Here I report a striking gesture unique to a single community of mandrills (Mandrillus sphinx) among nineteen studied across North America, Africa, and Europe. The gesture was found within a community of 23 mandrills where individuals old and young, female and male covered their eyes with their hands for periods which could exceed 30 min, often while simultaneously raising their elbow prominently into the air. This ‘Eye covering’ gesture has been performed within the community for a decade, enduring deaths, removals, and births, and it persists into the present. Differential responses to Eye covering versus controls suggested that the gesture might have a locally-respected meaning, potentially functioning over a distance to inhibit interruptions as a ‘do not disturb’ sign operates.

The present paper investigates a community of mandrills' (Mandrillus sphinx) unique gesture, hitherto unreported, which has persisted stably for a decade within a single community and has never been observed in any other communities of the species across three continents. In this paper I examine (1) whether the gesture is meaningful, in the sense of possessing a communicative function that involves socially influencing other community members from afar and (2) whether the gesture might qualify as a form of animal social culture. In addressing these two questions I (a) detail the form and temporal dynamics of the gesture; (b) catalogue the individuals that make use of the gesture; (c) provide the available history of the gesture's emergence and spread; (d) describe the circumstances surrounding one of the gesturer's deaths and a modification to the gesture that users subsequent-to-the-originator have added; (e) isolate the contexts in which the gesture occurs and the responses it elicits in others; and finally (f) I suggest new experiments that might shed light on how cultural forces may shape the way nonhumans perceive and propagate gestures.

The most likely candidate taxon for possession of such a gesture would seem to be apes, since sparse evidence has been available for any type of manual gesturing in monkeys [16] , [32] – [34] , let alone the creation of gestures de novo [35] . Notably, ape gesturing has been studied in detail across several populations of all four species of great ape [33] and these studies have revealed complex patterns, including sensitivity to the audience's attentional state and comprehension [36] , [37] , referential communication about external objects in the environment [38] , and cultural variation in the presence of certain gestures across groups [27] . Given how few intensive studies have investigated possible monkey gestures across different groups of the same species, it is perhaps not surprising that, outside of humans, nearly all culturally-based gestures identified thus far have been restricted to apes [16] . It has been maintained, therefore, that: “free hand gestures are a unique feature of ape and human communication; they are not found in the monkeys” [Ref 27, p.19.] Recently, however, new cases of relatively sophisticated monkey gesturing [30] , [39] have been revealed, raising the possibility that it is within monkeys' reach to culturally-craft a gesture for meaningful communication over a distance.

In our own species, variable modes of carrying out social interactions between different communities are often imbued with a deeper significance; and it is this added layer of meaning that makes these acts truly cultural, shared collectively by a community as whole [22] . One class of behaviors that can possess such meaning and that are found in human and nonhuman alike are ‘gestures,’ behaviors which Smuts [Ref 23, p. 301] defines as broadly encompassing “all nonvocal actions with potential communicative significance.” Some gestures, for instance manual gestures, involve movements of the hands and arms in the vicinity of conspecifics, possibly exerting social or communicative effects. For a gesture, manual or otherwise, to qualify as ‘meaningful’ though it should be demonstrated to influence others' behavior, altering their response pattern by either conveying information about the gesturer's mood or otherwise manipulating what onlookers do [24] , [25] . While it has been proposed that handclasp grooming might be a meaningful gesture, symbolizing close dyadic relationships [16] , [26] , to date no systematic analysis has been carried out to investigate what, if any, meaning this gesture holds for chimpanzees. Moreover, although other cases of cultural gestures in nonhuman primates have been discovered in addition to handclasp grooming [27] , these cases have involved mostly similar kinds of tactile gestures that operate intimately at close-range, such as scratching [28] , grooming [29] , or sucking and sniffing of others' body parts [30] , behaviors which it is less than clear should qualify as ‘meaningful’. Few cultural gestures thus seem to exist in nonhuman primates that operate visually from a distance to impart a meaning that is shared by a local community as a whole [20] , [31] .

