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Roian Egnor, Cory Miller & Marc Hauser

S.E. Roian Egnor, Harvard University, 33 Kirkland St., Cambridge, MA 02138Cory Miller, Dept of Biomedical Engineering, Johns Hopkins University School ofMedicine, 720 Rutland Ave. Baltimore, MD 21202Marc D. Hauser, Harvard University, 33 Kirkland St., Cambridge, MA 02138

Abstract.Nonhuman primates produce a large number of communicative signals, especiallyin the auditory channel, and these calls function in a wide range of contextsincluding mating, alarm, food discovery, affiliative social relationships, andaggressive competition. In this chapter, we explore the information encoded inthese signals and the perceptual decoding of and response to the signal. Anunderstanding of primate signal design, in combination with studies of signalperception, reveal an exceptionally rich communicative repertoire, while pointingthe way to future questions concerning the mechanisms underlying callproduction and categorization.

IntroductionAll primates live in social groups. Some,like orangutans, live a largely solitarylife, but come together for mating,aggressive competition, and offspringcare. Others, such as chimpanzees, livein large communities, but on a day today basis exist in small ephemeralparties. Independent of group size andcomposition, monkeys and apes engagein a wide variety of social and non-socialactivities including the discovery of food,the detection of predators, inter-groupencounters, group movement, play,grooming, aggressive at tacks,coalitions, submissive retreats, andreconciliatory actions designed toredress imbalances in a relationship. Inprinciple, one can readily imagine theadaptive significance of a signalingsystem capable of informing others ofthese various activities. Of particular usewould be a vocal system designed toconvey such information in the absenceof any other contextual information.Such a system would enable Monkey Ato inform Monkey B of the location,movement and type of predator, andmonkey B would be able to decode thisinformation and more, including the factthat monkey A is a member of the samespecies, same group, is high rankingand male. This hypothesis aboutadaptive design is only partly accurate.Nonhuman primates do producevocalizations in a variety of contexts,and listeners do extract considerableinformation from the signal. But thereare significant constraints on the kind ofinformation conveyed and the kind ofinformation extracted. Theseconstraints are both internal (peripheraland central processing mechanisms)and external (habitat, climate, distanceto receivers, competing acousticsignals) to the animals themselves.

Students of animal behavior have longargued over the proper definition ofcommunication (Hauser, 1996; Bradburyand Vehrencamp, 1998; Owings andMorton, 1998). Early theories, centeredprimarily in classical ethology, focusedon the veridical transmission ofinformation from sender to receiver. Onevariant of this view borrowed fromengineering, and in particular Shannon-W e a v e r i n f o r m a t i o n t h e o r y .Communication was said to occur if areceiver’s uncertainty about an eventwas reduced by the informationtransmitted in the sender’s signal. Criticsof this information perspective emergedwith the sociobiology revolution.Dawkins and Krebs (1978) argued that averidical signaling system was invadableby a mutant who generated the samesignal but with a different, and deceptivemotivation. Thus, for example, if anaggressive signal was designed toconvey information about the probabilityof escalating aggression, then a mutantwho always signaled the highest level ofaggressive intent, but was bluffing,would always win because receiverswould readily back down. Thus, soDawkins and Krebs originally argued,the adaptive function of communicationis for signalers to manipulate thebehavior of receivers. This view wasquickly criticized for being signaler-centric. Dawkins and Krebs respondedby modifying their original model toinclude both manipulative signalers andskept ica l rece ivers . Thus ,communication evolves as an arms racein which selection favors signalsdesigned to manipulate the behavior ofreceivers for fitness gains, and counter-selection favors receivers thatdistinguish between truths and lies.

Riding along with this selfish-geneperspective was Zahavi’s (Zahavi, 1975)handicap principle, often interpreted asa specific explanation for matingbehavior, but originally proposed as ageneral theory of signaling. For Zahavi,signals provide veridical informationabout the signaler if, and only if, thereare costs to signaling relative to currentcondition, and the capacity to generatesuch cost-bearing signals is heritable.Although there have been severalempirical examples supporting Zahavi’sintuition (e.g., stotting in gazelles,courtship displays in several birdspecies), it is also clear that honesty canemerge in the absence of significantcosts. For example, a series of studiesby Fitch and colleagues indicate thatphysical constraints anchor honesty inthe absence of costs (e.g., the length ofthe vocal tract correlates with body sizewhich provides, via formant frequencydispersion, an honest indicator of size(Fitch, 1997).

