Copying without rewards: socially influenced foraging decisions among brown capuchin monkeys

An individual’s foraging activity can be influenced by the choices made by nearby conspecifics. The interest shown in the location and characteristics of a feeding patch may depend on the feeding success of a conspecific there, a process that needs to be distinguished from choices guided by rewards to the observer itself. We investigated how rewards for both self and others influence the foraging choices of captive capuchin monkeys (Cebus apella). Thirteen adult capuchins observed familiar female conspecific models explore one of three opaque boxes under three conditions. In the first, there were no rewards available to either monkey; in the second, rewards were available to the model only; and in the third, both monkeys could retrieve a reward. Under all conditions, subjects more often explored the same box as the model than was expected by chance. Thus, without ever receiving a reward themselves or without seeing another receive rewards, subjects’ searches were directed at the box explored by another monkey. The tendency to match the model’s choice increased if the subject was rewarded. We compared these results to control conditions in which the model was either absent, or present but not allowed to demonstrate. Subjects’ located the reward less often in control conditions, than in the experimental conditions. We conclude that extrinsic rewards, while helpful, are not required for partners to influence the foraging choices of capuchins, and that the unrewarded copying of foraging choices demonstrated here may provide the basis for additional social influences on learning. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007)     

Gibbon travel paths are goal oriented

Remembering locations of food resources is critical for animal survival. Gibbons are territorial primates which regularly travel through small and stable home ranges in search of preferred, limited and patchily distributed resources (primarily ripe fruit). They are predicted to profit from an ability to memorize the spatial characteristics of their home range and may increase their foraging efficiency by using a ‘cognitive map’ either with Euclidean or with topological properties. We collected ranging and feeding data from 11 gibbon groups (Hylobates lar) to test their navigation skills and to better understand gibbons’ ‘spatial intelligence’. We calculated the locations at which significant travel direction changes occurred using the change-point direction test and found that these locations primarily coincided with preferred fruit sources. Within the limits of biologically realistic visibility distances observed, gibbon travel paths were more efficient in detecting known preferred food sources than a heuristic travel model based on straight travel paths in random directions. Because consecutive travel change-points were far from the gibbons’ sight, planned movement between preferred food sources was the most parsimonious explanation for the observed travel patterns. Gibbon travel appears to connect preferred food sources as expected under the assumption of a good mental representation of the most relevant sources in a large-scale space.     

Integrating information about location and value of resources by white-faced saki monkeys (<Emphasis Type="Italic">Pithecia pithecia</Emphasis>)

Most studies of spatial memory in primates focus on species that inhabit large home ranges and have dispersed, patchy resources. Researchers assume that primates use memory to minimize distances traveled between resources. We investigated the use of spatial memory in a group of six white-faced sakis (Pithecia pithecia) on 12.8-ha Round Island, Guri Lake, Venezuela during a period of fruit abundance. The sakis’ movements were analyzed with logistic regressions, a predictive computer model and a computer model that simulates movements. We considered all the resources available to the sakis and compared observed distances to predicted distances from a computer model for foragers who know nothing about the location of resources. Surprisingly, the observed distances were four times greater than the predicted distances, suggesting that the sakis passed by a majority of the available fruit trees without feeding. The odds of visiting a food tree, however, were significantly increased if the tree had been visited in the previous 3 days and had more than 100 fruit. The sakis’ preferred resources were highly productive fruit trees, Capparis trees, and trees with water holes. They traveled efficiently to these sites. The sakis choice of feeding sites indicate that they combined knowledge acquired by repeatedly traveling through their home range with ‘what’ and ‘where’ information gained from individual visits to resources. Although the sakis’ foraging choices increased the distance they traveled overall, choosing more valued sites allowed the group to minimize intragroup feeding competition, maintain intergroup dominance over important resources, and monitor the state of resources throughout their home range. The sakis’ foraging decisions appear to have used spatial memory, elements of episodic-like memory and social and nutritional considerations. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007).     

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.     

Humans’ folk physics is not enough to explain variations in their tool-using behavior

Two experiments examined adult humans’ folk physics (i.e., their naturally occurring and spontaneous understanding of the physical world) using variations of trap-table problems used to study chimpanzees’ folk physics. When presented with these problems, people unnecessarily avoided retrieving a reward by pulling a rake on the side of a table with a trapping hole—even though it was highly unlikely that the hole would trap the reward. However, when the distance between the reward and the trap was sufficiently large and the distance that the reward had to travel to be retrieved was sufficiently short, people preferred to retrieve a reward by pulling the rake on the side of the table with the trap. These results underscore that behavior during tool-use tasks has many possible causes, only one of which might be a subject’s folk physics.     

