Maternal and offspring behavior in free-ranging Japanese and moor macaques: A comparative approach.

Female primates represent the most important social partner for their developing offspring. However, mothers may strongly differ in the way they relate to their offspring (e.g., in terms of two different dimensions: protectiveness and rejection). In this study, we aimed to assess how dominance style predicts (i) changes in maternal behavior through offspring development, and (ii) the link between maternal behavior and offspring behavior. We conducted behavioral observations on 34 free-ranging immatures of two species of macaques with different dominance styles: less tolerant Japanese macaques (JM; Macaca fuscata) and more tolerant moor macaques (MM; Macaca maura). Our results showed that maternal behavior differed between JM and MM: maternal proximity and grooming decreased through offspring development more quickly in MM than in JM, whereas maternal rejection and aggression, which were generally more frequent in JM, decreased with offspring age similarly in both species. In contrast, maternal restraint of offspring decreased similarly with offspring age in both species. Furthermore, dominance style was differentially associated with the link between maternal and offspring behavior: in MM only, maternal grooming predicted an increase of the probability that offspring interacted with partners other than their mothers and engaged in solitary play, whereas maternal rejection predicted a decrease in the occurrence of solitary play. Overall, these results suggest interspecific variation in maternal behavior during offspring's first years of life, and point to the possibility that these differences may have an important role in shaping their behavioral development.

Naïve orangutans (Pongo abelii and Pongo pygmaeus) individually acquire nut-cracking using hammer tools.

Nut-cracking with hammer tools (henceforth: nut-cracking) has been argued to be one of the most complex tool-use behaviors observed in nonhuman animals. So far, only chimpanzees, capuchins, and macaques have been observed using tools to crack nuts in the wild (Boesch and Boesch, 1990; Gumert et al., 2009; Mannu and Ottoni, 2009). However, the learning mechanisms behind this behavior, and the extent of nut-cracking in other primate species are still unknown. The aim of this study was two-fold. First, we investigated whether another great ape species would develop nut-cracking when provided with all the tools and appropriate conditions to do so. Second, we examined the mechanisms behind the emergence of nut-cracking by testing a naïve sample. Orangutans (Pongo abelii and Pongo pygmaeus) have the second most extensive tool-use repertoire among the great apes (after chimpanzees) and show flexible problem-solving capacities. Orangutans have not been observed cracking nuts in the wild, however, perhaps because their arboreal habits provide limited opportunities for nut-cracking. Therefore, orangutans are a valid candidate species for the investigation of the development of this behavior. Four nut-cracking-naïve orangutans at Leipzig zoo (P. abelii; Mage = 16; age range = 10-19; 4F; at the time of testing) were provided with nuts and hammers but were not demonstrated the nut-cracking behavioral form. Additionally, we report data from a previously unpublished study by one of the authors (Martina Funk) with eight orangutans housed at Zürich zoo (six P. abelii and two P. pygmaeus; Mage = 14; age range = 2-30; 5F; at the time of testing) that followed a similar testing paradigm. Out of the twelve orangutans tested, at least four individuals, one from Leipzig (P. abelii) and three from Zürich (P. abelii and P. pygmaeus), spontaneously expressed nut-cracking using wooden hammers. These results demonstrate that nut-cracking can emerge in orangutans through individual learning and certain types of non-copying social learning.

Japanese Macaques' (Macaca fuscata) sensitivity to human gaze and visual perspective in contexts of threat, cooperation, and competition.

Gaze sensitivity allows us to interpret the visual perspective of others, inferring their intentions and attentional states. In order to clarify the evolutionary history of this ability, we assessed the response of free-ranging Japanese macaques (Macaca fuscata) to human gaze in three contexts: threat (Experiment 1), cooperation (Experiment 2), and competition (Experiment 3). Subjects interpreted the direct gaze of an approaching human as a sign of threat, showing a greater flight initiation distance and more threats towards the human in this condition than when the human gazed in another direction. Subjects also adapted their behavior to the attentional cues of a human who gave them food, by for example moving into his visual field. However, the macaques did not seem to take the visual perspective of a human competing with them over food, as they failed to first retrieve the food that was not visible to the human (i.e., located behind an opaque barrier). Our results support the idea that Japanese macaques can respond to a human's gaze flexibly depending on the context. Moreover, they highlight the importance of studying animal behavior across different species and contexts to better understand the selective pressures that might have led to its evolution.

Chimpanzees' (Pan troglodytes) internal arousal remains elevated if they cannot themselves help a conspecific.

