Quality, Quantity, Distribution and Audience Effects on Food Calling in Cotton—Top Tamarins

Despite extensive documentation in many taxa of vocalizations specific to feeding contexts, little is known of the variables leading to production of food-associated calls. We thus experimentally investigated food-associated calls in cotton-top tamarins ( Saguinus oedipus ). In one experiment, we examined the roles of food quantity, quality and distribution and of social condition of individuals on food-associated calling. Paired adults without offspring gave more vocalizations than immature individuals and adults with offspring. We observed no effects of food quantity or distribution on calling rate. Tamarins called more often to peaches, a food of intermediate preference that was also consumed the fastest. Tamarins gave more food-associated calls when in closer proximity to other group members. Low rates of moderate aggression were observed in single, but not multiple, feeder conditions. We saw no consistent evidence of dominance among adults, and all aggression in family groups was directed toward immature animals. In another experiment, we presented a tamarin with food in a separate cage, either in view of or visually isolated from its mate. Tamarins presented with food called at an equal rate whether or not their mates were visible, suggesting no effect of audience on calling. Individuals not presented with food called in response to the food calls of their mates equally often, irrespective of whether or not the mate or the food was visible. Since food calling occurs at extremely low rates in the absence of food, the food calling by tamarins that cannot see the food suggests that the calls of their mates provide representational information about food.     

Cooperative problem solving in a cooperatively breeding primate (Saguinus oedipus)

We investigated cooperative problem solving in unrelated pairs of the cooperatively breeding cottontop tamarin, Saguinus oedipus, to assess the cognitive basis of cooperative behaviour in this species and to compare abilities with other apes and monkeys. A transparent apparatus was used that required extension of two handles at opposite ends of the apparatus for access to rewards. Resistance was applied to both handles so that two tamarins had to act simultaneously in order to receive rewards. In contrast to several previous studies of cooperation, both tamarins received rewards as a result of simultaneous pulling. The results from two experiments indicated that the cottontop tamarins (1) had a much higher success rate and efficiency of pulling than many of the other species previously studied, (2) adjusted pulling behaviour to the presence or absence of a partner, and (3) spontaneously developed sustained pulling techniques to solve the task. These findings suggest that cottontop tamarins understand the role of the partner in this cooperative task, a cognitive ability widely ascribed only to great apes. The cooperative social system of tamarins, the intuitive design of the apparatus, and the provision of rewards to both participants may explain the performance of the tamarins.     

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. Am. J. Primatol. 72:287–295, 2010. © 2009 Wiley‐Liss, Inc.     

Can Auditory Playback Condition Predator Mobbing in Captive-reared <Emphasis Type="Italic">Saguinus oedipus</Emphasis>?

Captive reintroductions often suffer high mortality, with predation as one source. Many species learn about predators; thus training captive-born animals to recognize predators may increase survivorship. We adapted variants of methods developed for birds to attempt to condition monkeys to mob a predator. Captive-reared cotton-top tamarins (Saguinus oedipus) did not differentiate between a snake and a rat, confirming previous research that naïve cotton-top tamarins do not fear snakes. Tamarins then viewed a living snake during playback of mobbing calls. In posttests, tamarins did not mob the snake. We then eliminated the pretest to avoid potential habituation and placed a stillborn tamarin with the snake in an attempt to heighten arousal. In posttests, tamarins again did not mob the snake, although they did increase their rates of calls, indicating mild arousal. Overall, none of 8 groups of cotton-top tamarins learned to mob a predator. Potential reasons for failure include conditioning multiple subjects at once and the lack of an experienced demonstrator. Observing a demonstrator was not necessary for birds to acquire mobbing, but may be necessary for tamarins.     

Will travel for food: spatial discounting in two new world monkeys

Nonhuman animals steeply discount the future, showing a preference for small, immediate over large, delayed rewards. Currently unclear is whether discounting functions depend on context. Here, we examine the effects of spatial context on discounting in cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus), species known to differ in temporal discounting. We presented subjects with a choice between small, nearby rewards and large, distant rewards. Tamarins traveled farther for the large reward than marmosets, attending to the ratio of reward differences rather than their absolute values. This species difference contrasts with performance on a temporal task in which marmosets waited longer than tamarins for the large reward. These comparative data indicate that context influences choice behavior, with the strongest effect seen in marmosets who discounted more steeply over space than over time. These findings parallel details of each species' feeding ecology. Tamarins range over large distances and feed primarily on insects, which requires using quick, impulsive action. Marmosets range over shorter distances than tamarins and feed primarily on tree exudates, a clumped resource that requires patience to wait for sap to exude. These results show that discounting functions are context specific, shaped by a history of ecological pressures.     

