Comparative and familial analysis of handedness in great apes

Historically, population-level handedness has been considered a hallmark of human evolution. Whether nonhuman primates exhibit population-level handedness remains a topic of considerable debate. This paper summarizes published data on handedness in great apes. Comparative analysis indicated that chimpanzees and bonobos show population-level right handedness, whereas gorillas and orangutans do not. All ape species showed evidence of population-level handedness when considering specific tasks. Familial analyses in chimpanzees indicated that offspring and maternal (but not paternal) handedness was significantly positively correlated, but this finding was contingent upon the classification criteria used to evaluate hand preference. Overall, the proportion of right handedness is lower in great apes compared with humans, and various methodological and theoretical explanations for this discrepancy are discussed.     

Effects of experience on preference between forced and free choice

Preference between forced choice and free choice in concurrent-chain schedules of reinforcement was investigated in pigeons after exposure to particular combinations of terminal links. In Experiment 1, in which terminal links always ended with reinforcers, one of three pairs of terminal links was arranged as preexposure: (a) both terminal links had only one key (forced choice), (b) both terminal links had two keys (free choice), or (c) a combination of forced and free choice was arranged across sessions. In test sessions following the preexposure, pigeons' preferences rapidly shifted to the terminal links with which they had no recent experience. In Experiment 2, the same procedure was repeated except that each terminal link ended intermittently with reinforcers with a probability of .5 and there was no terminal-link arrangement with a combination of free and forced choice. Pigeons showed the same preference changes as in Experiment 1, but the preference changes did not appear immediately at the beginning of test sessions. These data suggest that recent previous experience was a more important determinant of preference than the difference between forced-choice and free-choice terminal links.     

Behavioral cues that great apes use to forage for hidden food

We conducted three studies to examine whether the four great ape species (chimpanzees, bonobos, gorillas, and orangutans) are able to use behavioral experimenter-given cues in an object-choice task. In the subsequent experimental conditions subjects were presented with two eggs, one of which contained food and the other did not. In Study 1 the experimenter examined both eggs by smelling or shaking them, but only made a failed attempt to open (via biting) the egg containing food. In a control condition, the experimenter examined and attempted to open both eggs, but in reverse order to control for stimulus enhancement. The apes significantly preferred the egg that was first examined and then bitten, but had no preference in a baseline condition in which there were no cues. In Study 2, we investigated whether the apes could extend this ability to cues not observed in apes so far (i.e., attempting to pull apart the egg), as well as whether they made this discrimination based on the function of the action the experimenter performed. Subjects significantly preferred eggs presented with this novel cue, but did not prefer eggs presented with a novel but functionally irrelevant action. In Study 3, apes did not interpret human actions as cues to food-location when they already knew that the eggs were empty. Thus, great apes were able to use a variety of experimenter-given cues associated with foraging actions to locate hidden food and thereby were partially sensitive to the general purpose underlying these actions.     

Reaching around barriers: the performance of the great apes and 3–5-year-old children

Inhibitory control has been suggested as a key predictive measure of problem-solving skills in human and nonhuman animals. However, there has yet to be a direct comparison of the inhibitory skills of the nonhuman apes and their development in human children. We compared the inhibitory skills of all great ape species, including 3–5-year-old children in a detour-reaching task, which required subjects to avoid reaching directly for food and instead use an indirect reaching method to successfully obtain the food. We tested 22 chimpanzees, 18 bonobos, 18 orangutans, 6 gorillas and 42 children. Our sample included chimpanzees, bonobos and orangutans housed in zoos (N = 27) and others housed in sanctuaries in their native habitats (N = 37). Overall, orangutans were the most skilful apes, including human children. As expected older children outperformed younger children. Sanctuary chimpanzees and bonobos outperformed their zoo counterparts whereas there was no difference between the two orangutan samples. Most zoo chimpanzees and bonobos failed to solve the original task, but improved their performance with additional training, although the training method determined to a considerable extent the level of success that the apes achieved in a transfer phase. In general, the performance of the older children was far from perfect and comparable to some of the nonhuman apes tested.     

Chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) quantify split solid objects

Recent research suggests that gorillas’ and orangutans’ object representations survive cohesion violations (e.g., a split of a solid object into two halves), but that their processing of quantities may be affected by them. We assessed chimpanzees’ (Pan troglodytes) and bonobos’ (Pan paniscus) reactions to various fission events in the same series of action tasks modelled after infant studies previously run on gorillas and orangutans (Cacchione and Call in Cognition 116:193–203, 2010b). Results showed that all four non-human great ape species managed to quantify split objects but that their performance varied as a function of the non-cohesiveness produced in the splitting event. Spatial ambiguity and shape invariance had the greatest impact on apes’ ability to represent and quantify objects. Further, we observed species differences with gorillas performing lower than other species. Finally, we detected a substantial age effect, with ape infants below 6 years of age being outperformed by both juvenile/adolescent and adult apes.     

What does an intermediate success rate mean? An analysis of a Piagetian liquid conservation task in the great apes

The study investigates what an intermediate success rate means in bonobos, chimpanzees, and orangutans. Apes participated in liquid conservation experiments where they had to track the larger of two different quantities of juice after various kinds of transformations [Suda, C., & Call, J. (2004). Piagetian liquid conservation in the great apes (Pan paniscus, Pan troglodytes, and Pongo pygmaeus). Journal of Comparative Psychology, 118, 265-279). When making a decision, apes sometimes demonstrated hesitant behavior, concurrently pointing to both alternatives or successively changing their choice. Moderately successful apes showed more hesitation than highly successful or unsuccessful apes. The results are consistent with the cognitive conflict model: The experiments created a higher degree of cognitive conflict on moderately successful apes than on very successful or unsuccessful apes. This indicates that an intermediate performance reflects the joint operation and potential conflict between two different cognitive strategies (identity and appearance) inherent to the Piagetian conservation task.     

Great apes’ strategies to map spatial relations

We investigated reasoning about spatial relational similarity in three great ape species: chimpanzees, bonobos, and orangutans. Apes were presented with three spatial mapping tasks in which they were required to find a reward in an array of three cups, after observing a reward being hidden in a different array of three cups. To obtain a food reward, apes needed to choose the cup that was in the same relative position (i.e., on the left) as the baited cup in the other array. The three tasks differed in the constellation of the two arrays. In Experiment 1, the arrays were placed next to each other, forming a line. In Experiment 2, the positioning of the two arrays varied each trial, being placed either one behind the other in two rows, or next to each other, forming a line. Finally, in Experiment 3, the two arrays were always positioned one behind the other in two rows, but misaligned. Results suggested that apes compared the two arrays and recognized that they were similar in some way. However, we believe that instead of mapping the left–left, middle–middle, and right–right cups from each array, they mapped the cups that shared the most similar relations to nearby landmarks (table’s visual boundaries).     

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 spp.) may prefer tools with rigid properties to flimsy tools

Preference for tools with either rigid or flexible properties was explored in orangutans (Pongo spp.) through an extension of D. J. Povinelli, J. E. Reaux, and L. A. Theall's (2000) flimsy-tool problem. Three captive orangutans were presented with three unfamiliar pairs of tools to solve a novel problem. Although each orangutan has spontaneously used tools in the past, the tools presented in this study were novel to the apes. Each pair of tools contained one tool with rigid properties (functional) and one tool with flimsy properties (nonfunctional). Solving the problem required selection of a rigid tool to retrieve a food reward. The functional tool was selected in nearly all trials. Moreover, two of the orangutans demonstrated this within the first test trials with each of the three tool types. Although further research is required to test this statistically, it suggests either a preexisting preference for rigid tools or comprehension of the relevant features required in a tool to solve the task. The results of this study demonstrate that orangutans can recognize, or learn to recognize, relevant tool properties and can choose an appropriate tool to solve a problem.     

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.     

Pigeons' preference for free choice: number of keys versus key area.

In concurrent-chains schedules, pigeons prefer terminal links that provide two keys correlated with reinforcers (free choice) over those that provide only one key (forced choice), terminal-link reinforcement rates being equal. With same-size keys, free choice provides a larger area available for pecking. Preferences were examined using terminal links that differed in key number only (one or two) or key size only (small and medium or medium and large), or that equated the area of the two free-choice keys with that of the forced-choice key. Medium (standard) keys were typically preferred to small keys, but indifference was typically obtained between medium and large keys. The size preference usually overrode free-choice preference with one medium key pitted against two small keys, but free-choice preference was reliably observed with one large key pitted against two medium keys. In other words, preferences were a joint function of key number and key area, implying that free-choice preference is not reducible to preference for larger key areas. Free-choice preference requires separate keys rather than larger areas; the relevant behavioral units are the discriminated operants correlated with each terminal-link key rather than classes defined by topographical features such as area or perimeter.     

