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 .     

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.     

Problem solving and functional design features: experiments on cotton-top tamarins, Saguinus oedipus oedipus

In any problem-solving situation, there are features associated with the problem that are relevant from a functional perspective and other features that are irrelevant. To determine whether animals are sensitive to the distinction between functionally relevant and irrelvant features of a problem, we conducted two main experiments with a New World monkey, the cotton-top tamarin. In the first condition of both experiments, subjects were required to pull a piece of cloth to gain access to a piece of food. The first experiment involved choosing between food that was on the cloth and food that was off the cloth. The second experiment involved choosing between food that was on a connected piece of cloth and food that was on two pieces of cloth separated by a horizontal gap. Having learned to solve either of these two problems, we conducted a series of probe conditions to determine whether the tamarins would generalize to changes in the shape, size, colour, and texture of the cloth and food, the position of the food relative to the cloth, and the type of connection between two pieces of cloth. For most of the probe conditions, the tamarins readily generalized, showing no decrement in performance, even on the first trial. For other conditions, involving apparently more subtle discrimination (e.g. a narrow vertical gap between the two pieces of cloth), explicit training was required. These results indicate that tamarins solve means-end relationships, and that their ability depends on a discrimination between properties that are functionally relevant as opposed to irrelevant. Copyright 1999 The Association for the Study of Animal Behaviour.     

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.     

The role of social context and individual experience in novel task acquisition in cottontop tamarins, Saguinus oedipus

In socially tolerant settings, na?ve individuals may have opportunities to interact jointly with knowledgeable demonstrators and novel tasks. This process is expected to facilitate social learning. Individual experience may also be important for reinforcing and honing socially acquired behaviours. We examined the role of joint interaction and individual experience in the acquisition of a novel foraging task in captive cottontop tamarins. The task involved learning how to locate and access two hidden food rewards from among 10 differently cued forage sites. Tamarins were tested in three different conditions: (1) individually, (2) while interacting with a na?ve mate, and (3) while interacting with a mate trained as a knowledgeable demonstrator. For tamarins tested with mates present, we interspersed social input test days with exposure to the task while alone. Tamarins were tested again 17 months after their last exposure to the task, to assess long-term memory. All tamarins tested with knowledgeable demonstrators solved the task. In contrast, tamarins tested alone or with na?ve mates had similarly high levels of neophobia and low levels of task acquisition. We conclude that joint interaction occurs in mated pairs of cottontop tamarins and facilitates the spread of novel behaviour. Interspersing test days with a knowledgeable demonstrator present and test days alone with the task helped tamarins to achieve the ultimate goal of the task: obtaining food rewards. Tamarins performed similarly when tested 17 months later, regardless of their initial learning environment. Tamarins had memory deficits for the location of hidden food rewards, but retained memory of the necessary motor actions and solved the task.     

The Interleukin-17 Gene of Herpesvirus Saimiri

In comparison to wild-type herpesvirus saimiri, viral interleukin-17 gene knockout mutants have unaltered behavior regarding viral replication, T-cell transformation in vitro, and pathogenicity in cottontop tamarins. Thus, this gene is not required for T-cell lymphoma induction but may contribute to apathogenic viral persistence in the natural host, the squirrel monkey.     

Kea (Nestor notabilis) consider spatial relationships between objects in the support problem

The ‘Support Problem’ is a benchmark test to investigate the understanding of spatial relationships between objects. We tested kea parrots'' performance in a paradigm that has previously been studied in primates. Kea perform comparably well to tamarins when they are confronted with a choice between two support devices, one of which has a reward resting on it and the other slightly next to it, or when given a choice between a continuous and a disrupted support. Kea did better than chimpanzees in some tasks in which the perceptual connection of the food to the support was altered. The results indicate that kea are capable of assessing the spatial means–end relationships of this problem spontaneously and in a way that is comparable with primates.     

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.     

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.     

