Means-means-end tool choice in cotton-top tamarins (Saguinus oedipus): finding the limits on primates’ knowledge of tools

Most studies of animal tool use require subjects to use one object to gain access to a food reward. In many real world situations, however, animals perform more than one action in sequence to achieve their goals. Of theoretical interest is whether animals have the cognitive capacity to recognize the relationship between consecutive action sequences in which there may be one overall goal and several subgoals. Here we ask if cotton-top tamarins, a species that in captivity uses tools to solve means-end problems, can go one step further and use a sequence of tools (means) to obtain food (end). We first trained subjects to use a pulling tool to obtain a food reward. After this initial training, subjects were presented with problems in which one tool had to be used in combination with a second in order to obtain food. Subjects showed great difficulty when two tools were required to obtain the food reward. Although subjects attended to the connection between the tool and food reward, they ignored the physical connection between the two tools. After training on a two-tool problem, we presented subjects with a series of transfer tests to explore if they would generalize to new types of connections between the tools. Subjects readily transferred to new connections. Our results therefore provide the first evidence to date that tamarins can learn to solve problems involving two tools, but that they do so only with sufficient training.     

The relationship between problem solving and inhibitory control: cotton-top tamarin (Saguinus oedipus) performance on a reversed contingency task

To explore the relationship between problem solving and inhibitory control, the authors present 4 experiments on cotton-top tamarins (Saguinus oedipus) using a reverse-reward contingency task. In Experiment 1, 1 group of tamarins was given a choice between a small and a large quantity of food. Whichever quantity the tamarins reached for first, they received the alternative. The tamarins consistently picked the larger quantity, thereby receiving the smaller. A 2nd group of tamarins was given the same task, except that if they reached for the larger quantity of food, they received nothing. The tamarins continued to pick the larger quantity, even though this resulted in no food. In addition, most of the tamarins continued to pick the larger quantity even when the food payoff for choosing the smaller quantity was increased (Experiment 2) or when the visual salience of the food was reduced (Experiment 3). Experiment 4 was based on the finding that chimpanzees (Pan troglodytes) that have been trained on the concept of number can solve the reversed contingency task if the food is replaced by Arabic numerals. With the help of a color association, and a higher cost incurred by picking the color associated with 3 food items, the tamarins learned to pick the color associated with 1 food item. These results are compared with those obtained from studies of other primate species, highlighting the importance of comparative studies of problem solving that use comparable methods.     

Capuchin monkeys (Cebus apella) are sensitive to others’ reward: an experimental analysis of food-choice for conspecifics

The issue whether non-human primates have other-regarding preference and/or inequity aversion has been under debate. We investigated whether tufted capuchin monkeys are sensitive to others’ reward in various experimental food sharing settings. Two monkeys faced each other. The operator monkey chose one of two food containers placed between the participants, each containing a food item for him/herself and another for the recipient. The recipient passively received either high- or low-value food depending on the operator’s choice, whereas the operator obtained the same food regardless of his/her choice. The recipients were either the highest- or lowest-ranking member of the group, and the operators were middle-ranking. In Experiment 1, the operators chose the high-value food for the subordinate recipient more frequently than when there was no recipient, whereas they were indifferent in their choice for the dominant. This differentiated behavior could have been because the dominant recipient frequently ate the low-value food. In Experiment 2, we increased the difference in the value of the two food items so that both recipients would reject the low-value food. The results were the same as in Experiment 1. In Experiment 3, we placed an opaque screen in front of the recipient to examine effects of visual contact between the participants. The operators’ food choice generally shifted toward providing the low-value food for the recipient. These results suggest that capuchins are clearly sensitive to others’ reward and that they show other-regarding preference or a form of inequity aversion depending upon the recipients and the presence of visual contact.     

