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.     

Meaning attribution in the West African green monkey: influence of call type and context

The search for the evolutionary roots of human language has fuelled much research into the cognitive mechanisms underlying communication in nonhuman animals. One core issue has been whether the context-specific calls of nonhuman animals are meaningful, with call meaning inferred from recipients’ responses in the absence of supporting contextual cues. This direct inference may well offer an oversimplified view of how vocalisations are perceived, however, as responses under natural conditions are likely guided by contextual cues as well as by the signal. In this study, we investigate how the anti-predator responses of green monkeys, Chlorocebus sabaeus, are affected by alarm call structure and by context. We first simulated the presence of leopards and snakes to elicit alarm vocalisations and to identify predator-typical response behaviours. In both contexts, the monkeys produced chirp calls that revealed only graded variation in relation to predator type. We then carried out playback experiments to explore whether green monkeys would respond with predator-typical behaviour to leopard and snake chirps, and whether contextual cues, in the form of pre-exposure to a leopard or snake model, would modify these responses. Irrespective of context, subjects were more likely to respond to leopard chirps with a leopard-typical response. Predator priming did not have a significant effect on the type of response, but, together with call type, did affect response duration. This suggests that the immediate attribution of meaning was influenced by acoustic cues, whilst receiver’s prior knowledge was incorporated to guide subsequent behaviour.     

Comparing responses of four ungulate species to playbacks of baboon alarm calls

A growing body of evidence suggests that a wide range of animals can recognize and respond appropriately to calls produced by other species. Social learning has been implicated as a possible mechanism by which heterospecific call recognition might develop. To examine whether familiarity and/or shared vulnerability with the calling species might influence the ability of sympatric species to distinguish heterospecific alarm calls, we tested whether four ungulate species (impala: Aepyceros melampus; tsessebe: Damaliscus lunatus; zebra: Equus burchelli; wildebeest: Connochaetes taurinus) could distinguish baboon (Papio hamadryas ursinus) alarm calls from other loud baboon calls produced during intra-specific aggressive interactions (‘contest’ calls). Overall, subjects’ responses were stronger following playback of alarm calls than contest calls. Of the species tested, impala showed the strongest responses and the greatest difference in composite response scores, suggesting they were best able to differentiate call types. Compared with the other ungulate species, impala are the most frequent associates of baboons. Moreover, like baboons, they are susceptible to both lion and leopard attacks, whereas leopards rarely take the larger ungulates. Although it seems possible that high rates of association and/or shared vulnerability may influence impala’s greater ability to distinguish among baboon call types, our results point to a stronger influence of familiarity. Ours is the first study to compare such abilities among several community members with variable natural histories, and we discuss future experiments that would more systematically examine development of these skills in young ungulates.     

Rhesus macaques (Macaca mulatta) monitor uncertainty during numerosity judgments

Two rhesus macaques (Macaca mulatta) judged arrays of dots on a computer screen as having more or fewer dots than a center value that was never presented in trials. After learning a center value, monkeys were given an uncertainty response that let them decline to make the numerosity judgment on that trial. Across center values (3-7), errors occurred most often for sets adjacent in numerosity to the center value. The monkeys also used the uncertainty response most frequently on these difficult trials. A 2nd experiment showed that monkeys' responses reflected numerical magnitude and not the surface-area illumination of the displays. This research shows that monkeys' uncertainty-monitoring capacity extends to the domain of numerical cognition. It also shows monkeys' use of the purest uncertainty response possible, uncontaminated by any secondary motivator.     

Interference effects by spatial proximity and age-related declines in spatial memory by Japanese monkeys (Macaca fuscata): deficits in the combined use of multiple spatial cues

Spatial information processing was assessed in 3 young (4-10 years old) and 4 aged (24-25 years old) Japanese monkeys (Macaca fuscata) on 3 delayed nonmatching-to-position (DNMP) tests with relatively short delays of 5 s. Each test had 3 conditions of different horizontal distances between sample and to-be-nonmatched positions. Experiment 1 demonstrated that the performance on the DNMP test in both age groups was impaired when 2 stimulus positions were located next to each other; however, it was fairly accurate when they were located farther apart, suggesting that interference is introduced by spatial proximity. Experiment 2 revealed age-related differences in the situation in which an additional spatial cue, depth information, was available by extending the stimulus array of the DNMP test to a 4 x 2 matrix. In this test, young monkeys performed accurately irrespective of position distance between stimuli, whereas the aged monkeys' performance remained the same as before. Experiment 3 confirmed that the recognition ability in aged monkeys was well preserved on DNMP tests with different objects. These patterns of results indicate that the ability to use information from multiple spatial cues is not accessible to the aged monkeys.     

