Abstract The ability to understand emotion in others isone of the most important factors involved in regulatingsocial interactions in primates. Such emotional awarenessfunctions to coordinate activity among group members,enable the formation of long-lasting individual relation-ships, and facilitate the pursuit of shared interests. Despitethese important evolutionary implications, comparativestudies of emotional processing in humans and great apesare practically nonexistent, constituting a major gap in ourunderstanding of the extent to which emotional awarenesshas played an important role in shaping human behaviorand societies. This paper presents the results of two ex-periments that examine chimpanzees’ responses to emo-tional stimuli. First, changes in peripheral skin tempera-ture were measured while subjects viewed three cate-gories of emotionally negative video scenes; conspecificsbeing injected with needles (INJ), darts and needles alone(DART), and conspecific directing agonism towards theveterinarians (CHASE). Second, chimpanzees were re-quired to use facial expressions to categorize emotionalvideo scenes, i.e., favorite food and objects and veterinar-ian procedures, according to their positive and negativevalence. With no prior training, subjects spontaneouslymatched the emotional videos to conspecific facial ex-pressions according to their shared emotional meaning,indicating that chimpanzee facial expressions are pro-cessed emotionally, as are human expressions. Decreasesin peripheral skin temperature, indicative of negativesympathetic arousal, were significantly lower when sub-jects viewed the INJ and DART videos, compared to theCHASE videos, indicating greater negative arousal whenviewing conspecifics being injected with needles, andneedles themselves, than when viewing conspecifics en-gaged in general agonism.

Key words Emotion · Facial expressions · Skin temperature · Empathy

Introduction

The ability to understand emotion in others is one of themost important factors involved in regulating social inter-actions in primates. Such emotional awareness, or empa-thy, functions to coordinate activities among group mem-bers, enable the formation of long-lasting individual rela-tionships, and facilitate conciliatory tendencies (Goodall1968; de Waal 1989; Flack and de Waal 2000). The abil-ity to express emotional behavior and interpret its mean-ing in conspecifics has therefore played an important rolein the evolution of an interactive and moralistic social sys-tem that is regulated as much by conciliatory tendenciesas it is by dominance and aggression (de Waal 1996). At aproximate level, however, the way in which emotional in-formation is acquired and transmitted in nonhumanspecies is poorly understood, but remains central to ourunderstanding of the social function of emotional commu-nication and the evolution of empathy.

One of the primary ways in which humans are able tolearn about the emotional states of others is through affec-tive resonance, or emotional contagion. This refers to theautomatic and reflexive mimicry of facial expressions, vo-calizations, and postures in one individual in response tothe perception of these states in another (Hatfield et al.1994). Such mimicry can lead to physiological changesthat may be sufficient to initiate a similar emotional statein the observer, providing a mechanism for shared emo-tional experiences, or empathy, that is not dependent onconscious processes (A. Kappas, U. Hess, and R. Banse,unpublished work). This makes emotional contagion oneof the most powerful mechanisms for the passive trans-mission of affective information and the facilitation ofshared feelings and actions among social mammals, and alikely mechanism leading to the emergence of empathy inspecies related to humans.

Lisa A. Parr

Cognitive and physiological markers of emotional awareness in chimpanzees (Pan troglodytes)

Anim Cogn (2001) 4 :223–229DOI 10.1007/s100710100085

Received: 15 August 2000 / Accepted after revision: 8 April 2001 / Published online: 31 May 2001

ORIGINAL ARTICLE

L.A. Parr (✉ )Yerkes Regional Primate Research Center and Living Links,Emory University, 954 Gatewood Rd., Atlanta, GA 30329, USAe-mail: parr@rmy.emory.edu, Tel.: +1-404-7273653, Fax: +1-404-7273270

