Face processing in cotton-top tamarins (Saguinus oedipus)

Current research on face processing in primates has focused on a few species, mostly macaques and chimpanzees; to date, only one New World monkey, the squirrel monkey, has been tested. We explored face processing, and the inversion effect in particular, in a New World primate species, the cotton-top tamarin (Saguinus oedipus). In phase 1 of our study, we trained subjects to discriminate between two faces and two scrambled faces; we then presented the tamarins with a series of novel probes in order to determine the features underlying classification. Results showed that the tamarins relied on the external contour of the face for discrimination more than the internal features and their configuration. Statistical analyses revealed no differences in accuracy or response times to upright versus inverted stimuli, and thus no inversion effect. In phase 2, we provided subjects with additional training on the face versus scrambled face discrimination task in order to focus their attention on the configuration of the internal features. Accuracy data revealed individual differences in how tamarins classified these stimuli, even though each subject was trained in the same way. In phase 3, we tested for generalization to a new set of face stimuli, as well as for the capacity to show an inversion effect. For one subject who attended to the configuration of internal features, we found significant evidence of generalization, but no evidence for an inversion effect. Electronic Publication     

Spontaneous representation of number in cotton-top tamarins (Saguinus oedipus)

The "violation of expectancy" looking-time methodology has proven a powerful tool for exploring prelinguistic mental representations in human infants as well as in nonhuman primates. Four studies applying this methodology to the question of spontaneous number representations in cotton-top tamarins (Saguinus oedipus) are reported here. Monkeys were shown 1 + 1 events in which objects were placed behind a screen, 1 by 1. The screen was removed, revealing consistent (2 objects) and inconsistent (1, 3, or 1 large object twice the mass of original object) outcomes. In all studies, monkeys looked longer at the inconsistent than at the consistent outcome. When the monkeys view a 1 + 1 operation, they expect exactly 2 objects. It is likely that these numerical representations are spontaneously available to a variety of primate species and could provide a foundation on which humans' number sense was constructed over evolution and development.     

Donor payoffs and other-regarding preferences in cotton-top tamarins (Saguinus oedipus)

Helping others at no cost to oneself is a simple way to demonstrate other-regarding preferences. Yet, primates exhibit mixed results for other-regarding preferences: chimpanzees and tamarins do not show these effects, whereas capuchin monkeys and marmosets preferentially give food to others. One factor of relevance to this no-cost food donation is the payoff to the donor. Though donors always receive the same payoffs regardless of their choice, previous work varies in whether they receive either a food reward or no food reward. Here, I tested cotton-top tamarins in a preferential giving task. Subjects could choose from two tools, one of which delivered food to a partner in an adjacent cage and the other of which delivered food to an empty cage. Thus, subjects could preferentially give or withhold food from a partner. I varied whether subjects received food payoffs, whether a partner was present or absent, and whether the partner was a non-cagemate or the subject’s mate. Results showed that the subjects’ overall motivation to pull either tool declined when they did not receive any food. Additionally, they did not preferentially donate or withhold food, regardless of their own payoff or their relationship with the partner. Thus, cotton-top tamarins do not take advantage of cost-free food giving, either when they might gain in the future (mates) or when they have no opportunity for future interactions (non-cagemates).     

Long-term memory for calls of relatives in cotton-top tamarins (Saguinus oedipus)

Recognition of relatives is important for dispersing animals to avoid inbreeding and possibly for developing cooperative, reciprocal relationships between individuals after dispersal. We demonstrate under controlled captive conditions that cotton-top tamarins (Saguinus oedipus) have a long-term memory for long calls of relatives from which they had been separated for periods ranging from 4 to 55 months. Tamarins responded with lower levels of arousal behavior to playbacks of long calls from current mates and from separated relatives compared to calls of unfamiliar, unrelated tamarins. Four tamarins had been out of contact with relatives for more than 4 years and still showed recognition as evidenced by low levels of arousal. Results could not be explained in terms of proximity to former relatives. Long-term memory for vocal signatures of relatives is adaptive and may be much more common than has been demonstrated.     

