Great ape cognition is structured by stable cognitive abilities and predicted by developmental conditions.

Great ape cognition is used as a reference point to specify the evolutionary origins of complex cognitive abilities, including in humans. This research often assumes that great ape cognition consists of cognitive abilities (traits) that account for stable differences between individuals, which change and develop in response to experience. Here, we test the validity of these assumptions by assessing repeatability of cognitive performance among captive great apes (Gorilla gorilla, Pongo abelii, Pan paniscus, Pan troglodytes) in five tasks covering a range of cognitive domains. We examine whether individual characteristics (age, group, test experience) or transient situational factors (life events, testing arrangements or sociality) influence cognitive performance. Our results show that task-level performance is generally stable over time; four of the five tasks were reliable measurement tools. Performance in the tasks was best explained by stable differences in cognitive abilities (traits) between individuals. Cognitive abilities were further correlated, suggesting shared cognitive processes. Finally, when predicting cognitive performance, we found stable individual characteristics to be more important than variables capturing transient experience. Taken together, this study shows that great ape cognition is structured by stable cognitive abilities that respond to different developmental conditions.

Multicomponent and multisensory communicative acts in orang-utans may serve different functions.

From early infancy, human face-to-face communication is multimodal, comprising a plethora of interlinked communicative and sensory modalities. Although there is also growing evidence for this in nonhuman primates, previous research rarely disentangled production from perception of signals. Consequently, the functions of integrating articulators (i.e. production organs involved in multicomponent acts) and sensory channels (i.e. modalities involved in multisensory acts) remain poorly understood. Here, we studied close-range social interactions within and beyond mother-infant pairs of Bornean and Sumatran orang-utans living in wild and captive settings, to examine use of and responses to multicomponent and multisensory communication. From the perspective of production, results showed that multicomponent acts were used more than the respective unicomponent acts when the presumed goal did not match the dominant outcome for a specific communicative act, and were more common among non-mother-infant dyads and Sumatran orang-utans. From the perception perspective, we found that multisensory acts were more effective than the respective unisensory acts, and were used more in wild compared to captive populations. We argue that multisensory acts primarily facilitate effectiveness, whereas multicomponent acts become relevant when interaction outcomes are less predictable. These different functions underscore the importance of distinguishing between production and perception in studies of communication.

Immature wild orangutans acquire relevant ecological knowledge through sex-specific attentional biases during social learning.

As a part of growing up, immature orangutans must acquire vast repertoires of skills and knowledge, a process that takes several years of observational social learning and subsequent practice. Adult female and male orangutans show behavioral differences including sex-specific foraging patterns and male-biased dispersal. We investigated how these differing life trajectories affect social interest and emerging ecological knowledge in immatures. We analyzed 15 years of detailed observational data on social learning, associations, and diet repertoires of 50 immatures (16 females and 34 males), from 2 orangutan populations. Specific to the feeding context, we found sex differences in the development of social interest: Throughout the dependency period, immature females direct most of their social attention at their mothers, whereas immature males show an increasing attentional preference for individuals other than their mothers. When attending to non-mother individuals, males show a significant bias toward immigrant individuals and a trend for a bias toward adult males. In contrast, females preferentially attend to neighboring residents. Accordingly, by the end of the dependency period, immature females show a larger dietary overlap with their mothers than do immature males. These results suggest that immature orangutans show attentional biases through which they learn from individuals with the most relevant ecological knowledge. Diversifying their skills and knowledge likely helps males when they move to a new area. In sum, our findings underline the importance of fine-grained social inputs for the acquisition of ecological knowledge and skills in orangutans and likely in other apes as well.

Involuntary autobiographical memories and their relation to other forms of spontaneous thoughts.

Involuntary autobiographical memories are memories of personal events that come to mind spontaneously-that is, with no conscious initiation of the retrieval process. Such spontaneously arising memories were long ignored in cognitive psychology, which generally has focused on controlled and strategic forms of remembering, studied in laboratory settings. Recent evidence shows that involuntary memories of past events are highly frequent in daily life, and that they represent a context-sensitive, and associative way of recollecting past events that involves little executive control. They operate by constraints that favour recent events and events with a distinct feature overlap to the current situation, which optimizes the probability of functional relevance to the ongoing situation. In addition to adults, they are documented in young children and great apes and may be an ontogenetic and evolutionary forerunner of strategic retrieval of past events. Findings suggest that intrusive involuntary memories observed clinically after traumatic events should be viewed as a dysfunctional subclass of otherwise functional involuntary autobiographical memories. Because of their highly constrained, situation-dependent and automatic nature, involuntary autobiographical memories form a distinct category of spontaneous thought that cannot be equated with mind wandering. This article is part of the theme issue 'Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation'.