The role of landmarks in cotton-top tamarin spatial foraging: evidence for geometric and non-geometric features

We report experiments on captive cotton-top tamarins (Saguinus oedipus) designed to explore two components of spatial foraging. First, do tamarins have the capacity to extract geometric information concerning the spatial relationship between a landmark and a piece of food located above or below it? Second, when tamarins use a landmark to find a target location, what non-geometric features of the landmark do they encode? To explore these problems, we created an artificial jungle environment and trained subjects to find food either above or below a target object (i.e., landmark). Once subjects successfully located the food, we transformed various features associated with the landmark, including its color, orientation, and shape; we also manipulated the landmark-food reward distance, the overall shape of the jungle, and the number and position of landmarks. Results showed that the tamarins' success in finding the food reward was not affected by landmark color, orientation, number, or overall shape of the jungle, suggesting that with respect to the particular test conditions, these features are not relevant to the representation of a landmark. Subjects also generalized to novel landmark-food distances, suggesting that they had integrated geometric (i.e., above/below) with non-geometric (i.e., color/shape) features. Performance was negatively affected by changes to the shape of the landmark, indicating that this feature is critical to the representation of a landmark. Accepted after revision: 7 August 2001 Electronic Publication     

Are consonant intervals music to their ears? Spontaneous acoustic preferences in a nonhuman primate

Humans find some sounds more pleasing than others; such preferences may underlie our enjoyment of music. To gain insight into the evolutionary origins of these preferences, we explored whether they are present in other animals. We designed a novel method to measure the spontaneous sound preferences of cotton-top tamarins, a species that has been extensively tested for other perceptual abilities. Animals were placed in a V-shaped maze, and their position within the maze controlled their auditory environment. One sound was played when they were in one branch of the maze, and a different sound for the opposite branch; no food was delivered during testing. We used the proportion of time spent in each branch as a measure of preference. The first two experiments were designed as tests of our method. In Experiment 1, we used loud and soft white noise as stimuli; all animals spent most of their time on the side with soft noise. In Experiment 2, tamarins spent more time on the side playing species-specific feeding chirps than on the side playing species-specific distress calls. Together, these two experiments suggest that the method is effective, providing a spontaneous measure of preference. In Experiment 3, however, subjects showed no preference for consonant over dissonant intervals. Finally, tamarins showed no preference in Experiment 4 for a screeching sound (comparable to fingernails on a blackboard) over amplitude-matched white noise. In contrast, humans showed clear preferences for the consonant intervals of Experiment 3 and the white noise of Experiment 4 using the same stimuli and a similar method. We conclude that tamarins' preferences differ qualitatively from those of humans. The preferences that support our capacity for music may, therefore, be unique among the primates, and could be music-specific adaptations.     

Can dogs defy gravity? A comparison with the human infant and a non-human primate

We conducted four experiments with 56 adult dogs (Canis lupus familiaris) involving tasks where food was dropped through an opaque tube connected either vertically or diagonally to one of two or three goal boxes. In the first experiment, modelled after studies with children and primates, the dogs first searched significantly more often in the location directly beneath the drop-off point (a gravity bias), although this box was not connected with the tube. These results are comparable to those of human infants and cotton-top tamarins. Experiments 2–4 tested which problem solving strategy the dogs applied to find the food. Results show that they do not understand the physical mechanism of the tube itself, and they apply one of three search strategies: search the gravity box (the one below the drop-off box); search the box in the middle; learn the correct location of the goal box. When the goal box was in the same location the dogs learned to search there over trials, that is, they learned to ‘defy gravity’, but when the location of the goal box changed over trials they showed no learning. These findings are compared with those from human infants and cotton-top tamarins: like these species, the dogs can learn to overcome a gravity bias, but only when the reward is to be found in a consistent location.     

Ravens (Corvus corax) are indifferent to the gains of conspecific recipients or human partners in experimental tasks

Although cooperative behaviours are common in animals, the cognitive processes underpinning such behaviours are very likely to differ between species. In humans, other-regarding preferences have been proposed to sustain long-term cooperation between individuals. The extent to which such psychological capacities exist in other animals is still under investigation. Five hand-reared ravens were first tested in an experiment where they could provide food to a conspecific at no cost to themselves. We offered them two behavioural options that provided identical amounts of food to the actor and where one of the two options additionally delivered a reward to a recipient. Subsequently, we made the ravens play a no-cost cooperation game with an experimenter. The experimenter had the same options as the animals and matched the ravens’ choices, making the prosocial choice the more profitable option. In both conditions, ravens were indifferent to the effects of their choices and hence failed to help conspecifics and to cooperate with the experimenter. While our negative results should be interpreted with care, overall, our findings suggest that the ravens had no understanding of the consequences of their actions for a potential recipient. This study adds to several others that have used a similar set-up and have reported negative results on other-regarding preferences in animals.     

