Bonobos and chimpanzees remember familiar conspecifics for decades.

Recognition and memory of familiar conspecifics provides the foundation for complex sociality and is vital to navigating an unpredictable social world [Tibbetts and Dale, Trends Ecol. Evol. 22, 529-537 (2007)]. Human social memory incorporates content about interactions and relationships and can last for decades [Sherry and Schacter, Psychol. Rev. 94, 439-454 (1987)]. Long-term social memory likely played a key role throughout human evolution, as our ancestors increasingly built relationships that operated across distant space and time [Malone et al., Int. J. Primatol. 33, 1251-1277 (2012)]. Although individual recognition is widespread among animals and sometimes lasts for years, little is known about social memory in nonhuman apes and the shared evolutionary foundations of human social memory. In a preferential-looking eye-tracking task, we presented chimpanzees and bonobos (N = 26) with side-by-side images of a previous groupmate and a conspecific stranger of the same sex. Apes' attention was biased toward former groupmates, indicating long-term memory for past social partners. The strength of biases toward former groupmates was not impacted by the duration apart, and our results suggest that recognition may persist for at least 26 y beyond separation. We also found significant but weak evidence that, like humans, apes may remember the quality or content of these past relationships: apes' looking biases were stronger for individuals with whom they had more positive histories of social interaction. Long-lasting social memory likely provided key foundations for the evolution of human culture and sociality as they extended across time, space, and group boundaries.

Eye-tracking as a window into primate social cognition.

Over the past decade, noninvasive, restraint-free eye-tracking research with primates has transformed our understanding of primate social cognition. The use of this technology with many primate species allows for the exploration and comparison of how these species attend to and understand social agents and interactions. The ability to compare and contrast the cognitive capacities of various primate species, including humans, provides insight into the evolutionary mechanisms and selective pressures that have likely shaped social cognition in similar and divergent ways across the primate order. In this review, we begin by discussing noninvasive behavioral methods used to measure primate gaze and attention before the introduction of noninvasive, restraint-free eye-tracking methodologies. Next, we focus on findings from recent eye-tracking research on primate social cognition, beginning with simple visual and search mechanisms. We then discuss the results that have built on this basic understanding of how primates view images and videos, exploring discrimination and knowledge of social agents, following social cues, tracking perspectives and predicting behavior, and the combination of eye-tracking and other behavioral and physiological methods. Finally, we discuss some future directions of noninvasive eye-tracking research on primate social cognition and current eye-tracking work-in-progress that builds on these previous studies, investigating underexplored socio-cognitive capacities and utilizing new methodologies.

Great apes use self-experience to anticipate an agent's action in a false-belief test.

Human social life depends on theory of mind, the ability to attribute mental states to oneself and others. A signature of theory of mind, false belief understanding, requires representing others' views of the world, even when they conflict with one's own. After decades of research, it remains controversial whether any nonhuman species possess a theory of mind. One challenge to positive evidence of animal theory of mind, the behavior-rule account, holds that animals solve such tasks by responding to others' behavioral cues rather than their mental states. We distinguish these hypotheses by implementing a version of the "goggles" test, which asks whether, in the absence of any additional behavioral cues, animals can use their own self-experience of a novel barrier being translucent or opaque to determine whether another agent can see through the same barrier. We incorporated this paradigm into an established anticipatory-looking false-belief test for great apes. In a between-subjects design, apes experienced a novel barrier as either translucent or opaque, although both looked identical from afar. While being eye tracked, all apes then watched a video in which an actor saw an object hidden under 1 of 2 identical boxes. The actor then scuttled behind the novel barrier, at which point the object was relocated and then removed. Only apes who experienced the barrier as opaque visually anticipated that the actor would mistakenly search for the object in its previous location. Great apes, therefore, appeared to attribute differential visual access based specifically on their own past perceptual experience to anticipate an agent's actions in a false-belief test.

Representing knowledge, belief, and everything in between: Representational complexity in humans and other apes.

Building on Phillips and colleagues' case for the primacy of knowledge, we advocate for attention to diversity in mentalizing constructs within, as well as between, knowledge and belief. Ultimately, as great apes and other animals show, the development and evolution of theory of mind may reflect a much greater range of incremental elaborations of representational or computational complexity.

The application of noninvasive, restraint-free eye-tracking methods for use with nonhuman primates.