© Springer-Verlag 2001

In addition to emotional contagion, facial expressionsprovide a primary channel for the transmission of affec-tive information. Researchers have documented six uni-versally recognized and biologically determined facial ex-pressions of emotion in humans (Izard 1971; Ekman1972, 1973). These are anger, disgust, fear, happiness,sadness, and surprise. Furthering biological and evolu-tionary support for basic facial emotions is the evidencethat some facial expressions in human and nonhuman pri-mates are homologous, both in terms of their morpholog-ical structure, but also their social function (Preuschoftand van Hooff 1995). The bared-teeth display and the re-laxed open mouth face, or play face, in nonhuman pri-mates have been shown to be homologous with humansmiling and laughter, respectively (van Hooff 1973;Preuschoft 1992). In a cognitive task, chimpanzees wereable to discriminate five basic categories of facial expres-sions from photographs, i.e., bared-teeth display, scream,pant-hoot, play face, and relaxed-lip face, even whenthese expressions were made by different unfamiliar con-specifics (Parr et al. 1998). These results, in addition toother studies, support the conclusion that faces are an im-portant stimulus category involved in chimpanzee socialcognition (Parr and de Waal 1999; Parr et al. 2000). Thisis in contrast to rhesus monkeys that require considerabletraining on comparable face recognition tasks, and fail todiscriminate photographs of their facial expressions (Kana-zawa 1996; Parr et al. 2000).

To date only a few studies have attempted to quantifyemotional responsiveness, or examined the relationshipbetween facial expressions and emotion in nonhuman pri-mates, despite the overwhelming evidence for their relat-edness in humans (Chevalier-Skolnikoff 1973; Redican1982; Lanzetta and McHugo 1989; Fridlund 1994). R.E.Miller and colleagues, for example, demonstrated theability of rhesus monkeys to communicate affective infor-mation to one another using facial cues, some of which in-cluded facial expressions, like the fear grimace (Miller etal. 1959; Miller 1967). A stimulus monkey saw a condi-tioned stimulus (CS) that signaled an upcoming shock,while a responder monkey had access to a lever that,when pressed, would terminate the shock. The responder,however, could not see the CS directly, and only had vi-sual access to the face of the stimulus monkey. None-theless, the responder was able to use the facial cues givenoff by the stimulus monkey to successfully terminate theshock. Although both monkeys showed increased heartrate during the CS period, it is not clear from this studywhether these expressions were perceived emotionally be-cause both monkeys were scheduled to receive shock ifthe lever was not pressed (Miller et al. 1967).

In a more recent study, Parr and Hopkins (2001) mea-sured changes physiological arousal in chimpanzees usingtympanic membrane temperature (Tty), an index of sym-pathetically mediated changes in brain temperature, asthey viewed emotional videos. They reported significantincreases in right Tty in response to the negative emo-tional videos and increases in left Tty in response to thepositive emotional videos, although this effect was not as

strong as that found for right Tty. This study providedsupport for the lateralization of emotional processing inchimpanzees, in that the right hemisphere showed greaterarousal in response to negative emotional scenes.

Finally, G.G. Berntson and colleagues (Berntson et al.1989) showed changes in cardiac activity in chimpanzeesexposed to conspecific vocalizations. Heart rate was ac-celeratory in response to conspecific laughter, while re-sponses to screams were primarily deceleratory orientingresponses. Together, these studies provide evidence forthe physiological mediation of emotional processes innonhuman primates, and suggest ways in which emo-tional information may be transmitted in a social context,i.e., through facial cues and vocalizations. In addition,these data suggest that passively viewing emotional stim-uli can produce physiological changes in chimpanzeesthat are characteristic of emotional responses in humans.Based on these convergent lines of evidence, it becomesfundamental to our understanding of emotion and its phy-logenetic continuity to examine the extent to which chim-panzee facial expressions convey emotional information,and whether the passive transmission of emotional arousalin this species involves physiological changes similar tothose observed in humans.

This paper will examine two basic mechanisms for thetransmission of emotion in chimpanzees. First, the passivetransmission of emotional information will be measuredby recording changes in skin temperature as subjects viewemotional video scenes. Decreases in skin temperature re-flect sympathetic activity resulting from noradrenergicvasoconstriction, and have been associated with negativeemotional arousal in humans (Ekman et al. 1983; Rimm-Kaufman and Kagan 1996; Bauer 1998). Second, it willexamine the extent to which chimpanzees gain emotionalinformation from their facial expressions by requiringthem to categorize emotional video scenes presented on acomputer monitor by matching them to facial expressionsthat convey a similar emotional valence, e.g., positive ornegative. This task represents a novel version of the tradi-tional matching-to-sample paradigm in that instead ofmatching being based on recognizing stimuli according totheir shared perceptual features, like the same facial ex-pression made by two different individuals, it requiressubjects to recognize the emotional similarity between thestimuli presented. A hypodermic needle and a bared-teethdisplay, for example, both share a negative emotionalmeaning, but do not share physical features. Because thisnew dimension of matching is based on emotional simi-larity, or the emotional meaning shared by the stimuli, thetask is hereafter referred to as matching-to-meaning(MTM).

