Variable infant care contributions in cooperatively breeding groups of wild saddleback tamarins.

Among non-human primates, alloparental infant care is most extensive in callitrichines, and is thought to be particularly costly for tamarins whose helpers may suffer increased energy expenditure, weight loss, and reduced feeding time and mobility. The costs and benefits of infant care likely vary among group members yet very few wild studies have investigated variable infant care contributions. We studied infant care over an 8-month period in four wild groups of saddleback tamarins in Bolivia to evaluate: (a) what forms of infant care are provided, by whom, and when, (b) how individuals adjust their behavior (activity, vigilance, height) while caring for infants, and (c) whether individuals differ in their infant care contributions. We found that infant carrying, food sharing, and grooming varied among groups, and immigrant males-those who joined the group after infants were conceived-participated less in infant care compared to resident males. Adult tamarins fed less, rested more, and increased vigilance while carrying infants. Although we did not detect changes in overall activity budgets between prepartum and postpartum periods, tamarins spent more time scanning their environments postpartum, potentially reflecting increased predation risk to both carriers and infants during this period. Our study provides the first quantitative data on the timing and amount of infant carrying, grooming, and food transfer contributed by all individuals within and among multiple wild groups, filling a critical knowledge gap about the factors affecting infant care, and highlighting evolutionary hypotheses for cooperative breeding in tamarins.

Implicit learning in cotton-top tamarins (Saguinus oedipus) and pigeons (Columba livia).

There is considerable interest in the conditions under which human subjects learn patterned information without explicit instructions to learn that information. This form of learning, termed implicit or incidental learning, can be approximated in nonhumans by exposing subjects to patterned information but delivering reinforcement randomly, thereby not requiring the subjects to learn the information in order to be reinforced. Following acquisition, nonhuman subjects are queried as to what they have learned about the patterned information. In the present experiment, we extended the study of implicit learning in nonhumans by comparing two species, cotton-top tamarins (Saguinus oedipus) and pigeons (Columba livia), on an implicit learning task that used an artificial grammar to generate the patterned elements for training. We equated the conditions of training and testing as much as possible between the two species. The results indicated that both species demonstrated approximately the same magnitude of implicit learning, judged both by a random test and by choice tests between pairs of training elements. This finding suggests that the ability to extract patterned information from situations in which such learning is not demanded is of longstanding origin.

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.

Navigating in small-scale space: the role of landmarks and resource monitoring in understanding saddleback tamarin travel.

Recent studies of spatial memory in wild nonhuman primates indicate that foragers may rely on a combination of navigational strategies to locate nearby and distant feeding sites. When traveling in large-scale space, tamarins are reported to encode spatial information in the form of a route-based map. However, little is known concerning how wild tamarins navigate in small-scale space (between feeding sites located at a distance of ≤60 m). Therefore, we collected data on range use, diet, and the angle and distance traveled to visit sequential feeding sites in the same group of habituated Bolivian saddleback tamarins (Saguinus fuscicollis weddelli) in 2009 and 2011. For 7-8 hr a day for 54 observation days, we recorded the location of the study group at 10 min intervals using a GPS unit. We then used GIS software to map and analyze the monkeys' movements and travel paths taken between feeding sites. Our results indicate that in small-scale space the tamarins relied on multiple spatial strategies. In 31% of cases travel was route-based. In the remaining 69% of cases, however, the tamarins appeared to attend to the spatial positions of one or more near-to-site landmarks to relocate feeding sites. In doing so they approached the same feeding site from a mean of 4.5 different directions, frequently utilized different arboreal pathways, and traveled approximately 30% longer than then the straight-line distance. In addition, the monkeys' use of non-direct travel paths allowed them to monitor insect and fruit availability in areas within close proximity of currently used food patches. We conclude that the use of an integrated spatial strategy (route-based travel and attention to near-to-goal landmarks) provides tamarins with the opportunity to relocate productive feeding sites as well as monitor the availability of nearby resources in small-scale space.

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.

Is inferential reasoning a distinctly human cognitive feature? Testing reasoning in cotton-top tamarins (Saguinus oedipus).