Functional specifics of cortical associative regions participating in learning to differentiate visual information in monkeys

In 3 groups of monkeys: intact, those with their 7th field bilaterally removed, and those with bilateral removal of the sulcus principalis, functional specifics of the cortex' associative areas were studied. Removal of the 7th field practically does not affect processes of training for images with such features as spatial frequency, colour, and images of animals, but considerably impairs the learning characteristics in visual differentiation of objects' size and spatial interrelationships among objects. Removal of the sulcus principalis considerably impairs the characteristics of differentiation of objects' size and spatial interrelationships among them, as well as differently coloured stimuli. In both these groups, the stable motor response term and the probability of refusal increase. The data obtained suggest that the sensory processing results in forming a few (at least three) functional visual informational flows with which different cortical areas operate.     

Asymmetry of the cerebral hemispheres during comparison of paired visual stimuli

In conditions of tachistoscopic presentation of visual stimuli, healthy (male and female) right-handed subjects carried out a paired comparison of the stimuli presented unilaterally and in the center of the visual field. In case of recognition of images of words and objects, the number of correct answers and motor reaction time usually did not significantly differ at two interstimuli intervals (1 and 10 s). In comparing images of faces, there also were no differences by the number of reactions, and the reaction time was less at the intervals of 1 s. The left hemisphere dominated at the identification of words and female faces, the right one--at the recognition of male faces. When the right visual field was stimulated images of various classes were recognized more differentially than at the stimulation of the left visual field. The male subjects had more prominent interhemispheric differences than the females. The increase of the interstimuli interval from 1 to 10 s brought to a weakening of the functional interhemispheric asymmetry and decreasing of the differences between the male and female subjects. The obtained data show that in the processes connected with short-time memory, functional interhemispheric asymmetry is basically formed at the initial stages of the information processing.     

Automatic quantification of microvessels using unsupervised image analysis.

An automatic method for quantification of images of microvessels by computing area proportions and number of objects is presented. The objects are segmented from the background using dynamic thresholding of the average component size histogram. To be able to count the objects, fragmented objects are connected, all objects are filled, and touching objects are separated using a watershed segmentation algorithm. The method is fully automatic and robust with respect to illumination and focus settings. A test set consisting of images grabbed with different focus and illumination for each field of view, was used to test the method, and the proposed method showed less variation than the intraoperator variation using manual threshold. Further, the method showed good correlation to manual object counting (r = 0.80) on an other test set.     

Monitoring ovarian function in marmosets and tamarins by the measurement of urinary estrogen metabolites

Practical aspects of urinary estrogen analysis were considered with regard to establishing simple and reliable methods for monitoring ovarian function in marmosets and tamarins. Changes in the hormone:creatinine ratio in small volumes of urine from the common marmoset were significantly correlated with changes in 24-h excretion. Comparison of the metabolism and excretion of estrogens during the ovarian cycle in the common marmoset and cottontop tamarin revealed interesting species differences. High concentrations of conjugated estrone were measured in marmoset plasma, but estradiol 17β was the predominant estrogen in urine. In contrast, estrone was the most abundant estrogen measured in tamarin urine. Both species excreted very little estriol. Sulfates and glucuronides were present in urine in similar proportions before ovulation in the marmoset, although after ovulation sulfates were the more abundant. Conversely, most of the estrogens in tamarin urine appeared to be conjugated as glucuronides. Direct assay for estrone sulfate was applied to the measurement of urinary estrogen excretion during the ovarian cycle in a marmoset. The results compared well with those for total estradiol 17β after hydrolysis and ether extraction. The use of direct assays for conjugated estrogens in small volumes of urine is suggested as a practical method for monitoring ovarian function in marmosets and tamarins.     

Who Sees What in Pororan Marriage Exchange?