Biologists, psychologists, and anthropologists have now begun to systematically investigate the underlying processes and the ultimate products of culture across a diversity of species, comparing and contrasting mechanistic and functional elements of both animal and human culture to uncover how and why cultural abilities evolved [9] , [13] . Perhaps the most compelling cases of animal culture that have been identified thus far are those that center on how social interactions are mediated within a community. Unlike cases of animal culture in the foraging or technological domain (which can sometimes be readily explained as mere corollaries of local habitat) cases of animal ‘social culture’ appear to have less grounding in pure ecology [14] – [16] . A community, for instance, may conduct its affairs in a certain way while other communities never employ this way or use different ways, irrespective of environment [17] . Our closest evolutionary relatives, the nonhuman primates, have provided some of the strongest evidence for social culture [15] . A paradigm example is the so-called ‘grooming hand-clasp’ of chimpanzees [18] . This unique behavior, in which two apes clasp their hands overhead during mutual grooming, has been regarded as the “the first serious claim of culture in animals” [Ref 9, p.341] . Handclasp grooming has been observed extensively within some chimpanzee communities, both captive (e.g., Yerkes Regional Primate Research Center in Georgia) and wild (e.g., Taї Forest, Ivory Coast; Mahale, Tanzania; Kibale Forest, Uganda); but the behavior has never been detected elsewhere despite long-term observation of other communities with similar environments and genetic compositions (e.g., Bossou, Guinea; Gombe, Tanzania; Budongo Forest, Uganda) [18] – [20] . Notably, different chimpanzee communities that exhibit handclasp grooming have also been found to vary in the fine-grained nuances of how they perform the gesture, suggesting some degree of cultural standardization in ‘style’ within each local community [21] .

Around the world, human populations exhibit dramatic differences in behavior, much of it independent of ecology and genetics [1] , [2] . The concept of culture was originally formulated to describe such geographic differences in the behavior of human communities [3] , essentially variation in “the way we do things” [4] , [5] . Recently, however, the culture concept has been applied to examine parallel cases discovered in nonhumans [6] – [12] . Despite substantial wrangling over definitions of ‘animal culture’ as well as disagreement over whether animals should even be accorded culture [6] many scientists agree that, at least in some nonhuman species, individuals may possess a capacity to learn from others within their community. This capacity for social learning in animals can potentially generate population-level phenomena that bear some similarities to patterns of human culture [11] . One possible population-level consequence of social learning is that, over time, the behavior of an animal community can diverge from that which is found in other communities of the same species, resulting in a prominent between-community differences and within-community similarities in patterns of behavior [11] . Animal culture, in this minimalist sense, thus exists when socially-learned behavior that is shared in one animal community is absent in other communities of the same species [10] , [12] .

Results and Discussion

Mandrills, the largest of all monkeys, are endemic to the rain forests of equatorial West Africa and are housed in captive groups around the world. In a captive community of 23 mandrills in Colchester, England seven individuals (an adult female and six males of various ages; Table 1, S1, S2) were observed performing a prominent gesture in which one or both hands were brought overtop the face, covering the eyes (Figure 1; Video S1, S2, S3). This ‘Eye covering’ gesture was unique, not being observed in any of eighteen other mandrill groups distributed across the USA, Gabon, the United Kingdom, Germany, and Italy (Table S3). In addition to these groups, observed by the author over the course of 9 years, other colleagues commented on further groups (personal communications in Table S3), which were found in Israel, Gabon, Italy, the Czech Republic, and Belgium, some of which had been observed over multiple generations for more than a decade. Nevertheless, the Eye covering gesture has never been observed outside of Colchester, and nor has it been reported in any of the publications of prior mandrill researchers, despite multiple independent investigations of yet other communities of this species (Table S3).

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larger image TIFF original image Download: Figure 1. The unique Eye covering gesture of the Colchester community. (A) A male performs the gesture with his right hand while lying and while lifting his elbow prominently as a ‘flag’. (B) Another male performs the gesture while sitting with both hands held over his eyes, the left hand on top. (C) A female (the originator) performs the gesture with her left hand while sitting embraced with one of her offspring in the shade. https://doi.org/10.1371/journal.pone.0014610.g001

In the Colchester community, the Eye covering gesture was first observed in 1999 when a female ‘Milly’, then 3 yrs old, began performing the gesture spontaneously (personal communications from Liz Butcher, keeper during 1995–2000; Kirsty Stewart, keeper during 2000–2006; and Kate Harness, keeper during 2006-present). Neither during the gesture's origin nor anytime since has there been any human intervention to elicit or in any way encourage the mandrills to gesture (ibid; and personal communications from Sarah Forsyth, Curator, and Rebecca Perry, Director of Conservation, Education and Research at the Colchester Zoo). Mandrills perform Eye covering irrespective of whether humans are in the viewing vicinity of their exhibit, and the gesture has never once been observed being deployed in any human-geared contexts, as while being fed. Presently, the gesture's originator Milly, who is now an adult, continues to perform Eye covering regularly, as do several younger individuals within the group who began performing the gesture after Milly but are not her offspring (see Table S1 for timeline of acquisition). During two study periods separated by 1 yr I quantified how this unique gesture was used and examined its potential communicative value within the Colchester community.