Logical inference is often assumed a human-unique ability, although many species of apes and monkeys have shown some facility within a two-cup task in which one cup is baited, the primate is shown the cup which is empty (an exclusion cue), and subsequently chooses the other baited cup. In published reports, New World monkey species show a limited ability to choose successfully, often with half or more of the subjects tested not showing the ability with auditory cues or with exclusion cues. In this study, five cotton-top tamarins (Saguinus oedipus) were tested in a two-cup task with visual or auditory cues which revealed the presence or absence of bait, and in a second study, were tested with a four-cup array using a variety of walls to define the baiting space and a variety of visual cues including inclusion and exclusion. Tamarins demonstrated the ability to use either visual or auditory exclusion cues to find rewards in the two-cup study, although the visual cue required some exposure before accuracy was expressed. Experiment 2 revealed that two of three tamarins' first guesses to find rewards matched best a logic model. When they made errors, they typically chose cups adjacent to the cued location or made choices that seemed generated from avoiding empty cups. These results suggest that tamarins can deduce the location of food using reasoning, although the ability is only applied robustly to first guesses, while second guesses are motivated by approach/avoidance and proximity to cued locations. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Rules and metarules: Adult cotton-top tamarins (Saguinus oedipus) and 5-year-old children (Homo sapiens) can master both.

Developmental psychologists have noted a similar timeline of change for children's use of different perspectives about the same objects or events, as in the use of different labels for the same object, an aspect of language, and in understanding other's knowledge or beliefs, an aspect of social cognition as reviewed in the study by Neiworth et al. Comparative psychologists are interested to know what cognitive flexibility looks like in other species and how such variation relates to life history, ecology, and phylogeny. The general pattern of results to date indicates that monkeys can master both intra- and interdimensional shifts, but intradimensional shifts are learned far more quickly than interdimensional shifts (reviewed in the study by Neiworth et al, 2022). Neiworth et al. report that they have conducted exactly this kind of comparative study: They examined cognitive flexibility in adult cotton-top tamarins and human children in three age groups as they participated in a modified version of the Dimensional Change Card Sort (DCCS). Neiworth et al.'s study offers an example of careful consideration of one such possibility: that of using the experimenter's postural orientation to the cards as an inadvertent aid. Here the authors had the benefit of prior work showing that tamarins follow human-provided cues to make a spatially discriminated choice only if the experimenter's head, body, and eyes oriented to a particular location. Thus, in this study, the experimenter kept their head and body centered in the testing space between the two cards and looked at a point on the wall directly behind the midpoint of the testing tray. But the DCCS task, in abstract form, has potentially broader comparative value than to examine cognitive flexibility in primates alone. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

A modified version of the dimensional change card sort task tests cognitive flexibility in children (Homo sapiens) and cotton-top tamarins (Saguinus oedipus).

A modified Dimensional Change Card Sort (DCCS) task was used to test cognitive flexibility in adult cotton-top tamarins and children aged 19 months to 60 months. Subjects had to infer a rule from the experience of selecting between two cards to earn a reward, and the pairs of stimuli defined the rule (e.g., pick blue ones, not red ones, or pick trucks, not boats). Two different tests measured subjects' ability to shift to a reversal of the rule (intradimensional shift) and to shift to a new rule defined by a dimension previously irrelevant (interdimensional shift). Both adult tamarins and children aged 49-60 months were able to learn the initial rule and switch to a reversal and to a rule based on a different dimension. In contrast, the two younger groups of children, aged 19-36 months and aged 37-48 months, could switch when a reversal was imposed but took significantly longer to learn a new rule on a former irrelevant dimension. Experiment 2 presented a wider set of novel stimuli which shared some features with the original set to further explore the basis of rule learning. The result was that tamarins and 52- to 60-month-old children both chose novel stimuli that fit the rule and had no a priori associative strength, suggesting a rule application not solely based on associative strength. Importantly, novel items introduced some risk for choice, and children showed themselves to be risk-averse, whereas tamarins were risk-prone within a novel context. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Prosocial behaviour emerges independent of reciprocity in cottontop tamarins.

