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)     

Testing for social learning and imitation in common marmosets, <Emphasis Type="Italic">Callithrix jacchus</Emphasis>, using an artificial fruit

We tested for social learning and imitation in common marmosets using an artificial foraging task and trained conspecific demonstrators. We trained a demonstrator marmoset to open an artificial fruit, providing a full demonstration of the task to be learned. Another marmoset provided a partial demonstration, controlling for stimulus enhancement effects, by eating food from the outside of the apparatus. We thus compared three observer groups, each consisting of four animals: those that received the full demonstration, those that received the partial demonstration, and a control group that saw no demonstration prior to testing. Although none of the observer marmosets succeeded in opening the artificial fruit during the test periods, there were clear effects of demonstration type. Those that saw the full demonstration manipulated the apparatus more overall, whereas those from the control group manipulated it the least of the three groups. Those from the full-demonstration group also contacted the particular parts of the artificial fruit that they had seen touched (localised stimulus enhancement) to a greater extent than the other two groups. There was also an interaction between the number of hand and mouth touches made to the artificial fruit for the full- and partial-demonstration groups. Whether or not these data represent evidence for imitation is discussed. We also propose that the clear differences between the groups suggest that social learning mechanisms provide real benefits to these animals in terms of developing novel food-processing skills analogous to the one presented here.     

Cues to food location that domestic dogs (Canis familiaris) of different ages do and do not use

The results of three experiments are reported. In the main study, a human experimenter presented domestic dogs (Canis familiaris) with a variety of social cues intended to indicate the location of hidden food. The novel findings of this study were: (1) dogs were able to use successfully several totally novel cues in which they watched a human place a marker in front of the target location; (2) dogs were unable to use the marker by itself with no behavioral cues (suggesting that some form of human behavior directed to the target location was a necessary part of the cue); and (3) there were no significant developments in dogs’ skills in these tasks across the age range 4 months to 4 years (arguing against the necessity of extensive learning experiences with humans). In a follow-up study, dogs did not follow human gaze into “empty space” outside of the simulated foraging context. Finally, in a small pilot study, two arctic wolves (Canis lupus) were unable to use human cues to locate hidden food. These results suggest the possibility that domestic dogs have evolved an adaptive specialization for using human-produced directional cues in a goal-directed (especially foraging) context. Exactly how they understand these cues is still an open question. Received: 28 April 2000 / Accepted after revision: 2 September 2000     

Social learning of food types in zebra finches (<Emphasis Type="Italic">Taenopygia guttata</Emphasis>) is directed by demonstrator sex and feeding activity

In this study we examined how social learning of feeding preferences by zebra finches was affected by the identity of different demonstrators. We presented adult zebra finches with two demonstrators, one male and one female, that exhibited different food choices, and we recorded their subsequent preference when given a choice between the two food types. Previously it was found that young zebra finches' patterns of social learning are affected by the sex of the individual demonstrating a feeding behaviour. This result could be explained by the lack of exposure these animals had to the opposite sex, or by their mating status. Therefore, we investigated the social learning preferences of adult mated zebra finches. We found the same pattern of directed social learning of a different type of feeding behaviour (food colour): female zebra finches preferred the colour of food eaten by male demonstrators, whereas male zebra finches showed little evidence of any preference for the colour of food eaten by female demonstrators. Furthermore, we found that female observers' preferences were biased by demonstrators' relative feeding activity: the female demonstrator was only ever preferred if it ate less than its male counterpart. Electronic Publication     

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.     

Use of public information when foraging: effects of time available to sample foods

It has been proposed that use of socially acquired information by animals should increase as the time available for individual resource sampling decreases. We gave Norway rat “observers” either 2 or 5 h day^–1 to sample four foods. Three of these foods were relatively palatable, but protein-poor; the fourth was relatively unpalatable, but protein-rich. We found that observer rats that for 2 h day^–1 both sampled foods and interacted with demonstrators eating only the protein-rich food ate more of the protein-rich food than did observers that sampled for 2 h day^–1 but had no opportunity to interact with demonstrators. On the other hand, observer rats that could sample foods for 5 h day^–1 ate equal amounts of protein-rich food whether they interacted with a demonstrator fed protein-rich food or not. Subsequent analyses showed that the time available to observers to sample foods, rather than the opportunity to interact with demonstrators determined whether such interaction influenced observers’ food choices. The results are consistent with the hypothesis that animals increase their use of public information in response to temporal constraints on opportunities for resource sampling. Received: 22 December 1998 / Accepted after revision: 27 February 1999     

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).     