Methods

Subjects

Data were collected from three adult chimpanzees (Pan tro-glodytes), two males and one female, each approximately 12 yearsof age. The subjects were raised by humans in peer groups until

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four years of age when they were moved into enclosures with adultanimals (Bard 1994). All subjects had previous experience usingcomputer-based tasks (Hopkins 1997; Parr et al. 1998, 2000; Parrand de Waal 1999), but they had never been required to use facialexpressions as emotional markers, or to categorize emotionalscenes using facial expressions. Prior to these experiments, theyhad never seen the video stimuli presented. Subjects were notfood-deprived and all testing was voluntary.

General procedure

Stimuli consisted of high quality videos and photographs. Videoimages were filmed at the Yerkes Primate Center, Atlanta, Georgiausing a digital video camera (Cannon XL1) and later digitized at aresolution of 320×240 pixels, and compressed at 15 frames persecond using Cinepak codec. All video images were edited usingAdobe Premiere software. Still photographs were black and whiteand depicted only the head of unfamiliar chimpanzees making var-ious facial expressions. Most photographs depicted individuals liv-ing in colonies housed outside of the United States. Facial expres-sions included the bared-teeth face, scream face, pant-hooting, re-laxed-lip face, neutral portraits, relaxed open mouth expression (orplay face), and the whimper (van Hooff 1967). The ability of chim-panzees to discriminate among these expressions has been reportedelsewhere (Parr et al. 1998). These were scanned at a resolution of300 dots per inch (2.5 cm) and saved as bitmap files. The stimuliwere presented using a Pentium computer and 17-inch (43.5 cm)SVGA video monitor that were housed in an audio-visual cart.This was wheeled to the front of subjects’ home cage for testing.The joystick was mounted vertically to an opaque plastic panel at-tached to the subjects’ home cage so that the stick, approximately3 cm long, protruded through the mesh and could be manipulatedby the subject.

Stimuli and procedure: physiological measurements

Physiological measurements were made while subjects viewedvideos from four different categories, three examples of each(n=12). These videos were 6 s long. Three categories showed neg-ative emotional scenes and stimuli including CHASE, scenes ofveterinarians threatening chimpanzees with the dart-gun; INJ,scenes of chimpanzees being injected or darted during routinemedical procedures; and DART, scenes of hypodermic needles andthe dart-gun. The fourth category, WING, was a control categorythat showed scenes of the home environment including generalcaretaker activity, unfamiliar conspecifics not engaged in specificactivities, cage mesh, and transport boxes. The three scenes fromeach emotion category (CHASE, INJ and DART) were combinedwith an equal number of control scenes (WING) and presented tosubjects as three separate tasks (n=6). These three tasks were thenpresented to subjects in a counterbalanced order within a singletesting session. Subjects were tested consecutively so that subject1 saw CHASE, then subject 2 saw INJ, then subject 3 saw DART,then back to subject 1, and so on until each subject had seen eachof the three tasks (18 stimuli in total).

Video presentations were controlled by the subjects using thejoystick. First, subjects were presented with an orienting stimulus,an open white circle. They oriented to this by contacting it with thejoystick-controlled cursor. When this condition was met, the circleand cursor disappeared and the video scene played uninterruptedon the black background. This represented the completion of onetrial. After this the circle reappeared, and the chimpanzees had tomake another orienting response to engage another video. Eachvideo within a task was presented in a pseudorandom order so thateach video was seen once before any repetition. Testing was ter-minated when each chimpanzee had engaged each of the six videosin a task. Thus there was no repetition of stimuli.