Over the past 50 years there has been a strong interest in applying eye-tracking techniques to study a myriad of questions related to human and nonhuman primate psychological processes. Eye movements and fixations can provide qualitative and quantitative insights into cognitive processes of nonverbal populations such as nonhuman primates, clarifying the evolutionary, physiological, and representational underpinnings of human cognition. While early attempts at nonhuman primate eye tracking were relatively crude, later, more sophisticated and sensitive techniques required invasive protocols and the use of restraint. In the past decade, technology has advanced to a point where noninvasive eye-tracking techniques, developed for use with human participants, can be applied for use with nonhuman primates in a restraint-free manner. Here we review the corpus of recent studies (N=32) that take such an approach. Despite the growing interest in eye-tracking research, there is still little consensus on "best practices," both in terms of deploying test protocols or reporting methods and results. Therefore, we look to advances made in the field of developmental psychology, as well as our own collective experiences using eye trackers with nonhuman primates, to highlight key elements that researchers should consider when designing noninvasive restraint-free eye-tracking research protocols for use with nonhuman primates. Beyond promoting best practices for research protocols, we also outline an ideal approach for reporting such research and highlight future directions for the field.

Bonobos voluntarily hand food to others but not toys or tools.

A key feature of human prosociality is direct transfers, the most active form of sharing in which donors voluntarily hand over resources in their possession Direct transfers buffer hunter-gatherers against foraging shortfalls. The emergence and elaboration of this behaviour thus likely played a key role in human evolution by promoting cooperative interdependence and ensuring that humans' growing energetic needs (e.g. for increasing brain size) were more reliably met. According to the strong prosociality hypothesis, among great apes only humans exhibit sufficiently strong prosocial motivations to directly transfer food. The versatile prosociality hypothesis suggests instead that while other apes may make transfers in constrained settings, only humans share flexibly across food and non-food contexts. In controlled experiments, chimpanzees typically transfer objects but not food, supporting both hypotheses. In this paper, we show in two experiments that bonobos directly transfer food but not non-food items. These findings show that, in some contexts, bonobos exhibit a human-like motivation for direct food transfer. However, humans share across a far wider range of contexts, lending support to the versatile prosociality hypothesis. Our species' unusual prosocial flexibility is likely built on a prosocial foundation we share through common descent with the other apes.

Human ostensive signals do not enhance gaze following in chimpanzees, but do enhance object-oriented attention.

The previous studies have shown that human infants and domestic dogs follow the gaze of a human agent only when the agent has addressed them ostensively-e.g., by making eye contact, or calling their name. This evidence is interpreted as showing that they expect ostensive signals to precede referential information. The present study tested chimpanzees, one of the closest relatives to humans, in a series of eye-tracking experiments using an experimental design adapted from these previous studies. In the ostension conditions, a human actor made eye contact, called the participant's name, and then looked at one of two objects. In the control conditions, a salient cue, which differed in each experiment (a colorful object, the actor's nodding, or an eating action), attracted participants' attention to the actor's face, and then the actor looked at the object. Overall, chimpanzees followed the actor's gaze to the cued object in both ostension and control conditions, and the ostensive signals did not enhance gaze following more than the control attention-getters. However, the ostensive signals enhanced subsequent attention to both target and distractor objects (but not to the actor's face) more strongly than the control attention-getters-especially in the chimpanzees who had a close relationship with human caregivers. We interpret this as showing that chimpanzees have a simple form of communicative expectations on the basis of ostensive signals, but unlike human infants and dogs, they do not subsequently use the experimenter's gaze to infer the intended referent. These results may reflect a limitation of non-domesticated species for interpreting humans' ostensive signals in inter-species communication.

No evidence for contagious yawning in lemurs.

Among some haplorhine primates, including humans, relaxed yawns spread contagiously. Such contagious yawning has been linked to social bonds and empathy in some species. However, no studies have investigated contagious yawning in strepsirhines. We conducted an experimental study of contagious yawning in strepsirhines, testing ring-tailed and ruffed lemurs (n = 24) in a paradigm similar to one that has induced contagious yawning in haplorhines. First, in a control experiment, we investigated whether lemurs responded to projected video content in general (experiment 1). We showed them two videos to which we expected differential responses: one featured a terrestrial predator and the other a caretaker holding food. Next, to test for yawn contagion, we showed individual lemurs life-size video projections of groupmates and conspecific strangers yawning, and control footage of the same individuals at rest (experiment 2). Then, to examine whether a group context might enhance or allow for contagion, we exposed subjects to the same videos in a group setting (experiment 3). Lemurs produced alarm vocalizations and moved upward while viewing the predator, but not the caretaker, demonstrating that they do perceive video content meaningfully. However, lemurs did not yawn in response to yawning stimuli when tested alone, or with their groupmates. This study provides preliminary evidence that lemurs do not respond to yawning stimuli similarly to haplorhines, and suggests that this behavior may have evolved or become more exaggerated in haplorhines after the two major primate lineages split.