Spontaneous number discrimination of multi-format auditory stimuli in cotton-top tamarins (Saguinus oedipus)

Studies using operant training have demonstrated that laboratory animals can discriminate the number of objects or events based on either auditory or visual stimuli, as well as the integration of both auditory and visual modalities. To date, studies of spontaneous number discrimination in untrained animals have been restricted to the visual modality, leaving open the question of whether such capacities generalize to other modalities such as audition. To explore the capacity to spontaneously discriminate number based on auditory stimuli, and to assess the abstractness of the representation underlying this capacity, a habituation-discrimination procedure involving speech and pure tones was used with a colony of cotton-top tamarins. In the habituation phase, we presented subjects with either two- or three-speech syllable sequences that varied with respect to overall duration, inter-syllable duration, and pitch. In the test phase, we presented subjects with a counterbalanced order of either two- or three-tone sequences that also varied with respect to overall duration, inter-syllable duration, and pitch. The proportion of looking responses to test stimuli differing in number was significantly greater than to test stimuli consisting of the same number. Combined with earlier work, these results show that at least one non-human primate species can spontaneously discriminate number in both the visual and auditory domain, indicating that this capacity is not tied to a particular modality, and within a modality, can accommodate differences in format.     

Implicit chaining in cotton-top tamarins (Saguinus oedipus) with elements equated for probability of reinforcement

Three experiments examined the implicit learning of sequences under conditions in which the elements comprising a sequence were equated in terms of reinforcement probability. In Experiment 1 cotton-top tamarins (Saguinus oedipus) experienced a five-element sequence displayed serially on a touch screen in which reinforcement probability was equated across elements at .16 per element. Tamarins demonstrated learning of this sequence with higher latencies during a random test as compared to baseline sequence training. In Experiments 2 and 3, manipulations of the procedure used in the first experiment were undertaken to rule out a confound owing to the fact that the elements in Experiment 1 bore different temporal relations to the intertrial interval (ITI), an inhibitory period. The results of Experiments 2 and 3 indicated that the implicit learning observed in Experiment 1 was not due to temporal proximity between some elements and the inhibitory ITI. The results taken together support two conclusion: First that tamarins engaged in sequence learning whether or not there was contingent reinforcement for learning the sequence, and second that this learning was not due to subtle differences in associative strength between the elements of the sequence.     

Choosing and using tools: capuchins (Cebus apella) use a different metric than tamarins (Saguinus oedipus)

Cotton-top tamarins (Saguinus oedipus) selected canes positioned so that a straight inward pull brought food within reach (M. D. Hauser, 1997; see also record 1997-41347-003). Tamarins failed to retrieve food with canes in other positions, and they did not reposition these canes. In this study, tufted capuchin monkeys (Cebus apella) preferred canes they could pull straight in when these were present, but they also repositioned canes in individually variable ways, and their success at obtaining food with repositioned canes improved with practice. In accord with predictions drawn from ecological psychology, capuchins discovered affordances of canes through exploratory actions with these objects, whereas tamarins did not. Ecological theory predicts these differences on the basis of species-typical manipulative activity, and it provides a useful approach for the study of species differences in tool-using behavior.     

Monkey see, monkey plan, monkey do: the end-state comfort effect in cotton-top tamarins (Saguinus oedipus)

The way human adults grasp objects is typically influenced by their knowledge of what they intend to do with the objects. This influence is reflected in the end-state comfort effect: Actors adopt initially uncomfortable postures to accommodate later task demands. Although many experiments have demonstrated this effect, to the best of our knowledge its phylogenetic roots have not been investigated. In two experiments, we tested whether 9 cotton-top tamarin monkeys would show the end-state comfort effect. We did so by presenting the monkeys with a small cup containing a marshmallow. The cup was suspended in different orientations. The monkeys inhibited their natural grasping tendencies and adopted unusual grasping postures to accommodate subsequent task requirements, thus demonstrating the end-state comfort effect. This outcome provides evidence for more sophisticated motor planning than has previously been ascribed to this and related species.     