Prototype abstraction by monkeys (Macaca mulatta)

The authors analyze the shape categorization of rhesus monkeys (Macaca mulatta) and the role of prototype- and exemplar-based comparison processes in monkeys' category learning. Prototype and exemplar theories make contrasting predictions regarding performance on the Posner-Homa dot-distortion categorization task. Prototype theory--which presumes that participants refer to-be-categorized items to a representation near the category's center (the prototype)--predicts steep typicality gradients and large prototype-enhancement effects. Exemplar theory--which presumes that participants refer to-be-categorized items to memorized training exemplars-predicts flat typicality gradients and small prototype-enhancement effects. Across many categorization tasks that, for the first time, assayed monkeys' dot-distortion categorization, monkeys showed steep typicality gradients and large prototype-enhancement effects. These results suggest that monkeys--like humans--refer to-be-categorized items to a prototype-like representation near the category's center rather than to a set of memorized training exemplars.     

Reciprocal recognition of sifaka (<Emphasis Type="Italic">Propithecus verreauxi verreauxi</Emphasis>) and redfronted lemur (<Emphasis Type="Italic">Eulemur fulvus rufus</Emphasis>) alarm calls

Redfronted lemurs (Eulemur fulvus rufus) and Verreaux's sifakas (Propithecus verreauxi verreauxi) occur sympatrically in western Madagascar. Both species exhibit a so-called mixed alarm call system with functionally referential alarm calls for raptors and general alarm calls for carnivores and raptors. General alarm calls also occur in other contexts associated with high arousal, such as inter-group encounters. Field playback experiments were conducted to investigate whether interspecific recognition of alarm calls occurs in both species, even though the two species rarely interact. In a crossed design, redfronted lemur and sifaka alarm calls were broadcast to individuals of both species, using the alarm call of chacma baboons (Papio cynocephalus) as a control. Both species responded with appropriate escape strategies and alarm calls after playbacks of heterospecific aerial alarm calls. Similarly, they reacted appropriately to playbacks of heterospecific general alarm calls. Playbacks of baboon alarm calls elicited no specific responses in either lemur species, indicating that an understanding of interspecific alarm calls caused the responses and not alarm calls in general. Thus, the two lemur species have an understanding of each other's aerial as well as general alarm calls, suggesting that even in species that do not form mutualistic associations and rarely interact, common predator pressure has been sufficient for the development of heterospecific call recognition.     

Representation of serial order in monkeys (Cebus apella)

Cebus monkeys were trained on a five-item serial learning task, symbolized as ABCDE; the initial stages of training were on the shorter subseries AB, ABC, and ABCD. To assess the monkeys' knowledge of the sequential position of each item, pair-wise tests were given to 2 subjects after acquisition of the ABCD series and to 4 subjects after reaching criterion on the ABCDE series. In both tests, the monkeys performed at high levels on the interior pairs, which were BC for the ABCD series, and BC, BD, and CD for the ABCDE series. These results, as well as the orderly relations observed in the pair-wise tests between first-item response latency and first-item position and between second-item response latency and number of missing items, indicated that the monkeys had developed a well-organized internal representation of the four- and five-item series. Although pigeons are also capable of learning four-item and five-item series, they apparently do not develop a comparable representational structure. The disparity between the monkeys' and pigeons' representational competence for serial order is predictable from the difference in their capacities for associative transitivity.     

Change detection by rhesus monkeys (Macaca mulatta) and pigeons (Columba livia)

Two monkeys (Macaca mulatta) learned a color change-detection task where two colored circles (selected from a 4-color set) were presented on a 4 × 4 invisible matrix. Following a delay, the correct response was to touch the changed colored circle. The monkeys' learning, color transfer, and delay transfer were compared to a similar experiment with pigeons. Monkeys, like pigeons (Columba livia), showed full transfer to four novel colors, and to delays as long as 6.4 s, suggesting they remembered the colors as opposed to perceptual based attentional capture process that may work at very short delays. The monkeys and pigeons were further tested to compare transfer with other dimensions. Monkeys transferred to shape and location changes, unlike the pigeons, but neither species transferred to size changes. Thus, monkeys were less restricted in their domain to detect change than pigeons, but both species learned the basic task and appear suitable for comparative studies of visual short-term memory. (PsycINFO Database Record (c) 2012 APA, all rights reserved).     

