Characterization of Pan social systems reveals in-group/out-group distinction and out-group tolerance in bonobos.

Human between-group interactions are highly variable, ranging from violent to tolerant and affiliative. Tolerance between groups is linked to our unique capacity for large-scale cooperation and cumulative culture, but its evolutionary origins are understudied. In chimpanzees, one of our closest living relatives, predominantly hostile between-group interactions impede cooperation and information flow across groups. In contrast, in our other closest living relative, the bonobo, tolerant between-group associations are observed. However, as these associations can be frequent and prolonged and involve social interactions that mirror those within groups, it is unclear whether these bonobos really do belong to separate groups. Alternatively, the bonobo grouping patterns may be homologous to observations from the large Ngogo chimpanzee community, where individuals form within-group neighborhoods despite sharing the same membership in the larger group. To characterize bonobo grouping patterns, we compare the social structure of the Kokolopori bonobos with the chimpanzee group of Ngogo. Using cluster analysis, we find temporally stable clusters only in bonobos. Despite the large spatial overlap and frequent interactions between the bonobo clusters, we identified significant association preference within but not between clusters and a unique space use of each cluster. Although bonobo associations are flexible (i.e., fission-fusion dynamics), cluster membership predicted the bonobo fission compositions and the spatial cohesion of individuals during encounters. These findings suggest the presence of a social system that combines clear in-group/out-group distinction and out-group tolerance in bonobos, offering a unique referential model for the evolution of tolerant between-group interactions in humans.

Chimpanzees (Pan troglodytes) recognize that their guesses could be wrong and can pass a two-cup disjunctive syllogism task.

When chimpanzees search for hidden food, do they realize that their guesses may not be correct? We applied a post-decision wagering paradigm to a simple two-cup search task, varying whether we gave participants visual access to the baiting and then asking after they had chosen one of the cups whether they would prefer a smaller but certain reward instead of their original choice (experiment 1). Results showed that chimpanzees were more likely to accept the smaller reward in occluded than visible conditions. Experiment 2 found the same effect when we blocked visual access but manipulated the number of hiding locations for the food piece, showing that the effect is not owing to representation type. Experiments 3 and 4 showed that when given information about the contents of the unchosen cup, chimpanzees were able to flexibly update their choice behaviour accordingly. These results suggest that language is not a pre-requisite to solving the disjunctive syllogism and provides a valuable contribution to the debate on logical reasoning in non-human animals.

Chimpanzee and Human Risk Preferences Show Key Similarities.

Risk preference impacts how people make key life decisions related to health, wealth, and well-being. Systematic variations in risk-taking behavior can be the result of differences in fitness expectations, as predicted by life-history theory. Yet the evolutionary roots of human risk-taking behavior remain poorly understood. Here, we studied risk preferences of chimpanzees (86 Pan troglodytes; 47 females; age = 2-40 years) using a multimethod approach that combined observer ratings with behavioral choice experiments. We found that chimpanzees' willingness to take risks shared structural similarities with that of humans. First, chimpanzees' risk preference manifested as a traitlike preference that was consistent across domains and measurements. Second, chimpanzees were ambiguity averse. Third, males were more risk prone than females. Fourth, the appetite for risk showed an inverted-U-shaped relation to age and peaked in young adulthood. Our findings suggest that key dimensions of risk preference appear to emerge independently of the influence of human cultural evolution.

Do chimpanzees see a face on Mars? A search for face pareidolia in chimpanzees.

We sometimes perceive meaningful patterns or images in random arrangements of colors and shapes. This phenomenon is called pareidolia and has recently been studied intensively, especially face pareidolia. In contrast, there are few comparative-cognitive studies on face pareidolia with nonhuman primates. This study explored behavioral evidence for face pareidolia in chimpanzees using visual search and matching tasks. Faces are processed in a configural manner, and their perception and recognition are hampered by inversion and misalignment of top and bottom parts. We investigated whether the same effect occurs in a visual search for face-like objects. The results showed an effect of misalignment. On the other hand, consistent results were not obtained with the photographs of fruits. When only the top or bottom half of the face-like object was presented, chimpanzees showed better performance for the top-half condition, suggesting the importance of the eye area in face pareidolia. In the positive-control experiments, chimpanzees received the same experiment using human faces and human participants with face-like objects and fruits. As a result, chimpanzees showed an inefficient search for inverted and misaligned faces and humans for manipulated face-like objects. Finally, to examine the role of face awareness, we tested matching a human face to a face-like object in chimpanzees but obtained no substantial evidence that they saw the face-like object as a "face." Based on these results, we discussed the extents and limits of face pareidolia in chimpanzees.