The cooperative breeding hypothesis posits that cooperatively breeding species are motivated to act prosocially, that is, to behave in ways that provide benefits to others, and that cooperative breeding has played a central role in the evolution of human prosociality. However, investigations of prosocial behaviour in cooperative breeders have produced varying results and the mechanisms contributing to this variation are unknown. We investigated whether reciprocity would facilitate prosocial behaviour among cottontop tamarins, a cooperatively breeding primate species likely to engage in reciprocal altruism, by comparing the number of food rewards transferred to partners who had either immediately previously provided or denied rewards to the subject. Subjects were also tested in a non-social control condition. Overall, results indicated that reciprocity increased food transfers. However, temporal analyses revealed that when the tamarins' behaviour was evaluated in relation to the non-social control, results were best explained by (i) an initial depression in the transfer of rewards to partners who recently denied rewards, and (ii) a prosocial effect that emerged late in sessions independent of reciprocity. These results support the cooperative breeding hypothesis, but suggest a minimal role for positive reciprocity, and emphasize the importance of investigating proximate temporal mechanisms underlying prosocial behaviour.

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).

Characteristics of implicit chaining in cotton-top tamarins (Saguinus oedipus).

In human cognition there has been considerable interest in observing the conditions under which subjects learn material without explicit instructions to learn. In the present experiments, we adapted this issue to nonhumans by asking what subjects learn in the absence of explicit reinforcement for correct responses. Two experiments examined the acquisition of sequence information by cotton-top tamarins (Saguinus oedipus) when such learning was not demanded by the experimental contingencies. An implicit chaining procedure was used in which visual stimuli were presented serially on a touchscreen. Subjects were required to touch one stimulus to advance to the next stimulus. Stimulus presentations followed a pattern, but learning the pattern was not necessary for reinforcement. In Experiment 1 the chain consisted of five different visual stimuli that were presented in the same order on each trial. Each stimulus could occur at any one of six touchscreen positions. In Experiment 2 the same visual element was presented serially in the same five locations on each trial, thereby allowing a behavioral pattern to be correlated with the visual pattern. In this experiment two new tests, a Wild-Card test and a Running-Start test, were used to assess what was learned in this procedure. Results from both experiments indicated that tamarins acquired more information from an implicit chain than was required by the contingencies of reinforcement. These results contribute to the developing literature on nonhuman analogs of implicit learning.

Socially biased learning among adult cottontop tamarins (Saguinus oedipus).

We presented adult cottontop tamarins (Saguinus oedipus) with a novel foraging task that had been used previously to examine socially biased learning of juvenile observers [Humle & Snowdon, Animal Behaviour 75:267-277, 2008]. The task could be solved in one of two ways, and thus allowed for an analysis of behavioral matching between an observer and a skilled demonstrator (trained to use one of the two methods exclusively). Because the demonstrator was an adult in both this study and the juvenile study, the influence of the observer's age could be isolated and examined, as well as the behavior of demonstrators toward observers of different ages. Our main goals were to (1) compare adults and juveniles acquiring the same task to identify how the age of the observer affects socially biased learning and (2) examine the relationship between socially biased learning and behavioral matching in adults. Although adults spent less time observing the trained demonstrators than did juveniles, the adults were more proficient at solving the task. Furthermore, even though observers did not overtly match the behavior of the demonstrator, observation remained an important factor in the success of these individuals. The findings suggested that adult observers could extract information needed to solve a novel foraging task without explicitly matching the behavior of the demonstrator. Adult observers begged much less than juveniles and demonstrators did not respond to begging from adult. Skill acquisition and the process of socially biased learning are, therefore, age-dependent and are influenced by the behavioral interactions between observer and demonstrator. To what extent this holds true for other primates or animal species still needs to be more fully investigated and considered when designing experiments and interpreting results.

Social dynamics and individual plasticity of infant care behavior in cooperatively breeding cotton-top tamarins.

