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Dossier Déroutants primates : approches émergentes aux frontières de l’anthropologie et de la primatologie

Mutual coordination of behaviors in human–chimpanzee interactions: A case study in a laboratory setting1

Coordination mutuelle des comportements dans les interactions humains-chimpanzés: étude de cas en contexte de laboratoire
Akira Takada


Cette étude approfondit notre compréhension de la socialité qui s’instaure entre chimpanzés et humains en examinant l’organisation séquentielle de leurs interactions dans un contexte de laboratoire. Nous entreprenons une analyse interactionnelle de deux courts extraits vidéo à propos d’une situation de prise de mesures physiques sur des chimpanzés à L’Institut de Recherche sur les Grands Singes (GARI), Tamano, Japon. Les résultats indiquent que les chimpanzés manifestent comment ils perçoivent leur situation ou expriment ce qu’ils veulent par des mouvements du corps et des sons vocaux, tels que des gestes de la main, se gratter le corps, geindre, et crier. Les soigneurs produisent également des significations variées par des mouvements du corps et des déclarations verbales. Dans l’interaction avec les chimpanzés, ils favorisent notamment l’inclusion d’un type de communication typiquement humaine, le « tour de parole », en introduisant différents types de paires adjacentes. Ils produisent également d’autres types d’énoncés, par exemple des commentaires qui clarifient les comportements des chimpanzés, permettant de fluidifier le déroulement des interactions lorsque la réponse de ces derniers est obscure. La plupart des chimpanzés captifs et des humains du GARI semblent avoir formé des patterns d'interaction mutuellement coordonnés au cours de leurs histoires interactionnelles, ceci en dépit des différences entre  les ressources sémiotiques des deux espèces. Une exception est un nourrisson chimpanzé élevé par les humains : celui-ci n’a pas encore accumulé suffisamment d’histoires interactionnelles qui pourraient donner lieu à des configurations d’interaction stables avec les autres chimpanzés. Ceci a posé de sérieuses difficultés tant au nourrisson qu’aux autres chimpanzés, les empêchant notamment de bien s’entendre. Nos résultats suggèrent que les chimpanzés captifs peuvent s’adapter à une vie rythmée par les humains, au sein d’un milieu largement construit par ceux-là, et que les humains peuvent quant à eux coordonner leurs actions avec le rythme des chimpanzés. Ces résultats sont particulièrement importants et suggèrent que l’analyse des interactions humains-chimpanzés peut informer la recherche sur le fondement des sociétés humaines, chimpanzières, ainsi que de leurs sociétés partagées.

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1 Introduction: Studies of Communication among Chimpanzees

  • 1  This work is financially supported by JSPS Grant-in-Aid for Young Scientists (S)"Cultural formatio (...)

1A number of animal behavior studies have been conducted to help clarify various aspects of human sociality. Most of these have compared animal and human behaviors. Some research in the comparative cognitive sciences has focused on great apes, which are genetically similar to humans, and has explored the theme of hominization to reconstruct the evolutionary trajectory across species of great apes, including humans. Humans, chimpanzees, and gorillas are all hominoids that originated in Africa (Matsuzawa, 2006). Chimpanzees are an especially close evolutionary neighbor of humans and are genetically the most similar to them.

2Western scholars have focused on chimpanzees for a long time. According to Barnard (2011), London physician Edward Tyson recognized unexpected similarities between chimpanzees and humans at the end of the 17th century, particularly with regard to the brain, and he concluded that chimpanzees are located somewhere between Man and Common Ape (a category similar to Monkeys today). In the 18th century, Scottish judge Lord Monboddo believed that Orang Outang (a widely employed term used to mean today's great apes) habitually built huts, used tools, built fires, and even had a sense of honor. Jean Jacques Rousseau and Carolus Linnaeus also believed Orang Outang to be a ‘man,’ or, in Linnaean terms, to at least belong to the genus Homo. According to Cole (1996), Carolus Linnaeus, the father of systematic botany, also conducted a typological study of animal species. He divided the genus Homo into Homo sapience, which included Europeans,and Homo monstrous, which included Chinese, Hottentots, who are now known as Bushmen or the indigenous people of Southern Africa, and so on. These classifications illustrate the difference between how humans were once perceived, compared with present-day perceptions.

3In the 20th century, researchers began to conduct primatological and psychological studies using living chimpanzees. Of these, studies involving gestures and tool use are highly relevant to the main theme of this study: Analyzing the sequential organization of interactions between chimpanzees and humans.

4Chimpanzees can perform and learn gestures to a certain extent. A number of studies have identified similarities and differences between chimpanzees and human children in gestural communication. These findings are thought to be important when considering the origin of human language (Tomasello and Camaioni, 1997; Cartmill et al., 2014). Chimpanzees begin to touch objects by pointing a finger at the age of eight months, but unlike human children, do not point to objects located far away (Matsuzawa, 2005). Captive chimpanzees understand the meaning of human pointing and demonstrate ‘hand pointing’ in which they indicate an object by stretching out their arm toward it (Itakura, 1996; Itakura and Tanaka, 1998). According to Tomasello and Camaioni (1997), however, they do not make gestures to attract attention to other conspecifics or to humans or to indicate an object to them. In contrast, humans begin to use these gestures during the course of development. Cartmill and Byrne (2010) also concluded that whereas humans (even infants) use gestures to draw attention to an object or to comment on an aspect of the world, use of gestures among apes is primarily limited to requests that others interact or leave.