I'll (not) take that: The reverse-reward contingency task as a test of self-control and inhibition.

While searching for more evidence of quantitative skills in chimpanzees to add to what she already had found, Boysen discovered something else. When training chimpanzees to point at what they would not get, and not pointing at what they would get, none could do this for piles of food items. Even when those items in the pointed-at set were given away to another chimpanzee, and even with experience in the task, failure persisted. This test, the reverse-reward contingency test, has now been used with many species, as a means of assessing inhibitory control and perhaps self-control in animals. Typically, the task is difficult, and only specific manipulations have worked to allow primates to overcome the reversed contingencies. This includes using symbolic stimuli, adding another layer to the story, and more value to the task itself as a measure perhaps of forms of cognitive control in other species. I will discuss some of these empirical results, including from other chimpanzees who were given variations of the task, and how these studies have influenced numerous areas within comparative cognitive science.

Don't look back on failure: spontaneous uncertainty monitoring in chimpanzees.

During computer-controlled cognitive tasks, chimpanzees often look up at the food dispenser, which activates at the same time as feedback for the correct choice but not for feedback for the incorrect choice. Do these "looking back" behaviors also indicate signs of spontaneous monitoring of their confidence in their choices? To address this question, we delayed the feedback for 1 s after their choice responses and observed their look-back behaviors during the delay period. Two chimpanzees looked up at the food dispenser significantly less frequently when their choice was incorrect (but the feedback was not given) than when it was correct. These look-back behaviors have not been explicitly trained under experimental contexts. Therefore, these results indicate that chimpanzees spontaneously change the frequency of their look-back behaviors in response to the correctness or incorrectness of their own choices, even without external feedback, suggesting that their look-back behaviors may reflect the level of "confidence" or "uncertainty" of their responses immediately before.

Behavioral and physiological response to inequity in bonobos (Pan paniscus).

Inequity aversion (IA), the affective, cognitive, and behavioral response to inequitable outcomes, allows individuals to avoid exploitation and therefore stabilizes cooperation. The presence of IA varies across animal species, which has stimulated research to investigate factors that might explain this variation, and to investigate underlying affective responses. Among great apes, IA is most often studied in chimpanzees. Here, we investigate IA in bonobos, a reputedly tolerant and cooperative species for which few IA studies are available. We describe how bonobos respond to receiving less preferred rewards than a partner in a token exchange task. We show that bonobos respond to receiving less preferred rewards by refusing tokens and rewards, and by leaving the experimental area. Bonobos never refused a trial when receiving preferred rewards, and thus showed no advantageous IA. We also investigate the variability in the disadvantageous IA response on a dyadic level, because the level of IA is expected to vary, depending on characteristics of the dyad. Like in humans and chimpanzees, we show that the tolerance towards inequity was higher in bonobo dyads with more valuable relationships. To study the affective component of IA, we included behavioral and physiological measures of arousal: a displacement behavior (rough self-scratching) and changes in salivary cortisol levels. Both measures of arousal showed large variability, and while analyses on rough self-scratching showed no significant effects, salivary cortisol levels seemed to be lower in subjects that received less than their partner, but higher in subjects that received more than their partner, albeit that both were not significantly different from the equity condition. This suggests that although overcompensated bonobos showed no behavioral response, they might be more aroused. Our data support the cooperation hypothesis on an interspecific and intraspecific level. They show inequity aversion in bonobos, a reputedly cooperative species, and suggest that the variability in IA in bonobos can be explained by their socioecology. Most successful cooperative interactions happen between mothers and their sons and among closely bonded females. The limited need to monitor the partners' investment within these dyads can result in a higher tolerance towards inequity. We therefore suggest future studies to consider relevant socioecological characteristics of the species when designing and analyzing IA studies.

Teaching varies with task complexity in wild chimpanzees.

