Single and Multichannel Signal Composition: Facial Expressions and Vocalizations of Rhesus
Macaques (Macaca mulatta)
Author(s): Sarah R. Partan
Source: Behaviour, Vol. 139, No. 8 (Aug., 2002), pp. 993-1027
Published by: BRILL
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SINGLE AND MULTICHANNEL SIGNAL COMPOSITION:
FACIAL EXPRESSIONS AND VOCALIZATIONSOF RHESUS
MACAQUES (MACACA MULATTA)
SARAH R. PARTAN12)
(Animal BehaviorGroup,Universityof California,Davis)
A methodfor simultaneouslyexaminingvisual and vocal componentsof expressivebehavior
is described, compiled from video recordings of social behavior of a free-ranginggroup
of rhesus macaques on Cayo Santiago, Puerto Rico. I developed a catalog of expressive
movements, and chronicled detailed informationon visual and vocal components of 1215
individual behaviors. Two thirds of the events recorded were silent, supportingthe idea
1)Departmentof Psychology,Universityof SouthFloridaSt. Petersburg,1400 SouthSeventh
Avenue, St. Petersburg,FL 33701, USA. e-mail:[email protected]
2) This work is based on my dissertationresearchin Peter Marler'slaboratory.I would like
to give my heartfeltthanks to Dr. Marlerfor his encouragement,support,and advice, as
well as for his comments on several draftsof the manuscript.I am gratefulto Marc Hauser
for encouraging me to work on rhesus monkeys, and to William Mason for helping me
to understandrhesus behavior duringpilot observationsat the CaliforniaRegional Primate
Research Center.This project was developed duringdiscussions with Drs. Marler,Mason,
Hauser,ChristopherEvans and Joseph Macedonia.I would like to thankCharlesSnowdon,
CorreighGreene, Jill Soha, Katya Partan,and two anonymousreviewersfor comments on
the currentmanuscript;Dr. Mason, JohnEndler,and Arlene Alvaradofor commentson prior
versions; and J.A.R.A.M. van Hooff for a suggestion on terminology.Neal Willits and Tim
Allis provided key statistical advice; Renee Allen and Marc Fourriergave indispensable
assistance in the field, and Jeannine Logan, Rebecca Wylie, and Virginia Price in the
laboratory;Bill Patrickand Todd Hughes helped produceFigure 4. Finally, I would like to
thankJohn Berard,Matt Kessler, the University of PuertoRico, and the CaribbeanPrimate
ResearchCenterfor providingaccess to the field site and the genealogical data, and Edgar
Davila for introducingme to the monkeys.This studywas fundedby grantsfromthe National
Science Foundation,the L.S.B. LeakeyFoundation,the AnimalBehaviorSociety, and Sigma
( KoninklijkeBrill NV, Leiden, 2002
Also availableonline -
that visual behaviors are primary for short distance communication in these macaques.
Clustersof expressive componentsdetectedby PrincipalComponentAnalysis and Multiple
CorrespondenceAnalyses correspondedto threatening,submissive,and affiliativebehaviors
describedpreviously,providingquantitativesupportboth for these previousdescriptionsand
for the suggestion thatthese threepoles of behaviorare importantin daily social interaction.
Silent expressions involved a greater variety of mouth positions than did vocalizations,
which were produced with stereotypedmouth shapes. Other components of the face, not
involvedwith articulation,were nonethelessassociatedwith particularvocalizations:specific
associationswere found among barks,ears retracted,and head loweredon the one hand,and
pant-threats,ears forward, and head raised on the other.Screams and squeaks were highly
stereotyped,combinedwith prototypicalgrimace mouthpositions, crouchingand retreating.
Girney vocalizations were accompanied by lipsmacking. Grunts were unaccompaniedby
otherexpressivecomponents,evoking the suggestionthatthey may be predominantlyneutral
Although communicationinvolves the use of multiple sensory channels,
most researchersfocus on one sensory channel at a time, in isolation from
the full repertoireof the animal. The combinationof channels, however,
can have importantramificationsfor signal meaning and efficacy (Marler,
1965; Partan& Marler, 1999; Rowe, 1999). Human facial expression and
visual articulatorymovements,for example,play a role in speech perception
(McGurk& MacDonald, 1976; Massaro, 1998). In birds, odor cues from
prey can interactwith visual stimuli of particularcolors to produce food
aversionsthat do not occur withoutthe odor (Rowe & Guilford, 1996), and
odor plays an importantrole in combinationwith other cues during sexual
behaviorin baboons (Goldfoot, 1982). Signal componentsin multichannel
displays can be redundant(e.g. Conner,1987), or each componentmay play
an independentrole (e.g. Fusani et al., 1997). It is difficult, however, to
determinethe functionalrole of each componentof multicomponentsignals,
as Green (1975, p. 87) mentioned for Japanese macaques: "...their vocal
behavior is inextricablytied to simultaneousolfactory, tactile, and visual
signals, hence considerationsolely of evoked responses cannot disentangle
the roles of the concurrentsignals available by different sensory modalities
Before parsingthe role of each componentin communication,one needs
to determinewhich particularcomponentsarecombinedsimultaneouslyinto
multimodalsignals duringsignal production.Althoughresearchersstudying
the receptiveside of communicationhave developed sophisticatedmethods
for measuringthe perceptionof multichannelsignals (e.g. visual influences
on human speech perception,Massaro, 1998), there are to date few established methodsfor quantifyingnaturalmultichannelsignalproduction.
This study describes how naturalvisual signals of facial expressionand
body postureare associatedwith vocalizationsof rhesusmacaques(Macaca
mulatta),bridgingthe separateanalyses of visual and vocal signals of this
species (e.g. primarilyvisual analysesby Hinde & Rowell, 1962; van Hooff,
1962; Maxim, 1982, 1985; Zeller, 1986, 1996;Maestripieri& Wallen,1997;
and primarily vocal analyses by Rowell, 1962; Gouzoules et al., 1984;
Hauser, 1991, 1996; Hauser& Marler,1993). Although some authorshave
described visual and vocal signals together (e.g. Altmann, 1962; Rowell
& Hinde, 1962; Lindberg, 1971; Mason, 1985; Kalin et al., 1992), none
have reportedthe frequencieswith which particularvisual componentsare
associated with particularvocal components.This is an importantfirst step
towards an understandingof the multimodalnatureof communication.A
similar approachhas been taken by Adams & Schoel (1982) in a study of
stumptailmacaque(Macaca arctoides) communication:vocalizationswere
analyzedseparatelybut in parallelwith the simultaneousfacial and postural
componentsof behavior.My work also builds on the work of Hauseret al.
(1993), who suggestedthateach class of rhesusvocalizationis accompanied
by an unique articulatorygesture.Here I not only examine mouthposition,
but also includefacial expressionsandbody posturesuninvolvedwith actual
One goal is to explorethe variabilityin facial expressivecomponentsused
during communication.I constructeda catalog of expressive movements
of the face and head, grouping behaviors into 'morphological'categories
(classifiedby body part:eye, ear,head,etc.; cf. Reynolds, 1976). Withineach
category,I definedlogical, mutuallyexclusive statesfor each body part(e.g.
the ear categoryincludes earsforward,retracted,orflappedbackandforth).
This categorizationscheme is more detailed than previous rhesus catalogs
with regard to facial movements (see Zeller, 1986, 1996, for a detailed
look at the face of other Macaca species) but may not be as detailed with
regardto gross body movements.Reynolds (1976) thoroughlydocumented
and cross-referencedterms used by early rhesus monkey observers,and I
attempthere to use many of the terms of my predecessorsin the hope of
achieving marginalconsistency and common understanding.My terms for
the vocalizationsfollow most closely those used by Rowell & Hinde (1962)
and Hauseret al. (1993).
The behaviorof the animals was recordedaction by action in sequence.
An 'action' was identifiedas a discreteunit of behavior,which may include
multiple simultaneous components. This designation was based on my
impressionof a behavioral'unit.'Behavior,althoughit occurs in continuous
streams, can be described as being made up of sequences of more or
less discrete actions. The identificationof these action units can, however,
be difficult. I separatedthe behavioralstream into discrete actions based
partiallyon physical changes in the body (e.g. the head moving from raised
to lowered), and partially on timing considerations (if two components
of behavior occurred simultaneously,such as head lowered and bark, I
consideredthem to be componentsof the same action, whereasif there was
a time lag between them, they were consideredto be two separateactions).