Contrafreeloading and the value of control over visual stimuli in Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Contrafreeloading, which means that animals work for food even though identical food is freely available, has been reported in animals’ feeding behavior. This phenomenon has been assumed to be explained by the information primacy model, in which the information about a food resource as well as the food itself is valuable for animals. This study confirmed a contrafreeloading-like phenomenon using movies as rewards rather than food in Japanese macaques (Macaca fuscata) and investigated the motivational system that exists behind contrafreeloading. In the experiment, movies that were presented dependently on subjects’ responses (earned movies) and movies that were presented automatically (free movies) were supplied simultaneously. The subjects continued to make responses to obtain the presentation of the earned movies although identical movies were available as free movies. These results provide the first evidence of contrafreeloading that occurs with movie rewards. The motivation maintaining the contrafreeloading behavior for movies may be control over the environment according to the competence theory.     

Experimental evidence for route integration and strategic planning in wild capuchin monkeys

Both in captivity and the wild, primates are found to travel mostly to the nearest available resource, but they may skip over the closest resource and travel to more distant resources, which are often found to be more productive. This study examines the tradeoff between distance and reward in the foraging choices of one group of wild capuchin monkeys (Cebus apella nigritus) using feeding platforms in large-scale foraging experiments conducted over four years. Three feeding sites were arrayed in an oblique triangle, such that once the monkey group had chosen one site to feed, they had a choice between two remaining sites, a close one with less food and the other up to 2.3 times as far away but with more food. Sites were provisioned once per day. The capuchins generally chose the closer feeding site, even when the more distant site offered up to 12 times as much food. The distances to, rewards of, or various profitability measures applied to each alternative site individually did not explain the group’s choices in ways consistent with foraging theory or principles of operant psychology. The group’s site choices were predicted only by comparing efficiency measures of entire foraging pathways: (1) direct travel to the more rewarding distant site, versus (2) the longer ‘detour’ through the closer site on the way to the more distant one. The group chose the detour more often when the reward was larger and the added detour distance shorter. They appeared to be more sensitive to the absolute increase in detour distance than to the relative increase compared to the straight route. The qualitative and quantitative results agree with a simple rule: do not use the detour unless the energy gain from extra food outweighs the energy cost of extra travel. These results suggest that members of this group integrate information on spatial location, reward, and perhaps potential food competition in their choice of multi-site foraging routes, with important implications for social foraging. This contribution is part of the special issue “ A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007b).     

Wild chimpanzees (Pan troglodytes schweinfurthii) distinguish between different scream types: evidence from a playback study

When experiencing aggression from group members, chimpanzees commonly produce screams. These agonistic screams are graded signals and vary acoustically as a function of the severity of aggression the caller is facing. We conducted a series of field playback experiments with a community of wild chimpanzees in the Budongo Forest, Uganda, to determine whether individuals could meaningfully distinguish between screams given in different agonistic contexts. We compared six subjects’ responses to screams given in response to severe and mild aggression. Subjects consistently discriminated between the two scream types. To address the possibility that the response differences were driven directly by the screams’ peripheral acoustic features, rather than any attached social meaning, we also tested the subjects’ responses to tantrum screams. These screams are given by individuals that experienced social frustration, but no physical threat, yet acoustically they are very similar to screams of victims of severe aggression. We found chimpanzees looked longer at severe victim screams than either mild victim screams or tantrum screams. Our results indicate that chimpanzees attend to the informational content of screams and are able to distinguish between different scream variants, which form part of a graded continuum.     

