed mouth trill,and each differed significantly from the nullstimulus (P's < 0 .05). All subsequent stimuliwere responded to significantly less frequently(P's < 0 .001) than the closed mouth trill, butthese responses did not differ significantly fromthe response to the null stimulus . Note thesignificant difference in response rate thatoccurred when the stimulus was lengthened byonly 0 .008 s from 0 .249 to 0 .257 s .

The antiphonal response of the marmosets tovariations in the frequency range of the stimulusare shown in Fig . 7. The closed mouth trill isrepresented by the 7 .4 to 11 .4-kHz range andthe quiet trill represented by the 8 .9 to 9 .9-kHzrange. Three of the variations (7 .0 to 11 . 8,7 .6 to 11 .2, and 8 .9 to 9 .9, quiet trill) were notresponded to differently from the closed mouthtrill, whereas each of them was responded tosignificantly more than the null stimulus(P's < 0 .001). The remaining two variants(5 .7 to 13 . 1 and 8 .0 to 10 .8 kHz) were respondedto significantly less frequently than the closedmouth trill (P's < 0 .05) and did not differ inresponse level from the null stimulus. Notethat the synthesized quiet trill was responded toas frequently as the synthesized closed mouth trill,but that the intermediate stimulus (8 .0 to 10 .8kHz) was not responded to significantly morethan the null stimulus .

The antiphonal responses of the marmosetsto alterations in the centre-frequency are shownin Fig. 8 . Four of the variants (9, 10, 11 and 12

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Fig . 7 . Responses of pygmy marmosets to synthesizedtrills varying in frequency range . The 8 . 9 to 9 . 9 kHz isequivalent to the quiet trill .

kHz) were responded to at the same rate as thesynthesized closed mouth trill, and each of themelicited significantly greater responses than thenull stimulus (P < 0.001). The response to the7-kHz stimulus did not differ from that to thenull stimulus and was significantly less than theresponse to the CMT (P < 0 .001). The responseto the 8-kHz stimulus was intermediate differingsignificantly both from response to the closedmouth trill (P < 0 .05) and from the response tothe null stimulus (P < 0 .01). All centre fre-quencies 9 kHz and above were responded to asequivalent to the closed mouth trill .

The antiphonal responses to variations inrate of frequency modulation are shown in Fig .9. The responses to both the 20 and 30 Hzstimuli did not differ from the response to theclosed mouth trill (36 Hz) and were significantlygreater than the response to the null stimulus(P's < 0 .001). The two extreme variants (15and 45 Hz) were responded to significantly lessthan the closed mouth trill (P's < 0 .001)and not significantly different from the responseto the null stimulus . The response to 25 Hzwas intermediate differing both from theresponse to the closed mouth trill (P < 0 .001)and to the null stimulus (P < 0 . 05) .

DiscussionThe response patterns of the pygmy marmosets

to synthesized variations of their natural callsindicated that they tolerate a relatively widevariation in the signal before ceasing to respond .In this the responses of pygmy marmosets aresimilar to those of white-throated sparrowsstudied by Falls (1963, 1969) . However, despitethis tolerance of variation in signals, the pygmy

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Fig. 8. Responses of pygmy marmosets to synthesizedtrills varying in centre frequency.

marmoset responses appeared to reflect strictunderlying perceptual boundaries . The moststriking example of such a boundary appearedon the duration continuum where an increaseof only 8 ms produced a change in responselevels from one that was no different from theresponse to closed mouth trills to one that didnot differ from the response to a null stimulus .A similar perceptual boundary appeared whenthe frequency range was varied. A stimulussimilar to the quiet trill elicited responses thatdid not differ from those to the closed mouthtrill, but a stimulus intermediate between thetwo trills elicited responses that did not differfrom those to a null stimulus .

On the other hand, some acoustic dimensionsshowed no sharp boundaries between stimuli .All centre frequencies above 9 kHz wereresponded to equally. The adult closed mouthtrill centre frequency has a mean of 9 .4 kHz .Younger, smaller animals with smaller vocalcords would produce calls with correspondinglyhigher frequencies. Since growth to adult sizeis a continuous process, one might expect to finda continuity in the lowering of centre frequencyand, correspondingly, a continuity in theresponse to trills with centre frequencies thatare greater than the typical adult centre fre-quency.