5In addition to the use of gestures, the use of tools is considered highly relevant to discussions of the origin of human communication. Chimpanzee infants in the wild are motivated by intellectual curiosity and begin to associate two objects from the age of approximately 1.5 years. When they reach the age of 3.5–5 years, they begin to associate a third object with the two objects. Their operation of tools becomes increasingly elaborate until the age of approximately 10 years (Matsuzawa, 1994; Nishida and Hosaka, 2001; Matsuzawa, 2005; Hayashi et al., 2006). Captive chimpanzees may demonstrate effective tool use at younger ages (Hirata, 2006). Moreover, a number of researchers have reported between-group differences along with within-group homogeneity with regard to tool use in the wild, even in the absence of genetic and environmental differences between groups (e.g., Whiten et al., 1999; Gruber et al., 2009). These observations suggest that chimpanzees learn certain behavioral patterns by observation. However, it should be noted that observational learning among chimpanzees requires trial-and-error experiences over a much longer time period than required by humans. Tomasello and colleagues claimed that after an individual invents a type of behavior, others in the group must re-invent it, primarily by copying the product or engaging in ‘emulation learning’ (Tomasello, 1999). Chimpanzees are considered to have a very limited ability to imitate (i.e., immediately reproduce another’s intended behaviors). In contrast, there is little doubt that human children begin to imitate very actively, beginning around the age of nine months, and then develop various kinds of cooperative behavior (Tomasello and Camaioni, 1997; Tennie et al., 2009; Tomasello et al., 2012).

6Some scholars have argued that chimpanzees have a ‘culture,’ based on their tool use. Tetsuro Matsuzawa, one of the leading primatologists in Japan, defines ‘culture’ as the whole of knowledge or skills shared by members of a certain community, and this is transmitted across generations, such as from parents to children, through non-genetic channels. He argues that cultural transmission of knowledge or skills occurs among chimpanzees: Female chimpanzees reveal their knowledge or skills when they move into other groups, and their children inherit this cultural tradition. Consequently, neighboring chimpanzee communities often share cultural features even though they encounter varied constraints in their surrounding environment (Matsuzawa, 2006). Recent experimental studies of chimpanzees have explicated how such cultural transmission of skills occurs both within and across groups (see the review on chimpanzee cultural transmission in Whiten et al., 2009). Moreover, Whiten and colleagues (2009) analyzed the definition of and recent findings regarding imitation and argued that if copying the form of an action (the copied action may include the use of objects that are not directly observed) is considered imitation, then chimpanzees rely more on imitation and have more cultural capacity than previously acknowledged.

7Some researchers have tried to document the relationship between gestures, tool use, and the development of proto-languages (e.g., Bickerton, 2002; Falk, 2004; Cartmill et al., 2014). Many have proposed that the human linguistic structure first emerged in gestures and later spread to vocalizations (Cartmill et al., 2014). After reviewing the literature on caregiver–child interactions among chimpanzees, bonobos, and humans, Falk (2004) argued that during hominization, the development of bipedalism and loss of infant clinging made hominin mothers more likely to use prosodic markings in accordance with gestural markings to encourage juveniles to behave in certain ways. Consequently, the meaning of some utterances became conventionalized and eventually developed into proto-languages. Recent studies of grammaticalization suggest that early proto-languages of hominins probably did not include suffixes or functional words but did include nouns and verbs (Heine, 1997; Heine and Kuteva, 2002). Such proto-languages might have been used in contexts similar to those in which chimpanzees now use various kinds of gestures. According to Falk (2004), chimpanzees’ infant-directed gestural communication is much richer than their infant-directed vocal communication. Many of the emotional states of chimpanzees are similar to those of humans and are expressed using a variety of easily recognizable facial expressions that, in turn, are frequently linked with particular vocalizations. Based on these findings, Falk (2004) proposed the above hypothesis regarding the development of a proto-language in hominins.

8Interestingly, captive chimpanzees who interact with humans often display high levels of performance that are rarely observed among wild chimpanzees. For example, they may understand the meaning of human pointing and use ‘hand pointing’ (Itakura, 1996). They may also achieve certain levels of performance at a younger age compared with their wild counterparts, such as mastering tool use (Hirata, 2006) and using gestures (Bard et al., 2014). When they are taught human-designed communication systems (e.g., modified American Sign Language or computer-based symbols), their communication style resembles that of two-year-old human children in some respects (see the review in Cartmill et al., 2014). These phenomena are well known among experimental primatologists and psychologists: The standard interpretation is that chimpanzees have a universal ability that emerges in certain situations (Matsuzawa, 2000). However, few studies have focused specifically on in which context and how such performances are elicited (for a notable exception, see Rossano, 2013). Instead, most researchers who engage in experimental work with chimpanzees have tended to focus on the level of performance they can elicit from a chimpanzee under various conditions.

9Interaction analysis is one of the most promising and effective ways to investigate this under-studied research topic. Interaction analysis is an empirical method for determining why an action is selected at a specific place and time by deconstructing the micro-sequential context (i.e., clarifying the relevance of the adjacent actions; Nishizaka, 1997; Schegloff, 2007). This approach makes it possible to analyze the sequential organization of interactions, incorporating not only the results of actions under certain situations but also the procedural context within which the actions take place. It can help clarify the great differences in performance between captive and wild chimpanzees and shed new light on the findings of previous studies involving captive and wild chimpanzees. This kind of analysis also deepens our understanding of the sociality that can be established between chimpanzees and humans, beyond species-related limitations, and of human sociality in general.

10Therefore, the present study involved using video recordings of interactions between captive chimpanzees and human trainers and researchers to analyze how their actions were spatiotemporally organized. The process of mutual adjustment of actions between chimpanzees and humans was investigated by focusing on the use of body movements and vocal sounds.

- (1) Body movements: body movements constitute one of the central semiotic resources (Goodwin, 2000) for interactions between captive chimpanzees and human trainers and researchers, who often try to understand what chimpanzees will do next based on their body movements. Moreover, chimpanzees can learn gestures from humans and communicate with them using these gestures. Human trainers and researchers may try to convey their messages using various gestures, including those they have not taught to chimpanzees. They also give various objects, including food, to chimpanzees, which facilitates embodied interactions between them.
- (2) Vocal sounds: chimpanzees in the wild can distinguish between and use various types of vocal sounds depending on the situation (Goodall, 1986). Some of the vocal sounds inform group members about important information of which they may be unaware (e.g., the presence of food or a snake) and strengthen affiliative relationships with social partners (Slocombe et al., 2010b; Crockford et al., 2012). When chimpanzees listen to vocal interactions among other individuals, they can extract social information about the callers (e.g., higher or lower ranking, victim or aggressor) from their vocal sounds and thereby interpret what is happening within the wider social context (Slocombe et al., 2010a). Human trainers often talk to captive chimpanzees using various verbal and non-verbal sounds, including those they have not taught the chimpanzees. These vocal sounds play important roles in organizing their interactions.