All of these definitions of communicationhave pros and cons, and most side stepthe cognitive mechanisms underlyingboth the production and perception ofcommunicative signals. For purposes ofexposition, we borrow from thesedifferent definitions and focus on whatwe see as the most empirically tractableaspects: the information encoded in thesignal, the transmission medium, andthe perceptual decoding of andresponse to the signal (Fig 1).

Figure 1. The basic structure ofcommunication systems. Shown are thefour central elements that comprisecommunication: the sender emits a signalthat travels through a medium to a receiver.Shown is a vocal communication in whichthe signal is a vocalization and the mediumis a forested environment.

In the present manuscript, we focus ourdiscussion on communication innonhuman primates (see chapters ofthis volume for similar discussions ofother taxonomic groups). We focus onvocal communication because there hasbeen considerably more progress forthis sensory channel in primates than forall others. This is largely due to the factthat the analytical techniques foranalyzing the signal and testing itsperceptual significance in primates arefar more sophisticated than for thevisual, tactile or olfactory channels. Webegin with a discussion of call context,focusing on three functional problems:food, sex, and anti-predator alarm. Wethen focus on the potential for signalersto convey information about individual,sex, and group identity, and the capacityfor receivers to decode this information.We end this chapter with a discussion ofsome pressing gaps in ourunderstanding and the need to developnew analytic tools and comparative datasets.

Call Context

Primates produce an astonishing arrayof vocalizations—from the simple, tonalphees of the common marmoset (Fig2,a), to the spectrotemporally complexsyllable sequences of the chimpanzeepant hoot (Fig 2,b), to the movingformants found in rhesus monkeygirneys (Fig 2,c). There is enormousvariability in the spectrotemporalstructure of different call types within

species and in the acoustic properties ofparticular calls within and betweenindividuals. These observations raisetwo questions: to what extent is thevariabil ity in signal morphologybehaviorally relevant and how shall wego about quantifying call morphology?One method is to chart the associationbetween social and ecological situations

Figure 2. Spectrograms show inter-speciesvariation in the acoustic structure of primatevocalizations. For each spectrogram, the X-axis shows time and the Y-axis showsfrequency. Depicted are a) chimpanzee panthoot, b) common marmoset phee, and c)rhesus monkey girney.

and call morphology. More recent workhas extended these earlier findings toexplore the possibility that, like humanwords, primate vocalizations have thecapacity to pick out salient objects andevents in the environment, and conveythis information to listeners. We focushere on functional aspects of thesecalls, leaving aside discussion of theircognitive substrates.

FoodMany primates produce distinct callswhen discovering or eating food. Callrate appears to correlate with hunger inrhesus macaques (Macaca mulatta),with food preference in cotton-toptamarins (Saguinus oedipus), withamount of food and location in toquemacaques (M. sinica), and with amount

of food and whether that food is divisiblein chimpanzees (Pan troglodytes). Inaddition, distinct vocalizations for lowquality/common and high quality/rarefoods have been observed in rhesusmacaques (Hauser, 1996).

Rhesus macaques not only produceacoustically distinct vocalizations for lowand high quality food items, they alsoappear to recognize these categories.In a habi tuat ion-discr iminat ionexperiment (Hauser, 1996), habituationwas shown to transfer between two highquality food call types (‘warbles’ and‘harmonic arches’) despite the fact thatthey are acoustically distinctive; thissuggests that both calls are classified asfalling within the same functionalcategory. Information in rhesus foodcalls was shown to be relevant toconspecifics in another context as well(Hauser, 1996). Experimentersobserved individual rhesus followingdiscovery of food. Discoverersproduced food calls 45% of the time.However, because of the density of thepopulation, other conspecifics detectedthe food discovery 90% of the time. Onaverage, vocal discoverers consumedmore food than silent discoverersbecause silent discoverers, whendetected, were often chased away fromthe food or aggressively attacked.Similar results have also been observedin white-faced capuchins (C e b u scapucinus) (Gros-Louis, 2004).