Amplitude was the one acoustic variable notmanipulated in the study. We found no evidenceof amplitude modulation in the trills, and itseemed that absolute amplitude levels whichwould vary as a function of the distance betweenthe caller and recipient and the density of inter-vening sound attenuating features would not beuseful in distinguishing between calls .

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Fig. 9. Responses of pygmy marmosets to synthesizedtrills varying in modulating frequency.

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The pygmy marmosets responded equivalentlyto the stimuli that had been labelled as contextu-ally different: closed mouth trill, quiet trill, andjuvenile trill . While it was assumed that differentcontextual information was available in each ofthese calls, and although such information may,in fact, be utilized by the marmosets, a distinctionbetween these three calls was not reflected in theirbehavioural response . The similarity in responseto these three trills would seem to indicate thatthe function of each of these calls is similar .However, the marmosets did not respond tosyntheses approaching the duration parameterof the open mouth trill nor to extreme variationson other dimensions . Therefore, the playbacktechnique is useful in determining which distinc-tions made by human observers are behaviourallydistinguished by the animals using the signals .

It should be noted that the playback techniqueused here indicates only the animals' finalbehavioural response to a trill, a more or lessspontaneous or unconditioned response to asound. It is possible that the marmosets mightprove capable of making finer discriminationsbetween variants if pushed through the use ofoperant discrimination techniques or that finerdiscriminations would appear if an uncondi-tioned response such as a heart rate orientingresponse (see Morse & Snowdon 1975) wereused. Whether or not pygmy marmosets couldshow finer discriminations through more manipu-lative techniques, the present results indicate acategorization of stimuli at the level of aspontaneous behavioural response .

In general, for any social species there may bethree levels of information in a communicationsignal . The first level is the general message(after Smith 1965) which for the marmosets'trills would be described as `contact/location :'the animal either indicates a desire for contactwith others or indicates its location so thatsubsequent contact can be made with precision .The second level is specific contextual informa-tion, which for the marmosets would includewhether an animal is isolated from others,whether an animal is in visual as well as vocalcontact, or whether an animal is likely to engagein agonistic behaviour . The third level is indivi-dual identification : whether an animal is juvenileor adult, or which particular individual iscommunicating. Oddly enough, though indivi-dual identification and recognition has been wellstudied in birds (e .g . Beer 1970 ; Brooks & Falls1975a, b ; Falls & Brooks 1975) and in non-primate mammals (e.g. Patrinovitch 1974 ;


Epsmark 1975) individual recognition based onvocal cues has not been shown in a primatespecies. Marler & Hobbett (1975) have demon-strated acoustical individual differences inchimpanzee calls . Although they have notdemonstrated that chimpanzees can identifyeach other on the basis of these individualdifferences, it seems likely that individualrecognition based on vocal cues would occur inprimates, especially those species that relyheavily on vocal communication .An ideal communication system should be

efficient and precise. Efficiency would resultfrom a reduction of the number of separateproduction and reception mechanisms neededfor communication and could be accomplishedby the use of rather similar signals to communi-cate a general message . Possible adaptivefunctions of an efficient or limited repertoirehave been discussed by Smith (1969) . Precisionwould require that an animal be able to compre-hend all levels of signal information includingvariations due to individual differences andcontextual differences (in situations whereindividual and contextual differences are impor-tant) despite environmental degradation of thesignal . Broad tolerance of variation along anacoustic signal continuum with division of thecontinuum into discrete categories is onemeans by which both efficiency and precisioncould be obtained. The broad variability withina category allows for comprehension despiteindividual variability and environmental degrada-tion, while the sharp category boundariesallow the precise determination that a signal isassociated with one or another context and thushas a particular meaning.In summary, the pygmy marmosets did

respond to synthesized versions of their naturaltrill vocalizations and to a large number ofvariants of the natural vocalizations . Theyshowed both sharp boundaries between vocaliza-tions that indicated different contexts andequivalence of response to other vocalizationsthat seemed in our observations to have haddifferent contexts.Part 2 : Responses of Humans to Synthesized

Versions of Pygmy Marmoset VocalizationsIt is desirable to parallel the responses of thepygmy marmosets with those of humans fortwo reasons . The first relates to a verypractical problem in animal observation . Ourimpression of what animals do is processedthrough human perceptual systems which do notnecessarily correspond to the systems of the


animals under observation . This has been arecognized problem with respect to communi-cation systems using modalities such as odour,taste, electroreception and touch . It is alsoimportant to know whether species usingcommunication modalities used heavily byhumans (like audition) have perceptions similarto humans of stimuli on those modalities .