Individual variation in infant caretaking behavior is prevalent among marmoset and tamarin monkeys. Although most group members participate in infant care, the timing and amount provided differs greatly. In this study, we quantified general trends in infant carrying behavior by using a longitudinal database that included 11 years of instantaneous scan observations following 80 births of cotton-top tamarins. Using detailed focal observations on a subset of the same families (10 births) we identified influences that affected expression of infant care at the group and individual levels. Fathers were the primary carriers and paternal carry time gradually decreased with increasing infant age. Paternal carry time also decreased significantly with an increasing number of older sibling helpers. Most fathers began to carry on the first day postpartum. However, we report circumstances in which fathers delayed carrying until almost a month postpartum. Fathers retrieved infants the most, although adult brothers' rates of retrievals peaked and surpassed fathers' rates during week 4 postpartum. Fathers delayed rejection of infants until week 4, whereas mothers rejected infants immediately and throughout the eight weeks. Nonetheless, infants climbed onto their mothers more than onto any other family member. Mothers showed a high initial investment in carrying during the first two weeks, decreasing quickly thereafter. Maternal contributions to infant carrying remained low and relatively consistent regardless of group size. However, mothers dramatically increased their infant carrying behavior in families in which fathers were absent. Older siblings cared for infants more than did younger siblings, and brothers retrieved and carried infants more than did sisters. Individual expression of infant care changed to accommodate infant needs and changed according to varying social dynamics and circumstances across litters.

Hysteresis effects in a motor task with cotton-top tamarins (Sanguinus oedipus).

The way human adults grasp an object is influenced by their recent history of motor actions. Previously executed grasps are often more likely to reoccur on subsequent grasps. This type of hysteresis effect has been incorporated into cognitive models of motor planning, suggesting that when planning movements, individuals tend to reuse recently used plans rather than generating new plans from scratch. To the best of our knowledge, the phylogenetic roots of this phenomenon have not been investigated. Here, the authors asked whether 6 cotton-top tamarin monkeys (Saguinus oedipus) would demonstrate a hysteresis effect on a reaching task. The authors tested the monkeys by placing marshmallow pieces within grasping distance of a hole through which the monkeys could reach. On subsequent trials, the marshmallow position changed such that it progressed in an arc in either a clockwise or counterclockwise direction. The authors asked whether the transition point in right- versus left-handed reaches would differ depending on the direction of the progression. The data supported this hysteresis prediction. The outcome provides additional support for the notion that human motor planning strategies may have a lengthy evolutionary history.

Is a sense of inequity an ancestral primate trait? Testing social inequity in cotton top tamarins (Saguinus oedipus).

To address a controversy in the literature concerning whether monkeys show an aversion to inequity, individuals of a New World monkey species, cotton top tamarins (Saguinus oedipus) were tested in an offering task and in a bartering task. At issue was whether the monkeys rejected rewards because of a violation of expectancy of the preferred reward, or whether they rejected rewards because of a sensitivity to socially mediated inequity. The data from both tasks indicated that the subjects were more likely to reject when preferred rewards were presented, either because of another animal eating the reward (the social condition) or because of rewards being presented but inaccessible. The bartering task led to the only behavioral indication of aversion due specifically to social inequity, which was demonstrated when tamarins' sensitivity to the difference in rewards increased with exposure to other tamarins working to receive the preferred rewards. The results suggest that social inequity aversion will be assessed by tamarins, and possibly by other primates, only under conditions of limited resources and a requirement of work, which may make the situation a bit more competitive and thus drives attention toward both social and reward evaluation.

Cooperatively breeding cottontop tamarins (Saguinus oedipus) do not donate rewards to their long-term mates.

This study tested the hypothesis that cooperative breeding facilitates the emergence of prosocial behavior by presenting cottontop tamarins (Saguinus oedipus) with the option to provide food rewards to pair-bonded mates. In Experiment 1, tamarins could provide rewards to mates at no additional cost while obtaining rewards for themselves. Contrary to the hypothesis, tamarins did not demonstrate a preference to donate rewards, behaving similar to chimpanzees in previous studies. In Experiment 2, the authors eliminated rewards for the donor for a stricter test of prosocial behavior, while reducing separation distress and food preoccupation. Again, the authors found no evidence for a donation preference. Furthermore, tamarins were significantly less likely to deliver rewards to mates when the mate displayed interest in the reward. The results of this study contrast with those recently reported for cooperatively breeding common marmosets, and indicate that prosocial preferences in a food donation task do not emerge in all cooperative breeders. In previous studies, cottontop tamarins have cooperated and reciprocated to obtain food rewards; the current findings sharpen understanding of the boundaries of cottontop tamarins' food-provisioning behavior.

Grammatical pattern learning by human infants and cotton-top tamarin monkeys.

