Discussion post

Is Overimitation a Uniquely Human Phenomenon? Insights From Human Children as Compared to Bonobos

Zanna Clay University of Birmingham and Durham University

Claudio Tennie University of Birmingham and University of T€ubingen

Imitation is a key mechanism of human culture and underlies many of the intricacies of human social life, including rituals and social norms. Compared to other animals, humans appear to be special in their readiness to copy novel actions as well as those that are visibly causally irrelevant. This study directly compared the imitative behavior of human children to that of bonobos, our understudied great ape relatives. During an action-copying task involving visibly causally irrelevant actions, only 3- to 5-year-old children (N = 77) readily copied, whereas no bonobo from a large sample did (N = 46). These results highlight the distinctive nature of the human cultural capacity and contribute important insights into the development and evolution of human cultural behaviors.

Debate over the uniqueness of human culture and the role that imitation plays in its evolutionary and ontogenetic development has become the focus of increasing research attention (Caldwell & Millen, 2009; Meltzoff & Prinz, 2002; Tennie, Call, & Toma- sello, 2009; Tomasello, 1999; Whiten, 2016). In par- ticular, comparative research has attempted to identify what makes human culture special as com- pared to that of other great apes, and to identify

similarities and differences in the underlying social learning mechanisms (Tomasello, 1996; Tomasello, Savage-Rumbaugh, & Kruger, 1993; Vale et al., 2016; Whiten, 2013; Whiten, 2016). Imitation, which in this article we define as the faithful copying of others’ body movements, has elicited particular attention as it has been proposed to form a core component of human culture, enabling the acquisi- tion of causally opaque material culture and action- based cultures (e.g., gestures and dance), as well as contributing to their accumulation over time (Acerbi & Tennie, 2016; Dean, Kendal, Schapiro, Thierry, & Laland, 2012; Gergely & Csibra, 2006; Tennie et al., 2009; but see Caldwell & Millen, 2009; Caldwell, Schillinger, Evans, & Hopper, 2012; Morin, 2015). Imitation is also involved in many of the complexities of human social life, including norms, rituals, and conventions (Legare & Nielsen, 2015; Legare & Watson-Jones, 2015; Meltzoff & Prinz, 2002; Rakoczy, Warneken, & Tomasello, 2008).

A striking feature of human imitation is the extent to which humans are prepared to imitate actions that appear causally irrelevant (Horner & Whiten, 2005; Lyons, Young, & Keil, 2007; McGui- gan, Whiten, Flynn, & Horner, 2007). This phe- nomenon, termed “overimitation,” emerges early during childhood (Lyons et al., 2007; Over & Car- penter, 2012). It occurs in both Western and non-

[Article updated on July 26, 2017, after first online publication on July 24, 2017: University of T€ubingen was added to the affilia- tions of Dr. Claudio Tennie.]

We thank Claudine Andr�e, Fanny Minesi-Andre, Raphael Belais, Pierrot Mbonzo, Dominique Morel, and Valery Dhanani for their collaboration at Lola ya Bonobo Sanctuary and the Min- istry of Research and the Ministry of Environment in the Demo- cratic Republic of Congo for supporting our research (MIN.RS/ SG/004/2016). We thank the staff members at the Lola ya Bonobo Sanctuary for their support, particularly to Stany Mokando and Jean-Claude Nzumbi. We thank Brian Hare for support and Chris Krupenye for coordinating bonobo testing. and Charles Clay for developing the stimuli prototype We thank Lynsey Rutter, Lauren Deere, and the staff at ThinkTank Science Museum for enabling our research. We are grateful to all the children and families who participated in this research. We thank Polly Cowdell for reliability coding and Harriet Over, Eva Reindl, and Elisa Bandini for the comments on earlier drafts of the manuscript. We thank three anonymous reviewers for their valuable comments on this manuscript. This research was funded by the People Programme (Marie Curie Actions) and the Euro- pean Research Council under the European Union’s Seventh Framework Programme for research, technological development, and demonstration under REA grant agreement no. 628763 awarded to Zanna Clay. The research was also supported by a grant awarded to Claudio Tennie from the Economic and Social Research Council (ESRC; ES/K008625/1).

Correspondence concerning this article should be addressed to Zanna Clay Department of Psychology, Durham University, South Road, Durham, DH1 3LE, United Kingdom Email: [email protected].

© 2017 The Authors Child Development © 2017 Society for Research in Child Development, Inc. All rights reserved. 0009-3920/2018/8905-0007 DOI: 10.1111/cdev.12857

Child Development, September/October 2018, Volume 89, Number 5, Pages 1535–1544

Western cultures (Berl & Hewlett, 2015; Nielsen & Tomaselli, 2010) and gradually increases with age, starting from around 3 years old (McGuigan, Glad- stone, & Cook, 2012; McGuigan, Makinson, & Whiten, 2011; McGuigan et al., 2007). Overimitation is thought to underlie many human sociocultural behaviors including rituals and other forms of nor- mative behavior (Legare & Nielsen, 2015; Legare & Watson-Jones, 2015; Nielsen, Kapit�any, & Elkins, 2015). It is also involved in cumulative technologi- cal culture; thus, it was suggested that children’s overimitation is driven by their need to learn about causally opaque cultural artifacts (Lyons et al., 2007). This may be especially important in cases where cultural accumulation has led to artifacts whose causal properties have become complex and opaque; that is, copying is required to produce or use them (Gergely & Csibra, 2006; Lyons et al., 2007; Whiten, McGuigan, Marshall-Pescini, & Hop- per, 2009). Nevertheless, recent research has shown that overimitation is strongly motivated by social factors, such as to affiliate with or “be like the other” (Keupp, Behne, & Rakoczy, 2013; Nielsen, 2006; Nielsen & Blank, 2011) and to conform to per- ceived conventions and norms (Herrmann, Legare, Harris, & Whitehouse, 2013; Keupp et al., 2013; Legare & Nielsen, 2015). For instance, children are more likely to copy when the task is framed as being normative (Keupp et al., 2013; Legare & Niel- sen, 2015; Moraru, Gomez, & McGuigan, 2016) and after being primed with third-party ostracism (Over & Carpenter, 2009a, 2009b). They can infer friend- ship and social status from watching others imitate (Over & Carpenter, 2015) and trust individuals more that have imitated them (Over, Carpenter, Spears, & Gattis, 2013).