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.     

Recognition of heterospecific alarm vocalizations by bonnet macaques (Macaca radiata)

Recognition of heterospecific alarm vocalizations is an essential component of antipredator behavior in several prey species. The authors examined the role of learning in the discrimination of heterospecific vocalizations by wild bonnet macaques (Macaca radiata) in southern India The bonnet macaques' flight and scanning responses to playbacks of their own alarm vocalizations were compared with their responses to playbacks of vocalizations of Nilgiri langurs (Trachypithecus johnii), Hanuman langurs (Semnopithecus entellus), and sambar deer (Cervus unicolor). The study was conducted in 3 regions that differed in the frequency with which bonnet macaques encountered these species and included an urban setting. Call recognition was highest in adults and in regions where individuals were frequently exposed to the calling species; calls were not recognized by urban monkeys. Thus, age and experience are important factors in heterospecific call recognition by bonnet macaques.     

Strategic behavior in monkeys

In a recent paper, Lee et al. examined adaptive decision-making processes by training monkeys to play a competitive game against a computer programmed to play using various strategies. They found that the monkeys' responses were sensitive to the computer's strategies and consistent with reinforcement learning. Research such as this strongly complements current research in behavioral economics. We propose some potential future directions for this work, and put forward conjectures about what might be learned about decision-making in humans.     

Redundant food searches by capuchin monkeys (Cebus apella): a failure of metacognition?

This study investigated capuchin monkeys' understanding of their own visual search behavior as a means to gather information. Five monkeys were presented with three tubes that could be visually searched to determine the location of a bait. The bait's visibility was experimentally manipulated, and the monkeys' spontaneous visual searches before tube selection were analyzed. In Experiment 1, three monkeys selected the baited tube significantly above chance; however, the monkeys also searched transparent tubes. In Experiment 2, a bent tube in which food was never visible was introduced. When the bent tube was baited, the monkeys failed to deduce the bait location and responded randomly. They also continued to look into the bent tube despite not gaining any pertinent information from it. The capuchin monkeys' behavior contrasts with the efficient employment of visual search behavior reported in humans, apes and macaques. This difference is consistent with species-related variations in metacognitive abilities, although other explanations are also possible.     

Dynamic response-by-response models of matching behavior in rhesus monkeys

We studied the choice behavior of 2 monkeys in a discrete-trial task with reinforcement contingencies similar to those Herrnstein (1961) used when he described the matching law. In each session, the monkeys experienced blocks of discrete trials at different relative-reinforcer frequencies or magnitudes with unsignalled transitions between the blocks. Steady-state data following adjustment to each transition were well characterized by the generalized matching law; response ratios undermatched reinforcer frequency ratios but matched reinforcer magnitude ratios. We modelled response-by-response behavior with linear models that used past reinforcers as well as past choices to predict the monkeys' choices on each trial. We found that more recently obtained reinforcers more strongly influenced choice behavior. Perhaps surprisingly, we also found that the monkeys' actions were influenced by the pattern of their own past choices. It was necessary to incorporate both past reinforcers and past choices in order to accurately capture steady-state behavior as well as the fluctuations during block transitions and the response-by-response patterns of behavior. Our results suggest that simple reinforcement learning models must account for the effects of past choices to accurately characterize behavior in this task, and that models with these properties provide a conceptual tool for studying how both past reinforcers and past choices are integrated by the neural systems that generate behavior.     