Green (1975) also emphasizeddynamic transitionsin patternsas an aid to
Drummond(1981) provides an extensive and interestingdiscussion of
how we categorize and describe behavior. He notes that the stream of
behavior can be segmented at many differentlevels, each appropriateto a
differenttype of analysis. A common definitionof a 'unit' is as a reliably
recurringphenomenon(Drummond,1981, p. 13-14). Ethologists may have
to use intuition to determinewhere the breaks in behavior occur, but our
intuitionis based on tractabledata such as regularityin patternsor bouts of
behavior(Drummond,1981; see also Marler& Hamilton,1966, Chapter20).
The ultimatetest of our intuitionis to ask the animalsthemselves how they
categorizetheirown signals (see Marler,1982).
Describing real, complex behavior,involving multiple simultaneoussignal components,is a challenge. To simplify, I included only the visual and
acoustic channels. In addition,I typically analyzed only two classes of behavior simultaneously:vocalizations,along with one class of visual behaviors (e.g. eye gaze, or mouth position). My rationalewas to documentthe
bimodal visual and vocal behaviorsof these animals. Detailed quantitative
analyses of the compositions of facial and vocal expressions are presented
in an effort to describehow visual and auditorysignal componentsare combined in this populationof rhesus monkeys. For furthersuggestions of how
to analyzecomplex multicomponentbehaviors,see van Hooff (1982), Bradbury& Vehrencamp(1998), and Deputte(2000).
TABLE 1. Demographicsof main studyanimals
Adults (6 yrs +)
1)The numberof adult males was approximatesince males occasionally transferredamong
The subjectswere free-rangingmale and female rhesusmacaques,Macaca mulatta,on Cayo
Santiago, a 15.2-hectareisland off the southeastcoast of Puerto Rico (Rawlins & Kessler,
1986). The monkeys ranged freely and formed social groups, were provisionedwith food,
and had no naturalpredators.All of the animalswere trappedas yearlings and given tattoos
and ear notches for identification.At the time of the study, there were six social groups on
the island, rangingin size from approximately49 to 354 animalsper group.The study was
conductedon two groups: group 'Y' and group 'V' (see Table 1 for age demographicsof
the groups). Twenty-twoadult females and 13 adult males were the primaryfocal subjects.
Occasionalsamples were takenfrom animalsin neighboringgroups.
All datawere collected on audio and videotapefor subsequentanalysis. Adult animalswere
filmed during 30-minute focal-animalfollows. The primaryfocal animals had at least four
samples each. Two simultaneousvideo recordingsof the animals were taken: one camera
filmed a close-up shot of the facial expressions of the focal animal, and the other took
a wide-angle view that also encompassed the surroundinganimals. I collected 270 hours
of video tape footage on VHS & SVHS tape, summing from both cameras, along with
supplementaryaudio cassette tape recordings,during March and September-Decemberof
1994. Close-up videos used a PanasonicAG460 movie cameraand wide-anglevideos used a
PanasonicAG455. Both cameraswere mountedon Bogen 3179 tripods.A SennheiserMKH
816 shotgunmicrophonewith windcoverwas strappedto the close-up video cameraand fed
into the externalaudio inputfor betteraudio recordingson the videotape.I filmed only when
the focal animal was interactingwith other monkeys at relatively close range, so signals
propagatedby solitary monkeys, such as branch-shakingand food-calling (coos), were not
common. Signals concernedwith mating were infrequentbecause I collected data primarily
duringthe nonbreedingseason. (Publishedrecords,such as Rawlins& Kessler,1985, indicate
that the Cayo Santiago breeding season was from approximatelyJuly to November in the
1970's to early 80's. However,the season has shiftedforwardslowly over the years, currently
beginningin May and mostly over by September[M. Gerald,pers. comm., December2001].)
Data collectionfrom videotape
Of the 270 hours recorded on both cameras, I watched 230 hours of tape (approximately
130 hours of real time). In many instances, the two videos had to be watched one at a time
because they displayed different views of the same scene, and included differentplayers.
While watching the tapes, I sampled for social interactionsusing the 'behavior-sampling'
method(Martin& Bateson, 1993, p. 87). Specifically,I sampledfor any interactioninvolving
vocal or visual communicationbetween two or more individuals.This broad samplingrule
includedall social interactions,with the exceptionof groominginteractionsalreadyunderway
at the time the camerastartedto film, since they usuallydid not includevocal or visual signals.
If two animalsbeing filmedbegan to groom duringthe sampleperiod,however,this behavior
Once an interactionwas located and data collection began, data were collected continuously until either (a) the individualsceased interacting,or (b) one or both ran off screen and
out of view of both cameras. Since I was recordingin the field, with trees, bushes, and interveningtopography,many interactionsin the databaseended prematurely(i.e. the animals
went out of sight before they were done interacting).However, this is not problematicfor
the purposes of this study, since I am interestedhere in the structureof visual and auditory
signals, ratherthanthe outcomes of the interactions.
I described 402 social interactions(both agonistic and affiliative), watching the interactions in detail, often proceeding frame by frame to identify the components used in the
signals. The individualactions that each animal performed(which often included multiple
simultaneouscomponents,as defined in the introduction)were logged sequentially,totaling
to 1215 actions. The median numberof actions per interactionwas 2 (the range was 1-26;
the mean was 3). This means that most interactionswere short, with one animal emitting a
display and the other a response. Focal animals were all adults, but younger animals were
included when they interactedwith focal subjects.Although the primaryfocal animals each
had 4-10 focal follows, the total numberof actions performedby each focal animalranged
from 5 to 65 (dataon the numberof times each individualcontributedavailableon requestto
The databasecontainedone entryfor each action, with the following fields:the time of the
event (video frame);the identities of the actor and recipient(s)involved, including their sex
and age; anda set of eight componentsof the signaler'sbehavior.These included:vocalization
type, mouth position, eye gaze, ear position, head position, tail position, body posture, and
overall movement.If a particularbody partwas out of view, as could happenif the animal's
face was on the camerascreen but its tail was not, I left blank the correspondingcell in the
database.I did not include observationswith blank cells in my analyses.