The study that originally reported what came to be known as overimitation (Horner & Whiten, 2005) contrasted children’s copying with an appar- ent absence of this behavior in captive chim- panzees, a finding that has since been replicated for orangutans (Nielsen & Susianto, 2010). Children were willing to insert a stick into both an opaque and a clear box in order to retrieve a reward, even though the insertion in the latter was visibly cau- sally irrelevant. Although this influential study has stimulated a plethora of studies, it is limited in its ability to detect overimitation in the sense in which we define it here (i.e., with a focus on action copy- ing). This is because pure action copying could not be distinguished from other forms of social learn- ing due to the fact that the captive chimpanzees were already competent stick users. In other words, this stick-based task could detect copying

of the location of the stick insertion, rather than copying the action itself. Thus, for both the apes and the children, this task more accurately tested “local overenhancement” and/or overemulation learning (see Tennie, Call, & Tomasello, 2006 for discussion). Note this experiment also involved a “two-target task,” where objects could be moved to one of two sides. Copying here was likewise likened with imitation; however, although this task controlled for local enhancement, it could not fully pinpoint action-based imitation as it could not exclude so-called “object-movement reenactment” (Custance, Whiten, & Fredman, 1999; Heyes & Ray, 2000). Later studies, which added actions that neither changed nor moved objects, were generally unable to find action copying in chimpanzees (Ten- nie, Call, & Tomasello, 2012) but found it in chil- dren (Legare, Wen, Herrmann, & Whitehouse, 2015).

Given these constraints and the fact that no equivalent data are yet available for the capacities of our other closest living relative, the bonobo (Pan paniscus), the question of whether overimitation is uniquely human among the great apes remains unresolved. Nevertheless, it is acknowledged that some animals will copy some actions under certain conditions (Huber et al., 2009). This includes, for example, the so-called “Do as I do” studies which involve heavily trained animals (Call, 2001; Custance, Whiten, & Bard, 1995; Miles, Mitchell, & Harper, 1996). There is also evidence from “encul- turated” great apes that have received extensive experience in human-centered environments (Bjork- lund, Bering, & Ragan, 2000; Buttelmann, Carpen- ter, Call, & Tomasello, 2007; Byrne & Tanner, 2006; Call, 2001; Carrasco, Posada, & Colell, 2009; Hayes & Hayes, 1952; Miles et al., 1996). Importantly, however, the extent to which ecologically relevant animals—that is, those that are untrained and also unenculturated—spontaneously copy actions remains hotly debated (Whiten, 2016; Whiten, Cus- tance, Gomez, Teixidor, & Bard, 1996; Whiten, Hor- ner, Litchfield, & Marshall-Pescini, 2004; Zentall, 1996, 2006). The lack of resolution is partly due to methodological constraints in distinguishing imita- tion from other social learning processes (Heyes & Ray, 2000; Tennie et al., 2006).

To date, most research on great ape social learn- ing has focused on two-target tasks involving experimental puzzle boxes that can be opened in more than one way in order to retrieve a reward (Horner & Whiten, 2005; Horner, Whiten, Flynn, & de Waal, 2006; Whiten, Horner, & de Waal, 2005; Whiten et al., 1996, 2009). Although two-target

1536 Clay and Tennie

tasks provide many key insights into the factors shaping animal cultural transmission (Galef, 2015; Whiten, 2016), they cannot clearly distinguish imita- tion from other learning mechanism due to the fact that the demonstrator movements are confounded with the object movements (Custance et al., 1999; Whiten et al., 2004, 2009). Thus, animals can plausi- bly solve the tasks via emulation, which is the copying of results of actions on the environment (Heyes & Ray, 2000; Tennie et al., 2006). Moreover, given that chimpanzees are able to copy the move- ments of the apparatus in two-target tasks without seeing actions leading to these results (Hopper, Lambeth, Schapiro, & Whiten, 2008), emulation can- not be ruled out. Successful performance on two- target tasks (Custance et al., 1999) is also wide- spread in the animal kingdom (Galef, 2015; even in reptiles, Kis, Huber, & Wilkinson, 2015), thus limit- ing its usefulness for determining what truly makes human cultural learning special or why wild great apes, especially chimpanzees and orangutans, are such expert tool users (Meulman & van Schaik, 2013; Sanz, Call, & Boesch, 2013; Whiten et al., 1999).

Although some great apes will spontaneously copy familiar actions (Fuhrmann, Ravignani, Mar- shall-Pescini, & Whiten, 2014; Tennie et al., 2012), evidence of novel action copying— which is a core component of human culture—has not been convinc- ingly demonstrated using two-target tasks. This is because the target actions generally fall within the species-typical repertoire, such as pulling or poking (Tennie et al., 2012). Given the importance of copy- ing novel actions in human culture, it is essential to determine whether great apes can copy novel actions. So far, only two studies with captive chim- panzees have addressed this question, accounting for the various methodological confounds (Tennie et al., 2012; Tomasello et al., 1997). Both tested imitation of novel actions where no physical information about the task was available, that is, removing the possibil- ity of emulation. Although one of the studies found some evidence of familiar action copying in a single chimpanzee subject (Tennie et al., 2012), neither detected novel action copying in any subject.