PredatorsMany primates produce alarm calls inresponse to predators. Several species,including Barbary macaques (M.sylvanus), chacma baboons (Papiohamadryas), ring-tailed lemurs (Lemurcatta), redfronted lemurs (Eu lemurfu lvus rufus ), Verraux’s sifakas(Propithecus verreauxi verreauxi), Dianamonkeys (Cercopithecus diana), and

most famously, vervet monkeys (C.aethiops) (Cheney and Seyfarth, 1990),produce acoustically distinctive alarmcalls to different predators. Vervetsliving in Amboseli National Park, Kenya,produce acoustically distinctive alarmcalls to large felines (leopards, etc; Fig3,a), large raptors (martial eagles andcrowned eagles; Fig 3, b), snakes(pythons and mambas; Fig 3, c),baboons, and some humans (e.g., theMaasai who occasionally hunt orthreaten them). What information istransmitted in these signals? Twocriteria must be met for an alarmvocalization to transmit information

Figure 3. Spectrograms of the three majorvervet monkey alarm vocalizations. For eachspectrogram, the X-axis shows time and theY-axis shows frequency. Shown are thespecies-typical alarm calls produced inresponse to a) leopards, b) eagles and c)snakes.

about a specific predator as opposed topredators or fearful stimuli moregenerally: 1) the vocalization must beevoked by the presence of the specificpredator, and not by any other stimuliand 2) playback of the vocalizationalone must be sufficient to produce thesame response as the presence of thepredator. If these two criteria are met,the alarm call is considered ‘functionallyreferential’ (Marler, et al., 1992), that is,

it functions as if it conveys informationregarding a specific predator. Studieson vervet monkeys, ring-tailed lemursand Diana monkeys provide evidencefor functionally referential alarm calls.We focus here on the Diana monkey asthis work has included some of the mostdetailed perceptual experiments to date.

Diana monkeys live in small single male,multi-female groups. Female Dianamonkeys produce eagle alarm calls inresponse to playbacks of both crownedeagle shrieks and male Diana monkeyeagle alarm calls and produce leopardalarm calls to playbacks of both leopardgrowls and male leopard alarm calls(Zuberbuhler, et al., 1997). Becausemale alarm calls and the calls of thepredator that elicits them areacoustically distinct, the commonality inthe females’ response suggests thatwhat is driving the response is thecommonality of referent. Furtherevidence for this comes from an elegantpriming study in which responses to theacoustic and referential features of thecalls were assessed (Zuberbuhler, et al.,1999). In the study, a priming stimuluswas presented, followed five minuteslater by a probe stimulus (see Figure 4).The prime-probe pairs fell into threecategories: the baseline condition, inwhich the prime and the probe wereidentical (e.g. both leopard growls), atest condition, in which the prime andthe probe differed in acoustic structurebut had identical referents (e.g. a maleleopard alarm call followed by a leopardgrowl), and a control condition in whichthe prime and the probe differed in bothacoustic structure and referent (e.g. amale leopard alarm call followed by aneagle shriek). In the baseline conditionfemales produced significantly feweralarm calls to the probe than to theprime while in the control conditionfemales responded strongly to both the

probe and the prime. Habituationtherefore occurs when prime and probeshare both referential and acousticfeatures, and does not occur when theyshare neither referential nor acousticfeatures. The response of females tothe test condition, in which prime andprobe share referential but not acousticfeatures, was similar to that in thebaseline condition: females producedsignificantly fewer alarm calls to theprobe than to the prime, suggesting thatthey were attending to the referentialfeatures of the probe.

MatingA wide variety of primates producevocalizations in the context of mating.These vocalizations are typicallyreferred to as copulation calls, and areproduced immediately before, during orfollowing copulation. In some species itis the male who produces copulationcalls, in other species the female emitsthe vocalizations, and in a handful ofspecies both sexes produce copulationcalls (Hauser, 1996). Because of thevariability in the vocal behaviorsurrounding copulation calls, thefunctional significance of this class ofvocalizations has been difficult toascertain. However, some similaritiesexist between species that suggestthese calls are likely to play a role inmating behavior. For example,copulation calls are acousticallydistinctive within the repertoire, carryinformation about individual identity, andare often produced at high intensities.These properties enable groupmembers to identify and localize thecaller, as well as the context. Althoughcopulation calls have been investigatedin a wide range of species, including OldWorld monkeys and apes, the mostdetailed work concerning the function of

these calls comes from studies ofBarbary macaques.

Figure 4. Outline of the experimental designused in Zuberbuhler et al. 1999. Thisexperiment consists of two trials(prime/probe) for each of the three testconditions (baseline/test/control). For theseexperiments, the prime stimulus waspresented first, followed by the probestimulus. The logic here is that if theinformation provided to the subjects issimilar in both the prime and probe trials,then subjects should show a response to theprime stimulus, but not the probe stimulus.If, however, the information is different,subjects should show similar levels ofresponse in both trials.