Horse (Equus caballus) whinnies: a source of social information

Many animal species that rely mainly on calls to communicate produce individual acoustic structures, but we wondered whether individuals of species better known as visual communicants, with small vocal repertoires, would also exhibit individual distinctiveness in calls. Moreover, theoretical advances concerning the evolution of social intelligence are usually based on primate species data, but relatively little is known about the social cognitive capacities of non-primate mammals. However, some non-primate species demonstrate auditory recognition of social categories and possess mental representation of their social network. Horses (Equus caballus) form stable social networks and although they display a large range of visual signals, they also use long-distance whinny calls to maintain contact. Here, we investigated the potential existence of individual acoustic signatures in whinny calls and the ability of horses to discriminate by ear individuals varying in their degree of familiarity. Our analysis of the acoustic structure of whinnies of 30 adult domestic horses (ten stallions, ten geldings, ten mares) revealed that some of the frequency and temporal parameters carried reliable information about the caller’s sex, body size and identity. However, no correlations with age were found. Playback experiments evaluated the behavioural significance of this variability. Twelve horses heard either control white noise or whinnies emitted by group members, familiar neighbours or unfamiliar horses. While control sounds did not induce any particular response, horses discriminated the social category of the callers and reacted with a sound-specific behaviour (vigilance and attraction varied with familiarity). Our results support the existence of social knowledge in horses and suggest a process of vocal coding/decoding of information.     

Seeing how it’s done: matching conditions for observer rats (Rattus norvegicus) in the bidirectional control

In an attempt to increase the reliability of the demonstrator-consistent responding effect produced in the bidirectional control procedure, experiments 1–4 sought conditions that would magnify the matching effect. The aim was to produce a robust demonstrator-consistent responding effect in order that future analytic experiments could investigate the psychological processes responsible for this effect. The joystick responses of observer rats trained using the standard bidirectional control procedure parameters were compared with those of observers subject to conditions identified in the social learning literature as favourable for imitation. Unlike mice, observer rats in experiments 1 a and 1 b tended to push a joystick in the same direction as their demonstrators when the demonstrators were either familiar or unfamiliar males and females. Comparable demonstrator-consistent responding occurred following observation of a standard and a salient joystick response (experiment 2). Experiment 3 showed that the discriminative accuracy of a demonstrator’s responding was important for matching behaviour, and suggested that matching might be enhanced with more than the conventional single observation session. Experiment 4 confirmed that the bidirectional control effect is sensitive to the amount of observational experience; after six observation sessions, demonstrator-inconsistent responding occurs. The results of experiments 1–3 are, and those of experiment 4 are not, compatible with the hypothesis that demonstrator-consistent responding in the bidirectional control is caused by olfactory cues deposited by demonstrators on the joystick. Received: 29 May 2000 / Accepted after revision: 28 August 2000     

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     

Diffusion of novel foraging behaviour in Amazon parrots through social learning

While social learning has been demonstrated in species across many taxa, the role it plays in everyday foraging decisions is not well understood. Investigating social learning during foraging could shed light on the emergence of cultural variation in different groups. We used an open diffusion experiment to examine the spread of a novel foraging technique in captive Amazon parrots. Three groups were tested using a two-action foraging box, including experimental groups exposed to demonstrators using different techniques and control birds. We also examined the influence of agonistic and pilfering behaviour on task acquisition. We found evidence of social learning: more experimental birds than control birds interacted with and opened the box. The birds were, however, no more likely to use the demonstrated technique than the non-demonstrated one, making local or stimulus enhancement the most likely mechanism. Exhibiting aggression was positively correlated with box opening, whilst receiving aggression did not reduce motivation to engage with the box, indicating that willingness to defend access to the box was important in task acquisition. Pilfering food and success in opening the box were also positively correlated; however, having food pilfered did not affect victims’ motivation to interact with the box. In a group context, pilfering may promote learning of new foraging opportunities. Although previous studies have demonstrated that psittacines are capable of imitation, in this naturalistic set-up there was no evidence that parrots copied the demonstrated opening technique. Foraging behaviour in wild populations of Amazons could therefore be facilitated by low-fidelity social learning mechanisms.     