Here, we addressed the confounds of previous studies by designing a paradigm that could test for pure overimitation while excluding other social learning mechanisms. We did this by using purely manual gestures as the target actions where no physical information was provided about the solu- tion. In order to probe the potential for overimita- tion, some of the target actions were visibly causally irrelevant. We included target actions that

were, to our knowledge, novel or at least very unli- kely to be part of a species-typical repertoire.

To promote the possibility of demonstrating imita- tion by great apes, we focused our attention to bono- bos, a species of great ape that is equally as related to humans as chimpanzees yet comparatively less stud- ied. For a number of reasons, bonobos may represent a more promising candidate species to demonstrate imitation than chimpanzees. This is because bonobos outperform chimpanzees on sociocognitive tasks (Herrmann, Hare, Call, & Tomasello, 2010) and show enhanced social orientation (Kano, Hirata, & Call, 2015; Kret, Jaasma, Bionda, & Wijnen, 2016) and high levels of social tolerance (Hare & Kwetuenda, 2010). Given the inherently social nature of imitation, an activity requiring both social attention and social tol- erance, the enhanced social orientation of bonobos may enhance their imitative capacity. The current study explored evidence for pure, spontaneous action imitation in a large sample of untrained and nonenculturated sanctuary-living bonobos as com- pared to 3- to 5-year-old children. This sample is the largest of its kind ever used with a single great ape species for a pure action imitation study. If lower social tolerance and the methodological constraints emerging from the nature of previous tasks impede the performance of great apes, we should expect bonobos to show evidence of overimitation. If overimitation is a human unique behavior, we should not expect bonobos to copy any of the visibly causally irrelevant actions.

Method

Participants

Seventy-seven typically developing children, aged 3–5 years, participated in this study (Mage = 4.4 years, range = 3.1–5.9 years; N = 43 males). We selected this age range as children of this age are already manually competent, show reliable evidence of imitation behavior (e.g., Hopper et al., 2008; Horner & Whiten, 2005; McGuigan et al., 2007; Whiten et al., 1996), and are comfortable being tested individually, enabling more cross-species compar- isons. Children were recruited from ThinkTank Science Museum in Birmingham, West Midlands, UK, and randomly assigned to conditions. Child test- ing took place between April and December 2015. Using parental questionnaires, we determined that all were typically developing, had normal or cor- rected to normal vision, and spoke English as their first language: 69 children were monolingual, whereas eight were bilingual (English + Urdu/

Overimitation in Children as Compared to Bonobos 1537

Punjabi/Spanish/Sinhalese/French/Arabic/Polish). The sample comes from an area of high ethnic diver- sity consisting of approximately 58% Caucasian, 27% Asian/British Asian, 9% Black/African/Caribbean, 6% mixed children; the participants came from working middle-class backgrounds (estimated from census data for each county, Office of National Statistics, 2011). Five children refused to participate in the task and were excluded from analyses. The remaining children were randomly assigned to one of three conditions (N = 27 in the rub and rotate condition [uncommon actions]; N = 26 in the cross and trace condition [typical actions] and N = 19 in the control condition).

Forty-six nonenculturated and untrained bono- bos also participated (Mage = 11.3 years, range = 3– 29 years; N = 25 male). Testing took place in June 2015. The bonobos were housed at Lola ya Bonobo Sanctuary, a naturalistic forested sanctuary, in the Mont Ngafula district, Kinshasa, DR Congo (see Supporting Information). The majority of subjects were orphans, having arrived at the sanctuary as victims of the bushmeat and pet trades. Three were born and mother reared at the Sanctuary. Following several years of rehabilitation within a cohort group, individuals are integrated into large, mixed age groups. The majority of our subjects (N = 36) were housed in large, outdoor enclosures. We addi- tionally tested 10 juveniles housed in a nursery. Nursery individuals were cared for by human sub- stitute mothers within a naturalistic forested enclo- sure with age-matched peers. For subjects from the main enclosures, the experiments were conducted in their sleeping dormitories and before their morn- ing feed in order to maximize motivation. Testing rooms (15 m2) had a meshed ceiling with wide bars through which the experimenter could hand items to the subject, which they could then manipulate themselves inside their testing room. In the nursery, the experiments were conducted face to face with the experimenter within their enclosures and sleep- ing dormitories.

Materials and Procedure

For all participants, the task involved the opening of a small box (10 9 6 9 3 cm, Figure 1), made of two halves of a single piece of wood. A small cham- ber was carved out in the middle to place the reward, held in place by a peg and hole mechanism.

For both test conditions, each participant first took part in a demonstration phase followed by a test phase. All participants were tested individually in a quiet testing area. Children’s parents waited behind

an occluder so were not visible. All participants observed a human demonstrator who, facing the participant, looked at the box and then slowly per- formed two consecutive actions onto it before open- ing it to reveal the reward inside, which was provided to the participant. Due to health and safety reasons, children received stickers, whereas bonobos received a food reward (apple piece)—as is typical in such cross-species studies (e.g., Herrmann & Toma- sello, 2015; Hopper et al., 2008). This procedure was repeated three times. Between demonstrations, the demonstrator refilled the box behind an occluder, preventing the refilling and closing from being seen.

We tested imitation for actions that we considered plausibly typical or uncommon based on our direct observations of actions performed by bonobos and children, and our knowledge of their typical manual behaviors. In the “uncommon” action condition (rub–rotate), the demonstrator placed the back of the right hand on the top of the box and slowly rubbed it in a clockwise circular motion four times. Next, the demonstrator raised the right hand into the air next to the box and slowly rotated the wrist four times. Given the difficulty in ascertaining whether a demonstrated behavior is truly novel for a long-lived species (Zentall, 2001), we considered these two actions to be “uncommon” on the basis that, to our knowledge, they had not been previously observed in the study population or any other observed by the authors, and were also unlikely to occur within the species-typical repertoire. We also included a “typi- cal” action condition (cross–trace), which included actions that were rare but nevertheless fell within the ape species-typical repertoire and have also been observed in this bonobo population (Z. Clay, per- sonal observations). Here, the demonstrator held the box (left hand) and with the index finger, slowly traced a diagonal cross across the top of the box. Next, the demonstrator used this finger to trace around the groove of the box, around its full diame- ter. There was also a control condition (children only) in which everything remained the same except that no target actions were demonstrated.

