Recognition and categorization of biologically significant objects by rhesus monkeys (Macaca mulatta): the domain of food.

To survive, organisms must be able to identify edible objects. However, we know relatively little about how humans and other species distinguish food items from non-food items. We tested the abilities of semi-free-ranging rhesus monkeys (Macaca mulatta) to learn rapidly that a novel object was edible, and to generalize their learning to other objects, in a spontaneous choice task. Adult monkeys watched as a human experimenter first pretended to eat one of two novel objects and then placed replicas of the objects at widely separated locations. Monkeys selectively approached the object that the experimenter had previously eaten, exhibiting a rapidly induced preference for the apparently edible object. In further experiments in which the same objects were used as tools or were manipulated at the face but not eaten, we fail to observe an approach bias, providing evidence that the monkeys' pattern of approach in the earlier experiments was specific to objects that were eaten. Subsequent experiments tested how monkeys generalized their preference for an edible object by first allowing them to watch a human experimenter eat one of two objects and then presenting them with new objects composed of the same substance but differing from the original, edible object in shape or color. Monkeys ignored changes in the shape of the object and generalized from one edible object to another on the basis of color in conjunction with other substance properties. Finally, we extended this work to infant rhesus monkeys and found that, like adults, they too used color to generalize to novel food objects. In contrast to adults, however, infants extended this pattern of generalization to objects that were acted on in other ways. These results suggest that infant monkeys form broader object categories than adults, and that food categories become sharpened as a function of maturational or experiential factors.     

Responses to novelty in phobic and non-phobic cynomolgus monkeys: The role of subject characteristics and object features

In two previous studies it has been shown that most surrogate-reared cynomolgus monkeys became phobic of a harmless object (a big paper bag) while most mother-reared monkeys approached that object. Results of the first study seemed to indicate that the phobic reaction was restricted to the bag. Barnett and Cowan (Interdisciplinary Science Review, 1, 43–62, 1976) and Suomi (Anxiety disorder in childhood, pp. 1–23, 1986), however, reported that subjects (respectively rats and monkeys) that avoided a first novel object also avoided subsequent novel objects. In the present study we exposed phobic (bag-avoiding) and non-phobic (bag-approaching) monkeys from the study by Röder, Timmermans and Vossen (Behaviour Research and Therapy, 27, 221–231, 1989) to several big and small novel objects. Our results show that, irrespective of their rearing conditions, subjects that were phobic also avoided big novel objects while subjects that were non-phobic approached big novel objects. The reaction to small novel objects was independent of the previous reaction to the bag.     

Incidental learning,attention, and curiosity in squirrel monkeys calorie deprived as infants

The long-term effects of infantile malnutrition on information processing were studied in squirrel monkeys. From 2 through 8 weeks of age, four low-calorie infants were fed reduced amounts of a high protein diet, limiting their mean body weight gain to 23% of that of four well-fed controls, with all of this gain occurring during the first 2 weeks on the low-calorie diet. Thereafter, both groups received the standard diet ad libitum. At 68 weeks of age, incidental learning was tested by introducing shape cues that were redundant to the solution of a previously learned, two-choice, color discrimination. Removal of the color cues showed that the low-calorie monkeys had learned significantly less about the shape cues than had the controls. The basis for this incidental learning failure was then examined with an embedded-figures dicrimination, to measure attentional ability, and a novel stimulus substitution task, to measure curiosity. The groups did not differ in detecting embedded figures, but the low-calorie monkeys were significantly less likely than controls to select or handle novel stimuli that had been substituted for previously learned discriminative cues. It was concluded that undernutrition in infancy may induce a long-term strategy of only learning information which leads to an immediate reward, while suppressing the acquisition of information due to intrinsic curiosity.     

Acoustic classification of alarm calls by vervet monkeys (Cercopithecus aethiops) and humans (Homo sapiens): I. Natural calls

A 2-choice, operant-conditioning-based classification procedure was developed in which vervet monkeys (Cercopithecus aethiops) categorized species-typical snake and eagle alarm calls recorded from individually identified free-ranging animals. After preliminary training with a pair of calls from a single animal, 2 vervets were tested with novel exemplars produced by a variety of callers. Experiment 1 combined testing with continued training in routine classification of 14 new calls. In Experiment 2, the subjects were tested with 48 novel calls in rapid succession. Human (Homo sapiens) control subjects participated in the first study without extended preliminary training. Monkey and human subjects both showed immediate transfer to classification of unfamiliar alarm calls, despite variations both in voice characteristics and reproduction quality.     

