Playing together,laughing together: rapid facial mimicry and social sensitivity in lowland gorillas

In nonhuman animals, the phenomenon of rapid facial mimicry (RFM)—the automatic, involuntary, and rapid (<1 s) replication of others’ facial expressions—has been mainly investigated in the playful domain. In immature lowland gorillas Gorilla gorilla gorilla both play face (PF) and full PF (FPF) are rapidly mimicked between the players. This makes the species suitable to test hypotheses on the factors influencing RFM during play. The observations on 3 captive groups of lowland gorillas (N = 27) revealed that contrary to expectations, the closeness of social bond negatively influenced the occurrence of RFM but it did not affect either RFM latency or its overlapping index (OVERLAP). RFM was affected by the degree of symmetry of play fighting: the more balanced the session, the higher the occurrence of RFM. Players of the same sex class responded faster than players of different sex. These findings suggest that RFM may help synchronizing behaviors of playmates matching in size (same-sex) and promote symmetric playful interactions. “Laughing together” (measured by the RFM OVERLAP) lasted longer when the responder perfectly mirrored the partner expression (PF→PF; FPF→FPF). If PF and FPF convey information on the different play roughness degree, through “laughing together” the players could coordinate their actions and share positive moods and playful intensity. If the perfect congruency in the motor resonance, also known as social sensitivity, can foster a possible emotional dialogue between gorillas remains to be investigated.     

Concealing facial evidence of mood: Perspective-taking in a captive gorilla?

A captive female lowland gorilla was observed repeatedly to hide or inhibit her playface by placing one or both hands over the face. When this behaviour was seen play usually did not follow immediately, even if other signals associated with play were simultaneously being made by the gorilla. By contrast, a playface predicted that play would follow within a few seconds; this difference was statistically reliable. Several levels of interpretation of the behaviour are possible: hiding the playface may have functioned as a form of deception, a meta-communication, or merely an attempt to suppress the playface. However, by any of these interpretations, the behaviour implies that the gorilla is aware of her spontaneous facial expressions and the consequences they entail. Among the great apes, manual suppression of a facial expression has previously been reported once for chimpanzees but never for gorillas.     

Facial Displays in Cebus apella

Tufted capuchins are diurnal New World primates whose social interactions involve vocal and visual communication. We aimed to describe their facial displays and assessed the use (in relation to rank and age/sex classes of the sender or the receiver or both) and the social function of the most frequent ones. More specifically, we analyzed the temporal relationship between each facial display and specific classes of behaviors, e.g., play, aggression, performed by the sender and by the receiver (Pre-Post-Event Histogram [PPEH]). We observed 20 captives, belonging to 2 groups, for a total of 320 h. The capuchins displayed relaxed open-mouth, silent bared-teeth, open-mouth threat, lip-smacking, open-mouth silent bared-teeth, scalp lifting, and, rarely, protruded lips. The repertoire and the meanings of the different facial expressions are similar to those described for Catarrhini. In some cases, such as for the silent bared-teeth display, the meaning depends on the age of the sender. Silent bared-teeth is associated with play in juveniles and with submissiveness of the sender to the receiver and affiliative interactions in adults. The finding, and the fact that silent bared-teeth display is used during courtship (Carosi and Visalberghi, 2002), support Preuschoft and van Hooff’s (1995, 1997) power asymmetry hypothesis of motivational emancipation, according to which there is convergence between affiliative and submissive behaviors in species with a high degree of social tolerance.     

Body signals used during social play in captive immature western lowland gorillas

The play face is a well-established play signal in nonhuman primates that functions to invite play and convey a playful intent. However, recent evidence indicates that some species display repertoires of play signals that may have more specific meanings related to particular aspects of play. Furthermore, previous studies have inconsistently categorized gorilla behaviors as play signals versus actual play. Here we aim to identify behaviors displayed by two immature captive western lowland gorillas (Gorilla gorilla gorilla) at the Buffalo Zoo that meet three necessary criteria to be considered play signals. Specifically, we (1) investigate whether 21 candidate signals are significantly different from actual play behaviors, (2) and from similar signals used in non-play contexts, and (3) determine whether they predict the occurrence of social play. The results indicate that at least 18 of the 21 candidate signals have strong support for classification as play signals. These findings represent first steps in determining the function of multiple play signals in gorillas.     