Barbary macaques live in social groupsconsisting of multiple males andfemales. Their mating system istypically classified as polygynous, withboth males and females mating withmultiple individuals. During copulation,females produce acoustically distinctcopulation calls. Because these callscan be heard from several meters away,it was proposed that they could functionto incite competition between males(Hamilton and Arrowood, 1978). Suchcompetition could occur either throughdirect male-male competition, with thewinner of a fight gaining access to afemale, or through sperm competitionfrom mating with multiple males in a

Prime Probe

Eagleshriek

EagleshriekBaseline

Leopardgrowl

Leopardgrowl

Eaglealarmcall

EagleshriekTest

Leopardalarmcall

Leopardgrowl

Leopardalarmcall

EagleshriekControl

Eaglealarmcall

Leopardgrowl

short period of time. To address thisissue, Semple (Semple, 1998)conducted a series of field playbackexperiments. Results indicated thatmales were more likely to approachfemales following the playback of hercopulation call relative to controlssuggesting that copulation callsfunctioned to alert males that she wascurrently in estrous. Further, when twomales were in the vicinity of theplayback, only the more dominant maleapproached. These data providedevidence for both types of competitionbecause although males were drawn tofemales after hearing her copulationcalls (potentially leading to increasedsperm competition), dominant malesgained greater access to these femalesthan lower ranking males (consistentwith male-male competition). Furtherexperiments showed that the Barbarymacaque copulation calling systemconsisted of another layer of complexity.Analyses showed that copulation callsproduced during peak estrous wereacoustically distinct from those callsproduced early in the estrous cycle(Semple and McComb, 2000).Following this analysis, Semple andMcComb conducted a playbackexperiment in which peak estrous andearly estrous copulation calls werebroadcast to males. Results revealedthat male subjects were more likely toapproach females following playback ofcalls produced during peak estrous thanthose produced early in the estrouscycle, thus confirming that the acousticdifferences between calls produced atthese two periods of estrous were bothperceptible and meaningful to malemacaques. Overall, these data provideevidence that the Barbary macaquecopulation call is a salient acoustic cuethat plays a significant role inmodulating male mating behavior.

Caller Identity

In this section, we focus on three layersor levels of identity: individual, sex, andgroup. Major research questions in thisarea are 1) what are the necessary andsufficient acoustic features associatedwith an individual’s acoustic signature,and 2) to what extent do listenersrecognize specific individuals, their sex,or their group identity based onparticular features of the signal?

IndividualIt has long been known that individualidentification based on an acousticsignal is technically possible—in thesame way that genetics andenvironment combine to produceindividually distinctive faces, allindividuals have individually distinctivevoices. However, whether a conspecificcan identify an individual based purelyon a vocal signal depends on severalfactors. One important factor is purelyperceptual: the listener’s auditorysystem simply may not be sensitiveenough to detect the individualdistinctiveness in a vocalization.Another factor is the specific vocalsignal involved: just as somevocalizations appear to be designed tobe either difficult or easy to localize(Marler, 1955), vocalizations appear tovary in their degree of individualdistinctiveness. One candidate for theacoustic basis of individual recognitionin primate vocal signals is the spectralpatterning introduced by vocal tractfiltering. The spectral peaks introducedby the vocal tract have been shown tobe individually distinctive across twovery different calls (coos and grunts) inthe rhesus macaque (Rendall, et al.,1998). The vocal tract filteringhypothesis is supported by theobservation that screams, calls that donot display prominent vocal tract filtering

peaks, are also less individuallydistinctive in playback experiments.However, other experiments in rhesusand pigtail macaques (Gouzoules, et al.,1984; Gouzoules and Gouzoules, 1990)have found individual recognition withscreams, raising the possibility of adifferent, or at least an additional,acoustic substrate for individualrecognition. Another candidate forindividual recognition is the degree ofacoustic variability within and betweencalls (Fitch, et al., 2002).

Regardless of the specific substrate,there are many a priori reasons forthinking that primates would benefitfrom the ability to recognize the identityof a vocalizer: 1) many primates live indense cover and are often out of sight ofgroup members, 2) success in thesocial domain often depends on supportfrom conspecifics (particularly kin), and3) an acoustic signal is better suited toeliciting support from social partnersthan a visual signal because acousticsignals can travel in 360 degrees andover large distances. Individualrecognition by voice has been elegantlydemonstrated in vervet monkeys.