2 Methods

11We obtained approval from the ethics committee of the Great Ape Research Institute (GARI) at Hayashibara Bio-chemical Research Institute. I have periodically visited GARI to study interactions between captive chimpanzees and humans since 2008. GARI was founded in Tamano, a city in Okayama Prefecture, Japan, to promote research about the evolutionary foundations of human intelligence, behavior, livelihood, society, and culture by comparing great apes and humans. The GARI building is located at the tip of a small peninsula near a quiet seashore. Eight chimpanzees were being raised at GARI while I conducted my research (2008–2013). Regrettably, GARI was closed in 2013 due to financial problems: All chimpanzees (but none of the trainers) were transferred to the Kyoto University Kumamoto sanctuary, where they remain.

12I collected a large amount of video (approx. 400 hours in total) and other materials with the generous cooperation of the trainers and researchers at GARI. I conducted a preliminary analysis of the video materials and selected two short video clips that recorded a physical measurement event (specifically, ‘morph-physiological measurement’), in which chimpanzees actively interacted with human trainers in a narrow room. The clips reveal several of the fundamental patterns characterizing human–chimpanzee interactions at GARI, although we will need to further examine the rest of the dataset to draw generalizations about these patterns. The following analyses are based on systematic transcriptions of interactions in the video clips. First, I made detailed transcriptions of the verbal and non-verbal behaviors of each interactant along with the timeline for the two video clips. Here, because of space constraints, I have translated the utterances and omitted the original utterances made in Japanese.

13Utterances were transcribed according to a modified version of the conventions developed for conversation analysis research (for details, see Sacks et al., 1974; Schegloff, 2007). Information important to the utterance is indicated in double parentheses: (( )). Equal signs (=) indicate run-on utterances or an utterance that is interrupted by someone else. Pause length is marked in parentheses, in tenths of a second (e.g., (0.6)). Overlapping utterances are marked by square brackets: [ ]. Two degree signs (° °) enclose remarks that were markedly softer in tone compared with the discussion surrounding them. An up arrow (↑) indicates an increase in the pitch of the voice. Talk between ‘more-than’ and ‘less-than’ symbols has been compressed (> <) or slowed (< >). Audible laughter is indicated by the letter ‘h,’ and multiple uses of ‘h’ indicate more laughter. Stressed words have been underlined, and single parentheses indicate that an utterance was unintelligible or made by an unidentifiable source.

14I also loaded the video clips into Windows Live Movie Maker to capture still images from these interactions. By combining these materials, I was able to analyze how the interactions were spatiotemporally organized during these events.

3 Results and Discussion

3.1 Mutual coordination of behaviors between chimpanzees and humans

15During this kind of physical measurement session, the trainers would usually invite one or two chimpanzees, in turn, into the room from the outside field. Excerpt 1 was extracted from a video of the physical measurement of two female chimpanzees: TB (aged 12 years at the time) and NT (aged 3 years and 2 months). The following humans were involved in the data collection: F (a male trainer responsible for measuring the body parts of the chimpanzees), K (a female trainer responsible for helping F measure these body parts), H (a male researcher responsible for recording the video), and S (a male trainer responsible for recording the results of the measurement). S was excluded from transcription because he rarely interacted with other participants in the excerpt. Along with female chimpanzees TB and NT, a female infant chimpanzee HT (aged 1 year and 2 months) appeared in the video excerpt. HT and NT are half-siblings as they have the same father. Unlike NT, who was nursed by her mother TB, HT had been abandoned by her birth mother, MS, who appears in excerpt 2. Thus, HT had been raised by human trainers and researchers at GARI. Child abandonment is common among captive chimpanzees: As many as half of infants may be abandoned. In contrast, wild chimpanzee mothers form intimate relationships with their infants (Tomonaga et al., 2003; Matsuzawa, 2005). The close mother–child bond is shaped by mutual coordination between the mother and the baby: Mothers hold babies while babies cling to mothers (Matsuzawa, 2006). According to Matsuzawa (2005), it is particularly important for female chimpanzees to have sufficient physical contact with other chimpanzees, at least during their first year of life, to ensure they will successfully nurse a child later. This finding suggests that chimpanzees must learn to rear infants and that learning plays an important role in the life of a chimpanzee.

16On the day of the video recording, F entered the room while carrying HT under his arm. Before long, F carried out the physical measurements for NT and then TB. They engaged in physical measurements for approximately 11 minutes and then the activity shifted to a semi-free session. K measured TB’s heart rate using a stethoscope and then cut TB’s nails. K then measured NT’s heart rate. The video clip began at this point.

Table I (Excerpt 1)

Table I (Excerpt 1)

Physical measurement session for NT (born 2005.7.8) and TB (born 1996.2.17: Mo of NT).
Session de prise de mesures physiques sur NT (née le 8/7/2005) et sur TB (née le 17/2/1996 : mère de NT).

17At first, NT and TB climb on bars facing the next room and look outside. Then, TB comes back to the center of the room and squats on the stair set in front of the exit. TB looks at F, who is sitting in front of the tray with food inside, while stretching out her left arm toward him (line 3). This action is used to request food. Moreover, TB moves her left fingers repeatedly, as if she is reiterating the request (line 4). Immediately after TB squats on the stair, K utters a ‘change-of-state’ token “oh, really” (line 3) and then places a paper cup under TB’s genitals. H makes a comment “((TB is going to)) urinate” (line 4). TB starts urinating and looks at the exit. K makes an utterance to TB “okay, good girl TB” while receiving urine in the cup (line 5). Then TB’s urine seems to splash a bit. K and F say “wait” simultaneously (line 6). Following this, K makes a command to TB, saying “just wait ((it)) comes from various points.” and then “↑oh, wait, don't move.” in lines 7 and 8. After moving her left fingers again, TB leans toward F (line 10). Responding to this behavior F says “[oh wait, wait wait wait” in line 10. The utterances work as commands. Overlapping with F’s utterance, K also talks to TB saying “wait [TB, ahh hh” (line 10). TB then sits up straight. TB finishes urinating, and the urine seems to be caught in the cup. K says “okay” (line 11), and then K and F simultaneously say “yes” (line 12).