Prior to testing, subjects had been trained to extend their fin-gers through the cage mesh. Before the video presentations, a tem-perature transducer (16×17×8 mm) was attached to the palmar sur-face of the distal phalanx of the left middle finger with a strap of

Velcro. The left hand was chosen because of the subject’s strongright hand bias for manipulating the joystick (Hopkins et al. 1996).This signal was then amplified with the lower response frequencyset to measure relative temperature change using a 0.05-Hz high-pass filter, and a sampling rate of 50 samples per second (BioPacSystems, Inc.). A 30-s baseline recording period preceded the at-tachment of the joystick to habituate subjects to the presence of thecomputer, experimenter, and temperature transducer before videopresentation. These data were digitized online and later analyzedusing Acknowledge software (BioPac Systems, Inc.).

Stimuli and procedure: matching-to-meaning

Stimuli in the matching-to-meaning experiment included four ex-amples of videos from seven categories (n=28); two were controlsand five were experimental. These videos were 5 s long. The firstcontrol category (CON1) included scenes of conspecifics engagedin severe aggression and intense play. A correct response was tomatch these scenes with still photographs of conspecifics makingscream and play faces, respectively. These were paired with hoots,whimpers, the relaxed-lip face, and neutral portraits as the non-matching comparisons. Subjects had been exposed to these videosin a prior experiment (L.A. Parr, unpublished work). In brief, thisexperiment involved presenting subjects with 20 videos depictingpositive and negative social contexts, i.e., five examples each ofscenes of intense and mild aggression, and intense and mild play.These were to be matched to scream or bared-teeth expressions,and play faces, respectively. Control scenes consisted of matchingfacial expression (similar to what was reported in Parr et al. 1998although involving videos), but these details are not important forthe present experiment. Subjects were given this task until theirperformance averaged above 85% correct for two consecutive test-ing sessions (50 trials per day1). Two examples of the severe ag-gression and intense play scenes were then chosen for use in theMTM task. Therefore, these CON1 videos controlled for motiva-tion during the MTM in that poor performance on this categorywould indicate low motivation since high levels of performancehad already been achieved. Good performance on this categoryduring the MTM task, but poor performance on the experimentalcategories, would be interpreted as a failure to understand the emo-tional similarity between the videos and facial expressions.

The second category (CON2) was a random control. It showedscenes of chimpanzees while they were resting or asleep. Thesewere arbitrarily paired with facial expressions that would not nor-mally occur in those situations, e.g., play faces, screams, hoots,and whimpers. Thus, CON2 provided a control for whether sub-jects were learning the discriminations according to their history ofreinforcement on those trials. If subjects performed well on exper-imental categories, but poorly on the CON2 controls, then it couldbe concluded that they understood the emotional similarity be-tween the videos and facial expressions. Because there was nosimilarity between the CON2 videos and their paired facial expres-sions, performance was not expected to exceed chance levels onthis category.

Stimuli from five experimental categories depicted positive andnegative emotional scenes and stimuli. The negative emotionvideos included the CHASE, DART and INJ categories describedabove. Also included were scenes of anaesthetized chimpanzeeslying on a gurney (KD). The correct comparisons for these videoswere negative facial expressions like scream faces and bared-teethdisplays. These were paired with other facial expressions includinghoots, play faces, relaxed-lip faces, and neutral portraits as thenonmatching comparisons. The positive emotion videos (POS) in-cluded scenes of the computer-testing apparatus and favorite foods.The correct comparisons for these videos were play faces. Incorrectcomparisons included hoots, screams, the relaxed-lip face, andneutrals.

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1 Subjects required an average of 433 trials to perform above 85%for 100 trials on this task (300–500 trials)

The stimulus presentation procedure was similar to that de-scribed for the physiological measurements, however, after sub-jects engaged the video they were presented with two comparisonfacial expression. The correct expression depicted an emotionalmeaning similar to that portrayed in the video, while the non-matching comparison was a facial expression that conveyed a dif-ferent emotional meaning, or was emotionally neutral, as describedabove (Fig.1). To make a response, subjects moved the joystick-controlled cursor to contact one of the two facial expressions(chance was therefore 50%). Correct responses were rewardedwith a squirt of grape juice and an inter-trial interval (ITI) of 3 s,while incorrect responses were not rewarded and followed by anITI of 10 s. Subjects received 56 trials during a daily session, rep-resenting two exposures to each of the 28 unique trials (4 examplesfrom 7 categories psuedorandomly presented as described above).Testing continued until performance averaged >85% over two ses-sions (n=112 trials).

