Transport of tools to food sites in tufted capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Tool use and transport represent cognitively important aspects of early hominid evolution, and nonhuman primates are often used as models to examine the cognitive, ecological, morphological and social correlates of these behaviors in order to gain insights into the behavior of our early human ancestors. In 2001, Jalles-Filho et al. found that free-ranging capuchin monkeys failed to transport tools (stones) to food sites (nuts), but transported the foods to the tool sites. This result cast doubt on the usefulness of Cebus to model early human tool-using behavior. In this study, we examined the performance of six captive tufted capuchin monkeys (Cebus apella) in a tool transport task. Subjects were provided with the opportunity to transport two different tools to fixed food reward sites when the food reward was visible from the tool site and when the food reward was not visible from the tool site. We found that the subjects quickly and readily transported probing tools to an apparatus baited with syrup, but rarely transported stones to a nut-cracking apparatus. We suggest that the performance of the capuchins here reflects an efficient foraging strategy, in terms of energy return, among wild Cebus monkeys.     

Food and token quantity discrimination in capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Quantity discrimination is adaptive in a variety of ecological contexts and different taxa discriminate stimuli differing in numerousness, both in the wild and in laboratory settings. Quantity discrimination between object arrays has been suggested to be more demanding than between food arrays but, to our knowledge, the same paradigm has never been used to directly compare them. We investigated to what extent capuchin monkeys’ relative numerousness judgments (RNJs) with food and token are alike. Tokens are inherently non-valuable objects that acquire an associative value upon exchange with the experimenter. Our aims were (1) to assess capuchins’ RNJs with food (Experiment 1) and with tokens (Experiment 2) by presenting all the possible pair-wise choices between one to five items, and (2) to evaluate on which of the two proposed non-verbal mechanisms underlying quantity discrimination (analogue magnitude and object file system) capuchins relied upon. In both conditions capuchins reliably selected the larger amount of items, although their performance was higher with food than with tokens. The influence of the ratio between arrays on performance indicates that capuchins relied on the same system for numerical representation, namely analogue magnitude, regardless of the type of stimuli (food or tokens) and across both the small and large number ranges.     

Joystick acquisition in tufted capuchins (<Emphasis Type="Italic">Cebus apella</Emphasis>)

A number of nonhuman primate species have demonstrated the ability to use a joystick to control a cursor on a computer screen, yet the acquisition of this skill has not been the focus of systematic inquiry. Here, we examined joystick acquisition in four tufted capuchins under two directional relationships of joystick movement and resultant cursor displacement, isomorphic and inverted. To document the natural history of the acquisition of this skill, we recorded the development of visual tracking of the cursor and body tilting. Rates of acquisition were comparable between the two conditions. After mastering the task in one condition, subjects remastered the task at an accelerated rate in the opposing condition. All subjects significantly increased or maintained high proportions of cursor tracking throughout acquisition. All subjects demonstrated a postural tilt while moving the cursor from the mid-phase of acquisition through task mastery. In the isomorphic condition, all subjects tilted significantly more often in the direction of goal location than in the opposite direction. In three of the four series of tilting that were scored for subjects in the inverted condition, tilting occurred significantly more often toward the direction of goal location than the direction of required hand movement. Together these findings suggest that body tilting participates in the organization of directional movement of the cursor rather than reflecting merely the motoric requirements of the task (to manipulate a joystick).     