For each of the eight componentsof the signal, I compiled a list of possible expressive
positions or states (Table 2). This list provides a detailed repertoireof rhesus monkey
communicativebehavior,focused largelyon movementsof the face and head. I avoidedusing
2. Repertoire of communicativebehaviors of rhesus macaques:
expressivecomponentsof theface, voice and body
LS with tongue
loud, voiced, harsh(broadband)sound
softer,more breathyharshsoundusually emittedin a rapid
bout of threeunits
loud sound, can be harshor tonal (includesnoisy, archedand
mixed call that startswith barkand ends with scream
quiet, harshsoundusually not repeated
frequencymodulated,quiet sound, may be narrow-or
staccatoharshsounds,usually from infants
shortharshscream-likecalls given by some males during
vocalizationwhich cannotbe put in any of the above classes
mouthis closed, lips closed, loose
lowerjaw droppedso lips form 'o' shape,upperteeth
lips retractedhorizontallyto expose teeth,jaws can be
mouthis closed, lip cornersdrawnback to form straightline
lips moved repeatedlytogetherand apart;may be audible
same as above but with tongue rhythmicallymoving in and
out of mouth
mouthis closed, lips togetherand often pursed,chin is
same as above, but with lips makingsmall, rapidmovements
mouthrapidlyopens & closes; teeth exposed;may be audible
jaw opens and closes but lips remainclosed; may be audible
lips drawnforwardtogether,cheeks furrowed
mouthopens widely in stereotypedgaping movement
mouthopened to bite othermonkey
mouthopens only enough to emit a sound, andonly for the
durationof the sound,then closes
eyes relaxed,may be half shut, not looking in any particular
direct,prolonged,unwaveringlook at specific individual
look in directionof specific individual
look in directionobviously other than thatof specific
look rapidlybetween two or more otherindividuals
look rapidlyin severaldirections,often at distant
ears relaxed,in mediumposition (about45 degrees from
ears pointingperpendicularlyout from
ears retractedtightly to scalp
ears move quickly backwardsand forwardsmore thanonce
eyebrowsraised and remainup
eyebrows lowered and remaindown
eyebrowsmove quickly up and down
Tail up looped
Tail up crooked
Tail 45 degrees
head held up in high position
head held in low position, neck usually angled forward
head moved quickly and abruptlyup and down
head moved slowly and smoothly up and down, often
tail held in relaxed,low position
tail held up perpendicularto body, straightfrom base to tip
tail held straightup from base, but tip is curledin tight loop
tail held straightup from base, but tip is bent over
tail held up at 45 degrees from base, tip often slightly bent
tail held straightout parallelto body
tail held low, waving
Body positions & movements:
posturewith belly low, armsand legs bent
suddenand quick movementof upperor entirebody towards
mountothermonkey in typical posture
lean whole body away from anothermonkey
quick hit to ground,usually one handonly
TABLE 2. (Continued)
very closely, then suddenlybreakingapproachby bendingarms,
turningquickly aroundand moving away (headusually swings
aroundlast, so that actoris looking at recipientuntil last moment)
bounce up and down on branchor otherobject, holding on
with feet so thatthe substratemoves as well
body suddenlybecomes still
use handto grabhold of othermonkey
use handlarmto hit at othermonkey
use handto gently touch othermonkey
hairis raisedon body
fast-pacedagonistic interactioninvolving chasing, tumbling,
biting, barking,screamingall at once
presentown body for mountingusually by moving tail aside
and presentingrearend to othermonkey
presentown body for groomingusually by moving neck or
side or back towardsothermonkey,looking away,and becoming
Go in severaldirections
move rapidlyaway from othermonkey
move back and forth
leave anotherwith whom it had been associating(not rapidly)
walk close behindanothermonkey,same direction
2) Eye gaze directionwas determinedby head orientationas well
as eye gaze.
3) Includeshead movementsin the vertical,ratherthanhorizontal,domain.
names with functional connotationsto describe the elements of the expressions, with the
exception of pant-threat.I kept the 'threat'as a partof this name to be consistent with the
previousliterature(e.g. Rowell, 1962; Rowell & Hinde, 1962; Hauseret al., 1993).
All expressive components were defined as a departurefrom a neutral state (based on
Sade, 1973). A neutral expression was defined as the countenance of a relaxed monkey
(Fig. la). Neutralpositions of each body partwere recordedalong with expressivepositions
(see Table 2). Expressive positions are mutually exclusive within categories. For example,
when an individual'shead is raised, it cannot simultaneouslybe lowered; or if an animal
is barking,it cannotbe also cooing. The only categoryfor which internalmutualexclusivity
does not hold is the 'body' category,becauseit is possible, for instance,for an animaltofreeze
and crouchat the same time. In these cases I enteredthe most pronouncedbehavior,putting
Fig. I. (a) Sub-adultrhesus male (X85) with neutralfacial expression. Photo by author.
(b) Adult female (E76) with silent stare and open-mouth. Digitized from videotape using
Adobe Premieresoftwareand Panasonicediting stations.
the secondary behavior in an 'other' category. I chose to lump all body postures into this
one categorybecause I wanted to focus specifically on facial expressions and vocalizations.
Body posturewas of secondaryinteresthere, althoughcertainlyof great importancein social
Eye gaze direction is difficult to assess on videotape. I have followed Altmann (1962)
in his distinction of stare from look at, and I have included three other active states of the
eyes (see Table 2): look betweeni,look arounid(perhapssimilarto Altmann'sunit #35, 'looks
apprehensively'),and look away (similarto Altmann'sunit #34, 'avoids staringat'). In each
of the latterthree cases the eyes move quickly between, among, or away from social targets
were relaxed eyes, often half shut
in the environment,respectively.In contrast,eyes nieutrail
or gazing off into space, not moving quickly. In cases where I could not assess eye direction
from the videotape,I left the correspondingdatacell blank.
Head position was troublesometo categorizebecause the head often moves in conjunction
with other behavior, such as yawning (Deputte, 1994). Movements of the head are also
incorporatedinto gaze behavior. I decided to prioritize mouth and eye behavior, since
I was primarily interested in facial expression. Therefore yawn was categorized as a
mouth behavior,and all eye gaze directions involving both head and eye movements were
categorized as eye behaviors (e.g. look arounidand look between). Head movements that
occurredin the vertical domain (raised, lowered, bobbed,jerked) were included in the head
position category. My use of the term head bob refers to a slow, rhythmic up and down
motion, whereas head jerk is a sudden sharp movement, not repeated. I follow Hinde &
Rowell (1962) and Reynolds (1976) in their use of the term 'jerk' for the latter behavior
(departingfrom Altmann, 1962, and Drickamer,1975, in their use of the term 'bob' to refer
to quick head movementsduringthreat).
Vocalizationswere classified by ear from the audio trackof the videotape,aftercategories
were established via spectrographic analysis and verified by comparison to published
spectrograms(Rowell & Hinde, 1962; Hauser & Marler, 1993) and discussions with other
researchers(P. Marler,W. Mason, & M. Hauser,pers. comm.). Although rhesus screams
have been subdividedinto five categories by Gouzoules et al. (e.g. 1984), I could reliably
distinguish only two types by ear. One type, which I labeled scream, included 'noisy',
'tonal', and 'arched' screams (Gouzoules et al., 1984); the second type, which I called
squeak,includedscream-likevocalizationsthatwere very shortin duration('pulsed' screams,
Gouzouleset al., 1984). If a vocalizationhad severalsyllables (as was commonwith screams
andpant-threats),I enteredit only once into the database,to avoid inflatingthe numberof
Pilot observationsof mouth positions during vocal behaviorindicatedthat some vocalizations were producedwith a utilitarianor purely articulatoryuse of the mouth:the mouth
opened only to the degree and durationnecessaryfor sound emission. Othervocalizations,
however,were accompaniedby elaboratemouthmovementsthatexceeded eitherthe duration
of the call or the degree of opening necessaryto producethe sound. I distinguishedbetween
these possibilitiesby includinga categorycalled mouthmatchesvocalization(Table2), along
with the expressive mouth positions. This allowed me to set aside articulatorymovements
for particularanalyses (noted below). Note that all vocalizationsare 'simultaneouslymultimodal' in that each occurs with a particularmouthposition, providingboth visual and vocal
stimuli, regardlessof whetherthe mouth is open as long as or longer than the call. A finergrained temporalanalysis might consider the latter cases to include unimodal signaling of
mouthopening, followed by multimodalsignalingduringthe call, followed againby the unimodal mouthposition afterthe call has ended. However,here the behavioralunit includedthe
vocalizationin the context of the visual signals thatencompassedit; any actionthatincluded
a vocalizationwas considered 'multimodal'.
All dataanalysiswas done using SAS software.Any entries(observations)with missing data
for the behaviorbeing analyzedwere omittedpriorto analysis. This reducedthe sample size
differentiallyfor the differentanalyses,dependingon which behaviorswere being assessed.
I carriedout three main analyses. FirstI examinedthe entiredata set to determinewhich
components co-occurred,using Principal ComponentAnalysis (PCA) to examine overall
relationships among the variables. Since PCA requires numeric data, I transformedthe
nominal categories into a series of indicatorvariables which read '1' or '0' depending on
whetherthe particularbehaviorwas presentor absent(this methodis also used anddescribed
by Deputte,2000). I used all eight behavioralclasses (vocalizations,eye, ear, head position,
etc.). When I transformedthe data, there were a total of 57 columns, because the 8 classes
included 57 unique behavioralcomponentsor elements that were included in the analysis.
(All behavioralcomponentsin Table 2 were includedin the PCA except articulatorymouth
matchesvocalizationmovementsand some otherrarecomponents.)The raw datamatrixfor
the PCA analysis consisted of the 57 columns correspondingto each behavioralcomponent,
and 1215 rows correspondingto each event. The analysis thereforeproduceda correlation
matrixwith 57 columns and 57 rows, correlatingeach of the behavioralelements with each
other element. This matrix was then analyzed to produce 57 principalcomponents,the top
six of which had eigenvalueslarge enough (> 1.9) to warrantdiscussion.