Following each demonstration, the demonstrator pretended to refill the box behind the occluder but swapped it with a replica box, which was identical in dimensions and external appearance except that it did not actually open (the groove resembled that of the other box, but in reality was not deep enough to open). The use of a replica maximized the chances of observing imitation once species-typical solutions were individually discovered to be ineffective.

During the test phase, each participant was pro- vided with the replica box, without verbal

1538 Clay and Tennie

instruction. Participants were given up to 2 min to interact with the box. Regardless of performance, all participants were rewarded at the end of the trial. Tri- als were videotaped using a digital Sony Handcam CX330 camcorder (www.sony.co.uk) mounted on a tripod.

Coding

The occurrence of accurate matches of any of the four demonstrated actions was coded from video (yes or no). A second coder, blind to the hypotheses and conditions, recoded 25% of the videos. Interobserver reliability across all conditions was excellent (Cohen’s j = .94, SE = .05). Complete details of coding proto- col are provided in the Supporting Information.

Ethical Statement

We received ethical clearance from the University of Birmingham Ethical Review Committee (ERN_13- 1412) and the Marie Curie European Commission Ethical Screening Program (no. 628763). This study conformed to University of Birmingham’s Code of Practice for Research. For children, we received full approval and ethical clearance from ThinkTank Museum and full informed consent from parents. For the bonobos, we received full ethical approval to con- duct this study from “Les Amis des Bonobos du Congo” (ABC, Lola ya Bonobo Sanctuary). This study complied with all legal requirements required for conducting research in DR Congo (research permit: MIN.RS/SG/180/011/2016).

Results

We observed high levels of spontaneous imitation by children across both uncommon (rub–rotate) and typical (cross–trace) action conditions. The majority of children readily copied at least one of

the two observed actions in both conditions—rub– rotate: 77.8% of children (21/27); cross–trace: 81% of children (21/26). Of these children, approxi- mately one-third spontaneously copied both actions demonstrated to them—rub–rotate: 39% children (8/27); cross–trace: 27% children (7/26), see Fig- ure 2. For cases where children only copied one of the two actions, in both conditions it was most often the second demonstrated action that was cop- ied, suggesting a working memory constraint and/ or a recency effect (for single action responses, copying of the second demonstrated action

Figure 1. Image of the wooden box stimuli used in the imitation experiment (also showing a reward sticker provided to child partici- pants). [Color figure can be viewed at wileyonlinelibrary.com]

A

B

0.00

0.20

0.40

0.60

0.80

1.00

0

0.2

0.4

0.6

0.8

1

Figure 2. Results showing proportion of child (N = 52) and bonobo (N = 46) participants that spontaneously imitated the observed actions in the (A) uncommon (“rub–rotate”) condition and the (B) typical (“cross–trace”) condition. [Color figure can be viewed at wileyonlinelibrary.com]

Overimitation in Children as Compared to Bonobos 1539

occurred in 10/13 cases for rub–rotate and 12/15 cases for cross–trace). During a control condition, where everything remained the same except that no demonstration was performed, no child (N = 19) performed any of the target actions. In all cases of copying, the children copied the demonstrated (cau- sally irrelevant) actions first, before potentially per- forming any causally relevant actions to open the box (i.e., trying to pry open the box).

In contrast, no bonobo in our sample copied any of the target actions in either condition. Instead, they attempted to open the box using an array of causally relevant, species-typical methods, which included pounding, biting, kicking, and shaking. As no bonobo demonstrated any of the actions, we did not run a control condition for the bonobos.

Requests for assistance occurred in both species, but more in children, which is not surprising given their language skills. Of children, 48% (14/29) made direct verbal requests (e.g., “It’s too hard for me, can you do it?”) and/or gestural requests. Although actively returning objects in one’s possession is not typically observed in great apes, 21.8% of bonobos (10/46) in our sample actively returned the box to the experimenter after attempting to open it; thus, outwardly resembling a request for assistance.

Discussion

Our study identified striking contrasts in young chil- dren’s copying behavior as compared to that of bono- bos, our closest living relatives. Children readily copied the actions, which were visibly causally irrele- vant, whereas not a single bonobo did. Whether or not the bonobos were unable, unwilling, or both unable and unwilling to copy the demonstrated actions, the results highlight striking differences in human children’s cultural behaviors as compared to those of bonobos. Importantly, our study addressed methodological constraints of previous studies, thus providing a true test for overimitation which allowed us to compare the performances of both children and bonobos. Combining our results with earlier findings for chimpanzees (Tennie et al., 2012; Tomasello et al., 1997), our findings indicate that bodily overimitation —at least in high frequencies—is a uniquely human capacity, which likely plays a key role in explaining why human culture can accumulate over time.

This study focused on bonobos, an understudied species of great ape that might be expected to show higher imitative potential than chimpanzees, given their enhanced social orientation (Kano et al., 2015; Kret et al., 2016) and high social tolerance (Hare &

Kwetuenda, 2010). The fact that the bonobos failed to overimitate demonstrates that even enhanced social orientation may not be enough to trigger human-like cultural learning behaviors. These results thus demonstrate an important qualitative difference between humans and great apes with regard to the capacity or motivation to copy visibly causally irrelevant actions. Differences in the capac- ity for action copying may relate to cognitive con- straints in great apes’ abilities to understand goals and intentions as humans do (Call & Tomasello, 2008). Differences in motivation are likely to relate to the strong affiliative and normative drivers of imitation in humans but not in great apes (Legare & Nielsen, 2015; Over & Carpenter, 2012).