Captive cotton‐top tamarins' (Saguinus oedipus oedipus) use of landmarks to localize hidden food items

Seventeen captive cotton‐top tamarins (Saguinus oedipus oedipus) were individually tested on their use of spatial relationships between landmarks to locate multiple hidden food items. In two experiments, the tamarins were presented with a spatial‐foraging task in which positions of hidden food rewards were fixed in relation to an array of visual cues. In Experiment 1, the cues+hidden food configuration was rotated 90° and the tamarins were successful in locating the food items significantly above chance levels (P<0.01). In Experiment 2 the cues+hidden food configuration was translated (up, down or sideways) from the previously learned configuration, and the monkeys successfully localized the hidden food items (P<0.001). Results indicate that the tamarins relied on the spatial relationship between the multiple landmarks to locate hidden food items rather than on an associative or beacon strategy. The results of these experiments support the contention that when contextually appropriate these captive New World monkeys have the capacity to rely on the spatial relationship or positions of several cues as an array to localize points in their environment. Am. J. Primatol. 71:316–323, 2009. © 2009 Wiley‐Liss, Inc.     

The social transmission of spatial information in homing pigeons

We adapted a technique to explore the social transmission of spatial information in homing pigeons Columba livia. Five demonstrator pigeons were first trained to find a food goal within an indoor arena. This arena consisted of nine lidded cups laid out within a 12x12 grid on the floor. The task was to find the goal cup and flip the lid to obtain the food hidden within. Once the demonstrators had reached criterion the experiment proper began. During stage 1 of the experiment, 10 target birds, which had not previously been trained to find the goal, were introduced to the spatial task either in isolation or paired with a demonstrator. We measured how long they took to complete the task, the number of squares crossed on the grid, and the number of incorrect lids flipped. In stage 2, the target birds were introduced to the arena a second time, by themselves, and we compared the performance of the birds in the two treatments. The pigeons that had been introduced to the task with a demonstrator in stage 1 walked further and made more incorrect choices when searching for the food goal in stage 2 than the pigeons that were introduced to the task alone. This indicates that pigeons learn a spatial, food-finding task more effectively when performing the task alone than when accompanied by a knowledgeable conspecific. We discuss possible reasons for this in the light of previous experiments. Copyright 1999 The Association for the Study of Animal Behaviour.     

Social Learning in the Caracara Chimango,Milvago chimango (Aves: Falconiformes): an Age Comparison

Milvago chimango is a gregarious raptor showing great ecological plasticity. Their ability to explore new resources has allowed them to survive in areas with increasing human modification. In this study, we evaluated the social learning ability in wild‐caught individuals of M. chimango. In particular, we tested whether an ‘observer’ individual could improve the acquisition of a novel behaviour by watching a ‘demonstrator,’ and we examined the effects of age of both observers and demonstrators on social learning. We measured the ability of 18 observers to open an opaque Plexiglas box containing food, and we compared their performance to that of 10 control birds who did not watch a demonstrator solve the task. Prior to watching a demonstrator, only two of the observers and two of the control birds were able to open the box. After watching a demonstrator, 67% of observers were able to open the box, outperforming control birds in speed and success. Juvenile observers were more successful and faster than adults at contacting and opening the box. The age of the demonstrator did not influence the observers’ likelihood of success. These results showed that M. chimango are able to learn a box‐opening task with a hidden food reward by observing the behaviour of a conspecific and that this behaviour persisted over several days. Social learning ability in M. chimango might allow certain behavioural patterns, such as those related to novel resource acquisition in modified environments, to be socially transmitted among individuals in a population.     

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.     