Social processes in communication and cognition in callitrichid monkeys: a review

Studies of vocal development in nonhuman primates have found little evidence for plasticity in vocal production, somewhat more for usage of calls, with the greatest plasticity arising in response to calls of others. Generally, similar results were obtained with callitrichid monkeys, the marmosets and tamarins, but with several interesting exceptions. Infant pygmy marmosets show babbling behavior with improvement in adult call structure related to the amount and diversity of babbling. Adult marmosets alter call structure in response to changes in social partners, and wild marmosets have vocal dialects and modify call structure according to how far they are from other group members, suggesting the potential to modify call structure in different social and environmental contexts, though direct learning of novel vocalizations has not been observed. Infant cotton-top tamarins do not produce adult-like calls in appropriate contexts, at least in the first few months of life, but through food sharing from adults infants learn about appropriate foods and the appropriate contexts for food vocalizations. Tamarins modify call structure and usage with changes in social status. Tamarins, unlike other monkeys tested, can learn to avoid noxious foods through observation of other group members, and can learn about novel food locations. Recent studies provide evidence of contextual imitation in marmosets. The plasticity in vocal communication and evidence of social learning in marmosets and tamarins relative to other monkeys may be related to the cooperative breeding system of marmosets and tamarins. With a high degree of behavioral coordination among group members, there is a priority on monitoring signals and behavior of others and adjusting one's own signals and behavior. This creates the context for vocal plasticity and social learning. Accepted after revision: 23 May 2001 Electronic Publication     

Demonstration of a socially transmitted flavor aversion in rats? Kuan and Colwill (1997) revisited

In each of three experiments that differed only in procedural detail, observer rats interacted with pairs of conspecific demonstrators, one fed a cocoa-flavored diet (Diet Coc) and the other a cinnamon-flavored diet (Diet Cin). Immediately after both members of a pair of demonstrators had been fed, and 5 min before they interacted with an observer or observers, one of the demonstrators was made ill by intraperitoneal injection with lithium chloride. After interacting with a pair of demonstrators for 15 min, each observer was allowed to choose between Diet Cin and Diet Coc for 22 h. In all three experiments, observer rats consumed as much Diet Cin after interacting simultaneously with both an ill demonstrator that had eaten Diet Cin and a healthy demonstrator that had eaten Diet Coc as after interacting simultaneously with both a healthy demonstrator that had eaten Diet Cin and an ill demonstrator that had eaten Diet Coc. These results raise questions about the generality of Kuan and Colwill’s (1997) demonstration of socially transmitted flavor aversions in Norway rats.     

Modulation of physical understanding by common marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>)

The understanding of physical causality in common marmosets was tested using support problems in which a pair of sheets was presented to determine whether subjects would choose the sheet that had a food item on it (i.e., the sheet was supporting the food item). In two experiments, the conditions were manipulated in terms of the length of the sheet, the distance between the sheet and the food item, the presence of a gap separating the two sheets, and the size of the food item. In Experiment 1, the marmosets had difficulty rejecting an irretrievable food item when it was located closer to them than a retrievable item. Although their performance was strongly affected by the size of the irretrievable food item, they quickly learned to reject that alternative. In contrast, no improvement was found when one sheet was divided into two pieces such that the food item could not be retrieved when its near side was pulled. A similar response tendency was observed in Experiment 2, in which the effects of the large food item were examined in three different conditions. Thus, common marmosets were influenced by the perceptual features of the food in solving the support problems, as are other non-human primates. In addition, they consistently failed to appreciate the presence of a gap and, therefore, failed to reject the distracter alternative. However, all animals rapidly learned that the size of the food item was an irrelevant variable, and some showed an elementary conceptual understanding of support. These findings suggest that marmosets’ physical understanding may improve with experience.     

Root versus roof: automatic activation of location information during word processing

In four experiments, participants were presented with nouns referring to entities that are associated with an up or down location (e.g., roof, root). The required response either was compatible with the referent location or was not (e.g., upward vs. downward movement after reading roof). Across experiments, we manipulated whether the experimental task required word reading or not, as well as whether the response involved a movement or was stationary. In all experiments, participants’ responses were significantly faster in the compatible than in the incompatible condition. This strongly suggests that location information is automatically activated when nouns are being processed.     

Ability evaluation through social comparison

Two experiments were conducted to clarify and extend social comparison theory for abilities. In the first experiment, the hypothesis was supported that people want information about their ability level more when they anticipate making a decision about an action based on the ability than when the decision has already been made. The evaluative need is thus primarily a predecision phenomenon. The second experiment showed that the preference for comparison with similar others predicted by social comparison theory is strongest when those others have had experience utilizing the ability in situations relevant to subjects' decisions.