Dogs are able to solve a means-end task

Dogs, although very skilled in social-communicative tasks, have shown limited abilities in the domain of physical cognition. Consequently, several researchers hypothesized that domestication enhanced dogs’ cognitive abilities in the social realm, but relaxed selection on the physical one. For instance, dogs failed to demonstrate means-end understanding, an important form of relying on physical causal connection, when tested in a string-pulling task. Here, we tested dogs in an “on/off” task using a novel approach. Thirty-two dogs were confronted with four different conditions in which they could choose between two boards one with a reward “on” and another one with a reward “off” (reward was placed next to the board). The dogs chose the correct board when (1) both rewards were placed at the same distance from the dog, when (2) the reward placed “on” the board was closer to the dog, and (3) even when the reward placed “off” the board was much closer to the dog and was food. Interestingly, in the latter case, dogs did not perform above chance, if instead of a direct reward, the dogs had to retrieve an object placed on the board to get a food reward. In contrast to previous string-pulling studies, our results show that dogs are able to solve a means-end task even if proximity of the unsupported reward is a confounding factor.     

“We will work for you” – Social influence may suppress individual food preferences in a communicative situation in dogs

The level of motivation (i.e. incentive power) is thought to be one of the most important factors affecting performance and learning in various tasks. We investigated whether reward quality has an effect on the performance of family dogs in a two-way object choice test in which they can find the hidden food by relying on distal momentary human pointing cues. In three experiments we varied (1) the type of food reward according to the subjects’ own preference; (2) the quality of the reward offered at the same time in the indicated and not-indicated locations; and (3) the order of the high or low quality rewards in consecutive sessions. In Experiment 1, we first tested whether dogs prefer one kind of reward over another. Then one group was tested with the ‘preferred’ food as reward in the indicated bowl, while dogs in the other group received the ‘non-preferred’ food as reward. We did not find any difference between the performance and choice latencies of the two groups. In Experiment 2 for the first group, the indicated bowl contained a piece of carrot and the not-indicated bowl was empty. In the second group the indicated bowl contained carrot, but the not-indicated bowl contained sausage. According to a preliminary preference test, most dogs prefer sausage over carrot invariably. After 20 trials, the two groups performed surprisingly similarly. There was no difference found between groups in the number of correct choices, incorrect choices and non-choices. However, the comparison between the first and last five trials revealed that subjects who found sausage when they chose the not-indicated bowl (did not follow the pointing) chose the non-indicated bowl significantly more often toward the end of their test session. In Experiment 3, each dog received two sessions with 12 pointing trials in each. For the first session, one group was rewarded with sausage and the other with carrot upon choosing the indicated bowl. In the second session, the indicated bowl contained dry dog food for both groups. We found that correct choices and response latencies did not change over two sessions in the ‘sausage’ group. In the ‘carrot’ group, the dogs chose faster in the second session, but their performance did not improve; in fact, they chose the not-indicated bowl more often than the indicated bowl. As a conclusion, we can say that reward quality had some effect on dogs’ choice behavior in these experiments. The drop in their performance was not drastic, taking into account the general refusal to eat one of the ‘rewards’ (carrot) during the preference tests and also during the test trials. It seems that incentive contrast may play a relatively minor role in dog-human social interactions. Appropriate reward quality can be very important in asocial problem solving tasks, but, when interacting with humans, following human signals may override the effect of changed incentive power.     

Is your choice my choice? The owners’ effect on pet dogs’ (Canis lupus familiaris) performance in a food choice task

This study investigates the influence of owners on their dogs’ performance in a food choice task using either different or equal quantities of food. Fifty-four pet dogs were tested in three different conditions. In Condition 1 we evaluated their ability to choose between a large and small amount of food (quantity discrimination task). In Condition 2 dogs were again presented with a choice between the large and small food quantity, but only after having witnessed their owner favouring the small quantity. In Condition 3 dogs were given a choice between two equally small quantities of food having witnessed their owner favouring either one or the other. A strong effect of the owner on the dogs’ performance was observed. In Condition 1 dogs as a group chose significantly more often the large food quantity, thus showing their ability to solve the quantity discrimination task. After observing their owner expressing a preference for the small food quantity they chose the large quantity of food significantly less than in the independent choice situation. The tendency to conform to the owner’s choice was higher when the dogs had to choose between equally small quantities of food (Condition 3) rather than between a large and a small one (Condition 2). These results provide evidence that dogs can be influenced by their owners even when their indications are clearly in contrast with direct perceptual information, thus leading dogs to ultimately make counterproductive choices.     