Modeling alliance activity: Opportunity cost effects and manipulations in an iterated prisoner’s dilemma with exit option

We model the two-firm alliance as an iterated prisoners’ dilemma game with an exit option and test several theoretical predictions over two experimental studies. A new major effect on alliance performance arises by including the exit option (i.e., the option to end the alliance and receive a fixed payoff that is less than the payoff for mutual cooperation but greater than the payoff for mutual defection). The opportunity cost levels of the firms either directly or indirectly influence alliance cooperation and alliance payoffs through affecting the alliance strategies that the firms choose. Implications for partner selection, alliance selection and structuring, and strategy choices along the alliance lifespan, build on these results.     

Context extinction following conditioning with delayed reward enhances subsequent instrumental responding

In Experiment 1, delayed reward generated low response rates relative to immediate reward delivered with the same frequency. Lister rats exposed to delayed reward subsequently responded at a higher rate in extinction if they received nonreinforced exposure to the conditioning context after instrumental training and prior to test, compared with animals that received home cage exposure. In Experiment 2, a signaled delay of reinforcement resulted in higher rates than an unsignaled delay. Nonreinforced exposure to the conditioning context elevated response rate for subjects in the unsignaled condition relative to a home cage group, but had no effect on response rates for subjects that had received the signaled delay. In Experiment 3, following an unsignaled reinforcement delay, groups receiving either no event or signaled food in the context responded faster in extinction than groups receiving no context exposure or unsignaled food.     

Inhibitory control and response selection in problem solving: how cotton-top tamarins (Saguinus oedipus) overcome a bias for selecting the larger quantity of food

When presented with a choice between 1 and 3 pieces of food in a type of reversed contingency task, 4 cotton-top tamarins (Saguinus oedipus) consistently chose the 3 pieces of food and received nothing, even though the choice of 1 piece would have yielded 3. However, in a task in which the tamarins received the 1 piece of food when they chose it, all subjects learned to select 1 over 3. Thus, the tamarins' prior failure on the reversed contingency task did not result entirely from an inherent inability to suppress the prepotent response of reaching to the larger of 2 quantities of food. After the experience of selecting the smaller quantity and receiving it, all of the tamarins solved the version of the reversed contingency task that they failed initially. These results suggest that the tamarins' initial failure may have reflected a difficulty with selecting an alternative response option.     

Working harder for less: Effect of incentive value on force of instrumental response in humans

The present article reports evidence from human subjects that high payoff for instrumental performance may cause reduced vigour of response compared to the vigour observed for lower payoffs. Vigour of response, as measured by force of pressing (Experiment 1) and number of fortune wheel turns (Experiment 2), was inversely related to payoffs, with higher vigour in the low payoff conditions. Experiment 2 further demonstrated this effect, regardless of whether or not payoff depended on performance. These findings are related to parallel animal data, and an analysis in terms of a learned incentive-effort hypothesis is offered. Experiment 3 presented support for this hypothesis. The results are argued to be of importance to the understanding of how reinforcers affect human instrumental performance.     

