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.     

Silhouettes elicit alarm calls from captive vervet monkeys (Cercopithecus aethiops).

In Part 1, we analyzed alarm calls produced by captive vervets (Cercopithecus aethiops) in response to naturally occurring stimuli. Females and juveniles regularly alarm called to airplanes, birds, and barking dogs. Juvenile females accounted for 60% of these alarm calls. In Part 2, we isolated several monkeys from the colony and presented them with life-sized silhouettes of a leopard, snake, eagle, baboon, vervet, and goose. Adult monkeys alarm called more than did juveniles. Alarm calls were elicited by leopard, snake, baboon, and vervet silhouettes, but none were elicited by eagle or goose silhouettes. Some leopard and snake alarm calls matched those recorded in the wild in the context of the vervets' natural predators. Results indicate that silhouette stimuli are a useful technique for eliciting monkey vocalizations in the laboratory.     

Operant conditioning of autogrooming in vervet monkeys: Cercopithecus aethiops

Vervet monkeys received food reinforcement contingent on autogrooming. Experiment 1 reinforced grooming on a schedule of increasing intermittency and grooming increased in frequency and duration; with only pauses reinforced, grooming decreased in frequency and duration. Experiment 2 demonstrated differentiation of operant autogrooming; in each session a different single form of grooming was reinforced (for example, grooming the tail only), and that form increased in frequency while other forms became less frequent. In Experiment 3 scratching was succesfully conditioned with a method that selectively reinforced variety in behavior; reinforcement was contingent on a shift in scratching form. In Experiment 4, with no contingencies on grooming, a prefood stimulus did not increase autogrooming whether or not grooming had previously resulted in contingent reinforcement. The form of conditioned autogrooming resembled the form of unconditioned autogrooming. The discussion suggests how reinforcement principles can account for changes in the topography of operant behavior.     

Hand preferences in unimanual and bimanual feeding by wild vervet monkeys (Cercopithecus aethiops)

Lateral preference was examined in spontaneous feeding actions in 2 troops of wild vervet monkeys (Cercopithecus aethiops). Processing of 4 foods (termites, leaf shoots, sugarcane, and fruit) was studied. Actions included unimanual reaching to moving objects, operating from an unstable posture, and coordinated bimanual processing. Between 19 and 31 subjects were available, according to the task. In 2 tasks, laterality of 2 independent stages was measured separately, giving 6 measures in all. On 4 of these measures, most monkeys were ambipreferent, and only a few showed significant hand preferences. Only for termite feeding and detaching material from fruits did the majority show significant lateralization; no tasks elicited exclusive use of 1 hand. Preference appeared labile, because in 2 tasks, population trends reversed with increasing age. No population trends to left or right were found; instead, these monkeys showed ambilaterality, with lateralization associated with task complexity.     

Absolute auditory thresholds in three Old World monkey species (Cercopithecus aethiops, C. neglectus, Macaca fuscata) and humans (Homo sapiens)

We investigated the absolute auditory sensitivities of three monkey species (Cercopithecus aethiops, C. neglectus, and Macaca fuscata) and humans (Homo sapiens). Results indicated that species-typical variation exists in these primates. Vervets, which have the smallest interaural distance of the species that we tested, exhibited the greatest high-frequency sensitivity. This result is consistent with Masterton, Heffner, and Ravizza's (1969) observations that head size and high-frequency acuity are inversely correlated in mammals. Vervets were also the most sensitive in the middle frequency range. Furthermore, we found that de Brazza's monkeys, though they produce a specialized, low-pitched boom call, did not show the enhanced low-frequency sensitivity that Brown and Waser (1984) showed for blue monkeys (C. mitis), a species with a similar sound. This discrepancy may be related to differences in the acoustics of the respective habitats of these animals or in the way their boom calls are used. The acuity of Japanese monkeys was found to closely resemble that of rhesus macaques (M. mulatta) that were tested in previous studies. Finally, humans tested in the same apparatus exhibited normative sensitivities. These subjects responded more readily to low frequencies than did the monkeys but rapidly became less sensitive in the high ranges.     