Vervet monkey females remain in theirnatal troupe while males emigrate.Each troupe, therefore, consists ofseveral groups of closely-relatedfemales. Alliances between close kinduring agonistic encounters arecommon and have repercussions interms of maintenance of dominancerank, access to scarce resources andreproductive success. When a juvenilevervet vocalizes during an agonisticencounter, its mother often intervenes tosupport her offspring. Cheney andSeyfarth (1980) took advantage of thisbehavior to test whether or not vervetfemales could recognize the vocalizationof an individual juvenile. They began by

locating three females whose juvenileoffspring were out of sight. They thenrecorded the behavior of the threefemales before and after playback of therecruitment scream of the juvenileoffspring of one of the females. Theyshowed that although all three femalesresponded to the playback by looking inthe direction of the concealed playbackspeaker, the mother of the juvenilewhose call had been played respondedwith a significantly shorter latency andlonger duration (Fig. 5) than did theother two, ‘control ’ , females.Interestingly, the control females werealso more likely to look at the motherafter playback. These two pieces ofdata together suggest that vervetfemales are able to recognize theindividual who produced a particularvocalization.

Figure 5. Bar graph showing results fromindividual recognition playback experimentsin vervet monkeys. In each playback,juvenile screams were played back to thejuvenile’s mother and two control femaleswho also had offspring. Results show thatmothers responded with a faster latency andwith longer looks than control females. They-axix plots responses in frames [18frames/second]. Redrawn from Cheney &Seyfarth (1980).

Similar abilities have been shown usinga variety of methodologies in yellowbaboons (P. cynocephalus), rhesusmacaques, Barbary macaques (where ithas been shown to emerge as early as10 weeks of age), pygmy marmosets(Cebuella pygmaea), chimpanzees,grey-cheeked mangabeys (Cercocebusalbigena), squirrel monkeys (Saimirisc iureus ) and cotton-top tamarins(Snowdon, 1986).

SexAs with many aspects of primatebehavior, sex differences exist inprimate vocal behavior. Sex differencesemerge both in the overt behaviorassociated with vocalizations, as well asthe acoustic structure of thevocalizations themselves. Producingvocalizations with sex differences maybe crucial for animals such as primatesthat must navigate complex socialsystems. Being able to determine anindividual’s sex without havingexperience with that individual is likely toprovide one with cues about how andwhether to interact with an animalbefore coming into physical or visualcontact with the individual. Although theacoustic differences between male andfemale primates are often reported, littleis known about the perceptual salienceand behavioral relevance of thisinformation.

Recently, researchers have begun toaddress this issue using differentexperimental techniques. In a study ofwild baboons, Rendall and colleagues(Rendall, et al., 2004) recorded grunts, aclose distance affiliative call. Acousticanalyses showed that the fundamentalfrequency and the first three formantfrequencies were lower in males thanfemales suggesting that these acousticdifferences could potentially be used to

determine the sex of a caller. To testthis possibility, Rendall and colleaguestrained captive baboons to discriminatebetween exemplars of male and femalegrunts in a psychophysical experiment.Results indicated that subjectssuccessfully discriminated betweengrunts produced by males and femalessuggesting that this could beaccomplished using the natural acousticdifferences present in the vocalizations.While these data show that the animalsare able to perceive a differencebetween male and female calls followingtraining, they do not address whetherthe animals are able to do this naturally.Evidence of spontaneous discriminationis critical for making arguments aboutwhether information about the caller’ssex is used in natural behavioralinteractions. This gap in ourunderstanding was recently addressedin a study of captive cotton-toptamarins.

Cotton-top tamarins produce a species-speci f ic vocal izat ion cal led acombination long call (CLC) whenseparated from group members. Thislong distance, multi-syllabic vocalizationtypically elicits antiphonal calls andapproach behavior from conspecifics.Acoustic analyses of CLCs showed thatmale calls consisted of significantlyshorter syllables than female calls. Totest the perceptual and behavioralsalience of these acoustic differences,Miller and colleagues (Miller, et al.,2 0 0 4 ) conducted a phonotaxisexperiment. In phonotaxis experiments,subjects are presented wi thvocalizations from two speakers situatedequidistant from subjects and scored forwhich speaker is approached first. Inthe first experiment, subjects werepresented with naturally producedexemplars of male and female CLCs.Subjects showed significant preference

to approach female CLCs suggestingthat they could discriminate between thesexes of the caller. When the syllabledurations were then manipulated to beidentical, subjects no longer showed thisbehavioral bias, suggesting that syllableduration is a critical feature in sexrecognition. Building on this result, asecond experiment tested whether thebasis for sex differences in CLCs wasdue to perceptual biases in signalreceivers. In this experiment, subjectswere first presented with CLCs fromanimals of the opposite sex in which thesyllable durations were manipulated tobe at the high and low end of thenaturally produced range. Resultsshowed that whereas males showed apreference for female calls with thelongest syllable durations, femalespreferred male calls with the shortestsyllable durations. When the syllabledurations were manipulated to beoutside the naturally produced range,this preference persisted suggestingthat sensory biases may imposeselective pressure on the structure ofCLCs.