Affiliative and submissive communication in rhesus macaques

This study analyzed the occurrence of selected facial expressions, gestures, and postures, in relation to sex and rank of sender and receiver, context, and responses elicited in a large multi-male multi-female group of rhesus macaques (Macaca mulatta) living in captivity. The group was observed for 100 hr during the mating and the birth season. Data were collected with the behavior sampling method. The bared-teeth display and the hindquarter presentation were the most prominent signals in the rhesus submissive and affiliative repertoire. Both signals were primarily displayed in response to aggression and approaches; bared-teeth in response to approaches from the front, presentation in response to approaches from the rear. Lip-smack had a submissive component like baredteeth and presentation but was more likely to be displayed by approaching individuals and followed by affiliation than these behaviors. The distribution of hip-touch and mount was different from that of bared-teeth, presentation, and lip-smack, these behaviors mostly occurring between males, irrespective of their dominance rank. Other infrequent signals and behavioral sequences were limited to specific male-female and mother-infant interactions.     

Use of buckets as tools by Western lowland gorillas

While all great apes have been documented to use tools, gorillas are arguably the least proficient tool users. In 2009, a Western lowland gorilla (Gorilla gorilla gorilla) at the Buffalo Zoo was observed using a bucket, which had been provided as part of normal enrichment, as a tool to collect water. We conducted a brief, ad libitum investigation to confirm the validity of the initial observation. We then carried out a systematic investigation of the behavior in 2010. We collected 72 hr of videotaped data and tested the null hypothesis that the gorillas did not differ in their prevalence of engaging in bucket-use behaviors. We documented that all four adult gorillas in the group used buckets as drinking tools; however, there was significant individual variation in frequency and type of use of buckets. Four of the eight behaviors showed significant variation among individuals. The silverback male and the youngest adult female contacted and held the bucket significantly more than the remaining two adult females. The young female carried and drank from the bucket significantly more than any other individual. Furthermore, she was observed to fill the bucket with water four of the six times during which this behavior was observed. These data provide evidence of the ability of gorillas to utilize tools, given the appropriate environmental conditions. We continue to explore the abilities of gorillas to recognize the functionality of buckets as tools.     

Ranging and grouping patterns of a western lowland gorilla group at Bai Hokou,Central African Republic

The ranging and grouping patterns of a gorilla group were studied during 27 months from 1990–1992 at the Bai Hokou study site, Central African Republic. The study group ranged far daily (average = 2.3 km/day) and had a large home range (22.9 km²), relative to mountain gorillas, and ranging patterns differed between years. During 1990–1992, the bimale study group foraged less cohesively and had more flexible grouping patterns than mountain gorillas. The study group sometimes split into two distinct foraging subgroups, each led by a silverback, and these subgroups occasionally slept apart (mean = 950 m apart). Lowland gorillas rely on many of the same fruit resources as sympatric chimpanzees, and under certain demographic situations gorillas, like sympatric chimpanzees, may adapt their foraging group size to reduce intragroup feeding competition. However, the fiber content of the lowland gorilla diet likely relaxes constraints on foraging party size and facilitates group cohesion relative to chimpanzees. Am. J. Primatol. 43:111–133, 1997. © 1997 Wiley-Liss, Inc.     

Behavioral responses of silverback gorillas (Gorilla gorilla gorilla) to videos

This study examined the impact of video presentations on the behavior of 4 silverback, western lowland gorillas (Gorilla gorilla gorilla). On each of 5 occasions, gorillas viewed 6 types of videos (blue screen, humans, an all-male or mixed-sex group engaged in low activity, and an all-male or mixed-sex group engaged in agonistic behavior). The study recorded behavioral responses and watching rates. All gorillas preferred dynamic over static videos; 3 watched videos depicting gorillas significantly more than those depicting humans. Among the gorilla videos, the gorillas clearly preferred watching the mixed-sex group engaged in agonistic behavior; yet, this did not lead to an increase in aggression or behavior indicating agitation. Further, habituation to videos depicting gorillas did not occur. This supports the effectiveness of this form of enrichment, particularly for a nonhuman animal needing to be separated temporarily due to illness, shipment quarantine, social restructuring, or exhibit modification.     