Eye covering was performed frequently (Mean ± SE: 6.3±4.4 times per h in focal samples across all community members ≥3 yrs of age; N = 13 individuals; Table 1 and S1). Up to three individuals at a time were observed performing the gesture concurrently, each at their own separate location and not apparently in any relation to one another. Unlike relatively instantaneous behavior, such as scratching, the Eye covering gesture was held continuously for extended periods, lasting uninterrupted up to 17 min and 6 s, or more than twice as long as the longest reported handclasp grooming bout in chimpanzees [19], [26]. The exact time between onset and offset of the gesture averaged 56±7 s (N = 275 from focal sampling). Typically though several Eye covering bouts were performed one after the other with only brief separations in which the gesturer switched hands or temporarily removed and replaced its hand while changing position. When such adjacent instances of gesturing (<1 min separation) were combined (henceforth termed ‘lumped bouts’), the duration of gesturing was substantial, averaging 8.8±1.5 min (range: 2 s – 36.2 min, N = 33; see Table S1 for data on each gesturer separately).

Holding the hand in place for so long might not entail negligible effort. Indeed, potential effort was also exhibited in another aspect of the gesture: individuals that were gesturing sometimes simultaneously elevated their elbow high in the air, keeping it aloft like a ‘flag’ (Figure 1A; Video S1). Besides the originator, who has never been observed lifting her elbow during the gesture, five of the six other gesturers exhibited this conspicuous behavior (Table S1), executing it exclusively during Eye covering. Elbow raising occurred in 31.5% of N = 89 lumped bouts that were performed by gesturers other than the originator, and the raised elbow was held in place on average 1.0±0.2 min (range: 0.03 – 3.4 min; N = 42 elbow raises from focal sampling). The possible muscular exertion involved in Eye covering and Elbow raising suggested a plausible function, one that might favor notifying others and amplifying the detectability of the gesture via an embellishment. Consistent with such social signaling, the gesture's function could not be reduced to basic environmental factors, like blocking light from entering the eyes: only 34.6% (of N = 208 gestures) were performed while the gesturer was in direct sunlight; all the rest were performed in the shade cast by opaque building structures or overhanging branches (39.9%), or when the sky was completely overcast (25.5%). In contrast to the lack of evidence for a sun-shielding function, observational evidence suggested that Eye covering might have a significant social function, mediating interaction among conspecifics.

Contextual and Response Patterns The social function of Eye covering did not appear to be geared toward initiating interactions: the gesture was never performed while individuals were locomoting or while they were standing, poised for interaction. Rather individuals were always stationary while gesturing, either lying (27.6%; Figure 1A) or sitting (72.4%, N = 359; Figure 1B, 1C). Interestingly, whereas most nonhuman primate gestures identified thus far, including non-cultural ones, have been embedded in intensely social activities, like agonism, play, or intimate bonding [32]–[34], the Eye covering gesture occurred primarily during rest, defined by the absence of any socializing between the gesturer and others (Figure 2A). Rest, however, did not imply actual sleep, and it was clear from several factors that gesturers did not necessarily keep their eyes closed while covering them. For instance, gesturers would frequently glance back and forth, apparently peeking through cracks between their fingers to survey the locations of other community members. And when a more dominant group mate approached, a gesturer would orient its gaze toward that dominant, immediately taking its hand off and avoiding if the dominant came too close. Gesturers also sometimes held their hands slightly away from their face (Video S2) or their hands sometimes gradually slid down their muzzle during the course of an extended gesturing bout, in both cases revealing open eyes. Thus, despite engaging in hardly any social activities while performing the gesture, gesturers nevertheless remained visually aware of their surroundings. PPT PowerPoint slide