Social processes in communication and cognition in callitrichid monkeys: a review

Studies of vocal development in nonhuman primates have found little evidence for plasticity in vocal production, somewhat more for usage of calls, with the greatest plasticity arising in response to calls of others. Generally, similar results were obtained with callitrichid monkeys, the marmosets and tamarins, but with several interesting exceptions. Infant pygmy marmosets show babbling behavior with improvement in adult call structure related to the amount and diversity of babbling. Adult marmosets alter call structure in response to changes in social partners, and wild marmosets have vocal dialects and modify call structure according to how far they are from other group members, suggesting the potential to modify call structure in different social and environmental contexts, though direct learning of novel vocalizations has not been observed. Infant cotton-top tamarins do not produce adult-like calls in appropriate contexts, at least in the first few months of life, but through food sharing from adults infants learn about appropriate foods and the appropriate contexts for food vocalizations. Tamarins modify call structure and usage with changes in social status. Tamarins, unlike other monkeys tested, can learn to avoid noxious foods through observation of other group members, and can learn about novel food locations. Recent studies provide evidence of contextual imitation in marmosets. The plasticity in vocal communication and evidence of social learning in marmosets and tamarins relative to other monkeys may be related to the cooperative breeding system of marmosets and tamarins. With a high degree of behavioral coordination among group members, there is a priority on monitoring signals and behavior of others and adjusting one's own signals and behavior. This creates the context for vocal plasticity and social learning. Accepted after revision: 23 May 2001 Electronic Publication     

Asymmetry of attentional set in rhesus monkeys learning colour and shape discriminations

We trained rhesus monkeys on six visual discrimination problems using stimuli that varied in both shape and colour. For one group of animals shape was always relevant in these six problems, and colour always irrelevant, and for the other animals vice versa. During these "intradimensional shifts" (ID) the problems were learned at equal rates by the two groups, shape-relevant and colour-relevant. We then trained three further problems in which the other dimension was now relevant ("extradimensional shifts", ED). The animals showed slower learning when shifting from colour-relevant to shape-relevant, but not when shifting from shape-relevant to colour-relevant. These results show that monkeys' ability to selectively attend to a relevant stimulus dimension and to ignore an irrelevant dimension depends on the experimenter's choice of relevant and irrelevant dimensions.     

Discrimination of artificial polymorphous categories by rhesus monkeys (Macaca mulatta)

Monkeys (Macaca mulatta) were trained to discriminate between sets of artificial stimuli such as those used by Jitsumori (1993) for pigeons and humans. The stimuli were arrays of symbols differing along three two-valued (positive or negative) dimensions. The discrimination required was between polymorphous categories in which a positive stimulus was defined by possession of any 2 out of 3 positive features. Of the 5 monkeys, 3 learned the discrimination much faster than did pigeons, but transfer to novel stimuli was less impressive than had been shown in pigeons. The 3 monkeys showed high levels of transfer to the stimuli that contained either all 3 positive or all 3 negative features, but 2 of the 3 monkeys failed to show transfer to stimuli that had 1 of the 3 features replaced with a novel one. Analysis of the monkeys' performance raised doubts on the additive integration of features but supported learning of feature combinations as a basis for the discrimination of polymorphous categories by this species.     

Juvenile vervet monkeys rely on others when responding to danger

Animal Cognition - Primate alarm calls are mainly hardwired but individuals need to adapt their calling behaviours according to the situation. Such learning necessitates recognising locally...     

Mother knows best: functionally referential alarm calling in white-tailed ptarmigan

Functionally referential alarm calls have stimulus specificity, distinct acoustic structure, and elicit different escape responses that are appropriate to the threat. The mechanisms by which escape responses are evoked are not fully understood and may range from eliciting innate responses to conveying representational information. White-tailed ptarmigan (Lagopus leucurus) are a long-lived alpine tundra grouse, which are preyed upon by aerial and terrestrial predators. We investigated the hypothesis that alarm calls of ptarmigan hens with chicks are functionally referential. We recorded hens’ alarm calls in response to naturally occurring and model predators in California’s Sierra Nevada alpine tundra for two summer seasons. We conducted playback experiments in the field to determine chick responses to alarm calls. Alarm calls commenced with an extended ‘alerting’ note followed by a series of staccato notes grouped into elements. Fundamental and dominant frequencies in element notes were significantly higher in terrestrial compared to aerial threat alarm calls. Playbacks of terrestrial threat alarm calls elicited an upright/alert position by chicks (75 % of responses). In response to aerial threat alarm call playbacks, chicks flattened to the ground and froze (80 % of responses). To our knowledge, this study provides the first empirical evidence of functionally referential alarm calling, including the responses of the receivers, in an avian species in the wild.