The comparative psychology of same-different judgments by humans (Homo sapiens) and monkeys (Macaca mulatta)

The authors compared the performance of humans and monkeys in a Same-Different task. They evaluated the hypothesis that for humans the Same-Different concept is qualitative, categorical, and rule-based, so that humans distinguish 0-disparity pairs (i.e., same) from pairs with any discernible disparity (i.e., different); whereas for monkeys the Same-Different concept is quantitative, continuous, and similarity-based, so that monkeys distinguish small-disparity pairs (i.e., similar) from pairs with a large disparity (i.e., dissimilar). The results supported the hypothesis. Monkeys, more than humans, showed a gradual transition from same to different categories and an inclusive criterion for responding Same. The results have implications for comparing Same-Different performances across species--different species may not always construe or perform even identical tasks in the same way. In particular, humans may especially apply qualitative, rule-based frameworks to cognitive tasks like Same-Different.     

Perception of cliff swallow calls by birds (Hirundo pyrrhonota and Sturnus vulgaris) and humans (Homo sapiens).

We tested for species differences in the perception of the cliff swallow chick begging call. One cliff swallow (Hirundo pyrrhonota), 3 European starling (Sturnus vulgaris), and 3 human (Homo sapiens) subjects were trained on go-no-go or repeating background tasks to discriminate between all possible stimulus pairs, measured by percentage of correct response and latency. We used multidimensional scaling to convert the similarity measures into a 2-dimensional map for each subject. Most of the maps were significantly correlated in Dimension 1 but not in Dimension 2. A cluster analysis separated bird and human maps. To identify the most important acoustic cues for each subject, we regressed the coordinates of each dimension on acoustic variables measured from the stimuli. For all subjects, center frequency was Dimension 1. Different acoustic cues were associated with Dimension 2, with agreement only on bandwidth, by the cliff swallow and 1 starling.     

Mechanisms of inferential order judgments in humans (Homo sapiens) and rhesus monkeys (Macaca mulatta)

If A > B, and B > C, it follows logically that A > C. The process of reaching that conclusion is called transitive inference (TI). Several mechanisms have been offered to explain transitive performance. Scanning models claim that the list is scanned from the ends of the list inward until a match is found. Positional discrimination models claim that positional uncertainty accounts for accuracy and reaction time patterns. In Experiment 1, we trained rhesus monkeys (Macaca mulatta) and humans (Homo sapiens) on adjacent pairs (e.g., AB, BC, CD, DE, EF) and tested them with previously untrained nonadjacent pairs (e.g., BD). In Experiment 2, we trained a second list and tested with nonadjacent pairs selected between lists (e.g., B from List 1, D from List 2). We then introduced associative competition between adjacent items in Experiment 3 by training 2 items per position (e.g., B?C?, B?C?) before testing with untrained nonadjacent items. In all 3 experiments, humans and monkeys showed distance effects in which accuracy increased, and reaction time decreased, as the distance between items in each pair increased (e.g., BD vs. BE). In Experiment 4, we trained adjacent pairs with separate 9- and 5-item lists. We then tested with nonadjacent pairs selected between lists to determine whether list items were chosen according to their absolute position (e.g., D, 5-item list > E, 9-item list), or their relative position (e.g., D, 5-item list < E, 9-item list). Both monkeys' and humans' choices were most consistent with a relative positional organization.     

Rational maximizing by humans (Homo sapiens) in an ultimatum game

In the human mini-ultimatum game, a proposer splits a sum of money with a responder. If the responder accepts, both are paid. If not, neither is paid. Typically, responders reject inequitable distributions, favoring punishing over maximizing. In Jensen et al.’s (Science 318:107–109, 2007) adaptation with apes, a proposer selects between two distributions of raisins. Despite inequitable offers, responders often accept, thereby maximizing. The rejection response differs between the human and ape versions of this game. For humans, rejection is instantaneous; for apes, it requires 1 min of inaction. We replicate Jensen et al.’s procedure in humans with money. When waiting 1 min to reject, humans favor punishing over maximizing; however, when rejection requires 5 min of inaction, humans, like apes, maximize. If species differences in time horizons are accommodated, Jensen et al.’s ape data are reproducible in humans.     