Social comparison mediates chimpanzees’ responses to loss,not frustration

Why do chimpanzees react when their partner gets a better deal than them? Do they note the inequity or do their responses reflect frustration in response to unattainable rewards? To tease apart inequity and contrast, we tested chimpanzees in a series of conditions that created loss through individual contrast, through inequity, or by both. Chimpanzees were tested in four social and two individual conditions in which they received food rewards in return for exchanging tokens with an experimenter. In conditions designed to create individual contrast, after completing an exchange, the chimpanzees were given a relatively less-preferred reward than the one they were previously shown. The chimpanzees’ willingness to accept the less-preferred rewards was independent of previously offered foods in both the social and individual conditions. In conditions that created frustration through inequity, subjects were given a less-preferred reward than the one received by their partner, but not in relation to the reward they were previously offered. In a social context, females were more likely to refuse to participate when they received a less-preferred reward than their partner (disadvantageous inequity), than when they received a more-preferred reward (advantageous inequity). Specifically, the females’ refusals were typified by refusals to exchange tokens rather than refusals to accept food rewards. Males showed no difference in their responses to inequity or individual contrast. These results support previous evidence that some chimpanzees’ responses to inequity are mediated more strongly by what others receive than by frustration effects.     

Category discriminability, base-rate, and payoff effects in perceptual categorization

The optimality of perceptual categorization performance under manipulations of category discriminability (i.e., d' level), base rates, and payoffs was examined. Base-rate and payoff manipulations across two category discriminabilities allowed a test of the hypothesis that the steepness of the objective reward function affects performance (i.e., the flat-maxima hypothesis), as well as the hypothesis that observers combine base-rate and payoff information independently. Performance was (1) closer to optimal for the steeper objective reward function, in line with the flat-maxima hypothesis, (2) closer to optimal in base-rate conditions than in payoff conditions, and (3) in partial support of the hypothesis that base-rate and payoff knowledge is combined independently. Implications for current theories of base-rate and payoff learning are discussed.     

Probing the limits of tool competence: Experiments with two non-tool-using species (Cercopithecus aethiops and Saguinus oedipus)

Non-human animals vary in their ability to make and use tools. The goal of the present study was to further explore what, if anything, differs between tool-users and non-tool-users, and whether these differences lie in the conceptual or motor domain. We tested two species that typically do not use tools-cotton top tamarins (Saguinus oedipus) and vervet monkeys (Cercopithecus aethiops)-on problems that mirrored those designed for prolific tool users such as chimpanzees. We trained subjects on a task in which they could choose one of two canes to obtain an out-of-reach food reward. After training, subjects received several variations on the original task, each designed to examine a specific conceptual aspect of the pulling problem previously studied in other tool-using species. Both species recognized that effective pulling tools must be made of rigid materials. Subsequent conditions revealed significant species differences, with vervets outperforming tamarins across many conditions. Vervets, but not tamarins, had some recognition of the relationship between a tool's orientation and the position of the food reward, the relationship between a tool's trajectory and the substance that it moves on, and that tools must be connected in order to work properly. These results provide further evidence that tool-use may derive from domain-general, rather than domain-specific cognitive capacities that evolved for tool use per se.     

What guides a search for food that has disappeared? Experiments on cotton-top tamarins (Saguinus oedipus).

When food is launched down a vertically positioned S-shaped opaque tube, cotton-top tamarins (Saguinus oedipus) search for the food in the position directly beneath the release point, even though over several trials it never appears in this position (B. M. Hood et al., 1999). Experiment 1 showed that when the trajectory of the food shifts from the vertical to the horizontal plane, tamarins no longer show systematic perseverative errors and, in general, perform better on this invisible displacement task. Experiment 2 showed that tamarins with experience on the horizontal task show less of a bias when tested on the vertical task but nonetheless fail overall to solve this invisible displacement problem; their performance is substantially worse than it was on the horizontal task. Experiment 3 revealed that when the vertically positioned tube is replaced by an occluded ramp, tamarins consistently search in the compartment below the release point, even though most of the tamarins had experience in Experiments 1 and 2. Overall, results indicate that tamarins have a significant gravity bias when searching for food that has disappeared along the vertical plane but also have more general problems finding food that has moved out of sight.     