18TB turns around and sits on the board (line 13). K then makes a request to TB, saying “hey TB, let me show your bud >↑show your bud:: <” (line 14) to wipe the genitals. Then TB gets up on all fours (line 15). Simultaneously, NT touches the board and grabs TB's back (line 15). Seeing this, K says “NT no, NT no, no, don't do that” (line 16). F also calls NT (lines 17 and 18) to get her away from TB, while K wipes TB’s genitals. K then makes an utterance “yes good” which gives a positive assessment to TB (line 19).

19F then calls TB in line 20. TB then slowly moves to F. F further utters a command “hey, come on” to TB (line 24). TB then moves toward F while H makes an utterance “((TB)) was called by F” (line 25) for recording it in the video. F tells TB “sit” (line 26), and she immediately sits on the ground. F then says “[°hey°” (line 27), while stretching out his right hand, which contains some food, to TB. F then says “take it” to TB (line 28). However, TB hesitates to take the food piece. TB touches her mouth with her left hand and grabs a stair with her right hand (line 30). F gives TB a candidate understanding of this gesture, namely the interpretation that TB wants to go back to the yard (lines 30 and 32). TB then turns around and faces the stairs while holding the stairs with both hands. She then looks back at F again while scratching her body with her left hand (line 32). F then reiterates the command saying “come here”, “TB, here, here” (lines 34 and 35). Simultaneously, F points to the ground while looking at TB. TB turns around and looks at F. When F makes a command “right on” in a stressed voice (line 36), she sits straight in front of F. F picks up a piece of food from his pocket (line 38). However, TB fidgets and looks away from F again while scratching her body (line 38). Looking at this F stretches his right hand toward TB and then gives an interpretation of TB’s behavior “((will you)) go back?” (line 40), which already appeared in lines 30 and 32. F then makes a comment about TB today, saying “((you are)) unusually on tenterhooks” (line 41) and asks her a question “why are you ((like that))?” (line 42). Without answering this question, TB then turns around and climbs up the stair (line 43). Seeing this, F gives an interjection “yoisho” in a spirited voice (line 43). Looking at this K murmurs “°((will you)) go back?°” (line 44). The utterance not only gives her a candidate understanding of TB’s behavior but also shows agreement with F’s understanding, manifested in line 40. F reiterates his candidate understanding “((will you)) go back?” again (line 45) and then makes a comment “you’re strange” to TB who in sitting on the board (line 46).

Use of body movements

20We identified several distinctive features of the body movements of the captive chimpanzees at GARI based on the above interactions. First, TB used a hand gesture to request food. Great apes are known to make several types of requests (Cartmill and Byrne, 2010; Rossano, 2013; Bard et al., 2014). The chimpanzees at GARI were prohibited from taking food from the tray directly. Instead, they were taught to make a hand gesture to request food or a pointing gesture to indicate which food they wanted. All chimpanzees at GARI learned these gestures. Accordingly, TB made a request to F for some food on the tray using a hand gesture (stretching out the left arm toward F and moving the fingers repeatedly) in lines 3 and 4 (Figure 1). However, F announced a hold on the request in line 6, as TB was going to urinate at that time. In response, TB moved her left fingers again (line 9), which reiterated the request. This is consistent with the observation the same gesture was sometimes repeated when it initially did not generate a response (Liebal et al., 2004; Cartmill and Byrne, 2010). However, F did not give her any food. Then, TB leaned toward F (line 10) to get closer to F in front of the food.

Figure 1

Figure 1

TB stretches out the left arm toward F (sitting outside of the frame).
TB déploie son bras gauche en direction de F (en dehors de l’image).

21As exemplified by the above interplay, food often works as an object encouraging interactions between chimpanzees and humans. Note that food is not only transferred from human to chimpanzee to be eaten: It is also used as a resource for eliciting an utterance or behavior from the recipient in the form of turn-taking during human–chimpanzee interactions (see the next section). The base sequence here is the adjacency pair of request and acceptance/rejection (Schegloff, 2007).

Figure 2

Figure 2

TB grabs a stair by the hand.
TB saisit un barreau de la main.

22The hand gesture functioned as an index of a wider sequence of actions. There is no doubt that chimpanzees can use indices (a type of sign in the classification developed by Peirce’s Sign Theory) in their interactions (Tanaka and Matsuzawa, 2000). We also recognized other forms of index in the above excerpt. For example, TB gestured by grabbing a stair by one hand (line 30; Figure 2), which indexes the movements to go back to the outside yard. F interpreted this as such and gave TB a candidate understanding (lines 30 and 32). TB then turned around and faced the stairs while holding the stairs, this time with both hands (line 32; Figure 3). It should be noted that TB used not only her hands but also her whole posture and gaze direction to index the movements to go back to the outside yard.

Figure 3

Figure 3

Figure 3 TB holds the stair by her both hands.
TB tient le barreau de ses deux mains.

23As another type of gesture, TB scratched her body several times to demonstrate frustration. For example, even though TB made gestures that indexed the movements to go back to the outside yard, F did not allow her to do that. Then, she scratched her body with her left hand while looking at F (line 32; Figure 4). Similar behavior is seen again later: after F made a command to sit straight and then picked up a piece of food from his pocket, TB scratched her body while looking away from F (line 38). The action of scratching is thought to be not a personal behavior to relieve itching, but rather a social behavior to show frustration in response to the unwelcome command made by F.

Figure 4

Figure 4

Figure 4 TB scratches her body by the left hand while looking at F.
TB gratte son corps de la main gauche tout en regardant F.