The second reason relates to investigation ofhuman speech perception . Liberman et al .(1967) have shown that there is an underlyingcontinuum of graded vocalizations in severaldimensions of human speech . However, humanadults do not perceive these stimuli as graded ;instead they perceive them in discrete categories .Human infants (Eimas et al . 1971) also show acategorical perception of adult speech sounds .This has led to speculations that categoricalperception of speech is a strictly human pheno-menon with possible specific neurologicalfeature detectors for the perception of speechsounds (Eimas & Corbit 1973 ; Stevens 1973) .

As an extension of this human-specificityhypothesis several recent studies have presentedhuman speech stimuli to non-human specieswith the expectation that the categorical respon-ding of humans to their own speech stimuliwould not appear. The results have beensomewhat equivocal . Morse & Snowdon (1975)working with rhesus macaques, and Sinnott(1974) with three species of Old World monkeys,found some evidence that monkeys perceivedthe human speech sounds (/ba/, /da/, and /ga/)in a different manner from humans, thoughthere were some clear similarities in perception .Kuhl & Miller (1975) working with chinchillas,and Waters & Wilson (1976) with rhesusmacaques, found that the perception of /da-ta/,/ba-pa/, and /ga-ka/ was not different from thatof humans .

The results from the playback experimentswith pygmy marmosets revealed responses totheir own synthesized vocalizations that wereanalogous to responses from humans respondingto synthesized versions of speech . That is, therewas a rather broad tolerance of variation in thesignal with sharp boundaries between func-tionally different stimuli in both species . Humanresponses to synthesized pygmy marmosetvocalizations should reveal whether there aredifferences in human versus marmoset responsesto marmoset vocalizations that might be ofimportance for human observers, and whetherhumans show a categorical perception of mar-moset stimuli .

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However, there are difficulties in testingmembers of one species with the sounds ofanother. Pygmy marmosets are obviously morefamiliar with their own sounds than any humanwould be. To try to circumvent this problemwe tested humans with three separate techniques,each placing slightly different demands on thesubject in terms of familiarity with and memoryfor normal marmoset vocalizations. One tech-nique was analogous to the technique used intesting pygmy marmosets. Humans heardexamples of the closed mouth trill and thenlabelled whether subsequent sounds they heardwere the same as or different from the closedmouth trill . The second technique was analogousto that used by Liberman et al . (1967) to studyhuman speech perception . Two sounds werepresented that were always different from eachother; then a third sound presented which wasidentical to either the first or second sound .Humans matched the third sound with one ofthe first two. The final technique tested only theduration continuum. Humans heard examples ofboth types of trills and then indicated whether agiven intermediate sounded more like a closedmouth trill or more like an open mouth trill .This technique is analogous to that used byWaters & Wilson (1976) on rhesus monkeysand Kuhl & Miller (1975) on chinchillas.

MethodSubjects. The subjects were eight volunteer

undergraduate students at the University ofWisconsin, Madison .

Procedure . The stimuli were generated by thesynthesizing equipment as described above andwere recorded on a Uher 4200 tape recorderat 19 cm per second . The subjects were seated in asound attenuated room facing the speaker . Theoutput from the tape recorder was amplifiedand played back through the same amplifierand speaker type used in the marmoset study .The synthesized closed mouth trill was used as astandard stimulus in all three tasks .