Cumulative culture is a transformative force in human evolution, but the social underpinnings of this capacity are debated. Identifying social influences on how chimpanzees acquire tool tasks of differing complexity may help illuminate the evolutionary origins of technology in our own lineage. Humans routinely transfer tools to novices to scaffold their skill development. While tool transfers occur in wild chimpanzees and fulfill criteria for teaching, it is unknown whether this form of helping varies between populations and across tasks. Applying standardized methods, we compared tool transfers during termite gathering by chimpanzees in the Goualougo Triangle, Republic of Congo, and in Gombe, Tanzania. At Goualougo, chimpanzees use multiple, different tool types sequentially, choose specific raw materials, and perform modifications that improve tool efficiency, which could make it challenging for novices to manufacture suitable tools. Termite gathering at Gombe involves a single tool type, fishing probes, which can be manufactured from various materials. Multiple measures indicated population differences in tool-transfer behavior. The rate of transfers and probability of transfer upon request were significantly higher at Goualougo, while resistance to transfers was significantly higher at Gombe. Active transfers of tools in which possessors moved to facilitate possession change upon request occurred only at Goualougo, where they were the most common transfer type. At Gombe, tool requests were typically refused. We suggest that these population differences in tool-transfer behavior may relate to task complexity and that active helping plays an enhanced role in the cultural transmission of complex technology in wild apes.

Rhythmic swaying induced by sound in chimpanzees (Pan troglodytes).

Music and dance are universal across human culture and have an ancient history. One characteristic of music is its strong influence on movement. For example, an auditory beat induces rhythmic movement with positive emotions in humans from early developmental stages. In this study, we investigated if sound induced spontaneous rhythmic movement in chimpanzees. Three experiments showed that: 1) an auditory beat induced rhythmic swaying and other rhythmic movements, with larger responses from male chimpanzees than female chimpanzees; 2) random beat as well as regular beat induced rhythmic swaying and beat tempo affected movement periodicity in a chimpanzee in a bipedal posture; and 3) a chimpanzee showed close proximity to the sound source while hearing auditory stimuli. The finding that male chimpanzees showed a larger response to sound than female chimpanzees was consistent with previous literature about "rain dances" in the wild, where male chimpanzees engage in rhythmic displays when hearing the sound of rain starting. The fact that rhythmic swaying was induced regardless of beat regularity may be a critical difference from humans, and a further study should reveal the physiological properties of sound that induce rhythmic movements in chimpanzees. These results suggest some biological foundation for dancing existed in the common ancestor of humans and chimpanzees ∼6 million years ago. As such, this study supports the evolutionary origins of musicality.

Familiarity mediates apes' attentional biases toward human faces.

In zoos, primates experience markedly different interactions with familiar humans, such as the zookeepers who care for them, compared with those with unfamiliar humans, such as the large volume of zoo visitors to whom they are regularly exposed. While the behaviour of zoo-housed primates in the presence of unfamiliar, and to a lesser extent familiar, humans has received considerable attention, if and how they spontaneously distinguish familiar from unfamiliar people, and the cognitive mechanisms underlying the relationships they form with familiar and unfamiliar humans, remain poorly understood. Using a dot-probe paradigm, we assessed whether primates (chimpanzees and gorillas) show an attentional bias toward the faces of familiar humans, with whom the apes presumably had a positive relationship. Contrary to our predictions, all subjects showed a significant attentional bias toward unfamiliar people's faces compared with familiar people's faces when the faces showed a neutral expression, both with and without a surgical face mask on, but no significant attentional bias when the faces showed a surprised expression. These results demonstrate that apes can spontaneously categorize humans based on familiarity and we argue that the attentional biases the apes showed for unfamiliar human faces reflect a novelty effect.

Chimpanzees consider freedom of choice in their evaluation of social action.

Judgements of wrongdoing in humans often hinge upon an assessment of whether a perpetrator acted out of free choice: whether they had more than one option. The classic inhibitors of free choice are constraint (e.g. having your hands tied together) and ignorance (e.g. being unaware that an alternative exists). Here, across two studies, we investigate whether chimpanzees consider these factors in their evaluation of social action. Chimpanzees interacted with a human experimenter who handed them a non-preferred item of food, either because they were physically constrained from accessing the preferred item (Experiment 1) or because they were ignorant of the availability of the preferred item (Experiment 2). We found that chimpanzees were more likely to accept the non-preferred food and showed fewer negative emotional responses when the experimenter was physically constrained compared with when they had free choice. We did not, however, find an effect of ignorance on chimpanzee's evaluation. Freedom of choice factors into chimpanzees' evaluation of how they are treated, but it is unclear whether mental state reasoning is involved in this assessment.

The origins of cognitive flexibility in chimpanzees.