Ranging Patterns of a Western Gorilla Group During Habituation to Humans in the Dzanga-Ndoki National Park,Central African Republic

The ranging patterns of western gorillas have been described in relation to their more frugivorous diet as compared to mountain gorillas. However, the lack of data from habituated groups prevents a full understanding of their ranging behavior and its implications for western gorilla social behavior. Unhabituated gorillas often flee from approaching researchers, possibly resulting in longer daily ranges and home range expansions and/or shifts. I report on the influence of habituation on the ranging patterns of a western gorilla group. I analyzed progress in habituation through changes in gorilla reactions, displayed upon detecting the observers. I measured daily path length and home range while following the group's trails and monitored diet via fecal analyses and direct observations. During the study period, habituation progressed and the gorillas increasingly ignored the arrival of observers. As a result, daily path lengths were longer during the early stages of habituation, when the gorillas were avoiding observers. There was no range expansion or shift, though the measure is more difficult to investigate, being subject to error due to variation in sample size. We recorded seasonal changes in the consumption of fruit by gorillas, but no direct effect on ranging patterns is detectable with the data available, which is likely a consequence of the combined effect of habituation and seasonality on group movements. The findings are not only important for understanding the extent of human influence while conducting research on wild gorillas but also suggest the need for caution when interpreting results from non-habituated gorillas.     

Impact of ecological and social factors on ranging in western gorillas

We examined the influence of ecological (diet, swamp use, and rainfall) and social (intergroup interaction rate) factors on ranging behavior in one group of western gorillas (Gorilla gorilla gorilla) during a 16-month study. Relative to mountain gorillas, western gorillas live in habitats with reduced herb densities, more readily available fruit (from seasonal and rare fruit trees), and, at some sites, localized large open clearings (swamps and "bais"). Ranging behavior reflects these ecological differences. The daily path length (DPL) of western gorillas was longer (mean=2,014 m) than that of mountain gorillas, and was largely related to fruit acquisition. Swamp use occurred frequently (27% of days) and incurred a 50% increase in DPL, and 77% of the variation in monthly frequency of swamp use was explained by ripe fruit availability within the swamp, and not by the absence of resources outside the swamp. The annual home-range size was 15.4 km2. The western gorilla group foraged in larger areas each month, and reused them more frequently and consistently through time compared to mountain gorillas. In contrast to mountain gorillas, intergroup encounters occurred at least four times more frequently, were usually calm rather than aggressive, and had no consistent effect on DPL or monthly range size for one group of western gorillas. High genetic relatedness among at least some neighboring males [Bradley et al., Current Biology, in press] may help to explain these results, and raises intriguing questions about western gorilla social relationships.     

Sex differences in play among western lowland gorilla (Gorilla gorilla gorilla) infants: implications for adult behavior and social structure

Mammalian play is believed to improve motor skills as well as facilitate the development of social relationships. Given the marked sexual dimorphism in gorilla body size and the role assumed by the male in protecting the group from conspecifics and predators, the motor-training hypothesis of play predicts that male infants should exhibit higher frequencies of social play than female infants, and that males should prefer to play with other males. Given that adult female gorillas are strongly attracted to adult breeding males and form only weak social bonds with unrelated adult females, the social-relationship hypothesis of play predicts that female infants should prefer to play with males. These hypotheses were tested in a 22-month study of 12 gorilla infants, aged between 0-5 years, living in three zoological parks in Chicago and Atlanta. Consistent with the hypotheses, male infants played more than female infants did, and both male and female infants preferred to play with males rather than with females. These findings suggest that sex differences in play in the great apes and other primates can be predicted by the characteristics of adult behavior and social structure above and beyond the patterns of sex-biased dispersal or coalition formation with same-sex kin.     