Spontaneous use of tools as straws in great apes

Great apes can use multiple tools to extract food embedded in substrates and can invent new ways to exploit those resources. We tested five bonobos, five chimpanzees, and six orangutans in a task in which they had to use (and modify) a tool as a straw to drink the juice located inside a container. Experiment 1 showed that four orangutans and one chimpanzee invented the use of a piece of electric cable to get the juice. Experiment 2 investigated whether subjects could transform a non-functional hose into a functional one by removing blockages that impeded the free flow of juice. Orangutans outperformed chimpanzees and bonobos by differentially removing those blockages that prevented the flow of juice, often doing so before attempting to extract the juice. In Experiment 3, we presented chimpanzees and orangutans with four 3-tool sets (each tool set contained a single straw-like tool) and allowed them to select one tool. Unlike chimpanzees, orangutans succeeded in selecting the straw-like tool above chance levels without having to physically manipulate it. We suggest that orangutans’ superior performance is related to their greater reliance on mouth actions during foraging. Experiment 4 investigated whether orangutans were also capable of selecting the suitable tool not by its appearance, but by the effects that it produced. After witnessing the experimenter blow bubbles or absorb liquid with a functional tool but fail to accomplish the same thing with the non-functional tool, orangutans failed to select the functional tool above chance levels.     

Rhesus macaques (Macaca mulatta) as living fossils of hominoid personality and subjective well-being

Personality dimensions capturing individual differences in behavior, cognition, and affect have been described in several species, including humans, chimpanzees, and orangutans. However, comparisons between species are limited by the use of different questionnaires. We asked raters to assess free-ranging rhesus macaques at two time points on personality and subjective well-being questionnaires used earlier to rate chimpanzees and orangutans. Principal-components analysis yielded domains we labeled Confidence, Friendliness, Dominance, Anxiety, Openness, and Activity. The presence of Openness in rhesus macaques suggests it is an ancestral characteristic. The absence of Conscientiousness suggests it is a derived characteristic in African apes. Higher Confidence and Friendliness, and lower Anxiety were prospectively related to subjective well-being, indicating that the connection between personality and subjective well-being in humans, chimpanzees, and orangutans is ancestral in catarrhine primates. As demonstrated here, each additional species studied adds another fold to the rich, historical story of primate personality evolution.     

Freedom and knowledge: an experimental analysis of preference in pigeons

Relative responding in initial links of concurrent-chain schedules showed that pigeons preferred free to forced choices and informative to uninformative stimuli. Variable-interval initial links on two lower keys (white) of a six-key chamber produced terminal links on either two upper-left keys (blue and/or amber) or two upper-right keys (green and/or red). Terminal.links in which pecks on either of two lit keys produced fixed-interval reinforcement (free choice) were preferred to links with only one lit fixed-interval key available (forced choice). Terminal links with different key colors correlated with concurrent fixed-interval reinforcement and extinction (informative stimuli) were preferred to links with these schedules operating on same-color keys (uninformative stimuli). Scheduling extinction for one of the two free-choice keys assessed preference for two lit keys over one lit key, but confounded number with whether stimuli were informative. Fixed-interval reinforcement for both keys in each terminal link, but with different-color keys in one link and same-color keys in the other, showed that preference for informative stimuli did not depend on stimulus variety. Preferences were independent of relative responses per reinforcement and other properties of terminal-link performance.     

Apes' use of iconic cues in the object-choice task

In previous studies great apes have shown little ability to locate hidden food using a physical marker placed by a human directly on the target location. In this study, we hypothesized that the perceptual similarity between an iconic cue and the hidden reward (baited container) would help apes to infer the location of the food. In the first two experiments, we found that if an iconic cue is given in addition to a spatial/indexical cue - e.g., picture or replica of a banana placed on the target location - apes (chimpanzees, bonobos, orangutans, gorillas) as a group performed above chance. However, we also found in two further experiments that when iconic cues were given on their own without spatial/indexical information (iconic cue held up by human with no diagnostic spatial/indexical information), the apes were back to chance performance. Our overall conclusion is that although iconic information helps apes in the process of searching hidden food, the poor performance found in the last two experiments is due to apes' lack of understanding of the informative (cooperative) communicative intention of the experimenter.     