Group membershipSimilarities in the spectrotemporalproperties of vocalizations withinprimate social groups have been shownin a variety of species: chimpanzees,Barbary macaques, pigtail macaques( M. nemestrina), rhesus macaques,cotton-top tamarins, and mouse lemurs(Microcebus murinus). These acousticsimilarities are called different things bydifferent authors: dialects, vocalsignatures or vocal accommodation(Fischer, 2002). However, they all mayserve the purpose of signaling currentgroup membership. This may beparticularly useful in species in whichgroup membership is relatively fluid, orin species, such as most of the OldWorld monkeys, in which there are

many different kin groups within a singletroupe.

A group level signature has been shownin the chimpanzee’s pant hoot. Thisvocalization, which consists of a anintroductory phase of long tonalsyllables, a build-up phase with shorterelements, a loud and high frequencyclimax phase and a short let downphase (See Fig 2, b), is a long distancevocalization used by males to maintaincontact between allies. Mitani andGros-Louis (Mitani and Gros-Louis,1998) recorded pant hoot chorusesbetween a variety of males in MahaleMountains National Park in Tanzania.They observed that the pant hoots ofmales that chorus together are moresimilar to each other than when they arechorusing with other males, providing apotential cue for current alliancemembership. Variation in pant hootstructure was also shown by Marshalland colleagues (Marshall, et al., 1999),who described the introduction of aspectrally distinct pant hoot syllable (the‘Bronx cheer’ or ‘raspberry’ variant) by asingle individual into a captive colony ofchimpanzees. Finally, Crockford andcolleagues (Crockford, et al., 2004),have observed variation in pant hootstructure between neighbor ingchimpanzee communities, but notbetween isolated communities. Theseauthors suggest that groups that arewithin acoustic contact actively modifytheir vocalizations to make themdist inct ive, al lowing communityallegiance to be detectable at adistance.

However, all studies on group-specificsignatures to date have beenobservational. It is still an openquestion whether these signatures aremeaningful to receivers, though it seemslikely, given that the tendency to

produce such signatures appears to bewidespread among pr imates .Demonstrating the salience of suchsignatures, however, will be challenging,as any discrimination based on a group-specific signature might also besupported by individual recognition. Itwill therefore be necessary to createsynthetic calls in which a signature atthe individual level is maintained, whilethe group level signature is manipulated.

Future directions

Primate senders can clearly transmit avariety of information to primatereceivers. This information can range,as we have discussed, from informationabout the sender’s location, size, or sex,to information about an external object,such as quality of food or predator type.In addition, other experiments haveshown that signalers can conveyinformation about dominance rank,degree of risk in an agonistic encounter,call bout termination and contact withanother conspecific group. Given therichness of information transfer, whatare the next steps in the study ofprimate vocal communication?

Initially primate vocal repertoires werecharacterized as either “discrete” or“graded”. Discrete vocal repertoirescontain calls whose spectrotemporalfeatures are distinct from one another,while graded systems are those in whichthere are intermediate forms betweenmany of the calls types. One problemwith this sort of distinction is that asparsely sampled (either in terms oftotal number of calls recorded, or typeand complexity of social contextsobserved) graded system will look like adiscrete system. More critically,describing a system as graded ord i sc re te assumes tha t the

experimenters estimation of the relevantacoustic parameters matches those ofthe species under study. Selection ofappropriate acoustic features is implicitin identifying call types and critical toasking experimental ly r igorousquestions. This task is complicated bythe fact that primate vocalizations areextremely variable, both within andbetween individuals. How do wedetermine what variation is meaningful?Historically vocalizations have beenanalyzed based on features that areobv ious in a spec t rog ram.Unfortunately, there is no guarantee thatthe acoustic features that are obvious toa human observer in a spectrogram arefeatures that are behavioral lymeaningful to a non-human primate(Owren and Linker, 1995). We aretherefore faced with a three-foldproblem: 1) what features exist in thevocalizations? 2) Of these features,which features are behaviorallyrelevant? and 3) Are these featuresperceived as discrete or graded?Addressing question 1 requires analysistechniques suitable to the high-dimensional and variable nature ofprimate vocalizations. Addressingquestions 2 & 3 requires behavioralexperiments in which identified featuresare tested for behavioral relevance.