“Laughter” and “Smile” in Barbary Macaques (Macaca sylvanus)

In an observational study on semi-free Barbary macaques it was investigated whether the phylogenetic roots of human laughter and smile can be traced back to the genus Macaca. On the basis of morphological similarity a ‘relaxed open-mouth display’ as the phylogenetic precursor of the laughter, and a ‘silent bared-teeth display’ as the possible ancestor of the smile can be distinguished in the repertory of the Barbary macaque. Behavioural sequences from focal animal protocols were analyzed in order to establish message and meaning of both displays. Relaxed open-mouth display is regularly observed in the play interactions of juveniles. It is associated with partner-directed behaviour, it is frequently answered by a relaxed open-mouth display of the receiver, and accompanied by a special vocalization. Although up to 50% of the juvenile's play partners were higher ranking than themselves voluntary participation was the rule. Most characteristically, the behaviour patterns shown by both play partners are highly symmetrical and synchronized. Silent bared-teeth display is typically accompanied by evasive or submissive body movements, and occurs primarily in dyadic interactions, mainly by the lower ranking individual. It is not an unidirectional sign of a linear dominance hierarchy, though. Silent bared-teeth display is a frequent answer to aggressive behaviour shown by the receiver. After its performance, an increase of body contact between sender and receiver was observed. Behavioural sequences of senders and receivers are complementary, but lose their asymmetry after occurrence of the display. It is concluded that these results further support Van Hooff 's (1972) view that human laughter and smile have different phylogenetic roots: while silent bared-teeth display is a signal of submission and appeasement, relaxed open-mouth display is rightly called the ‘play face’, and is an expression of fun.     

Visual communication in social play of a hierarchical carnivore species: the case of wild spotted hyenas

Communication relies on signals that can be produced via different sensory modalities to modify receivers’ behavior. During social interactions, the possibility to perceive subtle visual cues enhances the use of facial expressions to exchange information. One of the most appropriate fields to explore the specific design features of visual signals is play fighting. Here, we explored the production and potential role of Relaxed Open Mouth (ROM) and Head Bobbing (HB) in regulating play fighting of wild spotted hyenas Crocuta crocuta, a highly hierarchical carnivore species. In accordance with the assumptions of the signal optimization theory, wild hyenas produced ROM and HB almost exclusively when the sender was in direct visual contact with the receiver thus suggesting that senders were attentive to the playmates’ face. Contrary to HB, the sequential analysis revealed that ROM often anticipated offensive patterns such as play biting thus supporting the hypothesis that ROM, but not HB, is a metacomunicative signal. Moreover, when the offensive patterns were biased toward one of the 2 players, the session was punctuated by a higher number of ROMs. Our findings support the general hypothesis that these 2 visual signals can play different roles in the management of play fighting in this carnivore species. The complementary use of ROM and HB would suggest that spotted hyenas are highly competent and fast in processing facial displays of different nature to correctly “read others’ intentions” and respond with appropriate motor actions to avoid misunderstanding during one of the most multifaceted and risky social interaction.     

Relationship between behavior, adrenal activity, and environment in zoo-housed western lowland gorillas (Gorilla gorilla gorilla)

Monitoring adrenal activity through noninvasive fecal hormone sampling is rapidly gaining popularity as a tool to assess zoo animal welfare. However, few studies have sought to investigate the interrelationships between behavior, adrenal activity, and environment, and ask whether both behavioral and adrenal monitoring strategies are required to assess welfare sufficiently. We present the findings of a 9-month study of a small group (one male, two females) of Western lowland gorillas, Gorilla gorilla gorilla. First, we examined the effect of environmental variables on gorilla behavior. Second, we examined the effect of environmental variables on the concentration of fecal glucocorticoid metabolites (FGC) and the relationship between behavior and FGC. Environmental variables had similar effects on all three gorillas. Negative vigilance of visitors (NVV; staring, posturing, and charging at visitors) significantly increased in all subjects as environmental noise levels increased, and food-related behavior significantly decreased in all subjects as crowd size increased. Exhibit modifications had a number of positive effects on behavior. Notably, when privacy screens were used, NVV significantly decreased in two subjects. We found no significant effects of environmental variables on FGC. However, we did find significant relationships between behavior and FGC in one female. Specifically, her NVV was significantly higher one day before, and on the same day as, raised FGC. Also, hair plucking significantly increased in the two days following raised FGC. Overall, this study demonstrates how concurrent noninvasive fecal and behavioral monitoring can be used for gorilla welfare assessment.     