Tufted capuchins (<Emphasis Type="Italic">Cebus apella</Emphasis>) attribute value to foods and tools during voluntary exchanges with humans

This research examined exchange and value attribution in tufted capuchin monkeys (Cebus apella). We presented subjects with opportunities to obtain various foods and a tool from an experimenter in exchange for the foods or tool in the subjects' possession. The times elapsed before the first chow biscuits were expelled and/or an exchange took place were recorded as the dependent measures. Laboratory chow biscuits, grapes, apples, and a metal bolt (a tool used to probe for syrup) were used as experimental stimuli. The subjects demonstrated the ability to recognize that exchanges could occur when an experimenter was present with a desirable food. Results indicate that subjects exhibited significant variation in their willingness to barter based upon the types of foods that were both in their possession and presented by the experimenter. Subjects more readily traded chow biscuits for fruit, and more readily traded apples for grapes than grapes for apples. During the exchange of tools and food, the subjects preferred the following in descending order when the probing apparatus was baited with sweet syrup: grapes, metal bolts, and chow biscuits. However when the apparatus was not baited, the values changed to the following in descending order: grapes, chow, and metal bolts. These results indicate that tufted capuchins recognize opportunities to exchange and engage in a simple barter system whereby low-valued foods are readily traded for more highly valued food. Furthermore, these capuchins demonstrate that their value for a tool changes depending upon its utility.     

Tool-use and instrumental learning in the Eurasian jay (<Emphasis Type="Italic">Garrulus glandarius</Emphasis>)

Recent research with Rooks has demonstrated impressive tool-using abilities in captivity despite this species’ classification as a non-tool-user in the wild. Here, we explored whether another non-tool-using corvid, the Eurasian Jay, would be capable of similar feats and investigated the relative contributions of causal knowledge and instrumental conditioning to the birds’ performance on the tasks. Five jays were tested on a variety of tasks involving water displacement. Two birds reliably interacted with the apparatuses. In these tasks, both birds showed a preference for inserting stones into a tube containing liquid over a tube containing a solid or a baited ‘empty’ tube and also for inserting sinkable items over non-sinkable items into a tube of water. To investigate the contribution of instrumental conditioning, subjects were then tested on a series of tasks in which different cues were made available. It was found that, in the absence of any apparent causal cues, these birds showed a clear preference for the rewarded tube when the food incrementally approached with every stone insertion, but not when it simply “appeared” after the correct number of stone insertions. However, it was found that subjects did not prefer to insert stones into a tube rewarded by the incremental approach of food if the available causal cues violated the expectations created by existing causal knowledge (i.e. were counter-intuitive). An analysis of the proportion of correct and incorrect stone insertions made in each trial across tasks offering different types of information revealed that subjects were substantially more successful in experiments in which causal cues were available, but that rate of learning was comparable in all experiments. We suggest that these results indicate that Eurasian jays use the incremental approach of the food reward as a conditioned reinforcer allowing them to solve tasks involving raising the water level and that this learning is facilitated by the presence of causal cues.     

Motivation and memory in zebra finch (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis>) foraging behavior

Remembering combinations of information such as what resources have been seen in which locations could play an important role in enhancing individual survival through increased foraging success. To date, there have been relatively few investigations of avian memory involving more than one category of information. This study explored zebra finches’ (Taeniopygia guttata) capacity to recall two categories in combination, namely food-type and spatial location. Birds were trained to remove variously weighted flaps to find two types of food hidden beneath. Memory for food-types and locations was assessed by pre-feeding the birds to satiety on and devaluing one food-type, and then testing the birds’ efficiency at finding the non-devalued food. When allowed one trial to learn locations of two food rewards that were hidden beneath lightly weighted flaps, birds performed better than chance at locating a food reward. However, they did not preferentially search for the non pre-fed food, suggesting that they were unable to recall both food type and location in combination. Zebra finches made fewer errors when tested on the one-trial task using more heavily weighted flaps than with lightly weighted flaps; there was equivocal evidence that they remembered which food type was hidden where on this task. When given repeated exposures to the locations of the two food rewards, finches located a food reward more accurately than on the one-trial tasks, and were also more likely to recall the locations of the different food types. In this foraging paradigm, experience and motivation may have influenced the birds’ performance.     