Spider monkey ranging patterns in Mexican subtropical forest: do travel routes reflect planning?

Although it is well known that frugivorous spider monkeys (Ateles geoffroyi yucatanensis) occupy large home ranges, travelling long distances to reach highly productive resources, little is known of how they move between feeding sites. A 11 month study of spider monkey ranging patterns was carried out at the Otochma’ax Yetel Kooh reserve, Yucatán, Mexico. We followed single individuals for as long as possible each day and recorded the routes travelled with the help of a GPS (Global Positioning System) device; the 11 independently moving individuals of a group were targeted as focal subjects. Travel paths were composed of highly linear segments, each typically ending at a place where some resource was exploited. Linearity of segments did not differ between individuals, and most of the highly linear paths that led to food resources were much longer than the estimate visibility in the woodland canopy. Monkeys do not generally continue in the same ranging direction after exploiting a resource: travel paths are likely to deviate at the site of resource exploitation rather than between such sites. However, during the harshest months of the year consecutive route segments were more likely to retain the same direction of overall movement. Together, these findings suggest that while moving between feeding sites, spider monkeys use spatial memory to guide travel, and even plan more than one resource site in advance. This contribution is part of the special issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007).     

Do cleaner fish learn to feed against their preference in a reverse reward contingency task?

The ability to control impulsive behaviour has been studied in animals with a standard test in which subjects need to choose the smaller of two food items in order to receive the larger one (reverse reward contingency). As a variety of mammals that have been tested so far (mostly primates) have great difficulties to solve the task, it has been proposed that it is generally cognitively demanding. However, according to an ecological approach to cognition, a species’ ability to solve the task should not depend on its general cognitive abilities but on whether its ecology causes selective pressure on the ability to restrain foraging behaviour. We tested this hypothesis using the cleaner wrasse (Labroides dimidiatus), a fish species that feeds against its preference in nature when engaging in cleaning interactions with so called ‘client fish’. None of the eight tested individuals learned to choose a non-preferred item after 200 trials. In a subsequent test, one subject learned to respond correctly in a large or none contingency task (only the choice of the small food was rewarded). After a short re-experience treatment, this individual learned to solve the reverse reward task after 30 trials. In conclusion, we did not find support for the general idea that interactions with clients prepared cleaners to quickly solve a reverse reward test. However, the results suggest that the potential to solve a reverse reward contingency may not be restricted to mammals but could be present also in a fish species in which the problem of choosing a non-preferred food over a preferred one is an ever present challenge in nature.     

Means to an end: Neotropical parrots manage to pull strings to meet their goals

Although parrots share with corvids and primates many of the traits believed to be associated with advanced cognitive processing, knowledge of parrot cognition is still limited to a few species, none of which are Neotropical. Here we examine the ability of three Neotropical parrot species (Blue-Fronted Amazons, Hyacinth and Lear’s macaws) to spontaneously solve a novel physical problem: the string-pulling test. The ability to pull up a string to obtain out-of-reach food has been often considered a cognitively complex task, as it requires the use of a sequence of actions never previously assembled, along with the ability to continuously monitor string, food and certain body movements. We presented subjects with pulling tasks where we varied the spatial relationship between the strings, the presence of a reward and the physical contact between the string and reward to determine whether (1) string-pulling is goal-oriented in these parrots, (2) whether the string is recognized as a means to obtain the reward and (3) whether subjects can visually determine the continuity between the string and the reward, selecting only those strings for which no physical gaps between string and reward were present. Our results show that some individuals of all species were able to use the string as a means to reach a specific goal, in this case, the retrieval of the food treat. Also, subjects from both macaw species were able to visually determine the presence of physical continuity between the string and reward, making their choices consistently with the recognition that no gaps should be present between the string and the reward. Our findings highlight the potential of this taxonomic group for the understanding of the underpinnings of cognition in evolutionarily distant groups such as birds and primates.     

A computerized test of self-control predicts classroom behavior

We assessed choices on a computerized test of self-control (CTSC) for a group of children with features of attention deficit hyperactivity disorder (ADHD) and a group of controls. Thirty boys participated in the study. Fifteen of the children had been rated by their parents as hyperactive and inattentive, and 15 were age- and gender-matched controls in the same classroom. The children were observed in the classroom for three consecutive mornings, and data were collected on their activity levels and attention. The CTSC consisted of two tasks. In the delay condition, children chose to receive three rewards after a delay of 60 s or one reward immediately. In the task-difficulty condition, the children chose to complete a difficult math problem and receive three rewards or complete an easier problem for one reward. The children with ADHD features made more impulsive choices than their peers during both conditions, and these choices correlated with measures of their activity and attention in the classroom.     