Behavioral Responses of Silverback Gorillas (Gorilla gorilla gorilla) to Videos

This study examined the impact of video presentations on the behavior of 4 silverback, western lowland gorillas (Gorilla gorilla gorilla). On each of 5 occasions, gorillas viewed 6 types of videos (blue screen, humans, an all-male or mixed-sex group engaged in low activity, and an all-male or mixed-sex group engaged in agonistic behavior). The study recorded behavioral responses and watching rates. All gorillas preferred dynamic over static videos; 3 watched videos depicting gorillas significantly more than those depicting humans. Among the gorilla videos, the gorillas clearly preferred watching the mixed-sex group engaged in agonistic behavior; yet, this did not lead to an increase in aggression or behavior indicating agitation. Further, habituation to videos depicting gorillas did not occur. This supports the effectiveness of this form of enrichment, particularly for a nonhuman animal needing to be separated temporarily due to illness, shipment quarantine, social restructuring, or exhibit modification.     

Tool use during display behavior in wild Cross River gorillas

During the course of a 3-year ecological study on Cross River gorillas (Gorilla gorilla diehli) at the Kagwene Mountain in Cameroon, we observed three cases of tool use which may be unique to the gorillas of this region and possibly learned through interactions with humans. A non-habituated group of Cross River gorillas threw fistfuls of grass toward humans in display contexts. An individual gorilla was also observed to throw a detached branch toward researchers during another encounter. The third encounter occurred between the focal group and a local man, in which the man threw stones at the gorillas and they reacted by throwing fistfuls of grass back at him. We describe these observations and speculate that this sub-population of gorillas developed this display behavior as a response to particular local conditions.     

Food dropping as a food transfer mechanism among western lowland gorillas in Moukalaba-Doudou National Park,Gabon

In this paper, I describe the food-dropping behavior of western lowland gorillas observed in Moukalaba-Doudou National Park, Gabon. I collected observational data of gorillas eating in trees, and recorded whether any individuals were positioned under the same tree. In 22 of the 24 cases of individuals being present under a tree, I observed the gorilla in a tree dropping food to the individual below. In most cases, the recipient was a silverback or an elder half-sibling of the dropper. The dropper’s elder full-sibling was never a recipient. The food-dropping behavior of Moukalaba western lowland gorillas is likely due to a combination of factors: their frugivory, arboreality, large body size, and the scarcity of terrestrial herbs. It is difficult for multiple gorillas to simultaneously feed in the same tree. Under such limitations, younger gorillas face difficulties in defending their feeding patches from older individuals. Nearly 90 % of the recipients were older than the food droppers. Furthermore, food droppers were significantly younger than non-food droppers who simultaneously fed on the same tree, and most-food recipients were significantly older than least-food recipients on the ground. Food dropping may, therefore, be a tactic employed by younger gorillas to defend a feeding site from older individuals. This study suggests that food dropping may reduce feeding contest competition in a gorilla group in Moukalaba. This is a preliminary study that indicates that food dropping may be intentionally used as a way to reduce feeding competition; nevertheless, further studies are needed.     

Play behaviour in lowland gorillas: Age differences,sex differences,and possible functions

A study on lowland gorilla (Gorilla gorilla gorilla) play behaviour was conducted on four exhibits at three different zoological parks so that 19 gorillas were observed. Juvenile gorillas played the most, but play continued at fairly high frequencies through adolescence. Most social play occurred between dyads. Triadic groups usually chased each other. No sex differences in type of play were observed, but gender differences in partner preferences were observed. Males played with both other males and females, while females seldom played together. These data support the social skills hypothesis (Baldwin & Baldwin, 1974) of play. Data were gathered while the author was a graduate student at Tulane University and a visiting lecturer at the University of California, Riverside.