Labelling. The subject heard five closed mouthtrills with a 1-s inter-stimulus interval . Thesetraining stimuli were followed by a 2-s pause andthen a series of 10 test sounds presented witha 1-s interval between each sound . The subjectwas asked to indicate whether the test soundheard was identical to the closed mouth trillor not . There was a 5-s break after every blockof five CMT and 10 test stimuli . Test stimuliwere grouped on one dimension for three trial

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blocks; thus, there would be a total of 30duration test stimuli before another dimensionwould be presented . Both the sequences ofdimensions and the order of test stimuluspresentation within a test block were determinedfrom a table of random numbers. As with thetest for the marmosets, there was a presentationof one closed mouth trill for each presentationof a variant stimulus . The test was continueduntil each subject had heard 30 presentations ofeach of the 21 variants of the closed mouth trill .

Discrimination. The subject heard three stimuliin succession each separated by a 1-s inter-stimulus interval . The first two stimuli alwaysdiffered from each other (A and B) and the thirdstimulus was always identical to either the firstor second stimulus . The subjects discriminatedwhich of the first two stimuli sounded closestto the third stimulus . One of the stimuli wasalways the closed mouth trill, and the remainingstimulus was one of the 21 variants used previ-ously. A 5-s interval separated each trial ofstimuli and a 10-s break occurred after every 10trials . The triads were arranged in every possiblecombination (i .e . ABA, ABB, BAB, and BAA)and the order of presentation of particular triadswas determined from a table of random numbers .The subjects completed 12 trials with eachstimulus variant a day, for 3 days for a total of36 responses to each stimulus triad .

Identification. Because the sharpest responsecategorization by the pygmy marmosets occurredon the duration dimension, this dimension wasselected for testing with human subjects . Onthis test three additional duration stimulibetween 241 and 273 ms were added . The sub-jects heard five synthesized closed mouth trillsfollowed by five synthesized open mouth trillsat the beginning of each block . Then they heardeach of 10 test stimuli separated by a 1-s inter-stimulus interval and identified each stimulusas a closed mouth or as an open mouth trill .After each block of 10 test trials, five trainingpresentations each of closed and open mouthtrills again preceded the next block . Stimuliwere presented randomly on the test trials .Testing continued until a subject identified eachof the nine different duration stimuli a total of60 times each . One subject failed to participateon this task .Data analyses . The mean response was

computed for each subject on each test stimulusfor each task . In the labelling task the percentageof times that a stimulus variant was labelledas a closed mouth trill was compared with the

percentage of correct labelling of the closedmouth trill itself using a correlated samplest-test. In the discrimination task the number oferrors made when each stimulus was tested in atrial with a closed mouth trill was comparedagainst chance performance (50 % errors). Inthe identification task the percentage identifica-tion of a stimulus as a closed mouth trill wascompared with the percentage identification ofimmediately adjacent stimuli as closed mouthtrills . A correlated samples t-test was used forthis analysis. This provides a means of testingcontinuous perception of the stimulus continuumversus categorical perception . All probabilityvalues reported are two-tailed .Results

Duration . Figure 10 shows the results of thelabelling and discrimination tasks for theduration continuum, On the labelling task eachduration variant was labelled significantlydifferently from the closed mouth trill stimulus(P's < 0 . 01) whereas in the discrimination taskall stimuli of 241 ms or greater duration werediscriminated from the closed mouth trill(P's < 0 .01). Figure 11 compares the identi-fication data of the human subjects with theresponse function of the marmosets. The resultsof the human identification task indicated thateach stimulus was identified as a closed mouthtrill significantly less frequently (P's < 0 . 05)than stimuli of shorter duration with two excep-tions. There was no difference between theresponses to 241 and 249 ms and no differencebetween responses to 265 and 273 ms. Thuswith these minor exceptions the human responsepattern was to respond to changes in the duration

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Fig . 10 . Responses of humans on labelling and dis-crimination tasks to synthesized trills varying in duration .Vertical lines represent ± 1 standard error of the mean(S .C .M .).

function in a continuous rather than categoricalfashion. The marmosets, on the other hand,showed a clear categorizing of the durationcontinuum. The humans also made finer dis-criminations and labellings of stimuli on theduration continuum than did the marmosets .