Data analysis

Physiological measurements

Skin temperature changes were measured by averaging the tem-perature slope during each 6-s video scene. Because the responsetime for the transducer was 1 s, measurement began 1 s after thevideo had engaged and extended to 1 s after it had finished. Negativeslopes indicated a decrease in temperature, while positive slopesindicate an increase in temperature. Data were then analyzed usinga repeated-measures ANOVA with three levels of emotion(CHASE, DART, and INJ). Stimulus type was the repeated-mea-sures variable. Each individual subject contributed an equal num-ber of data points to the analysis (n=9 for each emotion category).

Matching-to-meaning

Data are presented in terms of the mean performance on eachvideo category for the first (trials 1–56) and second testing ses-sions (trials 57–112). Binomial tests will determine whether sub-jects perform above chance levels on each category. This includedan assessment of whether social information present in the videos,such as vocalizations or presence of conspecifics, influenced per-formance. To do this, videos were lumped into four broad cate-

gories, CON1, CON2, SOCIAL (videos that contained social in-formation, CHASE, INJ), and STIM (videos with no social infor-mation, DART, POS, and KD). Alpha was set at P<0.05 for allanalyses.

Results

Physiological measurements

The mean slope of skin temperature changes (+SEM) inresponse to the emotion and control scenes can be seen inFig.2. This figure shows the largest temperature decreasesfor the INJ and DART conditions. Overall, a significantmain effect of emotion condition was found, F(2,16)=5.12,P<0.02, indicating that temperature changes differedacross the video conditions. Post hoc comparisons using aleast significant difference (LSD) test revealed that tem-perature decreases were significantly greater in both theINJ and DART conditions compared to CHASE, P<0.03,and P<0.01, respectively.

There was, however, no main effect for stimulus con-dition, i.e., whether the video showed a scene from theemotion or control (WING) category. Temperature changesin responses to the control and emotion scenes were simi-

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Fig.1a–c An example of the matching-to-meaning (MTM) taskformat. From left to right these panels illustrate: a the orientingstimulus and the cross-shaped cursor; b the digitized video stimu-lus presentation showing an example from the DART category;and c the two comparison facial expressions, one of which conveysa similar emotional valence as that depicted in the video, e.g., pos-itive or negative. In this example, the correct response is to movethe cursor to contact the negative facial expression, scream face,on the right. The nonmatching example shows a play face on theleft

Fig.2 Mean slope of finger temperature changes (+SEM) for sub-jects during the presentation of emotional and control videoscenes. The asterisks indicate where performance across the emo-tion groups differs

lar in each task (Fig.2). This may simply reflect the factthat temperature changes occurred too slowly to revealsignificant differences between the emotion or controlcategories when these videos were presented together inthe same testing session.

Matching-to-meaning

Subjects performed significantly above chance on theMTM discriminations on the very first testing session (allcategories, z=1.87, P<0.05). This was regardless of whetherthe emotional categories contained social information(SOCIAL=68.8%, z=2.60, P<0.005), or whether the stim-uli were of a nonsocial type (STIM=63.9%, z=2.35,P<0.01). As expected, subjects performed the best on thepreviously learned control trials (CON1=83.3%, z=3.27,P<0.001), indicating good motivation. Performance didnot exceed chance levels on the random control(CON2=50.0%, z=0, P=0.50), indicating that subjectswere not simply learning the reinforcement contingenciesassociated with each trial. By the second testing session(trials 57–112), each stimulus category, except CON2,was discriminated significantly above chance. Figure 3shows the mean performance for each individual stimuluscategory after the first and second testing sessions.Overall, subjects required an average of 205 trials beforereaching the final performance criterion of >85% for twoconsecutive testing sessions, slightly over seven presenta-tions of the 28 unique discriminations. Performance neverexceeded chance levels for the random control, CON2.