Core knowledge and its limits: The domain of food

Adults, preschool children, and nonhuman primates detect and categorize food objects according to substance information, conveyed primarily by color and texture. In contrast, they perceive and categorize artifacts primarily by shape and rigidity. The present experiments investigated the origins of this distinction. Using a looking time procedure, Experiment 1 extended previous findings that rhesus macaques (Macaca mulatta) generalize learning about novel food objects by color over changes in shape. Six additional experiments then investigated whether human infants show the same signature patterns of perception and generalization. Nine-month-old infants failed to detect food objects in accord with their intrinsic properties, in contrast to rhesus monkeys tested in previous research with identical displays. Eight-month-old infants did not privilege substance information over other features when categorizing foods, even though they detected and remembered this information. Moreover, infants showed the same property generalization patterns when presented with foods and tools. The category-specific patterns of perception and categorization shown by human adults, children, and adult monkeys therefore were not found in human infants, providing evidence for limits to infants’ domains of knowledge.     

Social learning in juvenile lemon sharks, Negaprion brevirostris

Social learning is taxonomically widespread and can provide distinct behavioural advantages, such as in finding food or avoiding predators more efficiently. Although extensively studied in bony fishes, no such empirical evidence exists for cartilaginous fishes. Our aim in this study was to experimentally investigate the social learning capabilities of juvenile lemon sharks, Negaprion brevirostris. We designed a novel food task, where sharks were required to enter a start zone and subsequently make physical contact with a target in order to receive a food reward. Naive sharks were then able to interact with and observe (a) pre-trained sharks, that is, ‘demonstrators’, or (b) sharks with no previous experience, that is, ‘sham demonstrators’. On completion, observer sharks were then isolated and tested individually in a similar task. During the exposure phase observers paired with ‘demonstrator’ sharks performed a greater number of task-related behaviours and made significantly more transitions from the start zone to the target, than observers paired with ‘sham demonstrators’. When tested in isolation, observers previously paired with ‘demonstrator’ sharks completed a greater number of trials and made contact with the target significantly more often than observers previously paired with ‘sham demonstrators’. Such experience also tended to result in faster overall task performance. These results indicate that juvenile lemon sharks, like numerous other animals, are capable of using socially derived information to learn about novel features in their environment. The results likely have important implications for behavioural processes, ecotourism and fisheries.     

Socio-spatial cognition in vervet monkeys

Safety in numbers is thought to be the principal advantage of living in groups for many species. The group can only provide protection against predators, however, when group cohesion is maintained. Vocalisations are used to monitor inter-individual distances, especially under conditions of poor visibility, but should be avoided in the presence of predators. Mentally tracking the movements of silent and invisible group members would allow animals foraging in dense vegetation to stay close to their group members while reducing the use of vocal contact. We tested the socio-spatial cognitive abilities of wild vervet monkeys (Chlorocebus pygerythrus) by comparing their reactions to plausible and implausible displacements of group members simulated by sound playbacks. Our methods are comparable to those used in studies of ‘object permanence’ and ‘invisible displacements’ of inanimate objects. Our results show that vervets can track the whereabouts of invisibly and silently moving group members, at least over short periods of time.     

Picture recognition of food by macaques (<Emphasis Type="Italic">Macaca silenus</Emphasis>)

Pictorial representations of three-dimensional objects are often used to investigate animal cognitive abilities; however, investigators rarely evaluate whether the animals conceptualize the two-dimensional image as the object it is intended to represent. We tested for picture recognition in lion-tailed macaques by presenting five monkeys with digitized images of familiar foods on a touch screen. Monkeys viewed images of two different foods and learned that they would receive a piece of the one they touched first. After demonstrating that they would reliably select images of their preferred foods on one set of foods, animals were transferred to images of a second set of familiar foods. We assumed that if the monkeys recognized the images, they would spontaneously select images of their preferred foods on the second set of foods. Three monkeys selected images of their preferred foods significantly more often than chance on their first transfer session. In an additional test of the monkeys’ picture recognition abilities, animals were presented with pairs of food images containing a medium-preference food paired with either a high-preference food or a low-preference food. The same three monkeys selected the medium-preference foods significantly more often when they were paired with low-preference foods and significantly less often when those same foods were paired with high-preference foods. Our novel design provided convincing evidence that macaques recognized the content of two-dimensional images on a touch screen. Results also suggested that the animals understood the connection between the two-dimensional images and the three-dimensional objects they represented.     