Chimpanzee gaze following in an object-choice task

Many primate species reliably track and follow the visual gaze of conspecifics and humans, even to locations above and behind the subject. However, it is not clear whether primates follow a human’s gaze to find hidden food under one of two containers in an object-choice task. In a series of experiments six adult female chimpanzees followed a human’s gaze (head and eye direction) to a distal location in space above and behind them, and checked back to the human’s face when they did not find anything interesting or unusual. This study also assessed whether these same subjects would also use the human’s gaze in an object-choice task with three types of occluders: barriers, tubes, and bowls. Barriers and tubes permitted the experimenter to see their contents (i.e., food) whereas bowls did not. Chimpanzees used the human’s gaze direction to choose the tube or barrier containing food but they did not use the human’s gaze to decide between bowls. Our findings allowed us to discard both simple orientation and understanding seeing-knowing in others as the explanations for gaze following in chimpanzees. However, they did not allow us to conclusively choose between orientation combined with foraging tendencies and understanding seeing in others. One interesting possibility raised by these results is that studies in which the human cannot see the reward at the time of subject choice may potentially be underestimating chimpanzees’ social knowledge. Received: 16 February 1998 / Accepted after revision: 5 July 1998     

What wild primates know about resources: opening up the black box

We present the theoretical and practical difficulties of inferring the cognitive processes involved in spatial movement decisions of primates and other animals based on studies of their foraging behavior in the wild. Because the possible cognitive processes involved in foraging are not known a priori for a given species, some observed spatial movements could be consistent with a large number of processes ranging from simple undirected search processes to strategic goal-oriented travel. Two basic approaches can help to reveal the cognitive processes: (1) experiments designed to test specific mechanisms; (2) comparison of observed movements with predicted ones based on models of hypothesized foraging modes (ideally, quantitative ones). We describe how these two approaches have been applied to evidence for spatial knowledge of resources in primates, and for various hypothesized goals of spatial decisions in primates, reviewing what is now established. We conclude with a synthesis emphasizing what kinds of spatial movement data on unmanipulated primate populations in the wild are most useful in deciphering goal-oriented processes from random processes. Basic to all of these is an estimate of the animal’s ability to detect resources during search. Given knowledge of the animal’s detection ability, there are several observable patterns of resource use incompatible with a pure search process. These patterns include increasing movement speed when approaching versus leaving a resource, increasingly directed movement toward more valuable resources, and directed travel to distant resources from many starting locations. Thus, it should be possible to assess and compare spatial cognition across a variety of primate species and thus trace its ecological and evolutionary correlates. This contribution is part of the special issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007b)     

Stereotyping starlings are more ‘pessimistic’

Negative affect in humans and animals is known to cause individuals to interpret ambiguous stimuli pessimistically, a phenomenon termed ‘cognitive bias’. Here, we used captive European starlings (Sturnus vulgaris) to test the hypothesis that a reduction in environmental conditions, from enriched to non-enriched cages, would engender negative affect, and hence ‘pessimistic’ biases. We also explored whether individual differences in stereotypic behaviour (repetitive somersaulting) predicted ‘pessimism’. Eight birds were trained on a novel conditional discrimination task with differential rewards, in which background shade (light or dark) determined which of two covered dishes contained a food reward. The reward was small when the background was light, but large when the background was dark. We then presented background shades intermediate between those trained to assess the birds’ bias to choose the dish associated with the smaller food reward (a ‘pessimistic’ judgement) when the discriminative stimulus was ambiguous. Contrary to predictions, changes in the level of cage enrichment had no effect on ‘pessimism’. However, changes in the latency to choose and probability of expressing a choice suggested that birds learnt rapidly that trials with ambiguous stimuli were unreinforced. Individual differences in performance of stereotypies did predict ‘pessimism’. Specifically, birds that somersaulted were more likely to choose the dish associated with the smaller food reward in the presence of the most ambiguous discriminative stimulus. We propose that somersaulting is part of a wider suite of behavioural traits indicative of a stress response to captive conditions that is symptomatic of a negative affective state.     

The development of prudence in the face of varying future rewards

The choice to delay gratification, opting for a greater reward later instead of a smaller reward now, has been used as a measure of preschoolers' ability to make future-oriented decisions. The present studies investigated to what extent these choice tasks reflect children's ability to make choices in favour of their future self. In Experiment 1, preschoolers were presented with choices between a smaller immediate reward of one sticker and larger delayed rewards varying in amount from two to five stickers. Whereas 3-year-olds showed no increased tendency to choose the delayed option as quantity increased from two to five, 4-year-olds' future-oriented choices reflected the value of the delayed reward. In Experiment 2, preschoolers chose between immediate and delayed rewards that were equal in amount and varied between one and four stickers. Three-year-olds reliably chose the immediate reward and showed no differentiation among rewards, whereas 4-year-olds chose in a manner that suggested they were trying to satisfy both immediate and future desires. Together these results support the notion that future-oriented prudence reflects growth in concern for the future self.     