Tufted capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>) show understanding of human attentional states when requesting food held by a human

Researchers have investigated to what extent non-human primates understand others’ attentional states, as this ability is considered an important prerequisite for theory of mind. However, previous studies using food requesting tasks have failed to show that non-human primates attribute perception to others as a function of their attentional states. One possible reason is that food requesting tasks may require subjects not only to take into account an experimenter’s attentional state but also to direct it toward the food. The present study tested tufted capuchin monkeys’ (Cebus apella) understanding of others’ attentional states in a food requesting task. In the first situation, monkeys were required only to attract an experimenter’s attention. In the second situation, the monkeys were required to both attract the experimenter’s attention and direct it toward food on a table. The results revealed that capuchin monkeys showed evidence of understanding the experimenter’s attentional variations only in the former condition. This suggests that previous tasks, requiring referential gestures, lacking in most non-human primates, failed to reveal sensitivity to human attentional states because the subjects might not have understood the requesting situation. In conclusion, capuchin monkeys can understand variations in others’ attentional states, although this ability appears limited compared to what is seen in humans.     

Orientation in the cuttlefish <Emphasis Type="Italic">Sepia officinalis</Emphasis>: response <Emphasis Type="Italic">versus</Emphasis> place learning

Several studies have demonstrated that mammals, birds and fish use comparable spatial learning strategies. Unfortunately, except in insects, few studies have investigated spatial learning mechanisms in invertebrates. Our study aimed to identify the strategies used by cuttlefish (Sepia officinalis) to solve a spatial task commonly used with vertebrates. A new spatial learning procedure using a T-maze was designed. In this maze, the cuttlefish learned how to enter a dark and sandy compartment. A preliminary test confirmed that individual cuttlefish showed an untrained side-turning preference (preference for turning right or left) in the T-maze. This preference could be reliably detected in a single probe trial. In the following two experiments, each individual was trained to enter the compartment opposite to its side-turning preference. In Experiment 1, distal visual cues were provided around the maze. In Experiment 2, the T-maze was surrounded by curtains and two proximal visual cues were provided above the apparatus. In both experiments, after acquisition, strategies used by cuttlefish to orient in the T-maze were tested by creating a conflict between the formerly rewarded algorithmic behaviour (turn, response learning) and the visual cues identifying the goal (place learning). Most cuttlefish relied on response learning in Experiment 1; the two strategies were used equally often in Experiment 2. In these experiments, the salience of cues provided during the experiment determined whether cuttlefish used response or place learning to solve this spatial task. Our study demonstrates for the first time the presence of multiple spatial strategies in cuttlefish that appear to closely parallel those described in vertebrates.     

Observational learning from tool using models by human-reared and mother-reared capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Studies of wild capuchins suggest an important role for social learning, but experiments with captive subjects have generally not supported this. Here we report social learning in two quite different populations of capuchin monkeys (Cebus apella). In experiment 1, human-raised monkeys observed a familiar human model open a foraging box using a tool in one of two alternative ways: levering versus poking. In experiment 2, mother-raised monkeys viewed similar techniques demonstrated by monkey models. A control group in each population saw no model. In both experiments, independent coders detected which technique experimental subjects had seen, thus confirming social learning. Further analyses examined fidelity of copying at three levels of resolution. The human-raised monkeys exhibited fidelity at the highest level, the specific tool use technique witnessed. The lever technique was seen only in monkeys exposed to a levering model, by contrast with controls and those witnessing poke. Mother-reared monkeys instead typically ignored the tool and exhibited fidelity at a lower level, tending only to re-create whichever result the model had achieved by either levering or poking. Nevertheless this level of social learning was associated with significantly greater levels of success in monkeys witnessing a model than in controls, an effect absent in the human-reared population. Results in both populations are consistent with a process of canalization of the repertoire in the direction of the approach witnessed, producing a narrower, socially shaped behavioural profile than among controls who saw no model. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Capuchins (<Emphasis Type="Italic">Cebus apella</Emphasis>) fail to show an asymmetric dominance effect