Ontogeny of tool use in cottontop tamarins, Saguinus oedipus: innate recognition of functionally relevant features

Adult cottontop tamarins are sensitive to the functionally relevant and irrelevant features of objects used as tools to gain access to food. We conducted four experiments designed to assess whether infant cottontop tamarins show comparable sensitivities to functionally relevant and irrelevant features. All subjects were reared in a species-typical social environment, but prior to the present studies had never participated in any experiments, and had no access to tools or other freely moving, manipulable objects with the exception of food. Despite their lack of experience, the pattern of object choice by infants precisely mirrored those obtained with adults. Specifically, having learned to use a hard blue cane to retrieve food (experiment 1), infant tamarins immediately generalized to other objects (experiments 2-4), recognizing that changes in colour and texture play no role in an object's functionality as a tool, whereas changes in size and shape do. These data suggest that for cottontop tamarins, a species that does not naturally use tools, and infrequently manipulates objects, that the capacity to distinguish between functionally relevant and irrelevant features develops in the absence of domain-specific experience.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Social Learning of a Novel Foraging Task by Big Brown Bats (Eptesicus fuscus)

Acquiring information via observation of others can be an efficient way to respond to changing situations or learn skills, particularly for inexperienced individuals. Many bat species are gregarious, yet few studies have investigated their capacity for learning from conspecifics. We tested whether big brown bats (Eptesicus fuscus) can learn a novel foraging task by interacting with knowledgeable conspecifics. In experimental trials 11 na?ve bats (7 juveniles, 4 adults) interacted freely with trained bats that were capturing tethered mealworms, while in control trials 11 na?ve bats (7 juveniles, 4 adults) flew with untrained bats. Na?ve bats were then assessed for their ability to capture tethered mealworms. While no bat in the control group learned the task, a significant number of experimental bats, including juveniles with little or no experience foraging, showed evidence of learning. Eighty-two per cent of experimental bats and 27% of control bats directed feeding buzzes (echolocation calls associated with prey capture) at the mealworm. Furthermore, seven experimental bats (64%) showed evidence of learning by attacking and/or capturing the mealworm, while no bat in the control group attacked or captured the prey. Analyses of high-speed stereo video recordings revealed increased interaction with demonstrators among bats attacking or capturing the mealworm. At the time they displayed evidence of learning, bats flew closer together during feeding buzzes than during other portions of trials. Our results demonstrate that social interaction with experienced bats, and listening to feeding buzzes in particular, may play an integral role in development of foraging skills in bats.     

Problem solving, inhibition and domain-specific experience: experiments on cottontop tamarins, Saguinus oedipus

We present the results of experiments on cottontop tamarins designed to explore the relationship between problem solving, inhibitory control and domain-specific experience. The colony was divided into two groups: tool-experienced (TE) and tool-inexperienced (TI). The TE group had previously participated in a series of tool-use experiments and revealed that, when selecting a tool, they used featurally relevant dimensions (e.g. shape, material, orientation) over featurally irrelevant dimensions (e.g. colour). The TI group, although experienced in other laboratory-based experiments, had never been tested on tool or other object manipulation problems. In Phase 1, involving three conditions, all subjects were tested on a series of means-end problems involving the use of a cloth to access a piece of food. Although the correct choice always involved picking the supporting cloth, we also built in an association between the correct cloth and its colour. Once the subjects reached criterion, we reversed the association between the cloth colour and the food reward in Phase 2. If the subjects solved the problems in Phase 1 by attending to cloth colour, then in Phase 2 they should have difficulty, especially given prior findings on tamarins demonstrating that reversal learning is difficult. If the subjects solved Phase 1 by attending to the functionality of the problem (i.e. the physical/causal relationship between the cloth and food), then reversing the colours in Phase 2 should have no effect on the subjects' performances. Finally, if the subjects attended to both colour and functionality, then reversing the colours should cause some decrement in performance, but less so than in the case where colour alone dominates. In Phase 2, although both groups showed a decrement in performance, indicating problems with reversal learning, TE subjects significantly outperformed TI subjects. Furthermore, the pattern of performance for TE subjects suggested that they had solved the initial problem by attending to a combination of colour and functionality or functionality alone, while TI subjects had attended to colour alone. We conclude that for tamarins with experience as tool users, colour represents a less salient feature, even when it is systematically associated with a food reward. For inexperienced tamarins, however, colour is salient and reversal learning is difficult. Together, these findings highlight the importance of exploring the relationship between inhibitory control and domain-specific problem solving. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Age-dependent social learning in a lizard

Evidence of social learning, whereby the actions of an animal facilitate the acquisition of new information by another, is taxonomically biased towards mammals, especially primates, and birds. However, social learning need not be limited to group-living animals because species with less interaction can still benefit from learning about potential predators, food sources, rivals and mates. We trained male skinks (Eulamprus quoyii), a mostly solitary lizard from eastern Australia, in a two-step foraging task. Lizards belonging to ‘young’ and ‘old’ age classes were presented with a novel instrumental task (displacing a lid) and an association task (reward under blue lid). We did not find evidence for age-dependent learning of the instrumental task; however, young males in the presence of a demonstrator learnt the association task faster than young males without a demonstrator, whereas old males in both treatments had similar success rates. We present the first evidence of age-dependent social learning in a lizard and suggest that the use of social information for learning may be more widespread than previously believed.     