Frequency range. Figure 12 presents the resultsof labelling and discrimination on the frequencyrange continuum. In the labelling task eachvariant was labelled as significantly differentfrom closed mouth trills (P's < 0 .01). In thediscrimination task the response to the 7 .0 to11 .8-kHz range was not different from chanceperformance but all other discriminations weresignificantly different from chance (P's < 0 .05) .Note that the humans had no difficulty witheither task in discriminating the 8 .9 to 9 .9-kHzstimulus from the closed mouth trill. Thisstimulus mimics the quiet trill which the marmo-sets in their responses treated as equivalent tothe closed mouth trill .

Centre frequency . Figure 13 presents thelabelling and discrimination results for thecentre frequency dimension. In the labelling taskeach variant stimulus was labelled as a closedmouth trill significantly less frequently than theclosed mouth trill itself (P's < 0 .01). In thediscrimination task each stimulus except the9-kHz stimulus was discriminated from theclosed mouth trill at better than chance level(P's < 0 .05) . Again the human responsesdiffered from those of the pygmy marmosetsthat did not discriminate at all between stimuliwith centre frequencies of 9 kHz or greater .

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Fig. 11. Responses of humans on identification taskcompared with responses of pygmy marmosets tosynthesized trills varying in duration . Vertical linesrepresent ± 1 s .e.m .

Rate of Modulation. Figure 14 presents thelabelling and discrimination results for the rateof modulation dimension . In the labelling taskall stimuli except that of '45 Hz were treated asdifferent from the closed mouth trill (P's < 0 .05) .However, in the discrimination task only thestimuli at 15 and 20 Hz were discriminatedfrom the closed mouth trill at better than chancelevels (P's < 0 .02). On this dimension alonethe humans demonstrated a response patternsimilar to that shown by the marmosets . Evenhere there was a difference in response betweenthe two species . The marmosets did respond tothe 45-Hz variant as different from the 36 Hzof the closed mouth trill, whereas the humansdid not.

DiscussionThese experimental results indicate that the

responses of humans and pygmy marmosets arequite different with respect to pygmy marmosetvocalizations . The human listeners made finerdistinctions between variant vocalizations, andthey showed a continuous differentiation ofsounds along the duration continuum ratherthan the categorical responses that the marmosetsdid . This is not to say that marmosetscannot make as fine a discrimination betweensounds as humans do. But if they do make finerdiscriminations, this is not indicated in theirbehavioural responses .

These results are analogous to the findingsof Morse & Snowdon (1975) and Sinnott (1974)who found evidence that monkeys perceivedhuman speech sounds in a continuous fashionrather than a categorical fashion . Therefore,

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Fig . 12. Responses of humans on labelling and dis-crimination tasks to synthesized trills varying in frequencyrange. Vertical lines represent + 1 s.e.m.

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although a process of categorical perception ofvocalizations might exist in many species, thosesounds that are perceived categorically mightwell be specific to the animals using them forcommunication. These results also emphasizethe problems with equating human and animalperceptual systems . Humans appeared to makefiner discriminations among marmoset vocaliza-tions than the marmosets themselves, at leastas shown by the techniques used here . Therefore,there is a risk of possibly over-distinguishing thevocalizations of another species, just as a rhesusmonkey listening to human speech sounds mightmake overly fine distinctions of our vocalizations .

General DiscussionMarler (1975) has proposed a hypotheticalstructure for the possible evolution of humanspeech. He argued for a progression throughprimate orders : from New World species, whichshow relatively stereotyped discrete vocaliza-tions ; through Old World species and apes,which display a large number of intergradedvocalizations ; to humans, where the inter-graded vocalizations are sorted into discretecategories .

However, Eisenberg (1976) has presented dataindicating rather extensive gradation in thevocalizations of the black spider monkey(Ateles fusciceps robustus) a New World species,and the data presented in Table I here indicatesthat there are intergradations between some ofthe trill-types in pygmy marmosets. In additionthe present results indicate that the pygmymarmoset shows categorical responses to itsown vocalization . The gradation of vocaliza-

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Fig. 13 . Responses of humans on labelling and dis-crimination tasks to synthesized trills varying in centrefrequency . Vertical lines represent ± I s .e .m .

tions in New World primates and the categoricalresponding to these vocalizations in the pygmymarmosets run counter to Marler's hypothesis.Earlier we advanced the notion that categoricalperception of some sounds used in communi-cation might be adaptive to many speciesbesides humans .