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larger image TIFF original image Download: Figure 2. Contexts surrounding the gesture's use. (A) Behavioral contexts (see Materials and Methods) in which the gesture was performed at least once. Based on N = 359 gestural occurrences from focal and behavioral sampling combined. (B) Whether the gesturer was alone or had other community members within 2 m at the time its gesture was first detected. Based on N = 266 occurrences from behavioral sampling. Included in the ‘alone’ category are instances in which an adult female was gesturing and was alone other than having her fully-dependent infant, which always remained embraced with or in arm's reach of her. https://doi.org/10.1371/journal.pone.0014610.g002 The sustained vigilance of gesturers in the absence of social involvement raises the possibility that Eye covering might serve to reduce the amount of disturbance a gesturer received. Such a function could be useful during periods when engagements with others are undesirable. To examine this possible anti-social, disturbance-reducing function I collected data both by behavioral sampling [40] (in which the presence or absence of other community members was quantified in the vicinity of observed gestures) and by focal animal sampling [41] (in which instances of received approaches and touches were recorded continuously while the same individuals were and were not gesturing). Results showed that if an individual was gesturing, then in most cases it was free of the company of other community members (Figure 2B). Furthermore, gesturing appeared to inhibit others from disturbing the gesturer: individuals received significantly fewer approaches (t-test assuming unequal variances: t = 4.30, df = 6.89, p = 0.0037; Figure 3A) and significantly fewer touches (t-test assuming unequal variances: t = 2.49, df = 6.53, p = 0.0440; Figure 3B) from other community members when they were performing the gesture compared to control periods when they were not performing the gesture but were otherwise postured similarly. Since the gesture was performed throughout the Colchester mandrills' entire habitat, these effects were not simply a result of individuals positioning themselves in some isolated locale while they gestured. Indeed, the gesture was performed most commonly in the center area of the enclosure, where the majority of the community and hence the majority of potential disturbances tended to be (Laidre, personal observation). PPT PowerPoint slide

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larger image TIFF original image Download: Figure 3. Individuals experience significantly reduced disturbance while gesturing. Disturbance rates (per h) when mandrills were and were not gesturing. Periods of non-gesturing represented controls in which the same individuals were in a stationary resting context with either a lying or sitting body posture, but were not covering their eyes. (A) Approach rate (others coming within 2 m of the focal individual). (B) Touch rate (others initiating tactile contact with the focal individual). Mean + SEM shown. See Tables S4 and S5 for data on each individual separately. https://doi.org/10.1371/journal.pone.0014610.g003 By covering their eyes with their hands, individuals possibly conveyed to others that they wanted to be left alone, and this message may have been respected as a ‘do not disturb’ sign. Regardless of a gesturer's rank, its hands were never removed from its eyes by another individual. It is notable though that the individuals who employed the gesture tended to occupy the bottom of the dominance hierarchy (Table 1), and thus would have benefited from regulating social disturbances. In particular, the five older male gesturers occupied the lowest five positions among the thirteen mature members of the Colchester community. Given these males' subordinate rank, approaches and tactile interactions could preface costly attacks and persecution from others, especially from higher ranking individuals. Indeed, within the period of the study, one of these males, Phoenix, was so severely wounded in an attack by a superior that he had to be euthanized (Table 1, S1). Similarly, the originator Milly was the second lowest-ranking among seven adult females. The pressure for this particular female to reduce social disturbances may have been especially strong at the time of the study, since she had a dependent infant as well as another older offspring, and would have benefited from moderating how often others interfered with her vulnerable progeny. Notably, many of this female's gestural performances (41.3% of N = 138 from behavioral sampling) were performed while she was embraced with or in arm's reach of one of her offspring but was otherwise separated from third parties. In these cases the gesture may have functioned to prevent third parties from interrupting her dyadic kin interactions. Finally, the seventh gesturer was an immature male who only began performing the gesture in the second study period. Given this male's young age and high social activity levels, it was unclear what utility the gesture could have for him. He executed the gesture on only five occasions, but on each occasion specifically after positioning himself within a meter of one of the older male gesturers who, at the time, was currently performing Eye covering or had performed it just moments before.