The production and perception of long calls by cotton-top tamarins (Saguinus oedipus): acoustic analyses and playback experiments

The authors' goal was to provide a better understanding of the relationship between vocal production and perception in nonhuman primate communication. To this end, the authors examined the cotton-top tamarin's (Saguinus oedipus) combination long call (CLC). In Part 1 of this study, the authors carried out a series of acoustic analyses designed to determine the kind of information potentially encoded in the tamarin's CLC. Using factorial analyses of variance and multiple discriminant analyses, the authors explored whether the CLC encodes 3 types of identity information: individual, sex, and social group. Results revealed that exemplars could be reliably assigned to these 3 functional classes on the basis of a suite of spectrotemporal features. In Part 2 of this study, the authors used a series of habituation-dishabituation playback experiments to test whether tamarins attend to the encoded information about individual identity. The authors 1st tested for individual discrimination when tamarins were habituated to a series of calls from 1 tamarin and then played back a test call from a novel tamarin; both opposite- and same-sex pairings were tested. Results showed that tamarins dishabituated when caller identity changed but transferred habituation when caller identity was held constant and a new exemplar was played (control condition). Follow-up playback experiments revealed an asymmetry between the authors' acoustic analyses of individual identity and the tamarins' capacity to discriminate among vocal signatures; whereas all colony members have distinctive vocal signatures, we found that not all tamarins were equally discriminable based on the habituation-dishabituation paradigm.     

Global and local processing in adult humans (Homo sapiens), 5-year-old children (Homo sapiens), and adult cotton-top tamarins (Saguinus oedipus)

This study compared adults (Homo sapiens), young children (Homo sapiens), and adult tamarins (Saguinus oedipus) while they discriminated global and local properties of stimuli. Subjects were trained to discriminate a circle made of circle elements from a square made of square elements and were tested with circles made of squares and squares made of circles. Adult humans showed a global bias in testing that was unaffected by the density of the elements in the stimuli. Children showed a global bias with dense displays but discriminated by both local and global properties with sparse displays. Adult tamarins' biases matched those of the children. The striking similarity between the perceptual processing of adult monkeys and humans diagnosed with autism and the difference between this and normatively developing human perception is discussed.     

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.     

Use of experimenter-given cues in visual co-orienting and in an object-choice task by a new world monkey species, cotton top tamarins (Saguinus oedipus)

Two methods assessed the use of experimenter-given directional cues by a New World monkey species, cotton top tamarins (Saguinus oedipus). Experiment 1 used cues to elicit visual co-orienting toward distal objects. Experiment 2 used cues to generate responses in an object-choice task. Although there were strong positive correlations between monkey pairs to co-orient, visual co-orienting with a human experimenter occurred at a low frequency to distal objects. Human hand pointing cues generated more visual co-orienting than did eye gaze to distal objects. Significant accurate choices of baited cups occurred with human point and tap cues and human look cues. Results highlight the importance of head and body orientation to induce shared attention in cotton top tamarins, both in a task that involved food getting and a task that did not.     

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.     

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.     

Tracking responses related to self-recognition: a frequency comparison of responses to mirrors, photographs, and videotapes by cotton top tamanins (Saguinus oedipus)

The frequency of responses cotton top tamarins (Saguinus oedipus) emitted indicative of self-recognition to a mirror was compared with the frequencies of responses emitted to digitized photographs of tamarins (Experiment 1) and to videotapes of real-time or prior tamarin action (Experiment 2). Results indicated more attentional responses toward the mirror in both studies, but behavioral indices of self-recognition were not consistently generated by the mirror. The 2 experiments confirmed that real-time self-reflection is a condition that generates heightened attention and rare examples of particular mirror-specific behaviors in tamarins.     