Cognitive flexibility is a core component of executive function, a suite of cognitive capacities that enables individuals to update their behavior in dynamic environments. Human executive functions are proposed to be enhanced compared to other species, but this inference is based primarily on neuroanatomical studies. To address this, we examined the nature and origins of cognitive flexibility in chimpanzees, our closest living relatives. Across three studies, we examined different components of cognitive flexibility using reversal learning tasks where individuals first learned one contingency and then had to shift responses when contingencies flipped. In Study 1, we tested n = 82 chimpanzees ranging from juvenility to adulthood on a spatial reversal task, to characterize the development of basic shifting skills. In Study 2, we tested how n = 24 chimpanzees use spatial versus arbitrary perceptual information to shift, a proposed difference between human and nonhuman cognition. In Study 3, we tested n = 40 chimpanzees on a probabilistic reversal task. We found an extended developmental trajectory for basic shifting and shifting in response to probabilistic feedback-chimpanzees did not reach mature performance until late in ontogeny. Additionally, females were faster to shift than males were. We also found that chimpanzees were much more successful when using spatial versus perceptual cues, and highly perseverative when faced with probabilistic versus consistent outcomes. These results identify both core features of chimpanzee cognitive flexibility that are shared with humans, as well as constraints on chimpanzee cognitive flexibility that may represent evolutionary changes in human cognitive development.

Understanding Language Evolution: Beyond Pan-Centrism.

Language does not fossilize but this does not mean that the language's evolutionary timeline is lost forever. Great apes provide a window back in time on our last prelinguistic ancestor's communication and cognition. Phylogeny and cladistics implicitly conjure Pan (chimpanzees, bonobos) as a superior (often the only) model for language evolution compared with earlier diverging lineages, Gorilla and Pongo (orangutans). Here, in reviewing the literature, it is shown that Pan do not surpass other great apes along genetic, cognitive, ecologic, or vocal traits that are putatively paramount for language onset and evolution. Instead, revived herein is the idea that only by abandoning single-species models and learning about the variation among great apes, there might be a chance to retrieve lost fragments of the evolutionary timeline of language.

To drum or not to drum: Selectivity in tree buttress drumming by chimpanzees (Pan troglodytes verus) in the Nimba Mountains, Guinea.

Chimpanzees live in fission-fusion social organizations, which means that party size, composition, and spatial distribution are constantly in flux. Moreover, chimpanzees use a remarkably extensive repertoire of vocal and nonvocal forms of communication, thought to help convey information in such a socially and spatially dynamic setting. One proposed form of nonvocal communication in chimpanzees is buttress drumming, in which an individual hits a tree buttress with its hands and/or feet, thereby producing a low-frequency acoustic signal. It is often presumed that this behavior functions to communicate over long distances and is, therefore, goal-oriented. If so, we would expect chimpanzees to exhibit selectivity in the choice of trees and buttresses used in buttress drumming. Selectivity is a key attribute of many other goal-directed chimpanzee behaviors, such as nut-cracking and ant dipping. Here, we investigate whether chimpanzees at the Seringbara study site in the Nimba Mountains, Guinea, West Africa, show selectivity in their buttress drumming behavior. Our results indicate that Seringbara chimpanzees are more likely to use larger trees and select buttresses that are thinner and have a greater surface area. These findings imply that tree buttress drumming is not a random act, but rather goal-oriented and requires knowledge of suitable trees and buttresses. Our results also point to long-distance communication as a probable function of buttress drumming based on selectivity for buttress characteristics likely to impact sound propagation. This study provides a foundation for further assessing the cognitive underpinnings and functions of buttress drumming in wild chimpanzees.

Manipulative repertoire of bonobos (Pan paniscus) in spontaneous feeding situation.

Comparative behavioral studies of hand use amongst primate species, including humans, have been central in research on evolutionary mechanisms. In particular, the manipulative abilities of our closest relatives, the chimpanzee (Pan troglodytes), have been widely described in various contexts, showing a high level of dexterity both in zoo and in natural conditions. In contrast, the study of bonobos' manipulative abilities has almost exclusively been carried out in experimental contexts related to tool use. The objective of the present study is to describe the richness of the manipulative repertoire of zoo-housed bonobos, in a spontaneous feeding context including various physical substrates to gain a larger insight into our evolutionary past. Our study describes a great variety of grasping postures and grip associations in bonobos, close to the range of manipulative repertoire in chimpanzees, confirming that the two species are not markedly different in terms of cognitive and morphological constraints associated with food manipulation. We also observed differences in manipulative behaviors between juveniles and adults, indicating a greater diversity in grip associations and grasping postures used in isolation with age, and a sex-biased use of tools with females using tools more often than males. These results are consistent with the previous results in the Pan genus and reinforce the hypothesis that the evolutionary mechanisms underlying the flexibility of manipulative behaviors are shared by both species and that these ecological strategies would have already evolved in their common ancestor.