Too good to be true? Psychological responses to uncommon options in risk–reward environments

Risks and rewards, or payoffs and probabilities, are inversely related in many choice environments. We investigated people's psychological responses to uncommon combinations of risk and reward that deviate from learned regularities (e.g., options that offer a high payoff with an unusually high probability) as they evaluated risky options. In two experiments (N = 183), participants first priced monetary gambles drawn from environments in which risks and rewards were negatively correlated, positively correlated, or uncorrelated. In later trials, they evaluated gambles with uncommon combinations of risk and reward—that is, options that deviated from the respective environment's risk–reward structure. Pricing, response times, and (in Experiment 2) pupil dilation were recorded. In both experiments, participants took more time when responding to uncommon compared to foreseeable options or when the same options were presented in an uncorrelated risk–reward environment. This result was most pronounced when the uncommon gambles offered higher expected values compared to the other gambles in the set. Moreover, these uncommon, high‐value options were associated with an increase in pupil size. These results suggest that people's evaluations of risky options are based not only on the options' payoffs and probabilities but also on the extent to which they fit the risk–reward structure of the environment.     

Does effort influence inequity aversion in cotton-top tamarins (Saguinus oedipus)?

The human sense of fairness entails sensitivity not just to equality, the equal division of resources, but also to merit, the relationship between an individual’s share of resources and how hard they worked for their share. Recent evidence suggests that our sensitivity to equality has deep phylogenetic roots: several nonhuman animal species show an aversion to unequal reward distributions. However, the extent to which nonhuman animals share sensitivity to merit remains poorly understood, largely because previous studies have failed to properly manipulate work effort in inequity aversion tasks. Here, we tested whether cotton-top tamarins (Saguinus oedipus) would exhibit a differential response to inequity when acquiring rewards was either (1) effortful or (2) effortless. Subjects engaged in a pulling task in which they had an opportunity to deliver a disadvantageously unequal distribution of food to themselves and a partner (one piece for self, four pieces for partner). We made delivery effortful by adding a weight to the pulling handle. Critically, effort was calibrated to each individual. Results show that individuals varied markedly in their response to effort, highlighting the importance of manipulating work effort at the individual level. Overall, subjects showed little aversion to inequity. However, subjects were slightly less likely to accept inequity when doing so was effortful, although this effect was pronounced in only one individual. Our findings suggest a new method for capturing individual variation in effort and for studying the roots of the concept of merit in nonhuman animals.     

Individual differences in the response to forgone payoffs: an examination of high functioning drug abusers

This study evaluates the effect of forgone payoffs in decision‐making tasks used for studying individual differences. We investigate whether the disclosure of forgone payoffs (defined as payoffs associated with un‐chosen alternatives) has selective effects for drug abusers. Evidence suggests that drug abusers are hypersensitive to signals of positive reward. Accordingly, because the forgone payoffs of risky high‐variability options include rewarding outcomes, this may create a distraction and lead drug abusers to make more risky choices. In a controlled experiment, we examined the behavior of high‐functioning drug abusers and healthy controls using the Iowa gambling task. The results showed that in a forgone payoff condition, drug abusers made more risky choices. The results demonstrate that adding information about forgone payoffs can be useful for studying individual differences, and that studying individual differences can be valuable in evaluating the effects of forgone payoffs. Copyright © 2005 John Wiley & Sons, Ltd.     

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     

Nonhuman primates prefer slow tempos but dislike music overall

Human adults generally find fast tempos more arousing than slow tempos, with tempo frequently manipulated in music to alter tension and emotion. We used a previously published method [McDermott, J., & Hauser, M. (2004). Are consonant intervals music to their ears? Spontaneous acoustic preferences in a nonhuman primate. Cognition, 94(2), B11-B21] to test cotton-top tamarins and common marmosets, two new-World primates, for their spontaneous responses to stimuli that varied systematically with respect to tempo. Across several experiments, we found that both tamarins and marmosets preferred slow tempos to fast. It is possible that the observed preferences were due to arousal, and that this effect is homologous to the human response to tempo. In other respects, however, these two monkey species showed striking differences compared to humans. Specifically, when presented with a choice between slow tempo musical stimuli, including lullabies, and silence, tamarins and marmosets preferred silence whereas humans, when similarly tested, preferred music. Thus despite the possibility of homologous mechanisms for tempo perception in human and nonhuman primates, there appear to be motivational ties to music that are uniquely human.