Bonobos and chimpanzees exhibit human-like framing effects.

Humans exhibit framing effects when making choices, appraising decisions involving losses differently from those involving gains. To directly test for the evolutionary origin of this bias, we examined decision-making in humans' closest living relatives: bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We presented the largest sample of non-humans to date (n = 40) with a simple task requiring minimal experience. Apes made choices between a 'framed' option that provided preferred food, and an alternative option that provided a constant amount of intermediately preferred food. In the gain condition, apes experienced a positive 'gain' event in which the framed option was initially presented as one piece of food but sometimes was augmented to two. In the loss condition, apes experienced a negative 'loss' event in which they initially saw two pieces but sometimes received only one. Both conditions provided equal pay-offs, but apes chose the framed option more often in the positive 'gain' frame. Moreover, male apes were more susceptible to framing than were females. These results suggest that some human economic biases are shared through common descent with other apes and highlight the importance of comparative work in understanding the origins of individual differences in human choice.

Ring-tailed lemurs (Lemur catta) exploit information about what others can see but not what they can hear.

Studies suggest that haplorhine primates are sensitive to what others can see and hear. Using two experimental designs, we tested the hypothesis that ring-tailed lemurs (N = 16) are also sensitive to the visual and auditory perception of others. In the first task, we used a go/no-go design that required lemurs to exploit only auditory information. In the second task, we used a forced-choice design where lemurs competed against a human who would prevent them from obtaining food if their approaches were detected. Subjects were given the choice of obtaining food silently or noisily when the competitor's back was turned. They were also given the choice to obtain food when the competitor could either see them or not. Here, we replicate the findings of previous studies indicating that ring-tailed lemurs are sensitive to whether they can be seen; however, we found no evidence that subjects are sensitive to whether others can hear them. Our findings suggest that ring-tailed lemurs converge with haplorhine primates only in their sensitivity to the visual information of others. The results emphasize the importance of investigating social cognition across sensory domains in order to elucidate the cognitive mechanisms that underlie apparently complex social behavior. These findings also suggest that the social dynamics of haplorhine groups impose greater cognitive demands than lemur groups, despite similarities in total group size.

In search of animal normativity: a framework for studying social norms in non-human animals.

Social norms - rules governing which behaviours are deemed appropriate or inappropriate within a given community - are typically taken to be uniquely human. Recently, this position has been challenged by a number of philosophers, cognitive scientists, and ethologists, who have suggested that social norms may also be found in certain non-human animal communities. Such claims have elicited considerable scepticism from norm cognition researchers, who doubt that any non-human animals possess the psychological capacities necessary for normative cognition. However, there is little agreement among these researchers about what these psychological prerequisites are. This makes empirical study of animal social norms difficult, since it is not clear what we are looking for and thus what should count as behavioural evidence for the presence (or absence) of social norms in animals. To break this impasse, we offer an approach that moves beyond contested psychological criteria for social norms. This approach is inspired by the animal culture research program, which has made a similar shift away from heavily psychological definitions of 'culture' to become organised around a cluster of more empirically tractable concepts of culture. Here, we propose an analogous set of constructs built around the core notion of a normative regularity, which we define as a socially maintained pattern of behavioural conformity within a community. We suggest methods for studying potential normative regularities in wild and captive primates. We also discuss the broader scientific and philosophical implications of this research program with respect to questions of human uniqueness, animal welfare and conservation.

Little evidence that Eurasian jays protect their caches by responding to cues about a conspecific's desire and visual perspective.

Eurasian jays have been reported to protect their caches by responding to cues about either the visual perspective or current desire of an observing conspecific, similarly to other corvids. Here, we used established paradigms to test whether these birds can - like humans - integrate multiple cues about different mental states and perform an optimal response accordingly. Across five experiments, which also include replications of previous work, we found little evidence that our jays adjusted their caching behaviour in line with the visual perspective and current desire of another agent, neither by integrating these social cues nor by responding to only one type of cue independently. These results raise questions about the reliability of the previously reported effects and highlight several key issues affecting reliability in comparative cognition research.