Over time, anthropologists working in Melanesia have provided increasingly nuanced analyses of exchange and, specifically, of the transformation of ‘objects’ and ‘images’ that people perceive in the course of particular revelatory sequences. One aspect of the complexity of exchange in Melanesia appears to have become sidelined, however, by a predominant interest in the temporal transformation of objects and images. This is the multiplicity of objects, images and sequences of their transformation that different participants perceive in the same sequence of events. The primary aim of this paper is to demonstrate this aspect of exchange ethnographically, and to discuss some of its implications on Pororan Island in Bougainville, Papua New Guinea.     

Modelling the influence of landscape connectivity on animal distribution: a functional grain approach

Landscape change may reduce the connectivity of landscapes and impact the movement of animals. If movement processes have been influenced by landscape connectivity, we hypothesize that animals may distribute themselves in larger connected regions of the landscape in order to minimize the movement costs associated with obtaining required resources and avoiding predators. We adopt the term functional grain to describe a set of functionally connected regions. In this spatial pattern, each region describes a contiguous area of the landscape within which an animal may move freely below a threshold amount of movement cost. We used telemetry data from woodland caribou Rangifer tarandus caribou to test hypothetical functional grains where connectivity was determined by the spatial configuration of resource patches (patch only), by the resistance to movement presented by landscape features (resistance only), and by a combination of the two (patch + resistance). To identify these functional grains, we used a grains of connectivity approach, and introduced a novel lattice‐based variant of this method to build the resistance only model. We developed a measure of fit that describes caribou distribution with respect to larger functionally connected regions in the grain, and used this to ask: 1) are seasonal caribou locations consistent with a random functional grain, implying that landscape connectivity has not shaped their distribution? 2) Given a functional grain model, are seasonal caribou locations distributed in larger functionally connected regions than random points, implying a response to the shape, size, and location of the connected regions. We found support for landscape connectivity influencing animal distribution using grains based on a landscape resistance model, and that support varied between behaviourally defined seasons. We also discuss how our novel lattice approach may be valuable for highly mobile mammals and other species where the identification of resource patches is a limitation.     

The Neural Basis of Object-Context Relationships on Aesthetic Judgment

The relationship between contextual information and object perception has received considerable attention in neuroimaging studies. In the work reported here, we used functional magnetic resonance imaging (fMRI) to investigate the relationship between aesthetic judgment and images of objects in their normal contextual setting versus images of objects in abnormal contextual settings and the underlying brain activity. When object-context relationships are violated changes in visual perception and aesthetic judgment emerges that exposes the contribution of vision to interpretations shaped by previous experience. We found that effects of context on aesthetic judgment modulates different memory sub-systems, while aesthetic judgment regardless of context recruit medial and lateral aspects of the orbitofrontal cortex, consistent with previous findings. Visual cortical areas traditionally associated with the processing of visual features are recruited in normal contexts, irrespective of aesthetic ratings, while prefrontal areas are significantly more engaged when objects are viewed in unaccustomed settings.     

Foraging and Spatial Memory in Wild Weddell’s Saddleback Tamarins (Saguinus fuscicollis weddelli) When Moving Between Distant and Out-of-Sight Goals

Two main types of cognitive maps, route-based and coordinate-based, have been proposed to explain how animals navigate through their environments. We examined patterns of feeding and ranging in Weddell’s saddleback tamarins (Saguinus fuscicollis weddelli) in northern Bolivia to assess which type of cognitive map best explains the tamarins’ movement patterns in large-scale space, e.g., when moving between distant and out-of-sight goals. We observed the tamarins for 236 h over the course of 32 d and used a GPS unit to record the location of nighttime sleeping sites and feeding trees and the locations of individuals at 10-min intervals. Based on an evaluation of 109 travel segments of >20 m in which the monkeys traveled from the tree of one major feeding species to another without stopping to rest, forage for insects, or interact with neighbors, we calculated a circuity index (actual distance traveled divided by the straight-line distance) of 1.43. We also plotted the monkeys’ daily movement patterns using GIS software. These analyses showed that tamarin travel was not random, that a limited set of route segments (N?=?29) was reused on multiple occasions, and that certain areas of the forest appeared to serve as switch points (N?=?9) where the monkeys reoriented travel. These results support the contention that the tamarins encoded the spatial relationships among many feeding and sleeping sites in their home range, and navigated in large-scale space using a route-based spatial representation. These results are consistent with those reported for a variety of primate taxa, suggesting that many primate species reuse a familiar set of travel routes and switch points to orient in large-scale space.     