Chimpanzees help conspecifics achieve their goals in instrumental situations, but neither their immediate motivation nor the evolutionary basis of their motivation is clear. In the current study, we gave chimpanzees the opportunity to instrumentally help a conspecific to obtain food. Following recent studies with human children, we measured their pupil diameter at various points in the process. Like young children, chimpanzees' pupil diameter decreased soon after they had helped. However, unlike children, chimpanzees' pupils remained more dilated upon watching a third party provide the needed help instead of them. Our interpretation is that chimpanzees are motivated to help others, and the evolutionary basis is direct or indirect reciprocity, as providing help oneself sets the conditions for a payback. This is in contrast to young children whose goal is to see others being helped-by whomever-presumably because their helping is not based on reciprocity. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Competitive children, cooperative mothers? Effect of various social factors on the retrospective and prospective use of theory of mind.

Our capacity to attribute mental states to others, or theory of mind (ToM), affects the way in which we manage social interactions. Likewise, the social scenario in which we find ourselves probably influences our use of ToM. In this study, 6-year-old children and adult women participated in pairs in a task where participants needed to infer their partner's behavior considering the partner's visual perception (Experiment 1), knowledge (Experiment 2), and false belief (Experiment 3) regarding the placement of rewards under cups. The results were analyzed according to the temporal direction of the inference (past or future behavior of the partner), the social context (competition or cooperation), and-in the case of women-the type of social relationship with their partner (another adult or their own child). Children solved only the visual perception task, and adults solved the three tasks but performed better in the visual perception task than in the false belief task, suggesting that not only developmental issues but also differences in the intrinsic difficulty of the tasks underlie children's results. The temporal direction of the inference, in contrast, did not influence their results. Whereas children performed better in the competition context, adults performed better in the cooperation context in one experiment. Moreover, women avoided competing against their own child, and even cooperated with her or him when this was against their own interest, suggesting that cooperation between mothers and children might have been a key driving force in the evolution of ToM in our species.

Comparing humans and nonhuman great apes in the broken cloth problem: Is their knowledge causal or perceptual?

When presented with the broken cloth problem, both human children and nonhuman great apes prefer to pull a continuous cloth over a discontinuous cloth in order to obtain a desired object resting on top. This has been interpreted as evidence that they preferentially attend to the functionally relevant cues of the task (e.g., presence or absence of a gap along the cloth). However, there is controversy regarding whether great apes' behavior is underpinned by causal knowledge, involving abstract concepts (e.g., support, connection), or by perceptual knowledge, based on percepts (e.g., contact, continuity). We presented chimpanzees, orangutans, and 2-, 3-, and 4-year-old children with two versions of the broken cloth problem. The Real condition, made with paper strips, could be solved based on either perceptual cues or causal knowledge. The Painted condition, which looked very similar, could be solved only by attending to perceptual cues. All groups mastered the Real condition, in line with previous results. Older children (3- and 4-year-olds) performed significantly better in this condition than all other groups, but the performance of apes and children did not differ sharply, with 2-year-olds and apes obtaining similar results. In contrast, only 4-year-olds solved the Painted condition. We propose causal knowledge to explain the general good performance of apes and humans in the Real condition compared with the Painted condition. In addition, we suggest that symbolic knowledge might account for 4-year-olds' performance in the Painted condition. Our findings add to the growing literature supporting the idea that learning from arbitrary cues is not a good explanation for the performance of apes and humans on some kinds of physical task.

Abstract knowledge in the broken-string problem: evidence from nonhuman primates and pre-schoolers.

There is still large controversy about whether abstract knowledge of physical problems is uniquely human. We presented 9 capuchin monkeys, 6 bonobos, 6 chimpanzees and 48 children with two versions of a broken-string problem. In the standard condition, participants had to choose between an intact and a broken string as means to a reward. In the critical condition, the functional parts of the strings were covered up and replaced by perceptually similar, but non-functional cues. Apes, monkeys and young children performed significantly better in the standard condition in which the cues played a functional role, indicating knowledge of the functional properties involved. Moreover, a control experiment with chimpanzees and young children ruled out that this difference in performance could be accounted for by differences of perceptual feedback in the two conditions. We suggest that, similar to humans, nonhuman primates partly rely on abstract concepts in physical problem-solving.

A reversed-reward contingency task reveals causal knowledge in chimpanzees (Pan troglodytes).