Discussion

These data provide support for affective sharing as a pos-sible mechanism by which chimpanzees acquire emo-tional information from conspecifics. In the physiologicalmeasurement study, decreases in skin temperature weresignificantly greater when subjects viewed scenes of con-specifics being injected with darts and needles, and scenesof needles themselves, than when they viewed scenes ofconspecifics engaged in general agonism. Because view-ing the scenes of general agonism did not elicit strongsympathetic arousal in subjects, something more thanprimitive emotional contagion may have contributed tothe physiological findings. In humans, for example, de-creases in skin temperature have been recorded during ex-periments designed to elicit fear and sadness in subjects(Ekman et al. 1983). It may be that temperature decreasesin response to the DART scenes reflected the subjects’own fear when exposed to these highly aversive stimuli,or an empathic fear in seeing conspecifics being injectedwith needles (INJ). There is no doubt that chimpanzeesrespond aversively to these stimuli when they themselves,or their cagemates, are approached by the veterinariansfor their annual medical survey. Further studies areneeded to determine whether these results are indeed in-dicative of empathic processes.

These data also support the conclusion that chimpanzeeshave some understanding, or awareness, about the basicemotional meaning of their facial expressions. Withoutelaborate training, they were able to use their facial ex-pressions to categorize video scenes according to theirpositive and negative emotional valence, indicating thatemotional valence may be used as a discriminatory cue.Furthermore, these data suggest that the way in whichchimpanzees categorize social information and familiarstimuli from their environment may be simplified by us-ing emotional valence as a superordinate level category,similar to what has been reported in humans (Ortony et al.1988).

From these data, it would be premature to concludethat the chimpanzees were consciously aware of their cat-egorization process, or that their emotional feelings arequalitatively similar to that experienced by humans, al-though they do show similar patterns of physiologicalarousal. Answers to these questions are still beyond thescope of scientific inquiry. But because the subjects werenot physically participating in the emotional situationspresented, and these scenes depicted primarily nonsocialconditions (DART, POS, KD), the selection of specific fa-cial expressions may be considered representational, inthat they were used as markers of emotional valence. Thisdoes not imply that personal experience and social contextare unimportant for learning the emotional meaning andsignificance of social information. To the contrary, previ-ous research has shown that experience is critical for bothhuman and nonhuman primates to learn the emotional sig-nificance of their social signals (Sackett 1966; Miller etal. 1967; Hoffman 1975; Suomi et al. 1976; Harlow and

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Fig.3 The mean performance (+SEM) on the first (trials 1–56)and second (trials 57–112) testing sessions of the MTM task, in-cluding the grouped categories of stim (dart, kd, pos) and social(inj, chase). The asterisk indicates where performance exceededchance levels for that category according to a binomial test

Mears 1983; Davis 1984; Nelson 1987). Nor do these datasuggest that subjective feelings were unrelated to cogni-tive performance. The physiological data presented heresupports the conclusion that chimpanzees actually experi-enced some degree of personal arousal when viewingarousal in others, or when exposed to emotionally arous-ing stimuli, at least in the case of INJ and DART condi-tions. This is consistent with previous findings in thisspecies that used different measures of autonomic activity(Boysen and Berntson 1986, 1989; Parr and Hopkins 2001).

The most parsimonious explanation may be that whenthe chimpanzees are exposed to meaningful, emotionalstimuli, like hypodermic needles or veterinarian proce-dures, they are subject to physiological changes similar tothose observed during fear and sadness in humans(Ekman et al. 1983). These physiological changes maythen function to color, or bias, their perception of the en-vironment, facilitating an ability to characterize the videosalong an emotional continuum. This is similar to the dis-positional effects of emotional contagion in humans (Hat-field et al. 1994; A. Kappas, U. Hess, and R. Banse, un-published work). While these two mechanisms may worktogether to allow chimpanzees to process emotional infor-mation from conspecifics, perhaps facilitating altruisticand empathic behavior, the degree to which nonhumanprimates have a concept of emotion, or perceive basicemotion categories like those described in humans (Ek-man 1992) is yet to be demonstrated, but remains centralto our understanding of emotional behavior and its phylo-genetic continuity.

Acknowledgements The author thank Samuel Fernández-Carriba,Frans B.M. de Waal, Jessica Flack, William D. Hopkins, andAgnès Lacreuse for comments on earlier versions of this manu-script, Darren Long and Richard Wagner for technical assistance,and the animal care staff at the Yerkes Regional Primate ResearchCenter. Special thanks to Tetsuro Matsuzawa, Masaki Tomonaga,and the participants of the COE International Symposium onPhylogeny of Cognition and Language for their spirited scholar-ship. The Yerkes Primate Center is fully accredited by theAmerican Association for Accreditation of Laboratory AnimalCare.

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