An alternative explanation to the lack of copying by the apes is that it was due to methodological con- straints. However, although small sample size is fre- quently a critique of great ape studies, this was not the case for our study. The combined results from the two related studies also make this explanation unli- kely for chimpanzees (Tennie et al., 2012; Tomasello et al., 1997). Age is also unlikely to be an explanatory factor, given that a full age range was tested, and no subject showed evidence of copying. Another possi- bility is that using a human demonstrator inhibited the bonobos’ motivation to imitate. However, a con- specific demonstrator was used in both chimpanzee studies (Tennie et al., 2012; Tomasello et al., 1997), yet no novel action copying occurred. Moreover, in a review of 23 studies directly comparing chimpanzee and human performance in experimental settings, Boesch (2007) concluded that the use of human demonstrators did not seem to influence observed species differences. Lack of motivation also does not appear to be a problem: The majority of apes per- sisted in this task and employed many alternative techniques while trying to open the box.

Although previous studies have shown that great apes will sometimes copy in certain circumstances, it appears to primarily occur after receiving extensive training and/or enculturation (Bjorklund et al., 2000; Byrne & Tanner, 2006; Call, 2001; Carrasco et al., 2009; Custance et al., 1995; Hayes & Hayes, 1952; Miles et al., 1996). Given that these factors are absent in wild apes, ecologically relevant findings must therefore come from untrained and unenculturated apes. In our study, not a single untrained and nonen- culturated bonobo copied any of the demonstrated actions, thus providing qualitative and ecologically valid evidence of the distinctive nature of the human cultural capacity as compared to that great apes: The copying of visibly causally irrelevant actions (espe- cially novel actions) appears to be uniquely human.

1540 Clay and Tennie

One relevant question is why children were so willing to copy these superfluous actions? It has been suggested that children copy in a blanket fashion due to the causal opaqueness of a task (Horner & Whiten, 2005; Lyons et al., 2007). However, chil- dren’s overimitation is also influenced by social moti- vations, such as to socially bond (Over & Carpenter, 2012) or conform to perceived rituals or norms, which are themselves initially opaque (Herrmann et al., 2013; Kenward, 2012; Kenward, Karlsson, & Persson, 2011; Keupp et al., 2013; Legare & Nielsen, 2015). The main answer therefore is likely to be the hypersocial nature of humans as compared to other animals (Claidiere, Bowler, & Whiten, 2011; Toma- sello, 2014; Tomasello, Melis, Tennie, Wyman, & Herrmann, 2012). The fact that the adult demonstra- tor remained present during the test phase in our study is likely to have enhanced the children’s moti- vation to copy (Harris, 2012; Nielsen & Blank, 2011; Tomasello, 2014). It is well known that children are more likely to copy causally irrelevant actions per- formed by adults as compared to by peers (Flynn, 2008; Horner & Whiten, 2005; McGuigan et al., 2011; Wood, Kendal, & Flynn, 2012). Children are also more likely to copy in the physical presence of adult observers as compared to if they leave the room (Nielsen & Blank, 2011). In this regard, young chil- dren in this study may have perceived the presence of an adult observer during the imitation phase as an implicit cue to overimitate. Although this may be the case, it could be likewise expected that overimitation in great apes would also be more likely to occur within an observer’s presence. The striking absence of overimitation for the bonobos even in such a con- text thus further highlights the apparently stark spe- cies differences that exist in this cultural capacity.

In sum, our results highlight profound differ- ences in the cultural behaviors of human children as compared to great apes. The copying of causally irrelevant actions represents a core component for both material and social cultures in humans, and thus the striking difference between children and great apes in this regard provides critical insights into why both the diversity and frequency of human cultural behaviors differ so vastly compared to that of other great apes (Acerbi & Tennie, 2016).

References

Acerbi, A., & Tennie, C. (2016). The role of redundant information in cultural transmission and cultural stabi- lization. Journal of Comparative Psychology, 130, 62. doi: 10.1037/a0040094

Berl, R. E., & Hewlett, B. S. (2015). Cultural variation in the use of overimitation by the Aka and Ngandu of the Congo Basin. PLoS ONE, 10, e0120180. doi: 10.1371/ journal.pone.0120180

Bjorklund, D. F., Bering, J. M., & Ragan, P. (2000). A two- year longitudinal study of deferred imitation of object manipulation in a juvenile chimpanzee (Pan troglodytes) and orangutan (Pongo pygmaeus). Developmental Psy- chobiology, 37, 229–237. doi:10.1002/1098-2302(2000)

Boesch, C. (2007). What makes us human (Homo sapiens)? The challenge of cognitive cross-species comparison. Journal of Comparative Psychology, 121, 227. doi: 10. 1037/0735-7036.121.3.227

Buttelmann, D., Carpenter, M., Call, J., & Tomasello, M. (2007). Enculturated chimpanzees imitate rationally. Developmental Science, 10, F31–F38. doi: 10.1111/j.1467- 7687.2007.00630.x

Byrne, R. W., & Tanner, J. E. (2006). Gestural imitation by a gorilla: Evidence and nature of the capacity. Interna- tional Journal of Psychology and Psychological Therapy, 6, 215–231.