Dexterity and technique in termite fishing by chimpanzees (Pan troglodytes troglodytes) in the Goualougo Triangle, Republic of Congo.

Although the phenomenon of termite fishing by chimpanzees (Pan troglodytes) has historical and theoretical importance for primatology, we still have a limited understanding of how chimpanzees accomplish this activity, and in particular, about details of skilled actions and the nature of individual variation in fishing techniques. We examined movements, hand positions, grips, and other details from remote video footage of seven adult and subadult female chimpanzees using plant probes to extract Macrotermes muelleri termites from epigeal nests. Six chimpanzees used exclusively one hand (left or right) to grip the probe during termite fishing. All chimpanzees used the same repertoire of actions to insert, adjust, and withdraw the probe but differed in the frequency of use of particular actions. Chimpanzees have been described as eating termites in two ways-directly from the probe or by sweeping them from the probe with one hand. We describe a third technique: sliding the probe between the digits of one stationary hand as the probe is extracted from the nest. The sliding technique requires complementary bimanual coordination (extracting with one hand and grasping lightly with the other, at the same time). We highlight the importance of actions with two hands-one gripping, one assisting-in termite fishing and discuss how probing techniques are correlated with performance. Additional research on digital function and on environmental, organismic, and task constraints will further reveal manual dexterity in termite fishing.

Joint Attention in Human and Chimpanzee Infants in Varied Socio-Ecological Contexts.

Joint attention (JA) is an early manifestation of social cognition, commonly described as interactions in which an infant looks or gestures to an adult female to share attention about an object, within a positive emotional atmosphere. We label this description the JA phenotype. We argue that characterizing JA in this way reflects unexamined assumptions which are, in part, due to past developmental researchers' primary focus on western, middle-class infants and families. We describe a range of cultural variations in caregiving practices, socialization goals, and parenting ethnotheories as an essential initial step in viewing joint attention within inclusive and contextualized perspectives. We begin the process of conducting a decolonized study of JA by considering the core construct of joint attention (i.e., triadic connectedness) and adopting culturally inclusive definitions (labeled joint engagement [JE]). Our JE definitions allow for attention and engagement to be expressed in visual and tactile modalities (e.g., for infants experiencing distal or proximal caregiving), with various social partners (e.g., peers, older siblings, mothers), with a range of shared topics (e.g., representing diverse socialization goals, and socio-ecologies with and without toys), and with a range of emotional tone (e.g., for infants living in cultures valuing calmness and low arousal, and those valuing exuberance). Our definition of JE includes initiations from either partner (to include priorities for adult-led or child-led interactions). Our next foundational step is making an ecological commitment to naturalistic observations (Dahl, 2017, Child Dev Perspect, 11(2), 79-84): We measure JE while infants interact within their own physical and social ecologies. This commitment allows us to describe JE as it occurs in everyday contexts, without constraints imposed by researchers. Next, we sample multiple groups of infants drawn from diverse socio-ecological settings. Moreover, we include diverse samples of chimpanzee infants to compare with diverse samples of human infants, to investigate the extent to which JE is unique to humans, and to document diversity both within and between species. We sampled human infants living in three diverse settings. U.K. infants (n = 8) were from western, middle-class families living near universities in the south of England. Nso infants (n = 12) were from communities of subsistence farmers in Cameroon, Africa. Aka infants (n = 10) were from foraging communities in the tropical rain forests of Central African Republic, Africa. We coded behavioral details of JE from videotaped observations (taken between 2004 and 2010). JE occurred in the majority of coded intervals (Mdn = 68%), supporting a conclusion that JE is normative for human infants. The JA phenotype, in contrast, was infrequent, and significantly more common in the U.K. (Mdn = 10%) than the other groups (Mdn < 3%). We found significant within-species diversity in JE phenotypes (i.e., configurations of predominant forms of JE characteristics). We conclude that triadic connectedness is very common in human infants, but there is significant contextualization of behavioral forms of JE. We also studied chimpanzee infants living in diverse socio-ecologies. The PRI/Zoo chimpanzee infants (n = 7) were from captive, stable groups of mixed ages and sexes, and included 4 infants from the Chester Zoo, U.K. and 3 from the Primate Research Institute, Kyoto University, Japan. The Gombe chimpanzee infants (n = 12) were living in a dynamically changing, wild community in the Gombe National Park, Tanzania, Africa. Additionally, we include two Home chimpanzee infants who were reared from birth by a female scientist, in the combined U.S., middle-class contexts of home and university cognition laboratory. JE was coded from videotaped observations (taken between 1993 and 2006). JE occurred during the majority of coded intervals (Mdn = 64%), consistent with the position that JE is normative for chimpanzee infants. The JA phenotype, in contrast, was rare, but more commonly observed in the two Home chimpanzee infants (in 8% and 2% of intervals) than in other chimpanzee groups (Mdns = 0%). We found within-species diversity in the configurations comprising the JE phenotypes. We conclude that triadic connectedness is very common in chimpanzee infants, but behavioral forms of joint engagement are contextualized. We compared JE across species, and found no species-uniqueness in behavioral forms, JE characteristics, or JE phenotypes. Both human and chimpanzee infants develop contextualized social cognition. Within-species diversity is embraced when triadic connectedness is described with culturally inclusive definitions. In contrast, restricting definitions to the JA phenotype privileges a behavioral form most valued in western, middle-class socio-ecologies, irrespective of whether the interactions involve human or chimpanzee infants. Our study presents a model for how to decolonize an important topic in developmental psychology. Decolonization is accomplished by defining the phenomenon inclusively, embracing diversity in sampling, challenging claims of human-uniqueness, and having an ecological commitment to observe infant social cognition as it occurs within everyday socio-ecological contexts. It is essential that evolutionary and developmental theories of social cognition are re-built on more inclusive and decolonized empirical foundations.