There is a surprising degree of overlapping structure evident across the languages of the world. One factor leading to cross-linguistic similarities may be constraints on human learning abilities. Linguistic structures that are easier for infants to learn should predominate in human languages. If correct, then (a) human infants should more readily acquire structures that are consistent with the form of natural language, whereas (b) non-human primates' patterns of learning should be less tightly linked to the structure of human languages. Prior experiments have not directly compared laboratory-based learning of grammatical structures by human infants and non-human primates, especially under comparable testing conditions and with similar materials. Five experiments with 12-month-old human infants and adult cotton-top tamarin monkeys addressed these predictions, employing comparable methods (familiarization-discrimination) and materials. Infants rapidly acquired complex grammatical structures by using statistically predictive patterns, failing to learn structures that lacked such patterns. In contrast, the tamarins only exploited predictive patterns when learning relatively simple grammatical structures. Infant learning abilities may serve both to facilitate natural language acquisition and to impose constraints on the structure of human languages.

Spatial cues more salient than color cues in cotton-top tamarins (Saguinus oedipus) reversal learning.

Animals living in stable home ranges have many potential cues to locate food. Spatial and color cues are important for wild Callitrichids (marmosets and tamarins). Field studies have assigned the highest priority to distal spatial cues for determining the location of food resources with color cues serving as a secondary cue to assess relative ripeness, once a food source is located. We tested two hypotheses with captive cotton-top tamarins: (a) Tamarins will demonstrate higher rates of initial learning when rewarded for attending to spatial cues versus color cues. (b) Tamarins will show higher rates of correct responses when transferred from color cues to spatial cues than from spatial cues to color cues. The results supported both hypotheses. Tamarins rewarded based on spatial location made significantly more correct choices and fewer errors than tamarins rewarded based on color cues during initial learning. Furthermore, tamarins trained on color cues showed significantly increased correct responses and decreased errors when cues were reversed to reward spatial cues. Subsequent reversal to color cues induced a regression in performance. For tamarins spatial cues appear more salient than color cues in a foraging task.

Behavioral effects of introducing pied tamarin (Saguinus bicolor) to black howler monkey (Alouatta caraya) and white-faced saki (Pithecia pithecia) in a zoological park.

Mixed-species primate exhibits are becoming more common in zoological parks as a means to display a diverse array of animals both more naturalistically and with more economy of space. Here, we describe behavioral changes during the introduction process of a pair of pied tamarins (Saguinus bicolor) to an established group of black howler monkeys (Allouatta caraya) and white-faced saki monkeys (Pithecia pithecia). Data were collected during six phases, representing introductions among the various species and to exhibit space and off-exhibit holding. The pied tamarins were consistently the most active of the three species. Although activity levels of the howler and saki monkeys remained constant throughout, that of the tamarins declined as the introduction progressed. Several episodes of aggression between the tamarins and the sakis were observed, but did not coincide with patterns predicted by previous intra-specific introductions. The three-species mix remained stable for several months; however, escalating aggression ultimately led to the removal of the sakis from the mixed-species exhibit. Despite our mixed results, we contend that only through continued trials, coupled with careful and systematic monitoring, can we ultimately identify stable mixes of species.

How long does it take? Reliable personality assessment based on common behaviour in cotton-top tamarins (Saguinus oedipus).

Individual variation in behaviour has been shown to have important ecological and evolutionary consequences. Research on animal personality has therefore received considerable attention, yet some methodological issues remain unresolved. We tested whether assessing personality by coding common behaviours is as time-consuming method as some researchers believe it to be. Altogether, 300 hours of observation were collected on 20 captive cotton-top tamarins (Saguinus oedipus). We first examined the repeatability of behavioural indices that represented the behavioural repertoire of cotton-top tamarins. We then compared the personality structures, based on different lengths of observation time, of these behavioural indices. The minimum observational time necessary to obtain a stable personality structure was 5 to 7 hours per individual. This stable structure included two components: Extraversion and Confidence, which were similar to those described in great apes, Old World monkeys, and other New World monkeys. Our findings suggest that, at least in the case of cotton-top tamarins, behavioural coding over relatively short periods of time can be used to assess personality and that longer observation periods may yield diminishing returns.