Caldwell, C. A., & Millen, A. E. (2009). Social learning mechanisms and cumulative cultural evolution is imita- tion necessary? Psychological Science, 20, 1478–1483. doi: 10.1111/j.1467-9280.2009.02469.x

Caldwell, C. A., Schillinger, K., Evans, C. L., & Hopper, L. M. (2012). End state copying by humans (Homo sapi- ens): Implications for a comparative perspective on cumulative culture. Journal of Comparative Psychology, 126, 161. doi: 10.1037/a0026828

Call, J. (2001). Body imitation in an enculturated orangu- tan (Pongo pygmaeus). Cybernetics & Systems, 32, 97–119. doi: 10.1080/019697201300001821

Call, J., & Tomasello, M. (2008). Does the chimpanzee have a theory of mind? 30 years later. Trends in Cog- nitive Sciences, 12, 187–192. doi: 10.1016/j.tics.2008.02. 010

Carrasco, L., Posada, S., & Colell, M. (2009). New evi- dence on imitation in an enculturated chimpanzee (Pan troglodytes). Journal of Comparative Psychology, 123, 385. doi: 10.1037/a0016275

Claidière, N., Bowler, M., & Whiten, A. (2012). Evidence for weak or linear conformity but not for hyper-confor- mity in an everyday social learning context. PLoS one, 7 (2), e30970.

Custance, D. M., Whiten, A., & Bard, K. A. (1995). Can young chimpanzees (Pan troglodytes) imitate arbitrary actions? Hayes & Hayes (1952) revisited. Behaviour, 132, 837–859. doi: 10.1163/156853995X00036

Custance, D., Whiten, A., & Fredman, T. (1999). Social learn- ing of an artificial fruit task in capuchin monkeys (Cebus apella). Journal of Comparative Psychology, 113, 13–23. doi: 10.1037/0735-7036.113.1.13

Dean, L. G., Kendal, R. L., Schapiro, S. J., Thierry, B., & Laland, K. N. (2012). Identification of the social and cognitive processes underlying human cumulative cul- ture. Science, 335, 1114–1118. doi: 10.1126/science. 1213969

Overimitation in Children as Compared to Bonobos 1541

Flynn, E. (2008). Investigating children as cultural mag- nets: Do young children transmit redundant informa- tion along diffusion chains? Philosophical Transactions of the Royal Society B, 363, 3541–3551. doi: 10.1098/rstb. 2008.0136

Fuhrmann, D., Ravignani, A., Marshall-Pescini, S., & Whiten, A. (2014). Synchrony and motor mimicking in chimpanzee observational learning. Scientific Reports, 4, 5283. doi: 10.1038/srep05283

Galef, B. G. (2015). Laboratory studies of imitation/field studies of tradition: Towards a synthesis in animal social learning. Behavioural Processes, 112, 114–119. doi: 10.1016/j.beproc.2014.07.008

Gergely, G., & Csibra, G. (2006). Sylvia’s recipe: The role of imitation and pedagogy in the transmission of cul- tural knowledge. In N. J. Enfield & S. C. Levenson (Eds.), Roots of human sociality: Culture, cognition, and human interaction (pp. 229–255). Oxford, UK: Berg.

Hare, B., & Kwetuenda, S. (2010). Bonobos voluntarily share their own food with others. Current Biology, 20, R230–R231. doi: 10.1016/j.cub.2009.12.038

Harris, P. L. (2012). Trusting what you’re told: How children learn from others. Cambridge, MA: Harvard University Press.

Hayes, K. J., & Hayes, C. (1952). Imitation in a home- raised chimpanzee. Journal of Comparative Physiology and Psychology, 45, 450–459. doi: 10.1037/h0053609

Herrmann, E., Hare, B., Call, J., & Tomasello, M. (2010). Differences in the cognitive skills of bonobos and chim- panzees. PLoS ONE, 5, e12438. doi: 10.1371/journal. pone.0012438

Herrmann, P. A., Legare, C. H., Harris, P. L., & White- house, H. (2013). Stick to the script: The effect of wit- nessing multiple actors on children’s imitation. Cognition: International Journal of Cognitive Science, 129, 536–543. doi: 10.1016/j.cognition.2013.08.010

Herrmann, E., & Tomasello, M. (2015). Focusing and shifting attention in human children (Homo sapiens) and chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 129, 268. doi: 10.1037/a0039384

Heyes, C. M., & Ray, E. D. (2000). What is the signifi- cance of imitation in animals? Advances in the Study of Behavior, 29, 215–245. doi: 10.1016/S0065-3454(08)60106- 0

Hopper, L. M., Lambeth, S. P., Schapiro, S. J., & Whiten, A. (2008). Observational learning in chimpanzees and children studied through “ghost” conditions. Proceed- ings of the Royal Society of London B: Biological Sciences, 275, 835–840. doi: 10.1098/rspb.2007.1542

Horner, V., & Whiten, A. (2005). Causal knowledge and imitation/emulation switching in chimpanzees (Pan tro- glodytes) and children (Homo sapiens). Animal Cognition, 8, 164–181. doi: 10.1007/s10071-004-0239-6

Horner, V., Whiten, A., Flynn, E., & de Waal, F. B. (2006). Faithful replication of foraging techniques along cultural transmission chains by chimpanzees and children. Proceedings of the National Academy of Sciences of the United States of America, 103, 13878– 13883. doi: 10.1073/pnas.0606015103

Huber, L., Range, F., Voelkl, B., Szucsich, A., Vir�anyi, Z., & Miklosi, A. (2009). The evolution of imitation: What do the capacities of non-human animals tell us about the mechanisms of imitation? Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364, 2299–2309. doi: 10.1098/rstb.2009.0060.