Common marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>) do not utilize social information in three simultaneous social foraging tasks

Social foraging is suggested to increase foraging efficiency, as individuals might benefit from public information acquired by monitoring the foraging activities of other group members. We conducted a series experiments with captive common marmosets (Callithrix jacchus) to investigate to what extent marmosets utilize social information about food location when foraging simultaneously with conspecifics. Subjects were confronted with dominant and subordinate demonstrators in three experiments which differed in the amount of information about food location available to the demonstrators. In all three experiments, the focal subjects’ performance in the social condition was not enhanced in comparison to a non-social control condition. Because we could rule out kleptoparasitism and aggressive displacements as explanations, we argue that the subjects’ tendency for scramble competition by avoiding others and dispersing over the foraging area seems to inhibit or mask the acquisition of social information about the location of rewarded patches.     

Making choices in anticipation of similar future choices can increase self-control

Two experiments tested the efficacy of linking a current choice with similar future choices as a means of increasing self-control. Participants were offered choices between smaller and sooner vs. larger and later amounts of money (Experiment 1, n = 60) or food (Experiment 2, n = 34). After a small-large pair for which the participant preferred the smaller reward was found, a choice between the same pair was offered as the 1st of 5 such choices to be offered over a period of weeks. The majority of participants in both experiments who chose between all 5 smaller and all 5 larger rewards chose the larger rewards. One third of participants in Experiment 1 who could choose independently on each pair in the series reversed their previous preference and chose the larger reward in the context of the series. These results suggest that self-control can be enhanced by viewing one's current choice as predictive of future choices.     

Are dogs (<Emphasis Type="Italic">Canis familiaris</Emphasis>) misled more by their owners than by strangers in a food choice task?

Dogs are highly skilled in understanding a large variety of human social cues and use them appropriately to solve a number of different cognitive tasks. They rely on human signals even when these are contradictory or misleading and ultimately prevent them from correctly solving a task. In the following two experiments, we investigated whether the owner and a stranger differently influenced dogs’ choices in food discrimination tasks. In Experiment 1, 48 dogs were tested in 3 different conditions: (1) choice between a large and a small amount of dog pellets with no demonstration; (2) choice between a large and a small amount of dog pellets after having witnessed the owner/stranger favouring the small quantity; (3) choice between two single food pellets after observing the owner/stranger choosing one of them. In Experiment 2, 48 dogs could choose between two foods of different palatability: in Condition 1, dogs chose between a slice of sausage and a dry pellet with no demonstration. In Condition 2, the same choice was available but with a person (owner/stranger) showing a preference for the dry pellet. In Condition 3, dogs chose between a single dry pellet and 8 slices of sausage, with the person (owner/stranger) showing a preference for the pellet. In both experiments, dogs conformed to the human’s indications even though these led to the selection of the less advantageous option (i.e. the smaller amount of food in Experiment 1 or the low quality food in Experiment 2). However, the owner and the stranger did not differently influence the dogs’ behaviour. Results show that dogs are willing to follow a person’s indication even when this is visibly (if perhaps only mildly) counterproductive to them and that they are socially prepared to rely equally on cues given by the owner and an unfamiliar friendly person.     

The win-stay rule in foraging decisions by free-ranging titi monkeys (Callicebus cupreus cupreus) and Tamarins (Saguinus imperator imperator and Saguinus fuscicollis weddelli)

Rainforest primates need to apply distinct foraging rules for efficiently using the spatial knowledge of the distribution of resources showing different temporal patterns of renewal. A win-stay rule is very important for exploiting abundant, long-lasting resources. Here, the author tests the use of this rule in wild groups of emperor tamarins (Saguinus imperator imperator), saddle-back tamarins (Saguinus fuscicollis weddelli), and titi monkeys (Callicebus cupreus cupreus) during a series of foraging tasks. Four feeding stations composed of 8 visually similar feeding platforms (2 containing a food reward and 6 containing a sham reward) were constructed. The location of food rewards was reliable during some experiments and unreliable during others. All 3 species consistently adopted a win-stay rule for returning to reward platforms when their location was predictable over time but stopped using it when their spatial distribution changed randomly across experimental trials.