Eurasian jays, Garrulus glandarius, are members of the crow family. These large-brained birds hide food when it is abundant, and eat it later, when it is scarce. Previous studies have found that jays avoid theft by other jays by carefully deciding what food to hide, and where. In one study, they preferred to hide their food behind an opaque barrier, rather than a transparent one, when another jay was watching. In a second study, they preferred to hide food that the watching jay had already eaten enough of, and thus did not want. These studies suggest that jays have flexible cognitive skills when it comes to protecting their food. They respond to whether a potential thief can see their hiding place and to how much a thief might want the food they are stashing. The next question is, can Eurasian jays combine these two pieces of information? For example, if a jay has two types of food they could hide when another jay is present, but only has one place to hide them (either in view or out-of-view of the other jay), does the first jay prefer to stash the food that the second jay has already eaten, and therefore does not want anymore, only when the hiding place is visible to second jay? To find out, Amodio et al. watched Eurasian jays hiding macadamia nuts or peanuts in the presence of another jay. In the first setup, jays were given one food to hide and two possible hiding places, one opaque and one transparent, while being watched by a jay that had either had its fill of the food, or not tried it. In the second setup, jays were given both foods to hide, but only had one place to hide them (either transparent or opaque); while being watched by a jay that had eaten enough of one of the foods. Contrary to expectations, the jays did not seem to be able to combine the information about what the other jay could see and what it had been eating. In fact, they seemed unable to respond to either piece of information. When Amodio et al. repeated the original experiments, the jays did not seem to prefer to hide food out of sight, or to hide food that the watcher had already eaten. These results raise questions about the repeatability of experiments on food hiding strategies in birds of the crow family. It suggests that previous findings should be further investigated, potentially to identify important factors that might affect the repeatability of food-hiding tactics. Repeating the experiments may show how best to investigate behavioural patterns in jays in the future.

Social bonds provide multiple pathways to reproductive success in wild male chimpanzees.

In most male mammals, fitness is strongly shaped by competitive access to mates, a non-shareable resource. How, then, did selection favor the evolution of cooperative social bonds? We used behavioral and genetic data on wild chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania, to study the mechanisms by which male-male social bonds increase reproductive success. Social bonds increased fitness in several ways: first, subordinate males that formed strong bonds with the alpha male had higher siring success. Independently, males with larger networks of strong bonds had higher siring success. In the short term, bonds predicted coalition formation and centrality in the coalition network, suggesting that males benefit from being potential allies to numerous male rivals. In the long term, male ties influenced fitness via improved dominance rank for males that attain alpha status. Together, these results suggest that male bonds evolved in chimpanzees by affording both short- and long-term pathways to reproductive success.

Erratum to "Bonobos and chimpanzees preferentially attend to familiar members of the dominant sex" [Animal Behaviour 177 (2021) 193-206].

[This corrects the article DOI: 10.1016/j.anbehav.2021.04.027.].

Implicit Measures Help Demonstrate the Value of Conservation Education in the Democratic Republic of the Congo.

Biodiversity is being lost at unprecedented rates. Limited conservation resources must be prioritized strategically to maximize impact. Here we introduce novel methods to assess a small-scale conservation education program in the Democratic Republic of Congo. Lola ya Bonobo is the world's only sanctuary for one of humans' two closest living relatives, bonobos, orphaned by the illegal trade in bushmeat and exotic pets. The sanctuary is situated on the edge of the country's capital, Kinshasa, its most densely populated region and a hub for the illegal wildlife trade that is imperiling bonobos and other endangered species. Lola ya Bonobo implements an education program specifically designed to combat this trade. Previous evaluation demonstrated the program's efficacy in transmitting conservation knowledge to children. In Study 1, we use novel implicit tests to measure conservation attitudes before and after an educational visit and document a significant increase in children's pro-conservation attitudes following direct exposure to bonobos and the education program. In Study 2, we show that adults exhibit high levels of conservation knowledge even before visiting the sanctuary, likely due to the sanctuary's longstanding education efforts in Kinshasa. In Study 3, we explored adults' empathetic attitudes toward bonobos before and after the sanctuary tour. Our results support the conservation education hypothesis that conservation education has improved relevant knowledge and attitudes in Kinshasa. Crucially, the present study validates new methods for implicitly assessing attitudes about environmental and social issues. These methods overcome typical biases in survey sampling and can be employed in diverse populations, including those with low literacy rates.

Theory of mind in animals: Current and future directions.