Individual differences in response to a stranger: social impulsivity as a dimension of temperament in vervet monkeys (Cercopithecus aethiops sabaeus)

Social impulsivity in response to a stranger was assessed in male vervet monkeys (Cercopithecus aethiops sabaeus) using the Intruder Challenge Test. Vervets (N = 128, ages 3-18 years) were presented with an unfamiliar adult male at the periphery of the home enclosure. An index of impulsivity reflecting variation in the tendency to rapidly approach, engage, and challenge the intruder was derived from factor analysis of behavioral responses. Scale reliability (alpha = .84) and test-retest consistency (intraclass correlation = .83) were high, indicating that this index reliably and efficiently measures a stable aspect of temperament from impulsive to inhibited. Impulsivity scores peaked at age 4, when vervet males typically emigrate from the natal group. The highest ranking males in each group were more likely to score in the moderate range, whereas lower ranking males were more likely to score in the highest (impulsive) or lowest (inhibited) quartiles.     

Detection of grouped and ungrouped parts in visual patterns by tufted capuchin monkeys (Cebus apella) and humans (Homo sapiens)

The authors investigated perceptual grouping in capuchin monkeys (Cebus apella) and humans (Homo sapiens). In Experiment 1, 6 monkeys received a visual pattern as the sample and had to identify the comparison stimulus featuring some of its parts. Performance was better for ungrouped parts than for grouped parts. In Experiment 2, the sample featured the parts, and the comparison stimuli, the complex figures: The advantage for ungrouped elements disappeared. In Experiment 3, in which new stimuli were introduced, the results of the previous experiments were replicated. In Experiment 4, 128 humans were presented with the same tasks and stimuli used with monkeys. Their accuracy was higher for grouped parts. Results suggest that human and nonhuman primates use different modes of analyzing multicomponent patterns.     

Flexible serial response learning by pigeons (Columba livia) and humans (Homo sapiens)

Experimental tasks designed to involve procedural memory are often rigid and unchanging, despite many reasons to expect that implicit learning processes can be flexible and support considerable variability. A version of the serial response time (SRT) task was developed, in which the locations of targets were probabilistically determined. Targets appeared in locations according to both a structured sequence and a cue validity parameter, and the time to respond to each target was measured. Pigeons (Columba livia) and humans (Homo sapiens) both showed response time facilitation at the highest tested value for cue validity, and the magnitude of that facilitation gradually weakened as cue validity was decreased. Both species showed evidence that response times were largely determined by the local predictabilities of individual cue locations. In addition, humans showed some evidence that explicit knowledge of the sequence affected response times, specifically when cue validity was 100%.     

Time preferences in long-tailed macaques (Macaca fascicularis) and humans (Homo sapiens)

Rosati et al. (Curr Biol 17(19):1663–1668, 2007) found in a self-control test in which choice was between a smaller, immediately delivered food and a larger, delayed food, that chimpanzees preferred the larger reward (self-control); humans, however, preferred the smaller reward (impulsivity). They attributed their results to a species difference in self-control. In Experiment 1, monkeys (long-tailed macaques) were exposed to a self-control task in two conditions: where the food was hidden under differently colored bowls and where it was visible. When these two conditions were compared, choice shifted from greater preference for the impulsive alternative in the hidden condition to greater preference for the self-control alternative in the visible condition. Additionally, in both conditions, preference shifted from self-control to impulsivity over sessions. These results were explained in terms of the reversed-contingency effect (a propensity to reach for more over less when rewards are visible) and not to a capacity for self-control. In Experiment 2, humans that demonstrated preference for more over less in choice preferred the impulsive alternative when choice to either alternative was followed by the same intertrial interval—a preference that accelerates trial rates relative to preference of the self-control alternative. When trial rates were equated so that neither choice accelerated session’s end, humans demonstrated self-control. These results suggest that Rosati et al.’s demonstration of impulsivity in humans was due to participants’ desire to minimize session time.     