Use of vocal sounds

24A number of semiotic resources can be used to frame turn-taking. Among others, verbal utterances by humans have various meanings in chimpanzee–human interactions. The offer made by F in lines 27 and 28 is one example: it worked as the first pair part of an offering sequence, a type of adjacency pair. The question asked by F in line 42 also works as the first pair part of a question–answer sequence, another type of adjacency pair (Schegloff, 2007). Moreover, the trainers frequently issued directives to chimpanzees, which also work as the first pair part of an adjacency pair. Directives are broadly defined as utterances designed to get (an) addressee(s) to perform a goal-oriented action or an “utterance intended to get the listener to do something” (Goodwin, 2006). Takada (2013) has proposed several sub-classes of directives in Japanese that depend on the intensity of action, ranging from (1) commands, to (2) requests, (3) suggestions, (4) prompts, and (5) invitations. In lines 7 and 8, K issued commands to TB by her utterance “just wait ((it)) comes from various points. ↑oh, wait, don’t move”, while setting a paper cup under TB’s genitals. Accordingly, TB kept sitting on the stair. In lines 26, F issued a command to TB by his utterance “sit” and a gesture (nodding his head), and TB then sat down on the ground. F further issued commands by his utterances “[°hey°, take it” and gesture (stretching out his right hand to TB) in lines 27 and 28, but TB did not accept it this time. When the trainers at GARI issue directives to chimpanzees, they mostly use commands, specifically utterances in which the verb takes the form of the imperative, together with certain non-verbal behaviors that also indicate directives.

25The chimpanzee’s responses to directives were often followed by third turn assessments (Pomerantz, 1984) by the human trainers. In the above excerpt, K issued several commands to make TB urinate without moving away (lines 6, 7, 8, and 10). Accordingly, TB finished urinating successfully. K then issued the positive assessments “okay, yes”, which complimented TB’s behavior (lines 11 and 12). Similar interplay between F and TB was identified on lines 10 to 12 as well. It should be noted that a third turn assessment can function to indicate that a certain behavioral sequence is completed. In the above example, immediately after the simultaneous assessment turns by F and K (line 12), TB started to shift her action, by turning around and sitting on the board (line 13). This shift in movement indicates that TB understood that the previous sequence of actions was completed and thus she was allowed to move on.

26Human trainers are able to issue a second pair part of an adjacency pair, for example F’s utterance “wait”, which held TB’s request in line 6. However, compared with the number of cases that were issued by the first pair part of adjacency pairs, human trainers appear to issue the second pair part relatively less frequently. This trend probably reflects the fact that chimpanzees issue the first pair parts of adjacency pairs less frequently than human trainers.

27Another type of verbal utterance made by the human trainers is giving a candidate understanding of certain chimpanzee behaviors. For example, seeing that TB hesitated to take the food piece (line 28), F said “will ((you)) go back?” (line 30). The utterance provided a candidate understanding of what the previous behavior by TB meant. Then, TB turned around and faced the stairs while holding the stairs with both hands (line 32; Figure 3). F gave TB a candidate understanding of this by saying “((do you)) wanna go back?” (line 32). The main feature of this type of verbal utterance (i.e., giving a candidate understanding of the prior behavior) is that the speaker takes the viewpoint of observer and can respond to whatever movement is initiated by and whatever state is experienced by the recipient. After the utterance, the recipient is not obliged to respond. Similar features are also recognized when human trainers make comments on the behaviors of chimpanzees, as exemplified by the utterances “((you are)) unusually on tenterhooks” in line 41 and “you’re strange” in line 46, as well as chanting together with the onset of chimpanzee behaviors, as exemplified by the utterance “yoisho”, made when TB climbed up the stairs (line 43). These types of verbal utterances are particularly useful for speakers to smooth the flow of interactions and when the speaker cannot expect a clear response from the recipients.

3.2 Caregiver–child interactions among chimpanzees and humans

28This section focuses on more complicated human–chimpanzee interactions, specifically interactions in which more than two chimpanzees are actively engaged. The analysis will illustrate some differences between human–chimpanzee and chimpanzee–chimpanzee interactions.

29Excerpt 2 was extracted from a video of the physical measurement of female chimpanzees MS (aged 9 years) and MZ (aged 11 years). These measurements were performed slightly before Excerpt 1, on the same day. This excerpt took place in the same small room with the same human trainers and researcher who appeared in Excerpt 1, along with the female infant chimpanzee HT. The humans (F, K, H, and S) had the same responsibilities as in Excerpt 1. S was again excluded from the transcription because he rarely interacted with other participants in the excerpt. As mentioned above, HT was raised by human trainers and researchers because her mother (MS) had stopped nursing her soon after birth. F entered the room carrying HT under his arm. At the time of recording, the group was enjoying a semi-free session before the onset of physical measurements.

Table II (Excerpt 2)

Table II (Excerpt 2)

Physical measurement session for MS (born 1999.1.14: Mo of HT) and MZ (born 1996.12.16).
Session de prise de mesures physiques sur MS (née le 14/1/1999 : mère de HT) et sur MZ (née le 16/12/1996).

30MZ curiously looks at HT, who is clinging to F, and touches HT’s head with her left hand. Seeing this, F gives a candidate understanding of MZ’s behavior by saying “do you need her?” (line 1). F then hands HT to MZ. MZ makes short grunts “o o” and receives HT (line 4), while HT whimpers “[huhuhu” (line 6). MS scratches her head and then moves behind MZ and HT toward the direction of K (line 3). Then, MS hugs K from the back and leans on her while K says “[hey you, why ((do you)) lean on me while your own child is over there?” (line 6). Although this utterance by K contains an accusatory nuance, K does not resist MS leaning on her back. K then starts swinging her body while MS is on her back and looks at the interplay between MZ and HT (line 7).

31After receiving HT with both hands, MZ swings her upside down and kisses HT’s back around the genitals (lines 7 and 8). HT struggles by moving her extremities. Seeing this, F makes an accusatory utterance “why [((do you)) (turn her upside down)?” in line 7. Overlapping with this utterance, H makes the comment “[((she)) immediately turns her upside down, umn” to the video (line 8). F then makes a comment “her genitals are slightly swollen” (line 10). K acknowledges this by saying “umn” in line 11.