The second analysis was a comparisonof the silent and vocal behaviorsof the animals,
basedon the frequenciesof occurrenceof each expressivecomponentduringsilent andvocal
behavioras a whole.
In the thirdset of analyses I examinedin detail the structureof the bimodal,visual/vocal
expressions.I conductedMultipleCorrespondenceAnalyses (MCA's)to explorethe distribution of componentstwo or threeclasses of behaviorat a time, andpresentedthe resultsgraphically. The frequencydata were taken from columns in the main database,with behavioral
componentsacrossthe columns, andone composite action per row. A correspondenceanalysis, like a PrincipalComponentAnalysis, detects trends in the data by establishing which
componentsare associated (see van der Heijden et al., 1990, for detailed explanation).The
analysis then defines 'dimensions' to describe the strongestassociations.Like the PCA, the
correspondenceanalysis has many dimensions, but only the two most importantones are
plotted in the graphs. Strong associations between variablesare shown in two ways on the
MCA graphs:by distance from the origin, and by trajectory.If two behavioralcomponents
plot out on the same trajectory,they are closely associated,andthe fartherthey areaway from
the origin, the strongerthe association. (Diagonal lines drawnon the graphsmake it easier
to see which variablesare associated.) Note that for the correspondenceanalysis of mouth
positions and vocalizations,I excluded the articulatorymouthmatchesvocalizationcategory.
Finally, I documentedwhich visual componentswere associated with each vocalization,
using frequencymatricesand histograms.
For all analyses, behavior was pooled across individuals. Although I am aware of the
potential dangers of pooling data for parametrictests (Machlis et al., 1985; Leger &
Didrichsons, 1994), my data are nominal frequencies that cannot be averaged. I cannot,
for example, find the mean of 10 open mouth threats and 5 fear grimaces to come up
with an 'average expression' for a given individual who produced these 15 expressions.
FurthermoreI collected data on myriad components of expression, with the individuals
involvedin manydifferentpossible dyadic combinations,makingthe concept of an 'average'
even less appropriate.Instead,the focus of analysis is on the frequencieswith which multiple
expressivecomponentsare combined,across all cases of expression.
Overallrelationshipsamong the behaviors
Principal Component Analysis yielded six top components (with largest
eigenvalues; Table 3). The clusters revealed by the PCA correspond to
behavioral suites that have been reportedpreviously in a more anecdotal
The most striking association in the data was among open mouth, stare,
earsforward, and head lowered (Fig. lb depicts the open mouthand stare).
This suite of behaviorscorrespondsto descriptionsof silent threatfrom the
literature.Grimacedid not occur with this cluster.
3. Principal ComponentAnalysis
Top six components.All variableswith Icoefficientl>0.2 are listed for each component.A
negativecoefficientindicatesthatthe variablewas negativelyassociated.
The second principalcomponentinvolvedbark,scream,lookingaround,and
movingin several directions.This is a typical suite of behaviorsinvolvedin
Steady, walking approach with tail raised. Typical behavior of dominant
males (Hinde, 1966; Lindburg, 1971).
TABLE4. Comparisonof visual componentsassociated withsilent and vocal
Row % Column %
Row % Column %
Back & Forth
Therewere a total of 760 silent behaviorsand 356 vocal ones, but the totals for each section
above are smaller,owing to dataunavailablebecause a particularbody partcould not be seen
Girney,lipsmack,ears back, tail wave. This is typical affiliativebehavior.
Grimacedoes not occur with these behavioralelements.
Lunge,chase, look at. This is typical of an aggressiveapproach.
Retreat, grimace, look at, ears back, chin-up. The first two behaviorsare
typical of submission. The last three are components of a solicitation
behaviordescribedby Altmann(1962, p. 378), in which a male approacheda
female with a stereotypedposture,head tilted back, chin up, and lips pursed
.... ...... ............
. . .......,,..
Images from videotape of vocalizing animals. Spectrograms were collected from
videotape at the same frame as the picture, using a Kay Digital Sona-Graphmodel 7800.
Horizontalbars mark I-kHz intervals(1-8 kHz). (a) Adult male barking,with open mouth
and ears back. (b) Adult female (845) giving a pant-threatvocalization.(c) Sub-adultfemale
(X70) giving a broadband('noisy') scream. (d) Adult male (C78) grunting. (e) Sub-adult
male girneying and waving his tail. Althoughthis girney contains primarilybroadbandcomponents, girneys can also include narrow-bandsounds (e.g. see spectrogramin Kalin et al.,
Figure 2a reprinted
from: Partan, S. & Marler, P.: Communication
Science 283(5406), p. 1272-1273; copyright 1999 American Association for the Advancementof Science.
and sometimes rapidlysmacking.He typically approachedvery close to the
female, almost touched his face to hers, and then immediately tured away
with a stereotyped 'dip' (arms bend quickly down), and walked away. Only
males were seen performingthe chin-up and dip-turn; when a recipientwas
identified, it was female (Partan, unpublished data).
Comparison of silent and vocal expressions
Four of the top six Principal Components were silent, and two were vocal. To
compare silent and vocal behavior, I explored which visual components were
associated with vocalizations. The presence or absence of a vocalization
could be reliablydeterminedfor 1116 out of the 1215 total events recorded.
Of these 1116 events, 68% (760) were silent and 32% (356) included
vocalizations.Silent and vocal expressionswere differentiallyaccompanied
by the various visual signal components(Table4). The 'Vocal' column in
Table4 lumps the six majorvocalizations,each of which occurred20 times
or more: barks, pant-threats, screams, squeaks, grunts, and girneys (see
Fig. 2 for spectrograms).Omittedfrom the table are vocalizationsthat were
recordedfewer thanten times (bark-screammixes, coos, geckers,copulation
calls, harmonicarches, and unclassifiablecalls).
The 'row %' column in Table 4 compares the silent to vocal behavior.
Silent expressionsinvolvedmore visual componentsthanvocal expressions.
This can be demonstratedby a quick scan over the 'row %' columns to
see the disparityin the numberof behaviors at 100% for the silent group
comparedto the vocal.
The mouthwas most often in a neutralposition duringsilence, but many
other mouth positions were used. All possible eye positions were recorded
duringsilent expressions,the most common being looking at the recipient,
followed by staring and neutral eye position. All ear and head positions
were also recorded during silent expressions, with the neutral position
predominantin both cases. Head bobs were predominantlysilent. Many
body and arm postures occurredduring silent expressions, although most
of the time the body was neutral.Presents,grabs, anddip-turnswere always
silent; lean away, touch,freeze, and slap ground usually so. During most
silent expressionsthe animalwas stationary.Pass by and lunge were always
silent;follows usually were as well.
Expressions including vocalizations incorporatedfewer visual components than did silent expressions overall. Mouth positions during the six
majorvocalizationsincludedopen mouths,grimaces, lipsmacks,and mouth
matchingthe vocalization.Therewere no vocalizationsduringyawns, bites,
tooth chomps,or chin-upmovements.
Lookingaroundoccurredmoreduringvocalizationsthanduringsilent behavior;lookingaway, however,predominantlyoccurredduringsilent behavior.Ear-flapping,lunging,crouching,fighting,andpiloerectionoccurredproportionatelymore often duringvocal thansilent behaviors,as did retreating,
chasing, and movingback andforth.
Structureof multimodalsignals: Visualbehaviorsassociated with each
I used Multiple CorrespondenceAnalysis to examine in greaterdetail how
behaviorswere associatedwhen consideringnot the entire data set, as in the
above PCA analysis, butjust two of the eight majorcategoriesat a time (e.g.
vocalization and mouth position). Associations among vocalizations and
mouthpositions are shown in Fig. 3, using only 'expressive'mouthpositions
(all positions except mouthmatchesvocalization).The componentssplit into
three groups, each of which contains behavioralelements devoted to one
of three functions describedpreviously in the literature:threat,submission,
and affiliation (Altmann, 1962; Hinde & Rowell, 1962; Rowell & Hinde,
1962; Lindburg,1971). Threatincludedbark,pant-threat,bark-scream,and
: .,:.; ,
Fig. 3. Multiple correspondence analysis of vocalizations (circles) and mouth positions
(triangles). Associations among variables are shown by common trajectory from the origin.