Perception of harmonics in the combination long call of cottontop tamarins, Saguinus oedipus

A number of nonhuman primates produce vocalizations with time-varying harmonic structure. Relatively little is known about whether such spectral information plays a role in call type classification. We address this problem by utilizing acoustic analyses and playback experiments on cottontop tamarins‘ combi nation long call, a species-typical vocalization with a characteristic harmonic structure. Specifically, we used habituation-discrimination experiments to test whether particular frequency components, as well as the relationship between components, have an effect on the perception and classification of long calls. In Condition 1, we show that tamarins classify natural and synthetic exemplars of the long call as perceptually similar, thereby allowing us to use synthetics to manipulate components of this signal precisely. In subsequent conditions, we tested the perceptual salience and discriminability of long calls in which we deleted (1) the second harmonic, (2) the fundamental frequency, or (3) all frequencies above the fundamental; we also examined the effects of frequency mistuning by shifting the second harmonic by 1000 Hz. Following habituation to unmanipulated long calls, tamarins did not respond (transferred habituation) to long calls with either a missing fundamental frequency or the second harmonic, but responded (discriminated) to long calls with the upper harmonics eliminated or with the second harmonic mistuned. These studies reveal the importance of harmonic structure in tamarin perception, and highlight the advantages of using synthetic signals for understanding how particular acoustic features drive perceptual classification in nonhuman primates. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Environmental Enrichment for New World Primates: Introducing Food-Irrelevant Objects and Direct and Secondary Effects

This study examined methods of environmental enrichment for zoo animals for 4 New World primate species: pygmy and Geoffrey's marmosets (Cebuella pygmaea and Callithrix geoffroyi), red-bellied tamarins (Saguinus labiatus), and golden- headed lion tamarins (Leontopithecus chrysomelus). Subjects were housed in groups at the Philadelphia Zoo. Baseline behavioral time budget data were collected, and stimulus objects were then introduced in succession to each enclosure. Each object included multiple manipulable subcomponents. Time budget data were collected while objects were in the enclosures, and subjects' contacts with objects were videotaped. Overall time budgets were significantly altered in only the red-bellied tamarins, the least active of the species, solely due to a shift from social grooming to passive social contact; when categories were collapsed into broader categories, this effect disappeared. Object contact occurred within the 1st hr for all species and ranged over nearly 2 orders of magnitude, from approximately 10 sec per subject (red-bellied tamarins) to approximately 700 sec per subject (Geoffrey's marmosets). Habituation was not evident within any 1st hr of observation but was shown when 1st hr observations were compared with those from subsequent days. This article discusses implications for environmental enrichment in zoos.     

Differences in the Postural Responses to Approaching and Receding Sound Images in Subjects with Different Perceptual Styles

A hypothesis on the universal character of perceptual style for analyzing the surrounding space during sensory interactions has been tested. The indices of postural responses to moving and stationary auditory images in the groups of field-dependent and field-independent subjects, i.e., those who perceive spatial information about the object considering or ignoring the background, respectively, have been investigated. The differences in the sway parameters in both groups were revealed only in the case of moving auditory images. Body sway was more prominent in the group of field-independent subjects, whereas in the subjects from the field-dependent group, backward body displacement was observed during listening to approaching auditory images. Therefore, the perceptual style is reflected in the vertical postural responses to auditory information about the motion in the acoustic space.