Preference for free or forced choice in Sumatran orangutans (Pongo abelii).

Empirical investigations of humans, pigeons, rats, and monkeys have indicated that these species will select free over forced choice, even when faced with identical outcomes. However, the same has yet to be quantitatively confirmed in nonhuman great apes. This experiment is the first systematic investigation of preference for free or forced choice in great apes using a paradigm in which extraneous variables are highly controlled. Three orangutans were given a choice of one of two virtual routes, one that provided a choice and one that did not via a touchscreen computer program. Choice of either route was rewarded with the same type and quantity of food. Initial results indicated a preference for free choice across all three participants. However, in two control conditions, orangutans' preferences varied, suggesting a weaker tendency to exercise choice than species previously tested. We suggest further investigation of preference for free and forced choice in orangutans and other great apes through alternative experimental paradigms that focus on increasing the fidelity of free and forced choice options.

Differences in novel food response between Pongo and Pan.

The diversity of great ape diets requires behavioral flexibility. Consequently, the exploration of potentially novel food sources is supposedly beneficial, but simultaneously, apes show high neophobia to prevent harmful and poisonous food intake. Social information, such as presence of group members or observations of non-naïve, experienced individuals have been demonstrated to affect the acceptance of novel food items in primates. Sociality may have evolutionary effects on the response of apes to novel foods. Here we assess the social information hypothesis, which predicts that selection favors higher neophobia in species where social information is abundant. We report the results from 134 great apes housed in multiple facilities from four closely related species that naturally differ in their degree of sociality: Pongo pygmaeus, Pongo abelii, Pan troglodytes and Pan paniscus. We examined individuals' reactions to novel foods when alone, which enabled us to detect any inherent differences and revealed significant distinctions between species. Chimpanzees and bonobos, that are naturally exposed to higher amounts of social information, were less likely to consume novel foods alone (showed higher neophobia) than the two more solitary orangutan species. Chimpanzees were especially cautious and showed higher explorative behaviors before tasting novel food than other species. Age influenced neophobia as younger individuals of all species took longer to taste novel foods than adults did.

The effects of sociability on exploratory tendency and innovation repertoires in wild Sumatran and Bornean orangutans.

It has been hypothesized that opportunities for social learning affect the size and complexity of the adult skill set of birds and mammals, their learning ability, and thus ultimately also their innovation frequency. To test these predictions we compared rates of social learning, rates of independent exploration (independent learning) and innovation repertoires between individuals of a highly sociable population of Pongo abelii at Suaq Balimbing and a less sociable population of Pongo pygmaeus wurmbii at Tuanan. Suaq immatures showed significantly higher rates of peering, even after controlling for differences in association time and diet complexity, implying that they make disproportionally greater use of their increased opportunities for social learning. As predicted, we found that immatures and adults at Suaq also showed significantly higher rates of exploratory behaviour. The difference between the individuals of the two popuations remained when controlling for association time, suggesting persistent developmental effects, intrinsic differences, or both. Accordingly, Suaq animals had a larger set of learned skills and a higher mean dietary complexity. Our findings show that population level sociability, individual rates of exploration and population-wide repertoires of innovations are positively linked, as predicted.

Great apes distinguish true from false beliefs in an interactive helping task.

Understanding the behavior of others in a wide variety of circumstances requires an understanding of their psychological states. Humans' nearest primate relatives, the great apes, understand many psychological states of others, for example, perceptions, goals, and desires. However, so far there is little evidence that they possess the key marker of advanced human social cognition: an understanding of false beliefs. Here we demonstrate that in a nonverbal (implicit) false-belief test which is passed by human 1-year-old infants, great apes as a group, including chimpanzees (Pan troglodytes), bonobos (Pan paniscus), and orangutans (Pongo abelii), distinguish between true and false beliefs in their helping behavior. Great apes thus may possess at least some basic understanding that an agent's actions are based on her beliefs about reality. Hence, such understanding might not be the exclusive province of the human species.