Kano, F., Hirata, S., & Call, J. (2015). Social attention in the two species of pan: Bonobos make more eye contact than chimpanzees. PLoS ONE, 10, e0129684. doi: 10. 1371/journal.pone.0129684

Kenward, B. (2012). Over-imitating preschoolers believe unnecessary actions are normative and enforce their performance by a third party. Journal of Experimental Child Psychology, 112, 195–207. doi: 10.1016/j.jecp.2012. 02.006

Kenward, B., Karlsson, M., & Persson, J. (2011). Over-imi- tation is better explained by norm learning than by dis- torted causal learning. Proceedings of the Royal Society of London B: Biological Sciences, 278, 1239–1246. doi: 10. 1098/rspb.2010.1399

Keupp, S., Behne, T., & Rakoczy, H. (2013). Why do chil- dren overimitate? Normativity is crucial. Journal of Experimental Child Psychology, 116, 392–406. doi: 10. 1016/j.jecp.2013.07.002

Kis, A., Huber, L., & Wilkinson, A. (2015). Social learning by imitation in a reptile (Pogona vitticeps). Animal Cogni- tion, 18, 325–331. doi : 10.1007/s10071-014-0803-7

Kret, M. E., Jaasma, L., Bionda, T., & Wijnen, J. G. (2016). Bonobos (Pan paniscus) show an attentional bias toward conspecifics’ emotions. Proceedings of the National Acad- emy of Sciences of the United States of America, 113, 3761– 3766. doi: 10.1073/pnas.1522060113

Legare, C. H., & Nielsen, M. (2015). Imitation and innova- tion: The dual engines of cultural learning. Trends in Cognitive Sciences, 19, 688–699. doi: 10.1016/j.tics.2015. 08.005

Legare, C. H., & Watson-Jones, R. E. (2015). The evolution and ontogeny of ritual. In D. M. Buss (Ed.), The hand- book of evolutionary psychology (Vol. 1, pp. 1 -19). doi: 10.1002/9781119125563.evpsych234

Legare, C. H., Wen, N. J., Herrmann, P. A., & White- house, H. (2015). Imitative flexibility and the develop- ment of cultural learning. Cognition, 142, 351–361. doi: 10.1016/j.cognition.2015.05.020

Lyons, D. E., Young, A. G., & Keil, F. C. (2007). The hid- den structure of overimitation. Proceedings of the National Academy of Sciences of the United States of Amer- ica, 104, 19751–19756. doi: 10.1073/pnas.0704452104

McGuigan, N., Gladstone, D., & Cook, L. (2012). Is the cultural transmission of irrelevant tool actions in adult humans (Homo sapiens) best explained as the result of an evolved conformist bias? PLoS ONE, 7, e50863. doi: 10.1371/journal.pone.0050863

McGuigan, N., Makinson, J., & Whiten, A. (2011). From over-imitation to super-copying: Adults imitate causally irrelevant aspects of tool use with higher fidelity than young children. British Journal of Psychology, 102, 1–18. doi: 10.1348/000712610X493115

1542 Clay and Tennie

McGuigan, N., Whiten, A., Flynn, E., & Horner, V. (2007). Imitation of causally opaque versus causally transpar- ent tool use by 3-and 5-year-old children. Cognitive Development, 22, 353–364. doi: 10.1016/j.cogdev.2007.01. 001

Meltzoff, A. N., & Prinz, W. (2002). The imitative mind: Development, evolution and brain bases (Vol. 6). Cam- bridge, UK: Cambridge University Press.

Meulman, E. J., & van Schaik, C. P. (2013). Orangutan tool use and the evolution of technology. In C. Boesch, J. Call, & C. M. Sanz (Eds.), Tool use in animals: Cogni- tion and ecology (pp. 176–202). Cambridge, Cambridge, UK: Cambridge University Press.

Miles, H. L., Mitchell, R. W., & Harper, S. E. (1996). Simon says: The development of imitation in an encul- turated orangutan. In A. Russon, K. A. Bard, & S. Park- ers (Eds.), Reaching into thought: The minds of the great apes (pp. 278–299). Cambridge, UK: Cambridge Univer- sity Press.

Moraru, C.-A., Gomez, J.-C., & McGuigan, N. (2016). Developmental changes in the influence of conventional and instrumental cues on over-imitation in 3-to 6-year- old children. Journal of Experimental Child Psychology, 145, 34–47. doi: 10.1016/j.jecp.2015.11.017

Morin, O. (2015). How traditions live and die. Oxford, UK: Oxford University Press.

Nielsen, M. (2006). Copying actions and copying out- comes: Social learning through the second year. Devel- opmental Psychology, 42, 555–565.

Nielsen, M., & Blank, C. (2011). Imitation in young chil- dren: When who gets copied is more important than what gets copied. Developmental Psychology, 47, 1050. doi: 10.1037/a0023866

Nielsen, M., Kapit�any, R., & Elkins, R. (2015). The perpet- uation of ritualistic actions as revealed by young chil- dren’s transmission of normative behavior. Evolution and Human Behavior, 36, 191–198. doi: 10.1016/j.evol humbehav.2014.11.002

Nielsen, M., & Susianto, E. W. (2010). Failure to find over- imitation in captive orangutans (Pongo pygmaeus): Impli- cations for our understanding of cross-generation infor- mation transfer. In J. Hakansson (Ed.), Developmental psychology (pp. 153–167). New York, NY: Nova Science.

Nielsen, M., & Tomaselli, K. (2010). Overimitation in Kalahari Bushman children and the origins of human cultural cognition. Psychological Science, 21, 729–736. doi: 10.1177/0956797610368808

Office for National Statistics. (2011). Census data. Retrieved from http://www.ons.gov.uk/ons/guideme thod/census/2011/census-data/index.html

Over, H., & Carpenter, M. (2009a). Eighteen-month-old infants show increased helping following priming with affiliation. Psychological Science, 20, 1189–1193. doi: 10. 1111/j.1467-9280.2009.02419.x

Over, H., & Carpenter, M. (2009b). Priming third-party ostracism increases affiliative imitation in children. Developmental Science, 12, F1–F8. doi: 10.1111/j.1467- 7687.2008.00820.x

Over, H., & Carpenter, M. (2012). Putting the social into social learning: Explaining both selectivity and fidelity in children’s copying behavior. Journal of Comparative Psychology, 126, 182. doi: 10.1037/a0024555

Over, H., & Carpenter, M. (2015). Children infer affiliative and status relations from watching others imitate. Developmental Science, 18, 917–925. doi: 10.1111/desc. 12275

Over, H., Carpenter, M., Spears, R., & Gattis, M. (2013). Children selectively trust individuals who have imi- tated them. Social Development, 22, 215–224. doi: 10. 1111/sode.12020

Rakoczy, H., Warneken, F., & Tomasello, M. (2008). The sources of normativity: Young children’s awareness of the normative structure of games. Developmental Psy- chology, 44, 875. doi: 10.1037/0012-1649.44.3.875

Sanz, C. M., Call, J., & Boesch, C. (2013). Tool use in ani- mals: Cognition and ecology. Cambridge, UK: Cambridge University Press.