Social models fail to induce diet and feeding site avoidance in naïve yearling steers

Social learning can be of critical importance to cattle grazing rangeland environments with high variability of food resources across space and time. Experienced individuals can greatly facilitate foraging decisions (what to eat and where to eat) of na?ve peers in such settings. We conducted an experiment with cattle to investigate strength and persistence of socially induced food and feeding site avoidance behaviours. Sixteen na?ve yearling steers were paired with 16 social models that had either not been trained (control) or been trained with an emetic (LiCl), electrical shock or both to avoid: (a) an unsafe high-quality food (LiCl); (b) an unsafe high-quality feeding site (shock); or (c) both the unsafe high-quality food and the unsafe high-quality feeding site (LiCl + shock). Ten-minute trials were conducted in an experimental arena containing three artificial feeding sites each consisting of groups of bowls with either high- (HQ) or moderate-quality (MQ) foods (HQ = barley and oat grain; MQ = Bermuda grass hay). Unsafe high-quality (UHQ, surrounded by traffic cones) and safe moderate-quality (SMQ) feeding sites consisted of nine rubber bowls containing either HQ or MQ foods. The safe high-quality (SHQ) feeding site consisted of two groups of eight bowls containing HQ food, which surrounded the UHQ and SMQ feeding sites. Social models did not induce diet and feeding site avoidance behaviours in na?ve steers; they exerted small and transient changes in the feeding behaviour of their na?ve counterparts. Consequences to the individual outweighed social influences; when na?ve animals experienced the same punishment contingencies as their social models, their behavioural patterns closely resembled those of their social model. Conditioned food and location aversions via LiCl were apparently influenced by prior exposure to target foods and the experimental arena. Conversely, conditioned feeding site avoidance via shock was apparently not influenced by prior exposure to target foods or the experimental arena.     

Avoidance of potentially harmful food cannot be socially transmitted between rats

The social transmission of food preferences(STFP) is a behavioural task of olfactory memory, in which an observer rat learns safe food odours from a demonstrator rat, and shows preference for this odour in a subsequent choice test. However, previous studies have failed to detect the transmission of information about food of potential danger and food aversion using STFP test. In this study, we tested how demonstrators' health affects the exchange of odour information and whether observers can learn danger information from an unhealthy demonstrator. As expected, the observer rat formed an odour preference after interacting with a demonstrator rat that had just eaten food containing a new odour, however, odour preference rather than aversion was also formed after interacting with a demonstrator rat injected with LiCl(used to induce gastric malaise). Furthermore, anaesthetized demonstrator rats and half-anaesthetized demonstrator rats, which showed obvious motor deficits suggesting an unhealthy state, also socially transmitted food preferences to observers. These results suggest that the social transmission of food preferences task is independent of a demonstrators' health, and that information about dangerous foods cannot be transmitted using this behavioural task.     

Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back

Altruistic food giving among genetically unrelated individuals is rare in nature. The few examples that exist suggest that when animals give food to unrelated others, they may do so on the basis of mutualistic or reciprocally altruistic relationships. We present the results of four experiments designed to tease apart the factors mediating food giving among genetically unrelated cotton-top tamarins (Saguinus oedipus), a cooperatively breeding New World primate. In experiment 1 we show that individuals give significantly more food to a trained conspecific who unilaterally gives food than to a conspecific who unilaterally never gives food. The apparent contingency of the tamarins' food-giving behaviour motivated the design of experiments 2-4. Results from all three experiments show that altruistic food giving is mediated by prior acts of altruistic food giving by a conspecific. Specifically, tamarins do not give food to unrelated others when the food received in the past represents the by-product of another's selfish actions (experiments 2 and 3) or when a human experimenter gives them food (experiment 4) as did the unilateral altruist in experiment 1. By contrast, if one tamarin gives another food without obtaining any immediate benefit, then the recipient is more likely to give food in return. Overall, results show that tamarins altruistically give food to genetically unrelated conspecifics, discriminate between altruistic and selfish actions, and give more food to those who give food back. Tamarins therefore have the psychological capacity for reciprocally mediated altruism.     