Great apes anticipate that other individuals will act according to false beliefs.

Humans operate with a "theory of mind" with which they are able to understand that others' actions are driven not by reality but by beliefs about reality, even when those beliefs are false. Although great apes share with humans many social-cognitive skills, they have repeatedly failed experimental tests of such false-belief understanding. We use an anticipatory looking test (originally developed for human infants) to show that three species of great apes reliably look in anticipation of an agent acting on a location where he falsely believes an object to be, even though the apes themselves know that the object is no longer there. Our results suggest that great apes also operate, at least on an implicit level, with an understanding of false beliefs.

Cognitive differences between orang-utan species: a test of the cultural intelligence hypothesis.

Cultural species can - or even prefer to - learn their skills from conspecifics. According to the cultural intelligence hypothesis, selection on underlying mechanisms not only improves this social learning ability but also the asocial (individual) learning ability. Thus, species with systematically richer opportunities to socially acquire knowledge and skills should over time evolve to become more intelligent. We experimentally compared the problem-solving ability of Sumatran orang-utans (Pongo abelii), which are sociable in the wild, with that of the closely related, but more solitary Bornean orang-utans (P. pygmaeus), under the homogeneous environmental conditions provided by zoos. Our results revealed that Sumatrans showed superior innate problem-solving skills to Borneans, and also showed greater inhibition and a more cautious and less rough exploration style. This pattern is consistent with the cultural intelligence hypothesis, which predicts that the more sociable of two sister species experienced stronger selection on cognitive mechanisms underlying learning.

Children's and Apes' Preparatory Responses to Two Mutually Exclusive Possibilities.

Animal brains have evolved to predict outcomes of events in the immediate environment [1-5]. Adult humans are particularly adept at dealing with environmental uncertainty, being able to mentally represent multiple, even mutually exclusive versions of the future and prepare accordingly. This capacity is fundamental to many complex future-oriented behaviors [6, 7], yet little is known about when it develops in children [8] and whether it is shared with non-human animals [9]. Here we show that children become able to insightfully prepare for two mutually exclusive versions of an undetermined future event during the middle preschool years, whereas we find no evidence for such a capacity in a sample of chimpanzees and orangutans. We gave 90 preschool children and 8 great apes the opportunity to catch an item dropped into a forked tube with two bottom openings. Children's performance improved linearly across age groups (2, 2.5, 3, 3.5, and 4 years), with none of the youngest group but most of the oldest group spontaneously covering both openings the first time they prepared to catch the item. The apes performed like 2-year-olds on the first trial, with none of them covering both openings. Some apes and 2-year-olds eventually passed the task, but only in a manner consistent with trial-and-error learning. Our results reveal the developmental trajectory of a critical cognitive ability that allows humans to prepare for future uncertainty, and they also raise the possibility that this ability is not shared with other hominids.

Sensitivity to Relational Similarity and Object Similarity in Apes and Children.

Relational reasoning is a hallmark of sophisticated cognition in humans. Does it exist in other primates? Despite some affirmative answers, there appears to be a wide gap in relational ability between humans and other primates--even other apes. Here, we test one possible explanation for this gap, motivated by developmental research showing that young humans often fail at relational reasoning tasks because they focus on objects instead of relations. When asked, "duck:duckling is like tiger:?," preschool children choose another duckling (object match) rather than a cub. If other apes share this focus on concrete objects, it could undermine their relational reasoning in similar ways. To test this, we compared great apes and 3-year-old humans' relational reasoning on the same spatial mapping task, with and without competing object matches. Without competing object matches, both children and Pan species (chimpanzees and bonobos) spontaneously used relational similarity, albeit children more so. But when object matches were present, only children responded strongly to them. We conclude that the relational gap is not due to great apes' preference for concrete objects. In fact, young humans show greater object focus than nonhuman apes.

Similar stimulus features control visual classification in orangutans and rhesus monkeys.

Many species classify images according to visual attributes. In pigeons, local features may disproportionately control classification, whereas in primates global features may exert greater control. In the absence of explicitly comparative studies, in which different species are tested with the same stimuli under similar conditions, it is not possible to determine how much of the variation in the control of classification is due to species differences and how much is due to differences in the stimuli, training, or testing conditions. We tested rhesus monkeys (Macaca mulatta) and orangutans (Pongo pygmaeus and Pongo abelii) in identical tests in which images were modified to determine which stimulus features controlled classification. Monkeys and orangutans were trained to classify full color images of birds, fish, flowers, and people; they were later given generalization tests in which images were novel, black and white, black and white line drawings, or scrambled. Classification in these primate species was controlled by multiple stimulus attributes, both global and local, and the species behaved similarly.