32HT keeps moving her extremities. Meanwhile, MS leaves K and then moves behind MZ and HT toward the direction of F (line 12). MS then hugs F from his left side (line 13). Grabbing MS’s left elbow with his left hand, F asks a question “Didn’t you return to be sane during the thunder” to MS (line 15). Thunder here indicates the recent heavy rain. By asking this tag question in a joking manner, F indicates that MS is insane, because she has not taken care of her child HT. MS leaves F and then touches her face to HT, held by MZ (line 16). HT is moving her extremities. F adds the comment “you won’t change unless it ((=thunder)) falls on you” (line 17). MS walks around MZ and looks at HT again (line 19). MZ changes his grip on HT and touches her face to HT (line 20). MZ then stands up and moves forward while holding HT (line 21). During the course of these actions, HT whimpers “huhuhuhuhu” (line 21) and then gives a short scream “hh kiki” (line 22) while opening her mouth wide and moving her extremities. MZ looks into HT’s face. MS follows MZ and looks at HT from MZ’s right side (line 22). HT keeps moving her extremities. Then, K says “((MZ)) is grabbed ((by HT))” (line 25) and “((MZ’s)) face hair is grabbed ((by HT))” (line 26). MZ then sits down while holding HT (line 27). H comments on this by saying “MZ holds her in a bad manner” in line 28. F then says to HT, “you too ((bad, because you)) always come to humans” in line 29. HT looks at F while moving her extremities. Then, F exchanges a few words, which are difficult to hear in the video, with K (lines 30 and 31). Then, MS comes to HT, who is whimpering by opening her mouth wide, and glances at her (line 33). However, MS immediately goes back to K and leans on the back of K (lines 34 and 36). K swings her body while having MS on the back (line 37).

33MZ then puts HT on the ground (line 37). Looking at this H says “what’s going to happen?” (line 38). HT whimpers “huhuhuhu” (lines 38 and 39). When MZ picks up HT and holds her in front, HT utters a short scream, “kiki, ki” (lines 40 and 41). HT then becomes quiet while MZ is holding her while MZ makes thrusting movements (line 41). Due to page restrictions, 12 lines are omitted here.

34In line 54, MZ stretches out her right hand to food and points to her face. This is a gesture requesting that F give her the food piece. F looks at MZ's face. H makes a comment, saying “((MZ is)) holding HT.” (line 56). MZ then touches F’s right hand as if to repeat the request (line 57). F replies to this action by saying “wait” in line 58. MZ then starts licking HT’s body (line 60). When she licks HT’s genitals, F says to MZ, “things are going to be complicated because you do like that” (line 62).

35F then looks to HT, held by MZ, and calls HT by saying “°little HT°” in line 63. HT looks at F and whimpers “huhuhu” while pursing her lips and moving her left arm (line 64). Looking at this, F gives a candidate understanding of HT’s reactions, saying “[you feel like coming to this side, don’t you?” (line 65). MZ licks HT's body again (line 66). MS leaves K and goes around MZ toward F (line 66). Then, MS immediately turns around and moves to K from her back (line 67). Although K says “what?” to MS, K allows MS to lean on her (line 68).

36MZ touches HT's face and grooms her with her right hand while looking at HT (lines 68 and 69). Then, F addresses HT by name by saying “°little HT°” again (line 70). HT moves her extremities as she tries to move toward F (line 71). MZ then holds HT tight in front of her (line 72). This action appears to hide HT from F and, at the same time, prevents her moving away. F says “umn” to MZ (line 73). Then K comes closer to MZ and looks at HT while holding MS on her back (line 74). MS then leaves K and goes around MZ toward F (line 74). However, MS immediately turns around and moves to MZ and curiously looks at HT (line 76). MS almost touches her face to HT. F looks at HT (line 77). MZ then looks away from them (line 78). MS follows HT and looks at HT again (line 78). F then says to MZ, “shall we do ((the physical measurement))? how do you do? give ((HT)) to me.” (line 79) and then takes HT from MZ (line 80). MZ scratches her body (line 81).

Uses of body movements

37In this video excerpt, one of the female chimpanzees, MZ, showed great interest in the infant chimpanzee HT. However, the mutual coordination of body movements between MZ and HT did not go well. For example, MZ touched HT (line 1) and then held her (line 6). When MZ held HT upside down and kissed around her genitals, HT started struggling by moving her extremities (lines 7 and 8; Figure 5). Moreover, HT uttered a short scream when MZ stood up and started moving forward while holding HT awkwardly. MZ then quizzically looked into HT’s face (line 22) while HT grabbed MZ’s face hair as if resisting her (lines 23). Soon, MZ put HT on the ground (line 37). HT whimpered, which indicates she was afraid (lines 38 and 39). When MZ picked up HT abruptly and held her tightly in front of her, HT again uttered a short scream (lines 40 and 41; see the next section regarding the vocal sounds that they made during these interplay).

Figure 5

Figure 5

MZ holds HT upside down, and HT struggles by moving her extremities.
MZ tient HT à l’envers, et HT se débat en remuant ses extrémités.

38Because HT had mainly been raised by humans, she was not used to the behavioral patterns of chimpanzees. For example, MZ often licked her body, while human trainers rarely did so. HT was more accustomed to the behavioral patterns of human caregiving. When F looked at HT and called her a name (lines 63), HT immediately responded by looking at him and whimpering while moving her left arm and pursing her lips (line 64). F quickly interpreted these actions to mean that HT wanted to move to his side (line 65) (for a discussion, see the next section as well).

39The other female chimpanzee, MS, also showed some interest in HT, who is her biological daughter. Nevertheless, MS could not interact with HT smoothly. In this video excerpt, MS touched HT’s face while HT was held upside down by MZ in line 16 (Figure 6). Then, she went back and forth around HT while HT was being held by MZ and looked at HT many times (lines 19, 22, 33, 76, and 78). However, she was not involved in any additional physical interaction with HT. Instead, MS hugged or leaned on F and K several times (lines 6, 13, 36, 59, and 68). K swung MS from side to side while she was on her back (lines 7 and 37). The human trainers had cared for MS since her childhood and had helped shape her behavioral patterns. When MS felt frustrated, these behavioral patterns appeared to ease her.

Figure 6

Figure 6

MS touches her face on HT held upside down by MZ.
MS touche HT de son visage tandis que celle-ci est tenue à l’envers par MZ.

40Adult chimpanzees other than mothers are known to enjoy holding infants. However, they are not permitted to do this unless the mother trusts them. Therefore, these adults often groom the mothers to gain their trust (Nishida and Hosaka, 2001; Matsuzawa, 2005). Interestingly, in this excerpt, although MS is HT’s birth mother, she probably had to gain the trust of MZ, who had primary access to HT, to get closer to HT.