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.     

A test of object permanence in a new-world monkey species,cotton top tamarins (<Emphasis Type="Italic">Saguinus oedipus</Emphasis>)

Cotton top tamarins were tested in visible and invisible displacement tasks in a method similar to that used elsewhere to test squirrel monkeys and orangutans. All subjects performed at levels significantly above chance on visible (n=8) and invisible (n=7) displacements, wherein the tasks included tests of the perseverance error, tests of memory in double and triple displacements, and "catch" trials that tested for the use of the experimenter's hand as a cue for the correct cup. Performance on all nine tasks was significantly higher than chance level selection of cups, and tasks using visible displacements generated more accurate performance than tasks using invisible displacements. Performance was not accounted for by a practice effect based on exposure to successive tasks. Results suggest that tamarins possess stage 6 object permanence capabilities, and that in a situation involving brief exposure to tasks and foraging opportunities, tracking objects' movements and responding more flexibly are abilities expressed readily by the tamarins. Electronic Publication     

Patterns of social preference across different social contexts in golden lion tamarins (Leontopithecus rosalia)

We investigated the role of mutual and circumstantial factors in maintaining exclusive social relationships in a New World primate. Four breeding pairs of golden lion tamarins (Leontopithecus rosalia rosalia) were allowed to interact with their mate or an unfamiliar, opposite-sex adult in each of 4 different social contexts: in view of the mate, out of the mate's view, with only the mate present, and with only the unfamiliar animal present. Males and females were in proximity to, approached, and sniffed their mates significantly more often than they did unfamiliar tamarins. These behaviors suggest a preference for the familiar mate. However, when mates were absent, tamarins demonstrated significantly higher levels of approach and sniffs toward unfamiliar animals. These patterns of behavior indicate that circumstantial factors, such as social context, may regulate social interactions between paired tamarins and unfamiliar, opposite-sex conspecifics.     

When quantity trumps number: discrimination experiments in cotton-top tamarins (<Emphasis Type="Italic">Saguinus oedipus</Emphasis>) and common marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>)

The capacity for non-linguistic, numerical discrimination has been well characterized in non-human animals, with recent studies providing careful controls for non-numerical confounds such as continuous extent, density, and quantity. More poorly understood are the conditions under which animals use numerical versus non-numerical quantification, and the nature of the relation between these two systems. Here we test whether cotton-top tamarins and common marmosets can discriminate between two quantities on the basis of the amount of food rather than on number. In three experiments, we show that when choosing between arrays containing different numbers and sizes of food objects, both species based their decisions on the amount of food with only minor influences of numerical information. Further, we find that subjects successfully discriminated between two quantities differing by a 2:3 or greater ratio, which is consistent with the ratio limits found for numerical discrimination with this species. These studies demonstrate that non-human primates possess mechanisms that enable quantification of total amount, in addition to the numerical representations demonstrated in previous studies, with both types of quantification subject to similar processing limits.     

Social anxiety and self-protective communication style in close relationships

People with higher social anxiety tend to reveal less information about themselves in interactions with strangers, and this appears to be part of a self-protective strategy adopted in situations in which the risk of negative evaluation is judged to be particularly high. This research examined whether a similar style of communication may be adopted by people with higher social anxiety in their close relationships, and whether it may be associated with decrements in the quality (support, depth, conflict) of these relationships. Over 300 people from the community completed a series of online questionnaires measuring social anxiety and depression, and disclosure in and quality of their close friendships and romantic relationships. After controlling for levels of depression, social anxiety was associated with a paucity of disclosure in both romantic relationships and close friendships in females, but not males. There was an indirect association between higher social anxiety and lower relationship quality (lower support, with a trend towards greater conflict) via lower self-disclosure in women's romantic relationships, but not their close friendships. Addressing disclosure in the context of close relationships may assist socially anxious women to develop more fulfilling and harmonious close relationships.