Contrasting responses to novelty by wild and captive orangutans.

Several studies have suggested that wild primates tend to behave with caution toward novelty, whereas captive primates are thought to be less neophobic, more exploratory, and more innovative. However, few studies have systematically compared captive and wild individuals of the same species to document this "captivity effect" in greater detail. Here we report the responses of both wild and captive orangutans to the same novel items. Novel objects were presented to wild orangutans on multiple platforms placed in the canopy and equipped with motion-triggered video cameras. The same and different novel objects were also presented to orangutans in two different zoos. The results demonstrate extreme conservatism in both Bornean and Sumatran wild orangutans, who gradually approached the novel objects more closely as they became familiar, but avoided contact with them over many encounters spanning several months. Their zoo-living conspecifics, in contrast, showed an immediate neophilic response. Our results thus confirm the "captivity effect." To the various ecological explanations proposed before (reduced risk and increased time and energy balance for captive individuals relative to wild ones), we add the social information hypothesis, which claims that individuals confronted with novel items preferentially rely on social cues whenever possible. This caution toward novelty disappears when human caretakers become additional role models and can also be eroded when all experience with novelty is positive.

Bonobos and orangutans, but not chimpanzees, flexibly plan for the future in a token-exchange task.

Non-human animals, including great apes, have been suggested to share some of the skills for planning that humans commonly exhibit. A crucial difference between human and non-human planning may relate to the diversity of domains and needs in which this skill is expressed. Although great apes can save tools for future use, there is little evidence yet that they can also do so in other contexts. To investigate this question further, we presented the apes with a planning token-exchange task that differed from standard tool-use tasks. Additionally, we manipulated the future outcome of the task to investigate planning flexibility. In the Exchange condition, subjects had to collect, save and transport tokens because they would need them 30 min later to exchange them for food with a human, i.e., "bring-back" response. In the Release condition, the collection and transport of tokens were not needed as no exchange took place after 30 min. Out of 13 subjects, eight solved the task at least once in the Exchange condition, with chimpanzees appearing less successful than the other species. Importantly, three individuals showed a clear differential response between conditions by producing more "bring-back" responses in the Exchange than in the Release conditions. Those bonobo and orangutan individuals hence adapted their planning behavior according to changing needs (i.e., they brought tokens back significantly more often when they would need them). Bonobos and orangutans, unlike chimpanzees, planned outside the context of tool-use, thus challenging the idea that planning in these species is purely domain-specific.

Human-animal relationships in zoo-housed orangutans (P. abelii) and gorillas (G. g. gorilla): the effects of familiarity.

I examined human-animal relationships (HARs) in zoo-housed orangutans (Pongo abelii) and gorillas (Gorilla gorilla gorilla) to see if they followed patterns similar to conspecific relationships in great apes and humans. Familiarity and social relationships guide humans' and great apes' behaviors with conspecifics. Inter-individual relationships, based on shared social history, and "generalized" relationships, based on a history of interactions with relevant classes of individuals, guide behavior with familiar and unfamiliar conspecifics, respectively. I examined whether both familiarity and social relationships similarly guides great apes' cross-species interactions with humans. I used repeated measures MANOVA to compare hourly rates and average durations of ape-initiated human-directed behaviors (HDBs) between familiar and unfamiliar humans and between great ape species. HDB patterns were consistent with familiarity-based HAR predictions, indicating more negative relationships with unfamiliar humans and more positive relationships with familiar humans. Findings for unfamiliar humans are consistent with negative effects of humans on apes' behavior reported in traditional visitor effect studies (VES). However, findings for familiar humans may be overlooked in VES due to pooling across levels of human familiarity or failure to consider humans other than primarily unfamiliar visitors. Additionally, species differences in apes' HDBs suggest that data pooling across species, common in many zoo studies, may mask important differences. These findings have important methodological implications for studies of human-animal interaction as well as for captive animal wellbeing.

Orangutans (Pongo abelii) and a gorilla (Gorilla gorilla gorilla) match features in familiar and unfamiliar individuals.