Reasons for Uniqueness Irrespective of whether the Eye covering gesture is meaningful or not, its uniqueness to the Colchester mandrills raises the question of why all the performers of this gesture should be restricted to just a single community. None of several hundred other mandrills (Table S3), including ones from communities with virtually identical social compositions to Colchester, ever covered their eyes, not even for a few seconds. And Eye covering has also never been observed among wild mandrills [42; Kate Abernethy, personal communication]. The absence of Eye covering in these other communities does not appear explicable based on insufficient sampling, human inducement, genetic variation, or ecological differences across communities. Sampling error, for instance, is an unlikely explanation for the gesture's absence at every other site, since some communities were observed over extended periods lasting across generations. Human inducement likewise is unlikely: despite the folk adage ‘monkey see, monkey do’ there has so far been no successful attempt in any study to train monkeys on the ‘do-as-I-do’ paradigm [43], in which animals are rewarded for copying the actions of a human. Monkeys, unlike great apes, dolphins, and dogs [43]–[48], thus evidently will not mimic human gestures they might happen to see. Also, neither genetic or habitat differences between communities appear to be viable explanations for the gesture's exclusive confinement to Colchester. In terms of genetics, gesturers had diverse parentage (Table S2), with as few as three generations connecting the Colchester community back to a wild gene pool; and captive management practices have ensured that breeding between different zoo mandrill communities occurs regularly, so hereditary differences do not accumulate. Likewise, habitat features and living conditions between the Colchester community and many of the other communities were broadly similar in design, having been arranged for the very same purpose of providing a safe environment for the animals where humans could easily watch them. The only environmental parameter that might be deemed relevant—density—was not higher in Colchester, which was the eleventh most dense of nineteen total study groups (Table S3). Accordingly, Eye covering did not emerge merely through convergent asocial responses to an elevated density. Overall, therefore, the most plausible explanation for the gesture's confinement to the Colchester community is that the gesture was, at least in part, culturally transmitted after its innovation by the originator Milly. The usage of such a peculiar manual act exclusively by seven individuals belonging to the same community makes it improbable that each of these seven separately fabricated the behavior. Abundant opportunities would clearly have been available for novices to notice and be influenced to reproduce the gesture, given its frequency and lengthy bouts. As yet though, there is no irrefutable experimental evidence for cultural transmission of the Eye covering gesture, let alone for any gesture in a nonhuman [33]. To date, only one experiment has been carried out to critically examine how nonhumans might socially learn their gestures from conspecifics. This study [49] trained two chimpanzee subjects to demonstrate an unusual gesture for requesting food from a human, finding no evidence that other chimpanzees ever acquired the gesture. The experiment is limited, however, in two key respects. First, the focal gesture had essentially no naturalistic relevance to the lifestyles of the chimpanzees, as it was not something they themselves came up with for intra-specific interactions but rather something humans trained them to execute arbitrarily for inter-specific interactions. Second, recent research has suggested that social learning in nonhuman primates is grounded in an inherent motivation to copy others that is independent of extrinsic rewards, like getting food, perhaps stemming from a desire simply ‘to belong’ and ‘fit in’ within one's social community [11], [16], [50]. Gestures whose purpose lies in obtaining rewards from a human would seem ill-suited to inducing such a social motivation to be like others. Clearly, more experiments are needed with less artificial—but still equally unique—gestures, ones like Eye covering that seem endowed with social relevance. Ultimately, it may be possible to employ experimental approaches with Eye covering, complementing and extending the ‘method of exclusion’ [51] of the present paper. For instance, future inter-zoo animal transfers, in which gesturers are translocated to new communities, could be opportunistically exploited as ideal tests of the sort that have rarely been feasible with primates [10], [52], [53]. Compelling evidence for social learning and cultural dissemination could then be gleaned if new communities which previously lacked the gesture later began performing it following the arrival of the transplanted gesturer. Equally informative could be experiments inside the Colchester community itself. Video playback, for instance, could be used to determine what responses Eye covering elicits compared to other gestures. And removal experiments as well as the provision of visual barriers could be used to test the flexibility of gesturers, determining whether they cease the Eye covering gesture if they are not liable to be disturbed or if others would be incapable of seeing their gesture. Finally, of foundational importance is continued, long-term monitoring within the Colchester community itself. For while acknowledging that non-experimental methods of characterizing animal culture are limited [8], [54], it is only through such longitudinal observations that we can document how long animal cultures like Eye covering endure and also detail what, if any, further diffusion dynamics they exhibit as new members become integrated into the community and others are removed or die out.