The distinction between graded versus discretevocalizations in primate communication mayresult from the imposition of a human per-ceptual system on the auditory or sonagraphdisplay of sounds of another species . As we haveshown here, variations in duration that humansubjects perceived as continuous (graded) weretreated by the pygmy marmosets as categorical(discrete). Therefore, a final determination ofwhether a particular set of vocalizations areresponded to by a species as continuous orcategorical must depend upon either somecorrelation of contextual differences and subse-quent behaviour with vocalization variants asGreen (1975) has done with Japanese macaques,or the sort of playback testing described here .There remains the possibility that other

primate vocalizations could be graded, with thecontact/location calls that both Green (1975)and the present study have focused on repres-enting a special case . The graded vocalizationsthat have been described in conjunction withagonistic behaviour (Rowell 1962) are likely tobe truly graded from the viewpoint of the animal .With these agonistic graded vocalizations, themessage appears to be the relative probabilityof aggression or fleeing . Since probabilitiesrepresent a continuous function, it seemspossible that the vocalizations that conveythese probabilities also represent a continuousfunction .

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Fig. 14. Responses of humans on labelling and dis-crimination tasks to synthesized trills varying in modula-ting frequency. Vertical lines represent ± 1 s .e .m .


These experiments have shown that playbackstudies on primates are feasible so long as everyprecaution is taken to make the playbacksituation as natural as possible . Speakers andother equipment must be hidden from theanimals ; the sounds must emanate from alocation where an animal is likely to be situatednormally ; a given location for a speaker mustbe used infrequently and for only a few conse-cutive trials ; the testing must be carried outover a long period of time so that habituationis minimized ; and finally the testing must becarried out within the context of as normal asocial environment as possible . The largenumber of trials needed by Symmes & Newman(1974) to obtain discrimination of isolationpeep variants in squirrel monkeys could be dueas much to the unnaturalness of their shockavoidance task as to any difficulty in actualdiscrimination. Additionally, their animals mayhave made somewhat finer distinctions betweenvariants than they might ordinarily have made inthe context of normal social interactions .

The playback technique developed here canbe used in studying additional calls of the pygmymarmoset where calls with similar acousticshave different contexts and functions . Thetechnique could also be used to determine whatcues characterize individual recognition basedon vocalization by synthesizing calls specificto a given individual and monitoring whetherother animals respond more or respond in adifferent way to familiar individuals than tounfamiliar individuals. Brooks & Falls (1975b)have shown that the broad range of variabilityin song to which white-throated sparrowsrespond in general becomes much more limitedwith respect to the response to songs of particularneighbours. Finally this playback techniquecan be extended to study the communication ofadditional mammalian species . Categoricalresponding to vocalizations may not be afunction of phylogenetic status as Marlerproposed but of ecological adaptations . Itwould be important to test species from differenthabitats that show differing degrees of emphasison vocal communication to see whether categor-izing is primarily found in the most vocal species .

AcknowledgmentsThis is publication 17-24 of the WisconsinRegional Primate Research Center . The workwith the pygmy marmosets and the developmentof the synthesis techniques was supported byU.S.P.H.S. Grant MH 24,999. We are grateful

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to Philip A . Morse for his suggestions about thedesign of the experiments with humans, toRobyn A. Lillehei for her assistance in prepar-ing the stimulus tapes and testing the humansubjects and to Alexandra Hodun and ThelmaRowell for their comments on the manuscript .

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Falls, J. B . 1963. Properties of bird song eliciting res-sponses from territorial males . Proceedings of theXIII International Ornithological Congress, pp .259-271 .

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ANIMAL

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Sinnott, J. M. 1974 . A comparison of speech sounddiscrimination in humans and monkeys. Unpub-lished Ph .D. dissertation, University of Michigan,Ann Arbor .

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(Received 4 June 1976 ; revised 19 October 1976 ;MS. number : A1876)

Documents

Interspecific and intraspecific responses to synthesized pygmy marmoset vocalizations