Great apes can perceive images as representative of corresponding real-life objects. Coupled with the potential advantages of identifying specific members of one's species and mounting evidence for individual recognition in other non-humans, it seems likely that great apes would have the ability to identify conspecifics in photographs. The ability of four orangutans and a gorilla to match images of individuals of their own and a closely related but unfamiliar species was examined here for the first time. First, the subjects matched photographs of familiar conspecifics taken at various time points in a delayed matching-to-sample procedure (Experiment 1). Second, they matched different photographs of unfamiliar individuals of a different species (Experiment 2) at above chance levels. These results suggest that the subjects matched photographs by matching physical features, not necessarily by recognizing the identity of the individuals depicted. However, they also quickly learned to select photographs of familiar individuals when these photographs were paired with photographs of unfamiliar individuals of their own species (Experiment 3), and three subjects showed transfer to novel images of familiar and unfamiliar individuals. Thus, the findings support the idea that subjects attended to physical features to identify individuals that they could categorize on the basis of familiarity.

Quantity matching by an orangutan (Pongo abelii).

An adult male orangutan (Pongo abelii) was presented with a series of delayed matching-to-sample (DMTS) tasks in which he was to match images based on (a) the number of individual animals depicted in the photograph (from 1 to 4), (b) the number of abstract shapes presented in the stimulus (from 1 to 4), or (c) the number of dots presented in the stimulus (from 1 to 4, 4-7, or 7-10). The spatial arrangement of the dots and the background color of the stimuli varied, and the size of the dots was manipulated to control for overall ratio of foreground to background. The subject's performance was not affected by these perceptual features, but was affected by the absolute difference and ratio between number of elements in the comparison stimuli. However, the relationship between these variables and his performance was not always linear as predicted by the analog magnitude model. In addition, the subject showed a high degree of transfer to novel numerosities up to ten, indicating that orangutans are capable of estimating quantity for a greater number of items than can presumably be subtilized by humans.

Can orangutans (Pongo abelii) infer tool functionality?

It is debatable whether apes can reason about the unobservable properties of tools. We tested orangutans for this ability with a range of tool tasks that they could solve by using observational cues to infer tool functionality. In experiment 1, subjects successfully chose an unbroken tool over a broken one when each tool's middle section was hidden. This prevented seeing which tool was functional but it could be inferred by noting the tools' visible ends that were either disjointed (broken tool) or aligned (unbroken tool). We investigated whether success in experiment 1 was best explained by inferential reasoning or by having a preference per se for a hidden tool with an aligned configuration. We conducted a similar task to experiment 1 and included a functional bent tool that could be arranged to have the same disjointed configuration as the broken tool. The results suggested that subjects had a preference per se for the aligned tool by choosing it regardless of whether it was paired with the broken tool or the functional bent tool. However, further experiments with the bent tool task suggested this preference was a result of additional demands of having to attend to and remember the properties of the tools from the beginning of the task. In our last experiment, we removed these task demands and found evidence that subjects could infer the functionality of a broken tool and an unbroken tool that both looked identical at the time of choice.

Orangutans (Pongo pygmaeus and Pongo abelii) understand connectivity in the skewered grape tool task.

Great apes appear to have limited knowledge of tool functionality when they are presented with tasks that involve a physical connection between a tool and a reward. For instance, they fail to understand that pulling a rope with a reward tied to its end is more beneficial than pulling a rope that only touches a reward. Apes show more success when both ropes have rewards tied to their ends but one rope is nonfunctional because it is clearly separated into aligned sections. It is unclear, however, whether this success is based on perceptual features unrelated to connectivity, such as perceiving the tool's separate sections as independent tools rather than one discontinuous tool. Surprisingly, there appears to be no study that has tested any type of connectivity problem using natural tools made from branches with which wild and captive apes often have extensive experience. It is possible that such ecologically valid tools may better help subjects understand connectivity that involves physical attachment. In this study, we tested orangutans with natural tools and a range of connectivity problems that involved the physical attachment of a reward on continuous and broken tools. We found that the orangutans understood tool connectivity involving physical attachment that apes from other studies failed when tested with similar tasks using artificial as opposed to natural tools. We found no evidence that the orangutans' success in broken tool conditions was based on perceptual features unrelated to connectivity. Our results suggest that artificial tools may limit apes' knowledge of connectivity involving physical attachment, whereas ecologically valid tools may have the opposite effect.