Amygdalectomy and responsiveness to novelty in rhesus monkeys (Macaca mulatta): generality and individual consistency of effects

Rhesus monkeys (Macaca mulatta) with bilateral ibotenic acid-produced lesions of the amygdala were compared with controls in several novel situations, including exposures to metal objects, toy animals, and a person. Early in testing, the monkeys with lesions showed reduced inhibitions on responsiveness compared with controls. With continuing exposures, differences between groups diminished sharply as inhibitions waned in the controls. This outcome is consistent with the hypothesis that the amygdala mediates caution in initial reactions to ambiguous or threatening novel situations, which, in the absence of adverse consequences, diminishes with repetition. Consistency of individual responsiveness across different situations, including pairing with other monkeys, was substantial in lesioned and normal monkeys, suggesting that stable qualities of temperament influenced the results in both groups.     

Testing problem-solving capacities: differences between individual testing and social group setting

Testing animals individually in problem-solving tasks limits distractions of the subjects during the test, so that they can fully concentrate on the problem. However, such individual performance may not indicate the problem-solving capacity that is commonly employed in the wild when individuals are faced with a novel problem in their social groups, where the presence of a conspecific influences an individual’s behaviour. To assess the validity of data gathered from parrots when tested individually, we compared the performance on patterned-string tasks among parrots tested singly and parrots tested in social context. We tested two captive groups of orange-winged amazons (Amazona amazonica) with several patterned-string tasks. Despite the differences in the testing environment (singly vs. social context), parrots from both groups performed similarly. However, we found that the willingness to participate in the tasks was significantly higher for the individuals tested in social context. The study provides further evidence for the crucial influence of social context on individual’s response to a challenging situation such as a problem-solving test.     

Capuchin monkeys’ use of human and conspecific cues to solve a hidden object-choice task

Learning by watching others can provide valuable information with adaptive consequences, such as identifying the presence of a predator or locating a food source. The extent to which nonhuman animals can gain information by reading the cues of others is often tested by evaluating responses to human gestures, such as a point, and less often evaluated by examining responses to conspecific cues. We tested whether ten brown capuchin monkeys (Cebus [Sapajus] apella) were able to use cues from monkeys and a pointing cue from a human to obtain hidden rewards. A monkey could gain access to a reward hidden in one of two locations by reading a cue from a conspecific (e.g., reaching) or a human pointing. We then tested whether they could transfer this skill from monkeys to humans, from humans to monkeys, and from one conspecific to another conspecific. One group of monkeys was trained and tested using a conspecific as the cue-giver and was then tested with a human cue-giver. The second group of monkeys was trained and tested with a human cue-giver and was then tested with a monkey cue-giver. Monkeys that were successful with a conspecific cue-giver were also tested with a novel conspecific cue-giver. Monkeys learned to use a human point and conspecific cues to obtain rewards. Monkeys that had learned to use the cues of a conspecific to obtain rewards performed significantly better than expected by chance when they were transferred to the cues of a novel conspecific. Monkeys that learned to use a human point to obtain rewards performed significantly better than expected by chance when tested while observing conspecific cues. Some evidence suggested that transferring between conspecific cue-givers occurred with more facility than transferring across species. Results may be explained by simple rules of association learning and stimulus generalization; however, spontaneous flexible use of gestures across conspecifics and between different species may indicate capuchins can generalize learned social cues within and partially across species.     

It's a sign of the kind: gestures and words guide infants' inductive inferences

The role of words and gestures in guiding infants' inductive inferences about nonobvious properties was examined. One hundred seventy-two 14-month-olds and 22-month-olds were presented with novel target objects followed by test objects that varied in similarity to the target. Objects were introduced with a novel word or a novel gesture or with no label. When target and test objects were highly similar in shape, both 14- and 22-month-olds inferred that these objects shared a nonobvious property, regardless of whether the objects were labeled with a word or a gesture or with no label. When objects were labeled with the same word, both 14- and 22-month-olds generalized the nonobvious properties to objects that shared minimal perceptual similarity. Finally, when objects were labeled with the same gesture, 14-month-olds, but not 22-month-olds, generalized the nonobvious properties to objects that shared minimal perceptual similarity. These results indicate that 14-month-olds possess a more generalized symbolic system as they will rely on both words and gestures to guide their inferences. By 22-months of age, infants treat words as a privileged referential form when making inductive inferences.     