Aggressive components clustered on upper left; submissive ones on right; neutral and friendly
Multiple correspondenceanalysis of vocalizations (circles), mouth positions (triangles), and eye gaze (squares).
open mouth; submission included scream, squeak, and grimace; affiliation
includedno vocalization,girney,grunt, coo, lipsmack,and chin-up.
To test whether these three clusters still appearedwhen combined with
a visual component uninvolvedwith phonation,I added eye gaze direction
to the vocal and mouth data and ran anotherMCA (Fig. 4). The same three
clustersoccurred.Stare fell into the aggressivecluster;look aroundand look
betweenfell with submission;look at and neutraleye with affiliation.
Along with the above associations predictedfrom the literature,the next
MCA analyses revealed several new and unexpected associations. These
depict a difference in visual accompaniments of the two vocalizations
considered to be aggressive, bark and pant-threat. Associations among
vocalizationsand ear position are shown in Fig. 5a. Threateningbehaviors
areon the right,andnonthreatening(affiliativeandsubmissive)behaviorsare
on the left. The nonthreateningvocalizations were loosely associated with
...' . i:
. '*.';:*/.' "ji '-' .:': "*' 'y v l:****:'
* .' '-:
* -,w .'' **r
-.w !; :y_
^ .:' . ****:* ' . -:
i . e! ! |l ,
!* '*'*^ '^* *' :" 'j .EX
j i ^
l . .',''
. . ..
t.;. A ..t
;- .--.'.', .'s1V;
i: ' '.;*':;
.. .. .. .
Fig. 5. Multiple correspondenceanalysis of (a) vocalizations (circles) and ear positions
(triangles), and (b) vocalizations (circles) and head positions (triangles). In both graphs,
aggressive behaviors fell to the right of the origin, and submissive and affiliative ones fell
primarilyto the left.
neutral ear position. The interesting finding is that the threat vocalization
bark was associated with ears back, while pant-threat was with ears forward.
Figure 5b shows the associationsamong vocalizationsand head position.
Affiliation and submission are on the left, weakly associated with neutral
head position. On the right, pant-threat vocalizations were associated with
head raised or forward, whereas barks were with head lowered.
. . ..
.*., .- ,:.[
-~ .. ..
. ,, ,:, ',',,
· . ,.
.. · I
I systematicallydocumentedthe visual componentsthat occurredsimultaneouslywith each of the six majortypes of vocal behaviors(Fig. 6). These
are presentedbelow, organizedaccordingto the visual components.
Mouth position was tightly linked to vocalization type (Fig. 6a). Barks
and pant-threats were accompanied by rounded open mouths, screams and
squeaks were accompanied by grimaces, and girneys (and, to a lesser
extent, grunts) were accompaniedby lipsmacks.Each vocalizationalso had
a significantproportionof mouth shapes that simply matched the sound,
synchronizedin time, opening and closing without any furtherexpressive
posture. For grunts, almost 80% involved no mouth expression other than
opening slightly for the grunt. The lowest matching scores were found
among screams and, especially, squeaks, which often occurredin the midst
of prolongedsilent grimaces. These vocalizationswere still simultaneously
multimodal:the squeaksco-occurredin time with grimaces.
All six vocalizationswere accompaniedby substantialproportionsof looking
directlyat the recipientandof lookingaround(Fig. 6b). The girneyinvolved
a higher percent of looking at the recipient (67% of all girneys), and a
lower proportionof lookingaround(only 17%).Barksandpant-threatswere
accompaniedby a high proportionof staring (37% of barks, and 50% of
pant-threats).Screams and squeaks had the highest proportionsof looking
between the recipient and a thirdparty (13% of screams; 30% of squeaks)
and of looking away from the recipient(5% of screams; 15%of squeaks).
Ear position (Fig. 6c) was predominantly(>80%) neutral for screams,
squeaks, girneys, and grunts. Barks and pant-threatsdiffered dramatically.
Ears were neutral in only 51% of barks and 40% of pant-threats.During
barks, the most common nonneutralposition was retracted(28%), but they
could also be juttingforward(10%)orflappedbackandforth(11%).Inpantthreatsthe ears were most oftenforward (35%) but also could be retracted
(15%) orflapped (10%).
Headposition (Fig. 6d) was always neutralfor screams,squeaks,andgrunts.
During girneys, the head was predominantly(92%) neutral, but in the
remainderof the cases showed a distinctive bobbing movement not seen
during any other vocalizations.Barks and pant-threatswere most variable
in head position.Barkswere accompanied16%of the time by head lowered,
3% by headjerked, and 2% by head raised. Pant-threatswere accompanied
more often thanbarksby head raised (20%)andheadjerked (10%),andless
often by head lowered (10%).
A wide array of body postures was observed (Fig. 6e). Grunts, girneys,
and pant-threats were given at least 95% of the time with neutral body
position. The remaining girneys were accompaniedby reaching out and
gently touching the recipient. The remainingpant-threats involved body
crouches. Barks, screams, and squeaks were relatively active. Barks were
accompanied 16% by lunges; 4% by crouching, and 3% by piloerection.
Screams were given 16% with crouching, 12% with lunging, 7% with
tumbling duringfighting, 4% with swatting, and 2% with leaning away.
Squeakswere emitted 7% with lunging or crouching,and 4% with leaning
away,freezing, or shiftingposition.
Movement (Fig. 6f) showed similar patternsto body posture, except for
girneys. 40% of girneys were stationary;52% involved approachingthe
recipient. Gruntsandpant-threatswere 90% stationary;for the remainder,
the actor approachedduring grunts, and either approachedor chased the
recipientduringpant-threats.Barkswere heardduringchases or approaches
13%each, duringretreats5%,and6%while movingbackandforth.Screams
and squeaks were commonly accompaniedby retreats (42% of screams;
36%of squeaks).They also were heardduringapproaches(12%of screams;
16%of squeaks)andwhile moving backandforth (14%of screams;10%of
This study provides quantitativesupportfor two areas of literature.First,
the data supportthe idea of three 'poles' of behaviorimportantduringsocial communication:aggression,submission,and affiliation.Deputte(2000,
p. 118) calls this the "3 A's concept (affiliation, aggression, and avoidance),"and Mason (1985) also singles out these three motivationalstates.
In the presentstudy this was shown most clearly in the MultipleCorrespondence Analyses of the associationsamongmouthposition, vocalization,and
eye gaze (see Figs 3 & 4). Previous work identifiedbehavior involved in
these threedomainsin rhesus (i.e. open mouthsand barksbeing aggressive;
E Matches Sound
SCREAM(62) SQUEAK(25) GIRNEY(20) GRUNT (19)
SCREAM(67) SQUEAK(27) GIRNEY(24) BRUNT (25)
SCREAM(09) SQUEAK(27) GIRNEY(23)
Fig. 6. Visual expressive components associated with each major vocalization. (a) Mouth
position; (b) eye gaze direction; (c) ear position; (d) head position; (e) body posture;
(f) overall movement. The N's are based on the numberof times that the vocalization was
SCREAM(75) SQUEAK(29) GIRNEY(24) GRUNT (20)
SCREAM(86) SQUEAK(29) GIRNEY(24) GRUNT (20)
SCREAM(92) SQUEAK(31) GIRNEY(25) GRUNT(20)
Fig. 6. (Continued)recordedin conjunctionwith any position of the mouth, eyes, etc. The
N's differ slightly among panels owing to cases lost hecause the particularvisual component
could not he seen.
screams, squeaks, and grimaces submissive;and girneys and lipsmacksaffiliative; Altmann, 1962; Hinde & Rowell, 1962; van Hooff, 1962, 1967;
Rowell & Hinde, 1962; Marler, 1965; Lindburg,1971; Drickamer,1975;
Redican, 1975; Mason, 1985; Boccia, 1986; Kalin et al., 1992; Maestripieri, 1997; Maestripieri& Wallen, 1997; Partan,1998). Van Hooff (1973)
providedquantitativeevidence for five behavioralstates importantin chimpanzees, including the three discussed here as well as play and excitement.