Tennie, C., Call, J., & Tomasello, M. (2006). Push or pull: Imitation vs. emulation in great apes and human chil- dren. Ethology, 112, 1159–1169. doi: 10.1111/j.1439-0310. 2006.01269.x

Tennie, C., Call, J., & Tomasello, M. (2009). Ratcheting up the ratchet: On the evolution of cumulative cul- ture. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 2405–2415. doi: 10.1098/rstb. 2009.0052

Tennie, C., Call, J., & Tomasello, M. (2012). Untrained chimpanzees (Pan troglodytes schweinfurthii) fail to imi- tate novel actions. PLoS ONE, 7, e41548. doi: 10.1371/ journal.pone.0041548

Tomasello, M. (1996). Do apes ape? In C. M. Heyes & B. G. Galef (Eds.), Social learning in animals: The roots of culture (pp. 319–346). London, UK: Academic Press.

Tomasello, M. (1999). The cultural origins of human cogni- tion. Cambridge, MA: Harvard University Press.

Tomasello, M. (2014). The ultra-social animal. Invited Hori- zon Article for European Journal of Social Psychology, 44, 187–194. doi: 10.1002/ejsp.2015

Tomasello, M., Call, J., Warren, J., Frost, T., Carpenter, M., & Nagell, K. (1997). The ontogeny of chimpanzee gestural signals. In S. Wilcox, (Ed.), Evolution of commu- nication (pp. 224–259). Amsterdam, The Netherlands/ Philadelphia, PA: John Benjamins.

Tomasello, M., Melis, A. P., Tennie, C., Wyman, E., & Herrmann, E. (2012). Two key steps in the evolution of human cooperation. Current Anthropology, 53, 673–692. doi: 10.1073/pnas.1421402112

Tomasello, M., Savage-Rumbaugh, E. S., & Kruger, A. C. (1993). Imitative learning of actions on objects by chil- dren, chimpanzees, and enculturated chimpanzees. Child Development, 64, 1688–1705.

Vale, G. L., Flynn, E. G., Pender, L., Price, E., Whiten, A., Lambeth, S. P., & Kendal, R. L. (2016). Robust retention and transfer of tool construction techniques in chim- panzees (Pan troglodytes). Journal of Comparative Psychol- ogy, 130, 24. doi: 10.1037/a0040000.

Overimitation in Children as Compared to Bonobos 1543

Whiten, A. (2013). Social cognition: Making us smart, or sometimes making us dumb? Overimitation, confor- mity, nonconformity, and the transmission of culture in ape and child. In M. Banaji, S. Gelman, (Eds.), Navigat- ing the social world.: What infants, children, and other spe- cies can teach us (pp. 150–154). New York, NY: Oxford University Press.

Whiten, A. (2016). Social learning and culture in child and chimpanzee. Annual Review of Psychology, 68, 1. doi: 10.1146/annurev-psych-010416-044108.

Whiten, A., Custance, D. M., Gomez, J. C., Teixidor, P., & Bard, K. A. (1996). Imitative learning of artificial fruit processing in children (Homo sapiens) and chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 110, 3–14.

Whiten, A., Goodall, J., McGrew, C., Nishida, T., Rey- nolds, V., Sugiyama, Y., & Boesch, C. (1999). Cultures in chimpanzees. Nature, 399, 682–685. doi: 10.1038/ 21415

Whiten, A., Horner, V., & De Waal, F. B. (2005). Confor- mity to cultural norms of tool use in chimpanzees. Nat- ure, 437, 737–740. doi: 10.1038/nature04047

Whiten, A., Horner, I., Litchfield, C. A., & Marshall-Pes- cini, S. (2004). How do apes ape? Learning & Behavior, 32, 36–52. doi: 10.3758/BF03196005

Whiten, A., McGuigan, N., Marshall-Pescini, S., & Hop- per, L. M. (2009). Emulation, imitation, over-imitation and the scope of culture for child and chimpanzee. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 2417–2428. doi: 10.1098/rstb.2009.0069

Wood, L. A., Kendal, R. L., & Flynn, E. G. (2012). Con- text-dependent model-based biases in cultural

transmission: Children’s imitation is affected by model age over model knowledge state. Evolution and Human Behavior, 33, 387–394. https://doi.org/10.1016/j.evol humbehav.2011.11.010

Zentall, T. R. (1996). An analysis of imitative learning in animals. In C. M. Heyes, & B. G. Galef Jr (Eds.). Social learning in animals: The roots of culture (pp. 221–243). London, UK: Academic Press.

Zentall, T. R. (2001). Imitation in animals: Evidence, function, and mechanisms. Cybernetics and Systems: An International Journal, 32, 53–96. doi: 10.1080/ 019697201300001812

Zentall, T. R. (2006). Imitation: Definitions, evidence, and mechanisms. Animal Cognition, 9, 335–353. doi: 10. 1007/s10071-006-0039-2

Supporting Information

Additional supporting information may be found in the online version of this article at the publisher’s website:

Video S1. Video Clip Showing Rub–Rotate Con- dition Performed by Child Participant

Video S2. Video Clip Showing Cross–Trace Con- dition Performed by Bonobo Participant

Data S1. Supplementary Methods Describing Additional Features of the Bonobo Study Site and Coding of the Actions.

1544 Clay and Tennie