Token mediated tool exchange between tufted capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Three experiments were conducted to test whether a pair of tufted capuchin monkeys (Cebus apella) could generalize their ability to exchange tokens and tool objects with a human experimenter to similar exchanges with a conspecific partner. Monkeys were tested in side-by-side enclosures, one enclosure containing a tool-use apparatus and one or more token(s), and the other enclosure containing one or more tool object(s). The monkeys willingly transferred tokens and tools to a conspecific with little practice. Following a small amount of training, we also found that the monkeys would select situation-appropriate tokens to exchange for specific tools, but did not select appropriate tool objects in response to another monkey’s token transfers. Implications regarding role reversal are discussed.     

How do rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) scan faces in a visual paired comparison task?

When novel and familiar faces are viewed simultaneously, humans and monkeys show a preference for looking at the novel face. The facial features attended to in familiar and novel faces, were determined by analyzing the visual exploration patterns, or scanpaths, of four monkeys performing a visual paired comparison task. In this task, the viewer was first familiarized with an image and then it was presented simultaneously with a novel and the familiar image. A looking preference for the novel image indicated that the viewer recognized the familiar image and hence differentiates between the familiar and the novel images. Scanpaths and relative looking preference were compared for four types of images: (1) familiar and novel objects, (2) familiar and novel monkey faces with neutral expressions, (3) familiar and novel inverted monkey faces, and (4) faces from the same monkey with different facial expressions. Looking time was significantly longer for the novel face, whether it was neutral, expressing an emotion, or inverted. Monkeys did not show a preference, or an aversion, for looking at aggressive or affiliative facial expressions. The analysis of scanpaths indicated that the eyes were the most explored facial feature in all faces. When faces expressed emotions such as a fear grimace, then monkeys scanned features of the face, which contributed to the uniqueness of the expression. Inverted facial images were scanned similarly to upright images. Precise measurement of eye movements during the visual paired comparison task, allowed a novel and more quantitative assessment of the perceptual processes involved the spontaneous visual exploration of faces and facial expressions. These studies indicate that non-human primates carry out the visual analysis of complex images such as faces in a characteristic and quantifiable manner.     

Discrimination Learning and Multiple Reversals in Young Adult and Older Monkeys Macaca arctoides

Two groups of five young adult and older stumptailed macaques (Macaca arctoides) were tested on a visual discrimination task followed by a reversal upon attainment of criterion; task and reversal were repeated until 20 reversals with the same pair of objects had been completed. Both groups required more trials to learn the first reversal than the original discrimination, with no significant difference between the groups. Older monkeys tended to show more perseverative errors on early reversals, but a striking improvement in their scores across successive blocks of reversals culminated in performances virtually indistinguishable from those of the young group by the end of testing.     

To whom the play signal is directed: a study of headshaking in black-handed spider monkeys (Ateles geoffroyi)

Spider monkeys shake their heads so as to facilitate amicable social contact. This occurs frequently during vigorous play fighting, and so is common during the juvenile period. Occasionally, juvenile spider monkeys use headshakes during nonsocial locomotor play. In this study, head shaking in early infancy and in adulthood was studied in a captive troop of spider monkeys, with a total of 8 infants studied from shortly after birth to just before weaning. Three hypotheses to account for these nonsocial headshakes were tested. The play as the experience of the unexpected hypothesis was found wanting because nonsocial headshakes were most common in early infancy, before the onset of the juvenile peak in play. The immature misdirection of signals hypothesis was also found wanting because the headshakes were correctly directed at other monkeys, but not at inanimate objects that were grabbed and mouthed. Both also failed to predict the occurrence of the observed nonsocial headshakes in adults. The hypothesis best supported by the data is that, under some situations, headshakes are self-directed to promote action when confronting contexts of uncertainty.     