He pointed out that the determinationof these groupingsdepends partially
on the degree of lumpingand splittingof the initialbehavioralelements that
make up the catalog. Adams & Schoel (1982) found six motivationalstates
in male stumptailmacaques,includingthe threediscussedhere, and defense
(which I includedwith submission),sexual behavior,and display.
Second, these data providequantitativesupportfor the previousdescriptions of behavioralclustersin rhesusmonkeys.For example,the top componentsof the PrincipalComponentAnalysis, each of which involveda suite of
behaviorsthat clusteredtogether,correspondedto behaviorsreported(usually in a nonquantitativefashion)to have been observedtogether.
Comparisonof silent and vocal expressions
Silent visual expressions dominated the communicationsignals used by
these monkeys at the close distances at which they were observed. This
agrees with Rowell's (1962) suggestion that the visual channel is primary
for rhesus macaques, and supportsthe argumentthat, owing to selective
pressuresimposed by the environment,terrestrialprimates such as rhesus
macaques rely more heavily on vision while arborealones rely more on
audition(Altmann,1967; Redican, 1975). A higherproportionof behaviors
in this studywere vocal (31.9%),however,thanwas trueof Altmann's(1962,
1965, 1967) study,in which only 5.1% of behaviorsincluded vocalizations.
These figures are difficult to compare, particularlybecause Altmann split
some categories of visual behaviorsmore finely than I did, increasing the
proportionof visual to vocal signals in his studyrelativeto mine.
The silent expressionsreportedhere were highly complex; in fact, silent
expressionsas a whole incorporateda widerrangeof visual componentsthan
did expressionsaccompaniedby vocalizations(see Table4). This may partly
be due to physicalconstraintsplacedon the mouthwhen an animalvocalizes,
inhibitingthe concurrenceof vocalizationswith certainmouth movements
such as yawning, biting, tooth chomping, or pursing or compressing the
lips. However,these particularmouth movements do not entirely preclude
vocalizing:yawns have been observedto coincide occasionallywith barksin
grey-cheekedmangabeys,for example (Deputte, 1994).
In additionto mouthpositions, some body posturesneveroccurredwhile
an animalvocalized, but did occur duringsilent behavior(see Table4). All
occasions when an individualpresented its body to another,whether for
grooming, occasional sexual interactions,or to indicate submission, were
silent. Also silent were chin-up and dip-turn, which Hinde and Rowell
referredto as 'dancing' (see Fig. 8b & c in Hinde & Rowell, 1962, p.
17). They did not mentionany vocalizationsoccurringduringthis behavior.
Altmann also described this behavior in detail, althoughhe did not name
it. He consideredit to be an 'extremeform' of 'smacks lips at' (Altmann,
1962, p. 378), and it did not occur in combinationwith any vocal units.
This behavior may be analogous to the 'stylized trot' describedby Green
(1975, p. 65) for Japanesemacaques.The facial componentmay be similar
to the 'LEN' observedin pigtailmacaques(Lips protruded-Eyebrows
raisedNeck forward;Jensen & Gordon, 1970, p. 268) and the 'pucker'described
by Maestripieri& Wallen (1997). The males I studied were silent during
the chin-up and dip-turnbehaviorregardlessof whether or not they were
lipsmacking. Hauser (1993) has reportedthat male rhesus monkeys who
vocalize duringcopulation,perhapsanalogous,aremorelikely to be attacked
by othermales thanthose who copulatesilently.
Visualsignals associated with vocalizations
Multimodalsignals are an importantpartof the rhesus macaquerepertoire:
in this studythey madeupjust over 30%of all behaviorsin the database.For
example,barkandpant-threatvocalizationswere accompaniedby particular
visual components(open mouth,staring, ears neutralor back, head neutral
or lowered,body neutralor lunging,and approaching,chasing or remaining
stationary)as suggested in the literature(Altmann, 1962; Hinde & Rowell,
1962; van Hooff, 1962, 1967; Rowell & Hinde, 1962; Redican, 1975;
de Waalet al., 1976; Boccia, 1986).
Novel findingsinclude a contrastin the frequenciesof the visual accompanimentsof the two aggressive vocalizations.Pant-threatswere more often accompaniedby staring, ears in the forward position, and head raised
orforward than were barks. Ear position duringthreathas been described
by others to be retracted(e.g. Drickamer,1975), but the two threatening
vocalizations have not been distinguishedpreviously in terms of these associated visual signals. Staring or looking at anotherindividualmay be a
method of indexing with the eyes, indicatingto whom a vocalizationis directed (Itani, 1963; Altmann, 1967; Mitchell, 1972; Argyle & Cook, 1976;
Green & Marler, 1979). Ears in the forwardposition may serve a similar
function, indicating the intended addressee (Partan& Marler,2002). The
correlationsbetween pant-threatand indexicaleye and ear positions suggest
that pant-threatsare typically directedat one or more targetedindividuals,
whereas barks are propagatedmore generally.Barks were more often accompaniedby looking around and looking between other individualsthan
were pant-threats. 'Broadcast' signals are not directed to any recipient in
particularbut are presented generally for all to see or hear. Other examples of broadcastsignals in rhesusincludebranchshaking,yawning,and tail
raising. In the stumptailmacaque,broadcastsignals such as branchshaking
(called 'bouncing') and patrollingwere also associated with barks (Adams
& Schoel, 1982).
The visual accompanimentsof the two submissivevocalizations,screams
andsqueaks,differed.Both were generallyaccompaniedby grimacing,looking at, around,or between two other animals,neutralears, heads, and bodies, and retreatingor remainingstationary(Fig. 6), in agreementwith previous studies (Altmann, 1962; Hinde & Rowell, 1962; van Hooff, 1962,
1967; Rowell & Hinde, 1962; de Waalet al., 1976; Maestripieri& Wallen,
1997). Not previously documented,however, are that the ears were never
held forward or flapped during submissive vocalizations,and that screams
and squeaks differed in the proportionsof their visual accompaniments.
Squeaks (shorterthan screams) occurredwith prolonged, stereotypicalgrimacing mouth positions, and were more often accompaniedby looking between the recipientand a thirdanimalthanwere screams.Squeaksneveroccurredduringactualfighting,however;they were morelikely to occurduring
breaksin fighting or afterthe fight was over. Since looking between can be
used for recruitment,squeaksmay have been used more often than screams
when soliciting supportfrom allies presentat the scene.
Two acoustically distinct vocalizations,girney and grunt, were the only
ones to be sometimes accompaniedby the affiliativebehaviorsof lipsmacking and, in the case of girneys, head bobbing (Fig. 6). Vocalizing animals
usually looked at the recipient, had neutral ear, head, and body positions,
and either approached(in the case of girneys) or remainedstationary.The
ears, as with submissivebehaviors,were neverheldforward orflapped during these two vocalizations.Girneysandgruntsdifferedin the proportionsof
theirvisual accompaniments.Girneyswere most often given with lipsmacking, an affiliativesignal (Hinde & Rowell, 1962; Mason, 1985; Maestripieri
& Wallen, 1997). Gruntswere much more likely than girneys to be given
withoutany mouthexpressionat all. Gruntswere also more likely thangirneysto be accompaniedby neutralpositionsof the eyes, ears,head,andbody,
andgruntswere usually not accompaniedby movementin any particulardirection. Adams & Schoel (1982) found that stumptailmacaquegruntswere
likewise not significantlyassociatedwith any particularacts or postures.