The role of propulsive muscles of the shoulder during quadrupedalism in vervet monkeys (Cercopithecus aethiops): implications for neural control of locomotion in primates

In comparative anatomical studies of the shoulder, the humeral retractors are often grouped together as propulsive muscles, which are important in the propulsive stroke of the forelimb during quadrupedal locomotion. Electromyographic (EMG) analyses of these muscles in opossums, cats, and dogs in general have confirmed such conclusions. An EMG study of chimpanzee shoulder muscles during knuckle-walking found, however, that the humeral retractors are either inactive or perform a function unrelated to propulsion (Larson & Stern, 1987). This contrast in muscle recruitment patterns between chimpanzees and more "typical" mammalian quadrupeds was attributed to the derived morphology of the chimpanzee shoulder. The present study examines the activity patterns of the humeral retractors in the vervet monkey, a primate more closely resembling nonprimate mammals in its shoulder morphology. The results of this EMG analysis show that despite the significant differences in anatomy between chimpanzees and vervets, the two species display very similar muscle recruitment patterns during quadrupedalism, and there is evidence for this same pattern in other species of primates. These differences in muscle activity patterns between primates and nonprimate mammals may be related to changes in the neurological control of locomotion in primates due to the evolutionary development of manipulative abilities in the primate forelimb.     

Enumeration of briefly presented items by the chimpanzee (Pan troglodytes) and humans (Homo sapiens)

In this study, we compared the performances on an enumeration task (numerical labeling task) of 1 chimpanzee (Pan troglodytes) and 4 humans. In this task, two types of trials, with different exposure durations of the sample that was to be enumerated, were used. In the unlimited-exposure trials, the sample remained on until the subject made a choice. In the brief-exposure trials, the sample was presented for 100 msec and then was masked. The results show clear differences between the different species. The main differences had to do with accuracy during the unlimited trials and response times during the brief trials. Detailed analyses of the pattern of response times for the chimpanzee and of looking-back behavior during the task suggests that the enumeration process underlying the subject's performance was not counting but estimation.     

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

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

Cognitive maps not used by humans (Homo sapiens) during a dynamic navigational task

To account for the impressive navigational ability of animals, some researchers have suggested that animals might use a cognitive map. Two groups of human participants (Homo sapiens) were tested for cognitive mapping using procedures similar to those used by B. M. Gibson and A. C. Kamil (2001). Participants who had to acquire spatial information about a hidden goal from the experimental contingencies alone showed patterns of search most like nutcrackers in the companion study (B. M. Gibson & A. C. Kamil, 2001). Surprisingly, postexperimental questionnaires revealed that most participants used an alternative strategy of vector integration rather than cognitive mapping during search for the hidden goal. The current study and its companion indicate that some simpler mechanisms of navigation are flexible enough to account for what appears to be map-based behavior in human and nonhuman species.     

Perception of emergent configurations in humans (Homo sapiens) and chimpanzees (Pan troglodytes)

We examined the perceptions of emergent configurations in humans and chimpanzees using a target-localization task. The stimulus display consisted of a target placed among multiple identical distractors. The target and distractors were presented either solely, within congruent contexts in which salient configurations emerge, or within incongruent contexts in which salient configurations do not emerge. We found that congruent contexts had similar facilitative effects on target localization by humans and chimpanzees, whereas similar disruptive effects emerged when the stimuli were presented within incongruent contexts. When display size was manipulated, targets under the congruent-context condition were localized in a parallel manner, but those under the no-context and incongruent-context conditions were localized in a serial manner by both species. These results suggest that both humans and chimpanzees perceive emergent configurations when targets and distractors are presented within certain congruent contexts and that they process such emergent configurations preattentively.     

Olfactory discrimination of mouse strains (Mus musculus) and major histocompatibility types by humans (Homo sapiens)

A series of experiments revealed that humans can use olfaction to discriminate closely related strains of mice, differing genetically only at the major histocompatibility gene complex (H-2). In Experiment 1, subjects were asked to distinguish between the whole-body odors of live mice. In Experiments 2 and 3, the odor source was mouse fecal pellets, and in Experiments 4 and 5, the odor source was mouse urine.