Learning and limits of use of eye gaze by capuchin monkeys (Cebus apella) in an object-choice task

The ability of 3 capuchin monkeys (Cebus apella) to use experimenter-given cues to solve an object-choice task was assessed. The monkeys learned to use explicit gestural and postural cues and then progressed to using eye-gaze-only cues to solve the task, that is, to choose the baited 1 of 2 objects and thus obtain a food reward. Increasing cue-stimulus distance and introducing movement of the eyes impeded the establishment of effective eye-gaze reading. One monkey showed positive but imperfect transfer of use of eye gaze when a novel experimenter presented the cue. When head and eye orientation cues were presented simultaneously and in conflict, the monkeys showed greater responsiveness to head orientation cues. The results show that capuchin monkeys can learn to use eye gaze as a discriminative cue, but there was no-evidence for any underlying awareness of eye gaze as a cue to direction of attention.     

Recognition of a 3D snake model and its 2D photographic image by captive black tufted-ear marmosets (Callithrix penicillata)

Two-dimensional (2D) displays of real three-dimensional (3D) objects are frequently used experimental tools in animal studies. Whether marmoset monkeys, with their highly diverse and complex anti-predation strategies, readily recognized 2D representations of potential threats has yet to be determined, as seen in other primates. Thus, the behavioral responses of adult captive black tufted-ear marmosets (Callithrix penicillata) toward an unfamiliar motionless snake-model and its photograph were assessed. Pictorially naïve subjects were randomly divided into two groups (n = 12/each) and submitted to two trials. Group 1 was initially exposed to the 3D object and after 1 week to its photograph. Group 2 was first presented the picture and only tested with the real object 1 week later. All 15-min trials were divided into three consecutive 5-min intervals: pre-exposure, exposure and post-exposure. In the presence of the 3D snake object, regardless of its presentation order, the frequency of direct gazes, head-cocks, tsik-tsik alarm/mobbing calls and genital displays increased significantly. The photograph induced a similar response, although only when the object had been previously presented, as significantly higher levels of these behaviors were seen in Group 1 than Group 2. Proximity to the stimulus, aerial scan, terrestrial glance, displacement activities and locomotion were not consistently influenced by the stimuli’s presence and/or order of presentation. Therefore, marmosets recognized and responded appropriately to biologically and emotionally relevant 3D and 2D stimuli. Since the aversive/fearful reactions toward the photograph were only seen after the snake object had been presented, the former seems to be essentially a learned response.     

The role of comparison in preschoolers’ novel object categorization

We examined the role of the comparison process and shared names on preschoolers’ categorization of novel objects. In our studies, 4-year-olds were presented with novel object sets consisting of either one or two standards and two test objects: a shape match and a texture match. When children were presented with one standard, they extended the category based on shape regardless of whether the objects were named. When children were presented with two standards that shared the same texture and the objects were named with the same noun, they extended the category based on texture. The opportunity to compare two standards, in the absence of shared names, led to an attenuation of the effect of shape. These findings demonstrate that comparison plays a critical role in the categorization of novel objects and that shared names enhance this process.     

Border collie comprehends sentences containing a prepositional object,verb, and direct object

This study tested the ability of a Border Collie, Chaser, to learn the syntax and semantics of sentences consisting of three elements of grammar, a prepositional object, verb, and direct object. Understanding of the syntax of the sentences required that Chaser emit responses consistent with three elements of grammar sentences, such as to ball take Frisbee. Understanding of the semantics of the sentences required that Chaser respond correctly when the meanings of the sentences were changed by reversing positions of the prepositional object and the direct object in the sentence, such as to Frisbee take ball. Chaser's understanding of the sentences was tested in three different scenarios: (a) when multiple and familiar objects were used in the syntax command sentence, (b) when novel objects were used in the syntax command sentence (novel in the sense that objects had not been used during training), and (c) when vision of objects was not possible at the time the syntax command was verbalized. Findings were statistically significant in all three scenarios. Successful findings were attributed to Chaser's intensive training in her first three years of life. Analysis of the data revealed that Chaser's successful understanding of the syntax sentences required the processing and retention of two sound-object mappings (names-objects) into memory, along with simultaneous judgments concerning which object to take to the other – that is, working memory. These two types of cognitive abilities, memory storage and working memory, raise the bar in terms of our expectations of a dog's potential ability to understand verbal communications. We propose that Chaser's understanding of our three elements of grammar sentences represents a giant leap in her referential understanding of language.