Optimal foraging theory predicts effects of environmental enrichment in a group of adult golden lion tamarins

The success of environmental enrichment programs in effecting specific changes in the behavior of captive animals has not always been uniform. Separate studies demonstrated both an increase in food competition and a decrease in food competition among captive group-living primates upon introduction of foraging devices. The objectives of this study were to measure the effects of variation in resource distribution and availability on food competition in a group of captive adult golden lion tamarins (Leontopithecus rosalia). The resource variables chosen were suggested from optimal foraging theory. The energy invested to obtain an item influenced food transfer and aggressive behaviors while food abundance did not. All individuals obtained an equivalent number of items over the course of the experiment from the foraging device, even though some tamarins obtained most of their food rewards directly from the device while others received their food rewards primarily through food transfer from other group members. Because the monkeys appeared highly motivated to obtain food from the test apparatus and did not habituate to it, the foraging device used in this experiment could be used as regular environmental enrichment for golden lion tamarins. One way to circumvent potentially unacceptable rates of aggression, with this or any feeding protocol that increases foraging task complexity and search time, may be to provide more than one foraging device per group. Zoo Biol 17:231–244, 1998. © 1998 Wiley-Liss, Inc.     

Mated pairs of owl monkeys (Aotus nancymaae) exhibit sex differences in response to unfamiliar male and female conspecifics

In socially monogamous species, mate‐guarding could be a reproductive strategy that benefits both males and females, especially when males contribute to parental care. By actively guarding mates, males may reduce their chances of being cuckolded, whereas females that mate‐guard may reduce the likelihood that their mates will desert them or acquire additional mates, and hence limit or reduce paternal care of offspring. Owl monkeys (Aotus spp.) are socially monogamous with biparental care of young and, hence, potential beneficiaries of mate‐guarding. We presented mated pairs of captive owl monkeys (A. nancymaae) with unfamiliar male and female conspecifics, to determine if either member of the pair exhibits intraspecific aggression toward an intruder or stays close to its mate, behaviors indicative of mate‐guarding. Male mates were more responsible for the maintenance of close proximity between mates than females. Male mates also exhibited elevated levels of behavior that signify arousal when presented with a male conspecific. These responses by mated male owl monkeys are consistent with patterns that may help prevent cuckoldry. Am. J. Primatol. 72:942–950, 2010. © 2010 Wiley‐Liss, Inc.     

The ecology and evolution of patience in two New World monkeys

Decision making often involves choosing between small, short-term rewards and large, long-term rewards. All animals, humans included, discount future rewards--the present value of delayed rewards is viewed as less than the value of immediate rewards. Despite its ubiquity, there exists considerable but unexplained variation between species in their capacity to wait for rewards--that is, to exert patience or self-control. Using two closely related primates--common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus)--we uncover a variable that may explain differences in how species discount future rewards. Both species faced a self-control paradigm in which individuals chose between taking an immediate small reward and waiting a variable amount of time for a large reward. Under these conditions, marmosets waited significantly longer for food than tamarins. This difference cannot be explained by life history, social behaviour or brain size. It can, however, be explained by feeding ecology: marmosets rely on gum, a food product acquired by waiting for exudate to flow from trees, whereas tamarins feed on insects, a food product requiring impulsive action. Foraging ecology, therefore, may provide a selective pressure for the evolution of self-control.     

When to approach novel prey cues? Social learning strategies in frog-eating bats

Animals can use different sources of information when making decisions. Foraging animals often have access to both self-acquired and socially acquired information about prey. The fringe-lipped bat, Trachops cirrhosus, hunts frogs by approaching the calls that frogs produce to attract mates. We examined how the reliability of self-acquired prey cues affects social learning of novel prey cues. We trained bats to associate an artificial acoustic cue (mobile phone ringtone) with food rewards. Bats were assigned to treatments in which the trained cue was either an unreliable indicator of reward (rewarded 50% of the presentations) or a reliable indicator (rewarded 100% of the presentations), and they were exposed to a conspecific tutor foraging on a reliable (rewarded 100%) novel cue or to the novel cue with no tutor. Bats whose trained cue was unreliable and who had a tutor were significantly more likely to preferentially approach the novel cue when compared with bats whose trained cue was reliable, and to bats that had no tutor. Reliability of self-acquired prey cues therefore affects social learning of novel prey cues by frog-eating bats. Examining when animals use social information to learn about novel prey is key to understanding the social transmission of foraging innovations.