In the reversed-reward contingency task, subjects are required to choose the less preferred of two options in order to obtain the more preferred one. Usually, this task is used to measure inhibitory skills, but it could also be used to measure how strong the subjects' preferences are. We presented chimpanzees with support tasks where only one of two paper strips could physically bring food into reach. Subjects were rewarded for choosing the non-functional strip. In Experiment 1, subjects failed to pick the non-baited strip. In Experiment 2, subjects failed to pick the broken strip. Chimpanzees performed worse in these tasks than in other similar tasks where instead of paper strips, there were similar shapes painted on a platform. The fact that subjects found the reversed-reward contingency task based on causality more difficult to solve than a perceptually similar task with no causality involved (i.e., arbitrary) suggests that they did not treat real strips as an arbitrary task. Instead, they must have had some causal knowledge of the support problem that made them prefer functional over non-functional strips despite the contrary reward regime.

Apes (Gorilla gorilla, Pan paniscus, P. troglodytes, Pongo abelii) versus corvids (Corvus corax, C. corone) in a support task: the effect of pattern and functionality.

Apes (Gorilla gorilla, Pan paniscus, P. troglodytes, Pong abelii) and corvids (Corvus corax, C. corone) are among the most proficient and flexible tool users in the animal kingdom. Although it has been proposed that this is the result of convergent evolution, little is known about whether this is limited to behavior or also includes the underlying cognitive mechanisms. We compared several species of apes (bonobos, chimpanzees, gorillas, and orangutans) and corvids (carrion crows and common ravens) using exactly the same paradigm: a support task with elements from the classical patterned-string tasks. Corvids proved able to solve at least an easy pattern, whereas apes outperformed corvids with respect to the complexity of the patterns solved, the relative number of subjects solving each problem, and the speed to reach criterion. We addressed the question of whether subjects based their choices purely on perceptual cues or on a more abstract understanding of the problem. This was done by using a perceptually very similar but causally different condition where instead of paper strips there were strip shapes painted on a platform. Corvids' performance did not differ between conditions, whereas apes were able to solve the real but not the painted task. This shows that apes were not basing their choices just on spatial or arbitrary perceptual cues. Instead, and unlike corvids, they must have had some causal knowledge of the task.

Great apes track hidden objects after changes in the objects' position and in subject's orientation.

Eight chimpanzees (Pan troglodytes), five bonobos (Pan paniscus), five gorillas (Gorilla gorilla), and seven orangutans (Pongo pygmaeus) were presented with two invisible object displacement tasks. In full view of the subject, a food item was hidden under one of three opaque cups resting on a platform and, after an experimental manipulation, the subject was allowed to select one of the cups. In the rotation task, the platform was rotated 180 degrees while the subject remained stationary. In the translocation task, the platform remained stationary while the subject walked to the opposite side from where she saw the reward being hidden. The final position of the food relative to the subject was equivalent in both tasks. Single displacement trials consisted of only one manipulation, either a rotation or a translocation, whereas double displacement trials consisted of both a rotation and a translocation. We also included no displacement trials in which no displacements took place. No displacement trials were easier than single displacements which, in turn, were easier than double displacements. Unlike earlier studies with children, there was no difference in performance between rotation and translocation displacements. Overall, apes performed above chance in all conditions, but chimpanzees outperformed the other species. This study reinforces the notion that the great apes use an allocentric spatial coding.

Mangabeys (Cercocebus torquatus lunulatus) solve the reverse contingency task without a modified procedure.

Problem solving often relies on generating new responses while inhibiting others, particularly prepotent ones. A paradigm to study inhibitory abilities is the reverse contingency task (Boysen and Berntson in J Exp Psychol Anim Behav Process 21:82-86, 1995), in which two different quantities of food are offered to an individual who receives the array he did not choose. Therefore, mastery of the task demands selecting the smaller quantity to obtain the larger one. Several non-human primates have been tested in the reverse contingency task. To date, only great apes and rhesus monkeys (Macaca mulatta) have succeeded in the original task, with no need of procedural modifications as the large-or-none contingency, correction trials or symbolic stimuli substituting for actual food quantities. Here, four mangabeys were presented with two stimulus arrays of one and four raisins in the context of the reverse contingency task. Three of them learned to perform the task well above chance without a modified procedure. They also reached above-chance performance when presented with two stimulus arrays of zero and four raisins, despite the initial difficulty of choosing a null quantity. After a period of 7-10 months, in which the animals were not tested on any task, all three subjects continued to perform well, even when presented with novel quantity pairs.