Population-specific social dynamics in chimpanzees.

Understanding intraspecific variation in sociality is essential for characterizing the flexibility and evolution of social systems, yet its study in nonhuman animals is rare. Here, we investigated whether chimpanzees exhibit population-level differences in sociality that cannot be easily explained by differences in genetics or ecology. We compared social proximity and grooming tendencies across four semiwild populations of chimpanzees living in the same ecological environment over three consecutive years, using both linear mixed models and social network analysis. Results indicated temporally stable, population-level differences in dyadic-level sociality. Moreover, group cohesion measures capturing network characteristics beyond dyadic interactions (clustering, modularity, and social differentiation) showed population-level differences consistent with the dyadic indices. Subsequently, we explored whether the observed intraspecific variation in sociality could be attributed to cultural processes by ruling out alternative sources of variation including the influences of ecology, genetics, and differences in population demographics. We conclude that substantial variation in social behavior exists across neighboring populations of chimpanzees and that this variation is in part shaped by cultural processes.

A Comparison of Focal and Opportunistic Sampling Methods when Studying Chimpanzee Facial and Gestural Communication.

Researchers frequently use focal individual sampling to study primate communication. Recent studies of primate gestures have shown that opportunistic sampling offers benefits not found in focal individual sampling, such as the collection of larger sample sizes. What is not known is whether the opportunistic method is biased towards certain signal types or signalers. Our goal was to assess the validity of the opportunistic method by comparing focal individual sampling to opportunistic sampling of facial and gestural communication in a group of captive chimpanzees (Pan troglodytes). We compared: (1) the number of observed facial and gestural signals per signal type and (2) the number of observed facial and gestural signals produced by each signaler. Both methods identified facial signals, gesture signals, and gesture signalers at similar relative rates, but the opportunistic sampling method yielded a more even distribution of signalers and signal types than the focal individual sampling method. In addition, the opportunistic sampling method resulted in larger sample sizes for both facial and gestural communication. However, the opportunistic method did not allow us to calculate the signals per time for each individual, which is easily done with the focal individual method. These results suggest that the opportunistic sampling method is (1) comparable to the focal individual sampling method in multiple important measures, (2) associated with additional sampling benefits, and (3) limited in measuring some variables. Thus, we recommend that future studies use a mixed-methods approach, as focal individual and opportunistic sampling have distinct strengths that complement each other's limitations.