Mathematical methods designed touncover the low-dimensional structureembedded in high dimensional datahave been developed in a variety offields and some, such as multi-dimensional scaling (MDS) and principlecomponents analysis (PCA), have beenadopted by bioacousticians. However,there are two drawbacks to thesemethods, one in implementation andone inherent to the analytic techniquesthemselves. The implementationproblem is that researchers usuallycarry out the feature extraction by hand,

and then use these handpicked featuresin the analysis (thus exposing theresults to bias). This problem can bemitigated, however, by selecting a largenumber of uncorrelated features foranalysis. The second problem is morecritical, namely that both MDS and PCArequire a large number of high qualityrecordings to be effective. Until recentlysuch data sets have been rare in theprimate literature, because of thedifficulty of recording vocalizations innormal social contexts.

In the past there has often been atradeoff between the quality of therecording and the naturalness of thesocial situation—it is no accident thatsome of the best studied vocalizationsare either very loud, commonvocalizations (like alarm calls) or callsthat can be elicited by isolation (e.g. theCLC of the cotton-top tamarin or theisolation peep of the squirrel monkey).The short range vocalizations ofprimates living in large social networks,with the most potential for informationtransmission of a high degree ofcomplexity, are often the most difficult torecord and then test experimentally. Toextend our investigations to the rest ofrepertoire, we need a method forcollecting large, high quality data sets,part icularly of rare and quietvoca l izat ions. Advances inradiofrequency transmitters, makingthem both smaller and more affordable,now allow the possibility of recordinglarge numbers of calls from freelybehaving animals, both in captivecolonies and in the wild. Theadvantages of such systems are 1) highquality recordings of clearly identifiedcallers are possible because themicrophone is attached to the animal, 2)recordings can occur during all socialcontexts, 3) a large number ofrecord ings can be co l lected

automatically and 4) if all members of asocial group carry transmitters,information about call sequencing andbout structure can also be collected.Such systems, in conjunction withobservations of behavioral context, willallow a deeper look into nonhumanprimate vocal behavior.

Finally, researchers must begin torecognize the limitations of currentperceptual tests. Most playbacks elicit asimple orienting response associatedwith a particular reaction time andduration—the robust behavioralresponses elicited by alarm calls, or theantiphonal calling to contact calls, arerelatively rare. Following the lead ofresearchers working on other non-primate systems, including frogs, birds,and humans, s ingle playbackexperiments must be extended toinclude habituation-dishabituationprocedures, phonotaxis, inter-activeplaybacks, and physiological measures(e.g., heart rate, skin conductance,neural recordings) to complementorienting responses.

Natural vocal communication offers aprivileged window into primate mentalprocesses, but studies of primate vocalcommunication to date have focused onthe transmission of relatively simpletypes of information. However, primatesproduce a richness of vocalization in adiversity of contexts. This variationsuggests that a considerable amount ofinformation is potentially encoded anddecoded about the signaler ’smotivational and affective state and thenature of the social and ecologicalenvironment. As the field of primatevocal communication advances toinclude more complex types ofinformation transmission, the study ofprimate vocal communication has thepotential to offer insight into the

cognitive substrates underlying theprimate mind.

Bibliography:

Books

Bradbury, J. W. & Vehrencamp, S. L. (1998) Principles of animal communication.,Oxford, Blackwell

Cheney, D. L. & Seyfarth, R. M. (1990) How monkeys see the world: Inside the mind ofanother species., Chicago, Chicago University Press

Hauser, M. D. (1996) The evolution of communication., Cambridge, MIT Press

Owings, D. H. & Morton, E. S. (1998) Animal vocal communication: A new approach,Cambridge, Cambridge University Press

Articles in Books

Dawkins, R. & Krebs, J. R. (1978) 'Animal signals: Information or manipulation' InBehavioural ecology (Krebs, J. R.&Davies, N. B., eds), pp Oxford UniversityPress

Fischer, J. (2002) 'Developmental modifications in the vocal behavior of non-humanprimates' In Primate audition: Ethology and neurobiology (Ghazanfar, A. A., ed),pp 109-125, CRC Press