The asymmetric dominance effect (ADE) occurs when the introduction of a partially dominated decoy option increases the choice share of its dominating alternative. The ADE is a violation of regularity and the constant-ratio rule, which are two derivations of the independence of irrelevant alternatives axiom, a core tenant of rational choice. The ADE is one of the most widely reported human choice phenomena, leading researchers to probe its origins by studying a variety of non-human species. We examined the ADE in brown capuchin monkeys (Cebus apella), a species that displays many other decision biases. In Experiment 1, we used a touchscreen method to elicit choice-based preferences for food rewards in asymmetrically dominated choice sets. In Experiments 2 and 3, we distinguished between different types of judgments and used a free selection task to elicit consumption-based preferences for juice rewards. However, we found no evidence for the ADE through violations of regularity or the constant-ratio rule, despite the similarity of our stimuli to other human and non-human experiments. While these results appear to conflict with existing literature on the ADE in non-human species, we point out methodological differences—notably, the distinction between value-based and perception-based stimuli—that have led to a collection of phenomena that are difficult to understand under a unitary theoretical framework. In particular, we highlight key differences between the human and non-human research and provide a series of steps that researchers could take to better understand the ADE.     

Effect of target animacy on hand preference in Sichuan snub-nosed monkeys (<Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis>)

Twenty-eight captive Sichuan snub-nosed monkeys (Rhinopithecus roxellana) were involved in the current study. Many individuals showed handedness, with a modest tendency toward left-hand use especially for animate targets, although no group-level handedness was found. There was no significant gender difference in the direction and strength of hand preference for both targets. Females showed a significantly higher overall rate of actions toward animate targets than inanimate targets for both hands, whereas males displayed almost the reversed pattern. There were no significant interactions between lateral hand use and target animacy for either males or females. Most individuals showed rightward or leftward laterality shift trends between inanimate and animate targets. These findings to some extent support the existence of a potential trend concerning a categorical neural distinction between targets demanding functional manipulation (inanimate objects) and those demanding social manipulation (animate objects), even though specialized hand preference based on target animacy has not been fully established in this arboreal Old World monkey species.     

Non-tool-using rooks, <Emphasis Type="Italic">Corvus frugilegus</Emphasis>, solve the trap-tube problem

The trap-tube problem is used to assess whether an individual is able to foresee the outcome of its actions. To solve the task, an animal must use a tool to push a piece of food out of a tube, which has a trap along its length. An animal may learn to avoid the trap through a rule based on associative processes, e.g. using the distance of trap or food as a cue, or by understanding relations between cause and effect. This task has been used to test physical cognition in a number of tool-using species, but never a non-tool-user. We developed an experimental design that enabled us to test non-tool-using rooks, Corvus frugilegus. Our modification of the task removed the cognitive requirements of active tool use but still allowed us to test whether rooks can solve the trap-tube problem, and if so how. Additionally, we developed two new control tasks to determine whether rooks were able to transfer knowledge to similar, but novel problems, thus revealing more about the mechanisms involved in solving the task. We found that three out of seven rooks solved the modified trap-tube problem task, showing that the ability to solve the trap-tube problem is not restricted to tool-using animals. We found no evidence that the birds solved the task using an understanding of its causal properties, given that none of the birds passed the novel transfer tasks.     

Task preparation in macaque monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>)

We investigated whether macaque monkeys possess the ability to prepare abstract tasks in advance. We trained two monkeys to use different stimulus-response (S-R) mappings. On each trial, monkeys were first informed with a visual cue which of two S-R mapping to use. Following a delay, a visual target was presented to which they would respond with a left or right button-press. We manipulated delay time between cue and target and found that performance was faster and more accurate with longer delays, suggesting that monkeys used the delay time to prepare each task in advance. Electronic Publication     

Comprehension of human pointing gestures in young human-reared wolves (<Emphasis Type="Italic">Canis lupus</Emphasis>) and dogs (<Emphasis Type="Italic">Canis familiaris</Emphasis>)