41When MS looked at HT, she tended to persistently gaze at her. For example, when MS looked at HT (line 19), MZ soon stood up and then moved forward while holding HT (line 21). However, MS followed MZ and looked at HT from MZ’s right side (line 22; Figure 7). Similarly, MS curiously looked at HT and almost touched her own face to HT’s (line 76). MZ then looked away from her as if to avoid the gaze. Nevertheless, MS followed HT and kept looking at HT (line 78). This kind of persistent gaze is a distinctive pattern of interaction among chimpanzees. Researchers have suggested that the pattern is highly relevant to their learning style; that is, taking a long time to observe and reiterating using trial-and-error countless times. Young chimpanzees are reportedly able to acquire a certain pattern of behavior by repeatedly observing the relevant behaviors as they are performed by nearby individuals. When they observe such behaviors, they often come very close to these individuals (Ueno, 2006; Fujimoto, 2008). Mothers are usually tolerant of their children looking at them, despite the fact that adult chimpanzees frequently fight with one another (Matsuzawa, 2005).

Figure 7

Figure 7

MS looks into HT from MZ’s right side.
MS regarde HT depuis le côté droit de MZ.

Uses of vocal sounds

42Goodall (1986) classified 34 discrete chimpanzee calls along with the emotions with which they are associated. However, vocalizations that lack signs of emotional arousal are rarely observed among chimpanzees (Tomasello and Camaioni, 1997; Goodall, 1986).

43Excerpt 2 illustrates several of the distinctive vocalization patterns of chimpanzees. When F handed HT to MZ, MZ made short grunts “o o” (line 4). This vocalization showed that MZ acknowledged that she received HT. HT’s whimpers of “[huhuhu” (line 6) and “huhuhuhuhu” (line 21) indicate that HT was afraid of being held awkwardly. Nevertheless, MZ stood up and moved forward while holding HT (line 21). The following short scream, “hh kiki”, and her facial expression (opening her mouth wide)(line 22) shows that HT was frightened of being carried in an uncomfortable position by MZ. The whimpers, screams, and facial expressions made by HT in lines 32–35 and 38–41 demonstrate a similar pattern of awkward interplay between MZ and HT.

44In contrast, HT was accustomed to interacting with human trainers using vocal sounds. When F looked at HT and called her name softly by saying “°little HT°” (line 63), HT immediately responded by whimpering “huhuhu” with her lips pursed. Moreover, she started moving her left arm widely while looking at him (line 64). F interpreted these reactions by HT to mean that she wanted to move to his side (line 65). A similar pattern of interactions was also observed between F and HT in lines 70 and 71. These call-and-response interplays exemplified one of the common types of adjacency pairs. As shown in these examples, the human trainers at GARI tended to treat HT as they would treat a human infant. HT coordinated her actions to respond to this treatment. Such coordination is understandable given that human-raised chimpanzee infants are known to develop several communicative gestures and to actively engage in various kinds of play with human caregivers (Bard et al., 2014). Indeed, even researchers who are skeptical about chimpanzees’ capacity to imitate have admitted that some human-raised chimpanzees seem to focus more on actions (Tennie et al., 2009). Additionally, researchers have demonstrated interesting similarities in the developmental process of chimpanzee and human children. For example, like human babies, chimpanzee babies are born with distinctive primitive reflexes such as the Moro reflex, rooting reflex (the reflex by which a newborn infant will turn his/her head toward anything that strokes his/her cheek or mouth, searching for the object by moving his/her head or mouth in steadily decreasing arcs), and the sucking reflex (Matsuzawa, 2006). Moreover, human and chimpanzee infants exhibit neonatal smiling (Tomonaga et al., 2003; Matsuzawa, 2005), neonatal imitation (Myowa, 1996), and general movements (a series of gross movements of variable speed and amplitude that involve all parts of the body) (Tomonaga et al., 2003). The features of eyesight are more or less identical between humans and chimpanzees (Matsuzawa, 2006). Chimpanzees even come to ‘laugh’ in association with vocalization during the course of development (Matsuzawa, 2005; also see the review of chimpanzee facial expressions in Waller and Micheletta, 2013).

45Human trainers teased the chimpanzees several times, which sounded like accusations about certain chimpanzee behaviors. For example, when MZ held HT upside down and kissed HT around the genitals, F made an accusatory utterance “why [((do you)) (turn her upside down)?” to MZ (line 7). MZ did not respond to F. Nevertheless, F did not make further accusations. F thus appears not to have expected that MZ would understand the meaning of his accusatory utterance when he made it in line 7. Rather, he appears to have intended the surrounding humans to be the hearers of his utterance addressed at MZ. Note that ‘hearer’ does not necessarily coincide with ‘addressee’ —an ‘addressee’ is the speaker’s view of a recipient, whereas the ‘hearer’ is a party other than the speaker who participates in a portion of the talk (Goffman, 1981: 131–133; Goodwin and Goodwin, 2004). F’s later utterance, “things are going to be complicated because you do like that” (line 62), exhibited a similar function of twitter.

4 Concluding Remarks

46Previous studies have reported that despite the well-known intelligence of chimpanzees, they have very a limited ability to use symbols, compared with humans. Some scholars have proposed the use of symbols as a distinctive feature of humans, playing a central role in communication (Piaget, 1937/1952, 1942/1951; Tomasello, 1999; Tennie et al., 2009; Cartmill and Byrne, 2010; Tomasello et al., 2012; Cartmill et al., 2014). The logical consequence of these claims is that the style of communication between humans and chimpanzees would be very constrained and imbalanced. However, this was not the case during the actual interactions between humans and chimpanzees examined here. Additionally, a number of researchers have expressed attitudes sympathetic to the behaviors of chimpanzees and have written about the emotional rapport they developed with them (Goodall, 1986; Matsuzawa, 2000; Nakamura, 2009; Bard et al., 2014).