Theory of mind (ToM; a.k.a., mind-reading, mentalizing, mental-state attribution, and perspective-taking) is the ability to ascribe mental states, such as desires and beliefs, to others, and it is central to the unique forms of communication, cooperation, and culture that define our species. As a result, for 40 years, researchers have endeavored to determine whether ToM is itself unique to humans. Investigations in other species (e.g., apes, monkeys, corvids) are essential to understand the mechanistic underpinnings and evolutionary origins of this capacity across taxa, including humans. We review the literature on ToM in nonhuman animals, suggesting that some species share foundational social cognitive mechanisms with humans. We focus principally on innovations of the last decade and pressing directions for future work. Underexplored types of social cognition have been targeted, including ascription of mental states, such as desires and beliefs, that require simultaneously representing one's own and another's conflicting motives or views of the world. Ongoing efforts probe the motivational facets of ToM, how flexibly animals can recruit social cognitive skills across cooperative and competitive settings, and appropriate motivational contexts for comparative inquiry. Finally, novel methodological and empirical approaches have brought new species (e.g., lemurs, dogs) into the lab, implemented critical controls to elucidate underlying mechanisms, and contributed powerful new techniques (e.g., looking-time, eye-tracking) that open the door to unexplored approaches for studying animal minds. These innovations in cognition, motivation, and method promise fruitful progress in the years to come, in understanding the nature and origin of ToM in humans and other species. This article is categorized under: Cognitive Biology > Evolutionary Roots of Cognition Psychology > Comparative Psychology Neuroscience > Cognition.

Bonobos Prefer Individuals that Hinder Others over Those that Help.

Humans closely monitor others' cooperative relationships [1, 2]. Children and adults willingly incur costs to reward helpers and punish non-helpers-even as bystanders [3-5]. Already by 3 months, infants favor individuals that they observe helping others [6-8]. This early-emerging prosocial preference may be a derived motivation that accounts for many human forms of cooperation that occur beyond dyadic interactions and are not exhibited by other animals [9, 10]. As the most socially tolerant nonhuman ape [11-17] (but see [18]), bonobos (Pan paniscus) provide a powerful phylogenetic test of whether this trait is derived in humans. Bonobos are more tolerant than chimpanzees, can flexibly obtain food through cooperation, and voluntarily share food in captivity and the wild, even with strangers [11-17] (but see [18]). Their neural architecture exhibits a suite of characteristics associated with greater sensitivity to others [19, 20], and their sociality is hypothesized to have evolved due to selection against male aggression [21-23]. Here we show in four experiments that bonobos discriminated agents based on third-party interactions. However, they did not exhibit the human preference for helpers. Instead, they reliably favored a hinderer that obstructed another agent's goal (experiments 1-3). In a final study (experiment 4), bonobos also chose a dominant individual over a subordinate. Bonobos' interest in hinderers may reflect attraction to dominant individuals [24]. A preference for helpers over hinderers may therefore be derived in humans, supporting the hypothesis that prosocial preferences played a central role in the evolution of human development and cooperation.

Eye tracking uncovered great apes' ability to anticipate that other individuals will act according to false beliefs.

Using a novel eye-tracking test, we recently showed that great apes anticipate that other individuals will act according to false beliefs. This finding suggests that, like humans, great apes understand others' false beliefs, at least in an implicit way. One key question raised by our study is why apes have passed our tests but not previous ones. In this article, we consider this question by detailing the development of our task. We considered 3 major differences in our task compared with the previous ones. First, we monitored apes' eye movements, and specifically their anticipatory looks, to measure their predictions about how agents will behave. Second, we adapted our design from an anticipatory-looking false belief test originally developed for human infants. Third, we developed novel test scenarios that were specifically designed to capture the attention of our ape participants. We then discuss how each difference may help explain differences in performance on our task and previous ones, and finally propose some directions for future studies.

A test of the submentalizing hypothesis: Apes' performance in a false belief task inanimate control.

Much debate concerns whether any nonhuman animals share with humans the ability to infer others' mental states, such as desires and beliefs. In a recent eye-tracking false-belief task, we showed that great apes correctly anticipated that a human actor would search for a goal object where he had last seen it, even though the apes themselves knew that it was no longer there. In response, Heyes proposed that apes' looking behavior was guided not by social cognitive mechanisms but rather domain-general cueing effects, and suggested the use of inanimate controls to test this alternative submentalizing hypothesis. In the present study, we implemented the suggested inanimate control of our previous false-belief task. Apes attended well to key events but showed markedly fewer anticipatory looks and no significant tendency to look to the correct location. We thus found no evidence that submentalizing was responsible for apes' anticipatory looks in our false-belief task.