Dogs have a remarkable skill to use human-given cues in object-choice tasks, but little is known to what extent their closest wild-living relative, the wolf can achieve this performance. In Study 1, we compared wolf and dog pups hand-reared individually and pet dogs of the same age in their readiness to form eye-contact with a human experimenter in an object-choice task and to follow her pointing gesture. The results showed that dogs already at 4 months of age use momentary distal pointing to find hidden food even without intensive early socialization. Wolf pups, on the contrary, do not attend to this subtle pointing. Accordingly in Studies 2 and 3, these wolves were tested longitudinally with this and four other (easier) human-given cues. This revealed that wolves socialized at a comparable level to dogs are able to use simple human-given cues spontaneously if the human’s hand is close to the baited container (e.g. touching, proximal pointing). Study 4 showed that wolves can follow also momentary distal pointing similarly to dogs if they have received extensive formal training. Comparing the wolves to naïve pet dogs of the same age revealed that during several months of formal training wolves can reach the level of dogs in their success of following momentary distal pointing in parallel with improving their readiness to form eye-contact with a human experimenter. We assume that the high variability in the wolves’ communicative behaviour might have provided a basis for selection during the course of domestication of the dog.     

Western scrub-jays (<Emphasis Type="Italic">Aphelocoma californica</Emphasis>) solve multiple-string problems by the spatial relation of string and reward

String-pulling is a widely used paradigm in animal cognition research to assess what animals understand about the functionality of strings as a means to obtain an out-of-reach reward. This study aimed to systematically investigate what rules Western scrub-jays (Aphelocoma californica) use to solve different patterned string tasks, i.e. tasks in which subjects have to choose between two or more strings of which only one is connected to the reward, or where one is more efficient. Arranging strings in a parallel configuration showed that the jays were generally capable of solving multiple-string tasks and acted in a goal-directed manner. The slanted and crossed configurations revealed a reliance on a “proximity rule”, that is, a tendency to choose the string-end closest to the reward. When confronted with strings of different lengths attached to rewards at different distances the birds chose according to the reward distance, preferring the reward closest to them, and were sensitive to the movement of the reward, but did not consistently prefer the shorter and therefore more efficient string. Generally, the scrub-jays were successful in tasks where the reward was closest to the string-ends they needed to pull or when string length and reward distance correlated, but the birds had problems when the wrong string-end was closest to the reward or when the food items were in close proximity to each other. These results show that scrub-jays had a partial understanding of the physical principles underlying string-pulling but relied on simpler strategies such as the proximity rule to solve the tasks.     

Global bias reliability in dogs (<Emphasis Type="Italic">Canis familiaris</Emphasis>)

Dogs enrolled in a previous study were assessed two years later for reliability of their local/global preference in a discrimination test with the same hierarchical stimuli used in the previous study (Experiment 1) and with a novel stimulus (Experiment 2). In Experiment 1, dogs easily re-learned to discriminate the positive stimulus; their individual global/local choices were stable compared to the previous study; and an overall clear global bias was found. In Experiment 2, dogs were slower in acquiring the initial discrimination task; the overall global bias disappeared; and, individually, dogs tended to make inverse choices compared to the original study. Spontaneous attention toward the test stimulus resembling the global features of the probe stimulus was the main factor affecting the likeliness of a global choice of our dogs, regardless of the type of experiment. However, attention to task-irrelevant elements increased at the expense of attention to the stimuli in the test phase of Experiment 2. Overall, the results suggest that the stability of global bias in dogs depends on the characteristics of the assessment contingencies, likely including the learning requirements of the tasks. Our results also clearly indicate that attention processes have a prominent role on dogs’ global bias, in agreement with previous findings in humans and other species.     