The ecological rationality of delay tolerance: insights from capuchin monkeys

Both human and non-human animals often face decisions between options available at different times, and the capacity of delaying gratification has usually been considered one of the features distinguishing humans from other animals. However, this characteristic can widely vary across individuals, species, and types of task and it is still unclear whether it is accounted for by phylogenetic relatedness, feeding ecology, social structure, or metabolic rate. To disentangle these hypotheses, we evaluated temporal preferences in capuchin monkeys, South-American primates that, despite splitting off from human lineage approximately 35 million years ago, show striking behavioural analogies with the great apes. Then, we compared capuchins’ performance with that of the other primate species tested so far with the same procedure. Overall, capuchins showed a delay tolerance significantly higher than closely related species, such as marmosets and tamarins, and comparable to that shown by great apes. Capuchins’ tool use abilities might explain their comparatively high preference for delayed options in inter-temporal choices. Moreover, as in humans, capuchin females showed a greater delay tolerance than males, possibly because of their less opportunistic foraging style. Thus, our results shed light on the evolutionary origins of self-control supporting explanations of delay tolerance in terms of feeding ecology.     

Focus on the essential: all great apes know when others are being attentive

When begging for food, all great ape species are sensitive to a human’s attention. However, studies investigating which cues are relevant for chimpanzees to assess the attentional state of others have produced highly inconsistent results. Some have suggested chimpanzees differentiate attention based on the status of the face or even the eyes, while others have indicated that body posture alone is the relevant cue. Kaminski et al. (Anim Cogn 7:216–223, 2004) compared the behaviour of chimpanzees, bonobos and orangutans while begging for food from a human experimenter who systematically varied his face and body orientation. Their results indicated that both factors, face and body orientation, affect apes’ begging behaviour. The authors claimed that while body orientation provides information about the experimenter’s general disposition to offer food, the visibility of the face provides information about the human’s attentional state. In the current study, we tested this hypothesis with all four great apes species. However, unlike Kaminski et al. (Anim Cogn 7:216–223, 2004), the experimenter was able to hand over food regardless of body orientation. The results show that as soon as the offering of the food was no longer restricted, the orientation of the face became the key factor. Therefore, we present the first evidence that all great ape species are able to assess the attentional state of a recipient based on the orientation of the face.     

Great apes’ capacities to recognize relational similarity

Recognizing relational similarity relies on the ability to understand that defining object properties might not lie in the objects individually, but in the relations of the properties of various object to each other. This aptitude is highly relevant for many important human skills such as language, reasoning, categorization and understanding analogy and metaphor. In the current study, we investigated the ability to recognize relational similarities by testing five species of great apes, including human children in a spatial task. We found that all species performed better if related elements are connected by logico-causal as opposed to non-causal relations. Further, we find that only children above 4 years of age, bonobos and chimpanzees, unlike younger children, gorillas and orangutans display some mastery of reasoning by non-causal relational similarity. We conclude that recognizing relational similarity is not in its entirety unique to the human species. The lack of a capability for language does not prohibit recognition of simple relational similarities. The data are discussed in the light of the phylogenetic tree of relatedness of the great apes.     

Task constraints mask great apes' ability to solve the trap-table task

Researchers have investigated animals' causal knowledge with a task requiring subjects to use a tool to bring a reward within reach whilst avoiding a trap. Previous studies have suggested limitations in the ability of several species to avoid traps in tubes or tables. However, certain features may have inflated task difficulty. We tested 20 chimpanzees (Pan troglodytes), 7 orangutans (Pongo pygmaeus), 5 bonobos (Pan paniscus), and 5 gorillas (Gorilla gorilla) in the trap-table--a task in which subjects have to pull one of two rakes prepositioned behind two rewards on a flat surface. One of the rewards is in front of a trap into which it will fall. We investigated the effect of trap type, tool type, the number of available tools, and reinforcement regime on performance. We replicated previous findings showing that apes failed to choose the correct rake above chance. However, when they could instead choose where to insert a single tool, around 80% of the apes solved the trap-table task in the first trial, revealing an important effect of task constraints on their performance.