Rowell & Hinde (1962) suggested that rhesus girneys (or 'girns') are
affiliative,and Kalin et al. (1992) providedempirical evidence for this in
infant monkeys. Hauser et al., (1993) classified both girneys and grunts
as affiliative.Hauser & Marler(1993) stated that grunts occur in multiple
contexts, including both affiliativeand food-related.Kaldor(1996) lumped
grunts with girneys in her analyses and empiricallyfound them togetherto
be affiliative. My data are consistent with the suggestion that girneys are
affiliative,but I have little evidence that grunts have any emotionalvalence
Mouthposition differs from the othervisual expressionsdiscussed in that it
is intricatelytied with vocal production.Althoughvocalizationsand mouth
shapes must to some extent be associated, there is disagreementabout
the order of events on an evolutionarytimescale. Darwin (1872, p. 91)
mentioned this as an "obscurepoint, namely, whether the sounds which
are produced under various states of the mind determine the shape of
the mouth, or whether its shape is not determinedby independentcauses,
and the sound thus modified".Rowell (1962) suggested that vocalizations
are secondaryto visual signals, postures, and breathingpatternsof rhesus
monkeys. Andrew(1963) agreedthat vocalizationsare dependenton mouth
shapes, althoughhe suggestedthatthe mouth shapesoriginatedprimarilyas
protectiveresponses towardnoxious environmentalstimuli. Ohala (1984),
however, indicated that the vocalizations were primary:he suggested that
mouth shape originatedin orderto produce specific types of sound. Ohala
based his ideas on Morton's (1977) 'motivational-structural
predictthatan aggressiveanimalwill attemptto appearlargeby using sounds
of lower frequencies,and submissiveanimalswill try to appearsmall, using
higher-pitchedsounds (but see Hauser et al. 1993). Ohala suggested that
large size could also be communicatedby a large resonantchamber,such as
that createdby the roundedmouth of a macaquedisplayingan open-mouth
threat.Conversely,smallness could be conveyed by high resonance,which
would occur if the monkey pulled its lips back, shorteningthe length of the
resonance chamber.Ohala suggested that throughritualization,the mouth
shapes, originally in service of vocalizations,became independentand are
now communicativeon theirown.
I distinguishedbetween articulatoryand expressive movements of the
mouth. I found that the most common mouth shapes accompanyingeach
vocalization either matched the vocalization exactly (i.e. the mouth was
opened only to the degree necessary to produce the sound) or were of a
shape perhapsconstrainedby the requisite sound production(grimace for
screamsand squeaks;roundedopen mouthfor barks;neutralor lipsmacking
for girneys).This providesquantitativesupportfor the illustrationsin Hauser
et al. (1993) of typical articulatorygestures accompanying eight main
vocalizations of rhesus macaques. These data suggest that the mouth and
the voice are not emancipatedduring bimodal (vocal) production.During
unimodal,silent (visual) behavior,the mouth took on a variety of postures
and movementsnot observedduringvocalizations,althoughthe silent open
mouths,grimaces, and lipsmackswere similarin gross structureto the vocal
I compared the proportionof each vocalization that was accompanied
by matchingmouth shapes (see Fig. 6a). Gruntshad the highest scores for
mouthpositions exactly matchingthe vocalization,indicatingthattherewas
no particularsilent expressiveshapeof the mouththataccompaniedgrunting.
Hauseret al. (1993) found, similarly,that grunts were producedwith little
separationof the lips. I foundthatscreamsandsqueaks,in contrastto grunts,
had low scores for mouthmatching,indicatingthatthese vocalizationswere
often accompaniedby extended mouth expressions, in this case grimaces.
Girneys also had low scores for mouthmatching,because they were often
producedsimultaneouslywith extensive lipsmacking.
Matching mouth positions may carry no new information,being purely
redundantwith the vocalization, whereas an extended expressive mouth
position may provide additionalinformation.For example, an expressive
mouth position such as a prolonged, exaggeratedgrimace might reflect a
higher intensity response than a more utilitarian(smaller,briefer)grimace
thatsimply matcheda scream(see Maestripieri,1997; Partan,1998). Marler
(1992) discussed the idea that certain componentsof a signal may reflect
intensityof responsewhile othersreflectreferentialinformation.
The detailed associations among visual and vocal components of rhesus
monkey expressions demonstratea method for quantifyingthe structureof
multichannelsignals. The results provide new insights into signal structure
and quantitativesupportfor previousdescriptionsof rhesusbehaviorfound
in the literature.That particularvocalizations are not always paired with
the exact same visual expressions reflects the fact that all behavior is
probabilistic (as Altmann, 1965, discussed for sequences of behavior).
However,some vocal expressionswere consistentlypairedwith predictable
visual components;this was more often the case for screams and squeaks
thanfor barksandpant-threats.Silent expressionswere the most variablein
termsof the numbersof associatedvisual components.
Adams,D.B. & Schoel, M.W. (1982). A statisticalanalysisof the social behaviorof the male
stumptailmacaque(Macaca arctoides).- Am. J. Primatol.2, p. 249-273.
Altmann,S.A. (1962). A field studyof the sociobiology of rhesusmonkeys,Macaca mulatta.
- Ann. N.Y. Acad. Sci. 102, p. 338-435.
- (1965). Sociobiology of rhesus monkeys. II: Stochasticsof social communication.
J. theoret.Biol. 8, p. 490-522.
- (1967). The structureof primatesocial communication.- In: Social Communication
Among Primates (S.A. Altmann, ed.). The University of Chicago Press, Chicago,
Andrew, R.J. (1963). The origin and evolution of the calls and facial expressions of the
primates.-Behaviour 20, p. 1-109.
Argyle, M. & Cook, M. (1976). Gaze and mutual gaze. - CambridgeUniversity Press,
Boccia, M.L. (1986). Groomingsite preferencesas a form of tactile communicationandtheir
role in the social relationsof rhesus monkeys. - In: Currentperspectivesin primate
social dynamics(D.M. Taub& F.A. King, eds). VanNostrandReinholdCo., New York.
Bradbury,J.W.& Vehrencamp,S.L. (1998). Principlesof animalcommunication. Sinauer
Associates, Inc., Sunderland,Massachusetts.
Conner,W.E. (1987). Ultrasound:Its role in the courtshipof the arctiidmoth, Cynia tenera.
- Experientia43, p. 1029-1031.
Darwin, C. 1872/1897. The expression of the emotions in man and animals. - Second
edition. D. Appleton& Co., New York.
Deputte, B.L. (1994). Ethological study of yawning in primates.I. Quantitativeanalysis and
study of causation in two species of Old World monkeys (Cercocebus albigena and
Macacafascicularis). - Ethology 98, p. 221-245.
(2000). Primate socialization revisited: Theoretical and practical issues in social
ontogeny.- Adv. Study Behavior29, p. 99-157.
Drickamer,L.C. (1975). Quantitativeobservationof behavior in free-rangingMacaca mulatta: Methodologyand aggression. -Behaviour 55, p. 209-236.
Drummond,H. (1981). The natureand descriptionof behaviorpatterns.- In: Perspectives
in ethology, Vol. 4 (P.P.G.Bateson & P.H. Klopfer,eds). Plenum,New York,p. 1-33.
Fusani, L., Hutchison, R.E. & Hutchison, J.B. (1997). Vocal-posturalco-ordinationof a
sexually dimorphicdisplayin a monomorphicspecies: The Barbarydove. - Behaviour
134, p. 321-335.
Goldfoot, D.A. (1982). Multiplechannelsof sexual communicationin rhesusmonkeys:Role
of olfactorycues. - In: Primatecommunication(C.T. Snowdon, C.H. Brown & M.R.
Petersen,eds). CambridgeUniversityPress, Cambridge,p. 413-428.
Gouzoules, S., Gouzoules, H. & Marler, P. (1984). Rhesus monkey (Macaca mulatta)
screams:Representationalsignalingin the recruitmentof agonisticaid. - Anim. Behav.
32, p. 182-193.
Green, S. (1975). Variationof vocal patternwith social situation in the Japanese monkey
(Macaca fuscata): A field study. - In: Primate behavior (L.A. Rosenblum, ed.).
Academic Press, New York,p. 1-102.
& Marler,P. (1979). The analysis of animal communication.- In: Handbook of
behavioralneurobiology,Vol. 3; Social behaviorand communication(P. Marler& J.G.
Vandenbergh,eds). PlenumPress, New York.
Hauser, M.D. (1991). Sources of acoustic variationin rhesus macaque (Macaca mulatta)
vocalizations.- Ethology 89, p. 29-46.
- (1993). Rhesus monkey copulationcalls: Honest signals for female choice? - Proc.