Marler, P., Evans, C. S. & Hauser, M. D. (1992) 'Animal signals? Reference, motivationor both?' In Nonverbal vocal communication: Comparative and developmentalapproaches. (Papoucek, H., Jürgens, U.&Papoucek, M., eds), pp 66-86,Cambridge University Press

Owren, M. J. & Linker, C. D. (1995) 'Some analysis methods that may be useful toacoustic primatologists' In Current topics in primate vocal communication(Zimmermann, E., Newman, J. D.&Juergens, U., eds), pp 1-27, Plenum Press

Snowdon, C. T. (1986) 'Vocal communication' In Comparative primate biology, vol. 2a,conservation and ecology (Mitchell, G.&Irwin, J., eds), pp 495-530, Alan R. Liss

Articles in Journals

Cheney, D. L. & Seyfarth, R. M. (1980) Vocal recognition in free-ranging vervetmonkeys. Animal Behaviour 28,362-367

Crockford, C., Herbinger, I., Vigilant, L. & Boesch, C. (2004) Wild chimpanzees producegroup-specific calls: A case for vocal learning? Ethology 110,221-243

Fichtel,C. & Kappeler, P.M. (2002) Anti-predator behavior of group-living Malagasyprimates: mixed evidence for a referential alarm call system. Behavioral Ecologyand Sociobiology, 51: 262-275.

Fitch, W. T. (1997) Vocal tract length and formant frequency dispersion correlate withbody size in rhesus macaques. Journal of the Acoustical Society of America102,1213-1222

Fitch, W. T., Neubauer, J. & Herzel, H. (2002) Calls out of chaos: The adaptivesignificance of nonlinear phenomena in mammalian vocal production. AnimalBehaviour 63,407-418

Gouzoules, H. & Gouzoules, S. (1990) Body size effects on the acoustic structure ofpigtail macaque (macaca nemestrina) screams. Ethology 85,324-334

Gouzoules, S., Gouzoules, H. & Marler, P. (1984) Rhesus monkey (macaca mulatta)screams: Representational signalling in the recruitment of agonistic aid. AnimalBehaviour 32,182-193

Gros-Louis, J. (2004) The function of food-associated calls in white-faced capuchinmonkeys, cebus capucinus, from the perspective of the signaller. AnimalBehavior 67,431-440

Hamilton, W. J., III & Arrowood, P. C. (1978) Copulatory vocalisations of chacmababoons (papio ursinus), gibbons (hylobates hoolock), and humans. Science200,1405-1409

Marler, P. (1955) Characteristics of some animal calls. Nature 176,6-7

Marshall, A. J., Wrangham, R. W. & Clark, A. P. (1999) Does learning affect thestructure of vocalizations in chimpanzees? Animal Behaviour 58,825-830

Miller, C. T., Scarl, J. S. & Hauser, M. D. (2004) Sex-specific sensory biases underliesex differences in tamarin long call structure. Animal Behaviour 68:713-720.

Mitani, J. & Gros-Louis, J. (1998) Chorusing and convergence in chimpanzees: Tests ofthree hypotheses. Behaviour 135,1041-1064

Rendall, D., Owren, M. J. & Rodman, P. S. (1998) The role of vocal tract filtering inidentity cueing in rhesus monkey (macaca mulatta) vocalizations. Journal of theAcoustic Society of America 103,602-614

Rendall, D., Owren, M. J., Weerts, E. & Hienz, R. D. (2004) Sex differences in theacoustic structure of vowel-like vocalizations in baboons and their perceptual

discrimination by baboon listeners. Journal of the Acoustical Society of America115,411-421

Semple, S. (1998) The function of barbary macaque copulation calls. Proceedings of theRoyal Society, London 265,287-291

Semple, S. & McComb, K. (2000) Perception of female reproductive state from vocalcues in a mammal species. Proceedings of the Royal Society, London 267,707-712

Zahavi, A. (1975) Mate selection: A selection for a handicap. Journal of TheoreticalBiology 53,205-214

Zuberbuhler, K., Cheney, D. L. & Seyfarth, R. M. (1999) Conceptual semantics in anonhuman primate. Journal of Comparative Psychology 113,33-42

Zuberbuhler, K., Noe, R. & Seyfarth, R. M. (1997) Diana monkey long-distance calls:Messages for conspecifics and predators. Animal Behaviour 53,589-604