47Our results suggest that humans and chimpanzees are able to mutually coordinate their behaviors to a considerable extent using diverse semiotic resources other than symbols. Using various kinds of body movements and vocal sounds (including hand gestures, scratching, facial expressions, grunts, whimpers, and screams), the chimpanzees demonstrated how they perceived their situation or what they would like to do. Human trainers also enacted various meanings by using their body movements and verbal utterances. In particular, they encouraged chimpanzee–human interactions through turn-taking, a distinctive style of human communication, by introducing several types of adjacency pairs. Additionally, when they did not expect clear responses from the chimpanzees, they used other types of utterances, such as offering a candidate understanding of chimpanzee behaviors, making comments about chimpanzee behaviors, and chanting together with the onset of chimpanzee behaviors, to help smooth the flow of the interactions.

48Semiotic resources used by humans overlap partially with those used by chimpanzees. Additionally, environmental settings affect which resources are available for the actual interactions. A multimodal approach is thus necessary to unravel how human–chimpanzee interactions are organized (cf., Goodwin, 2000; Waller et al., 2013). Our results suggest that the captive chimpanzees at GARI lived in accordance with the rhythm of the human trainers and researchers. The humans enabled the chimpanzees, on which they depended for their professional livelihood, to develop skills they would never have developed in the absence of interactions with humans while also adjusting their own actions in accordance with the rhythm of the chimpanzees. In this sense, the chimpanzees also domesticated the humans (Lestel, 1998). As they have accumulated interactional histories, the chimpanzees at GARI have formed a common context with human trainers and researchers despite the differences between species. Most of the ‘abilities’ that were attributed to chimpanzees were extracted from the behavioral patterns observed in those close humans.

49In contrast, the interactions between HT and adult chimpanzees reveal that their interactional history is currently insufficient to ensure stable interaction patterns among them. This resulted in serious interactional problems between HT and the other chimpanzees, which made it difficult for them to get along. This is quite different from Rossano’s (2013) findings about mother–infant interactions among captive bonobos: Mothers, and infants who were raised by their mothers, regularly engaged in successful adjacency pair-like sequences and persisted in soliciting responses when they were not forthcoming. The behavior of respondents was generally very cooperative and did not require much coercion or insistence by initiators.

50The interaction patterns between HT and adult chimpanzees reflects both the interactional history of these individuals and the more general features of captive chimpanzees who have spent a considerable proportion of their life in close contact with humans. Further research is needed to systematically distinguish these aspects from each other.

51By attempting to analyze how these cross-species interactions are organized, we worked to disentangle the deep congruence between nature and society from the perspective of the participants in the interactions (Sugawara, 2002). Furthermore, by accumulating such attempts, we may be able to redraw the boundaries between humans and chimpanzees.

52Most ethology and cognitive science research involving captive chimpanzees has tried to assess what chimpanzees can achieve within a framework of methodological individualism. These studies tend to be based on individualistic ability, especially the universal ability that allows each individual chimpanzee to operate objects or signs. In contrast, we did not disconnect the sender and the receiver of information in the actual interactions, but used the relationship between them as the unit of analysis. We also tried to clarify the mechanisms by which each action was embedded in the proximate social context as well as how it constructed the proximate social context for the next action.

53The two kinds of studies differ only in terms of approach. We cannot say which approach is ‘right,’ but an individualistic approach is less able to focus on sociality among humans and chimpanzees. As is often said, society is more than the sum of its individuals. By clarifying the mechanisms by which interactions are spatiotemporally organized, we will be able to reconsider the foundations of societies built by humans, those built by chimpanzees, and those co-built by humans and chimpanzees. This kind of approach will also open the way to empirical research about the dynamic processes by which individuals are socialized into a given society and how they may change the society.

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1  This work is financially supported by JSPS Grant-in-Aid for Young Scientists (S)"Cultural formation of responsibility in caregiver-child interactions" (Project No. 19672002 headed by Akira Takada) and JSPS Grant-in-Aid for Challenging Exploratory Research "Mutual understanding across species: Construction of ability in human-chimpanzee interactions" (Project No. 24650136 headed by Akira Takada).

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Table des illustrations

Titre Table I (Excerpt 1)
Légende Physical measurement session for NT (born 2005.7.8) and TB (born 1996.2.17: Mo of NT).Session de prise de mesures physiques sur NT (née le 8/7/2005) et sur TB (née le 17/2/1996 : mère de NT).
Fichier image/png, 135k
Titre Figure 1
Légende TB stretches out the left arm toward F (sitting outside of the frame).TB déploie son bras gauche en direction de F (en dehors de l’image).
Fichier image/png, 216k
Titre Figure 2
Légende TB grabs a stair by the hand.TB saisit un barreau de la main.
Fichier image/png, 242k
Titre Figure 3
Légende Figure 3 TB holds the stair by her both hands.TB tient le barreau de ses deux mains.
Fichier image/png, 236k
Titre Figure 4
Légende Figure 4 TB scratches her body by the left hand while looking at F.TB gratte son corps de la main gauche tout en regardant F.
Fichier image/png, 235k
Titre Table II (Excerpt 2)
Légende Physical measurement session for MS (born 1999.1.14: Mo of HT) and MZ (born 1996.12.16).Session de prise de mesures physiques sur MS (née le 14/1/1999 : mère de HT) et sur MZ (née le 16/12/1996).
Fichier image/png, 186k
Titre Figure 5
Légende MZ holds HT upside down, and HT struggles by moving her extremities.MZ tient HT à l’envers, et HT se débat en remuant ses extrémités.
Fichier image/png, 133k
Titre Figure 6
Légende MS touches her face on HT held upside down by MZ.MS touche HT de son visage tandis que celle-ci est tenue à l’envers par MZ.
Fichier image/png, 168k
Titre Figure 7
Légende MS looks into HT from MZ’s right side.MS regarde HT depuis le côté droit de MZ.
Fichier image/png, 146k
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Référence électronique

Akira Takada, « Mutual coordination of behaviors in human–chimpanzee interactions: A case study in a laboratory setting », Revue de primatologie [En ligne], 5 | 2013, document 69, mis en ligne le 12 avril 2014, consulté le 08 mai 2021. URL : ; DOI :

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Akira Takada

46 Yoshida-Shimoadachi, Sakyo, Kyoto 6068501 Japan, The Graduate School of Asian and African Area Studies, Kyoto University.
Author for correspondence:

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