R. Soc. Lond. B 254, p. 93-96.
- (1996). Vocal communicationin macaques:Causes of variation.- In: Evolutionary
ecology and behaviorof macaques(J.E.Fa & D. Lindburg,eds). CambridgeUniversity
- , Evans, C.S. & Marler,P. (1993). The role of articulationin the productionof rhesus
monkey,Macaca mulatta,vocalizations.- Anim. Behav. 45, 423-433.
- & Marler,P. (1993). Food-associatedcalls in rhesus macaques (Macaca mulatta):I.
Socioecological factors.- Behav. Ecol. 4, p. 194-205.
van derHeijden,P.G.,de Vries, H. & van Hooff, J.A.R.A.M.(1990). Correspondenceanalysis
of transitionmatrices,with special attentionto missing entriesandasymmetry.- Anim.
Behav.40, p. 49-64.
Hinde, R.A. (1966). Ritualizationand social communicationin rhesus monkeys. - Phil.
Trans.Roy. Soc. London251, p. 285-294.
& Rowell, T.E. (1962). Communicationby posturesandfacial expressionsin the rhesus
monkey (Macaca mulatta).- Proc. Zool. Soc. Lond. 138, p. 1-21.
van Hooff, J.A.R.A.M. (1962). Facial expressions in higher primates.- Symp. Zool. Soc.
Lond. 8, p. 97-125.
(1967). The facial displaysof the Catarrhinemonkeysandapes.- In:Primateethology
(D. Morris,ed.). Aldine Pub. Co., Chicago, p. 7-68.
(1973). A structuralanalysis of the social behaviour of a semi-captive group of
chimpanzees.- In: Social communicationand movement:Studies of interactionand
expression in man and chimpanzee (M.V. Cranach& I. Vine, eds). Academic Press,
(1982). Categoriesand sequencesof behavior:Methodsof descriptionand analysis.In: Handbookof methods in nonverbalbehaviorresearch(K.R. Scherer& P. Ekman,
eds). CambridgeUniversityPress, Cambridge,p. 362-439.
Itani,J. (1963). Vocal communicationof the wild Japanesemonkey.- Primates4, p. 11-66.
Jensen,G.D. & Gordon,B.N. (1970). Sequencesof mother-infantbehaviorfollowing a facial
communicativegestureof pigtail monkeys.- Biol. Psychiatry2, p. 267-272.
Kaldor,E.L. (1996). The meaning and social function of grunt and girney vocalizationsin
Macaca mulatta.- Msc thesis, Universityof California,Los Angeles.
Kalin, N.H., Shelton, S.E. & Snowdon,C.T. (1992). Affiliativevocalizationsin infantrhesus
macaques(Macaca mulatta).- J. Comp. Psychol. 106, p. 254-261.
Leger,D.W.& Didrichsons,I.A. (1994). An assessmentof datapooling andsome alternatives.
- Anim. Behav. 48, p. 823-832.
Lindburg,D.G. (1971). The rhesus monkey in North India: An ecological and behavioral
study. In: Primatebehavior:Developmentsin field research(L.A. Rosenblum,ed.).
Academic Press, New York,p. 1-106.
Machlis, L., Dodd, P.W.D. & Fentress,J.C. (1985). The pooling fallacy: Problems arising
when individualscontributemore than one observationto the data set. - Z. Tierpsychol. 68, p. 201-214.
Maestripieri, D. (1997). Gestural communication in macaques: Usage and meaning of
nonvocalsignals. Evol. Communic. 1, p. 193-222.
& Wallen, K. (1997). Affiliative and submissivecommunicationin rhesus macaques.
- Primates38, p. 127-138.
Marler,P. (1965). Communicationin monkeys and apes. - In: Primate behavior: Field
studies of monkeys and apes (I. DeVore,ed.). Holt, Rinehardtand Winston,New York,
(1982). Avian and primate communication:The problem of naturalcategories.
Neurosci. & Biobehav.Rev. 6, p. 87-94.
- (1992). Functions of arousaland emotion in primatecommunication:a semiotic approach.- In: Topics in primatology(T. Nishida,W.C.McGrew,P. Marler,M. Pickford
& F.B. deWaal,eds). Univ. of Tokyo Press, Tokyo,p. 225-233.
- & Hamilton,W.J. III (1966). Mechanismof animalbehavior.- John Wiley & Sons,
Martin, P. & Bateson, P. (1993). Measuring behaviour.- CambridgeUniversity Press,
Mason, W.A. (1985). Experientialinfluenceson the developmentof expressivebehaviorsin
rhesusmonkeys.- In: The developmentof expressivebehavior:Biology-environment
interactions(G. Zivin, ed.). Academic Press, New York,p. 117-152.
Massaro, D.W. (1998). Perceiving talking faces: From speech perception to a behavioral
principle. The MIT Press, Cambridge,Massachusetts.
Maxim, P.E. (1982). Contexts and messages in macaque social communication.- Am. J.
Primatol.2, p. 63-85.
(1985). Multidimensionalscaling of macaquesocial interaction.- Am. J. Primatol.8,
McGurk,H. & Macdonald,J. (1976). Hearinglips and seeing voices. - Nature264, p. 746748.
Mitchell, G. (1972). Looking behaviorin the rhesus monkey. J. Phenomenol.Psychol. 3,
Morton, E.S. (1977). On the occurrenceand significance of motivation-structural
some bird and mammalsounds. - Am. Nat. 111, p. 855-869.
Ohala,J.J. (1984). An ethologicalperspectiveon common cross-languageutilizationof Fo of
voice. - Phonetica40, p. 1-18.
Partan,S.R. (1998). Multimodalcommunication:The integrationof visual and vocal signals
by rhesusmacaques.- Dissertation,Universityof California.
- & Marler,P. (1999). Communicationgoes multimodal.- Science 283, p. 1272-1273.
(2002). The Umweltand its relevanceto animalcommunication.Introduction
to special issue. -J. Comp. Psychol. 116, p. 116-119.
Rawlins, R.G. & Kessler, M.J. (1985). Climate and seasonal reproductionin the Cayo
Santiagomacaques.- Am. J. Primatol.9, p. 87-99.
(1986). The history of the Cayo Santiago colony.
In: The Cayo Santiago
macaques: History, behavior and biology (R.G. Rawlins & M.J. Kessler, eds). State
Universityof New YorkPress, Albany,p. 13-45.
Redican, W.K. (1975). Facial expressions in nonhumanprimates.- In: Primatebehavior:
Developmentin field and laboratoryresearch(L.A. Rosenblum,ed.). Academic Press,
New York,p. 103-194.
Reynolds, V. (1976). The origins of a behavioralvocabulary:the case of the rhesusmonkey.
J. Theory Social Behav. 6, p. 105-142.
Rowe, C. (1999). Receiver psychology and the evolution of multicomponentsignals.
Anim. Behav. 58, p. 921-931.
& Guilford, T. (1996). Hidden colour aversions in domestic chicks triggered by
pyrazineodoursof insect warningdisplays. - Nature383, p. 520-522.
Rowell, T.E. (1962). Agonistic noises of the rhesus monkey (Macaca mulatta). - Symp.
Zool. Soc. Lond. 8, p. 91-96.
& Hinde, R.A. (1962). Vocalcommunicationby the rhesusmonkey (Macaca mulatta).
- Proc. Zool. Soc. Lond. 138, p. 279-294.
Sade, D.S. (1973). An ethogramfor rhesus monkeys:I. Antitheticalcontrastsin postureand
movement.- Am. J. Phys. Anthrop.38, p. 537-542.
de Waal, F.B.M., van Hooff, J.A.R.A.M. & Netto, W.J. (1976). An ethological analysis of
types of agonisticinteractionin a captivegroupof Java-monkeys(Macacafascicularis).
- Primates17, p. 257-290.
Zeller, A.C. (1986). Comparisonof componentpatternsin threateningand friendly gestures
in Macaca sylvanusof Gibraltar.- In: Currentperspectivesin primatesocial dynamics
(D.M. Taub& F.A. King, eds). VanNostrandReinholdCo., New York,p. 487-504.
(1996). The inter-playof organisationandfacial communicationin the macaques.- In:
Evolutionandecology of macaquesocieties (J.E.Fa & D.G. Lindburg,eds). Cambridge