Token mediated tool exchange between tufted capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Three experiments were conducted to test whether a pair of tufted capuchin monkeys (Cebus apella) could generalize their ability to exchange tokens and tool objects with a human experimenter to similar exchanges with a conspecific partner. Monkeys were tested in side-by-side enclosures, one enclosure containing a tool-use apparatus and one or more token(s), and the other enclosure containing one or more tool object(s). The monkeys willingly transferred tokens and tools to a conspecific with little practice. Following a small amount of training, we also found that the monkeys would select situation-appropriate tokens to exchange for specific tools, but did not select appropriate tool objects in response to another monkey’s token transfers. Implications regarding role reversal are discussed.     

Short-term observational spatial memory in Jackdaws (<Emphasis Type="Italic">Corvus monedula</Emphasis>) and Ravens (<Emphasis Type="Italic">Corvus corax</Emphasis>)

Observational spatial memory (OSM) refers to the ability of remembering food caches made by other individuals, enabling observers to find and pilfer the others' caches. Within birds, OSM has only been demonstrated in corvids, with more social species such as Mexican jays (Aphelocoma ultramarine) showing a higher accuracy of finding conspecific' caches than less social species such as Clark's nutcrackers (Nucifraga columbiana). However, socially dynamic corvids such as ravens (Corvus corax) are capable of sophisticated pilfering manoeuvres based on OSM. We here compared the performance of ravens and jackdaws (Corvus monedula) in a short-term OSM task. In contrast to ravens, jackdaws are socially cohesive but hardly cache and compete over food caches. Birds had to recover food pieces after watching a human experimenter hiding them in 2, 4 or 6 out of 10 possible locations. Results showed that for tests with two, four and six caches, ravens performed more accurately than expected by chance whereas jackdaws did not. Moreover, ravens made fewer re-visits to already inspected cache sites than jackdaws. These findings suggest that the development of observational spatial memory skills is linked with the species' reliance on food caches rather than with a social life style per se.     

Cooperative problem solving in giant otters (<Emphasis Type="Italic">Pteronura brasiliensis</Emphasis>) and Asian small-clawed otters (<Emphasis Type="Italic">Aonyx cinerea</Emphasis>)

Cooperative problem solving has gained a lot of attention over the past two decades, but the range of species studied is still small. This limits the possibility of understanding the evolution of the socio-cognitive underpinnings of cooperation. Lutrinae show significant variations in socio-ecology, but their cognitive abilities are not well studied. In the first experimental study of otter social cognition, we presented two species—giant otters and Asian small-clawed otters—with a cooperative problem-solving task. The loose string task requires two individuals to simultaneously pull on either end of a rope in order to access food. This task has been used with a larger number of species (for the most part primates and birds) and thus allows for wider cross-species comparison. We found no differences in performance between species. Both giant otters and Asian small-clawed otters were able to solve the task successfully when the coordination requirements were minimal. However, when the temporal coordination demands were increased, performance decreased either due to a lack of understanding of the role of a partner or due to difficulty inhibiting action. In conclusion, two species of otters show some ability to cooperate, quite similar to most other species presented with the same task. However, to draw further conclusions and more nuanced comparisons between the two otter species, further studies with varied methodologies will be necessary.     

Death,Rejuvenation and Immortality in Film: <Emphasis Type="Italic">On Golden Pond</Emphasis> (1981), <Emphasis Type="Italic">Cat on a Hot Tin Roof</Emphasis> (1958) and <Emphasis Type="Italic">Cocoon</Emphasis> (1985)

This paper seeks to highlight the developmental tasks of late adulthood with the help of three Hollywood movies. These tasks include: (i) struggling to maintain physical integrity, (ii) handling the "wound of mortality", (iii) maintaining activity and sexuality, and (iv) becoming wise. Among other challenges faced by an individual during this phase of life are loss of love objects, illness and possible compromise of mental functions, de-cathexis of material possessions and coming to terms with one's approaching death. All sorts of healthy and unhealthy psychosocial maneuvers come to the surface as a result of these stresses. This paper illustrates these dilemmas and their potential solutions via a discussion of three movies.