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.     

Causal cognition in a non-human primate: field playback experiments with Diana monkeys

Crested guinea fowls (Guttera pucherani) living in West African rainforests give alarm calls to leopards (Panthera pardus) and sometimes humans (Homo sapiens), two main predators of sympatric Diana monkeys (Cercopithecus diana). When hearing these guinea fowl alarm calls, Diana monkeys respond as if a leopard were present, suggesting that by default the monkeys associate guinea fowl alarm calls with the presence of a leopard. To assess the monkeys' level of causal understanding, I primed monkeys to the presence of either a leopard or a human, before exposing them to playbacks of guinea fowl alarm calls. There were significant differences in the way leopard-primed groups and human-primed groups responded to guinea fowl alarm calls, suggesting that the monkeys' response was not directly driven by the alarm calls themselves but by the calls' underlying cause, i.e. the predator most likely to have caused the calls. Results are discussed with respect to three possible cognitive mechanisms - associative learning, specialized learning programs, and causal reasoning - that could have led to causal knowledge in Diana monkeys.     

Call combinations in monkeys: compositional or idiomatic expressions?

Syntax is widely considered the feature that most decisively sets human language apart from other natural communication systems. Animal vocalisations are generally considered to be holistic with few examples of utterances meaning something other than the sum of their parts. Previously, we have shown that male putty-nosed monkeys produce call series consisting of two call types in response to different events. They can also be combined into short sequences that convey a different message from those conveyed by either call type alone. Here, we investigate whether ‘pyow-hack’ sequences are compositional in that the individual calls contribute to their overall meaning. However, the monkeys behaved as if they perceived the sequence as an idiomatic expression rather than decoding the sequence. Nonetheless, while this communication system lacks the generative power of syntax it enables callers to increase the number of messages that can be conveyed by a small and innate call repertoire.     

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.     

Context-related call combinations in female Diana monkeys

Non-human primates possess species-specific repertoires of acoustically distinct call types that can be found in adults in predictable ways. Evidence for vocal flexibility is generally rare and typically restricted to acoustic variants within the main call types or sequential production of multiple calls. So far, evidence for context-specific call sequences has been mainly in relation to external disturbances, particularly predation. In this study, we investigated extensively the vocal behaviour of free-ranging and individually identified Diana monkeys in non-predatory contexts. We found that adult females produced four vocal structures alone (‘H’, ‘L’, ‘R’ and ‘A’ calls, the latter consisting of two subtypes) or combined in non-random ways (‘HA’, ‘LA’ and ‘RA’ call combinations) in relation to ongoing behaviour or external events. Specifically, the concatenation of an introductory call with the most frequently emitted and contextually neutral ‘A’ call seems to function as a contextual refiner of this potential individual identifier. Our results demonstrate that some non-human primates are able to increase the effective size of their small vocal repertoire not only by varying the acoustic structure of basic call types but also by combining them into more complex structures. We have demonstrated this phenomenon for a category of vocalisations with a purely social function and discuss the implications of these findings for evolutionary theories of primate vocal communication.     

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     

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.     

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.     

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

In 2 experiments classification of synthetic versions of species-typical snake and eagle alarm calls by vervet monkeys (Cercopithecus aethiops) and human (Homo sapiens) control subjects was investigated. In a 2-choice, operant-conditioning-based procedure, this work followed up acoustic analyses that had used various digitally based algorithms (Owren & Bernacki, 1988). All subjects were first tested with alarm-call replicas that were based on analysis data. These models were classified in the same manner as natural stimuli, which verified the appropriateness of the acoustic characterizations. Synthetic stimuli were then presented to test the importance of specific acoustic cues. Spectral patterning was found to be the most salient cue for classification by the monkeys, whereas results from the human subjects were mixed. Implications for the study of nonhuman primate vocalizations and Lieberman's (1984) theory of speech evolution are discussed.     

Context-dependent alarm responses in wild vervet monkeys

Animal Cognition - The alarm calls of nonhuman primates are occasionally cited as functionally equivalent to lexical word meaning in human language. Recently, however, it has become increasingly...     

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.     

Prairie dog alarm calls encode labels about predator colors

Some animals have the cognitive capacity to differentiate between different species of predators and generate different alarm calls in response. However, the presence of any addition information that might be encoded into alarm calls has been largely unexplored. In the present study, three similar-sized human females walked through a Gunnison’s prairie dog (Cynomys gunnisoni) colony wearing each of three different-colored shirts: blue, green, and yellow. We recorded the alarm calls and used discriminant function analysis to assess whether the calls for the different-colored shirts were significantly different. The results showed that the alarm calls for the blue and the yellow shirts were significantly different, but the green shirt calls were not significantly different from the calls for the yellow shirt. The colors that were detected, with corresponding encoding into alarm calls, reflect the visual perceptual abilities of the prairie dogs. This study suggests that prairie dogs are able to incorporate labels about the individual characteristics of predators into their alarm calls, and that the complexity of information contained in animal alarm calls may be greater than has been previously believed.     

Effect of introducing novel configurational cues on a learned color discrimination in squirrel monkeys.

The study explored the effect of introducing novel cues on a learned color discrimination. 6 squirrel monkeys were initially trained to discriminate between plaques covered with green and brown construction paper. In a series of transfer tests, these color cues were then presented in 6 different patterns and varied in 4 sizes. The results indicate that some patterns will produce more disruption than others. Furthermore, reducing the size of the cues may also lead to a decrement in performance level. The outcome corresponds well with those of studies which show that contextual variables influence the acquisition of discriminative responses.     

Directedness and engagement in chimpanzee vocal ontogeny

Directedness and engagement during pre-verbal vocal communication play a major role in language development. What was their role in the evolution of language? This question invites us to examine these behaviours in chimpanzee vocal ontogeny. We collected observational data on infant (N = 15) and juvenile (N = 13) chimpanzees at Chimfunshi Wildlife Orphanage, Zambia. We examined the impact of age and vocalization type (grunts, whimpers, laughs and screams) on directed cues (gaze directedness and face directedness) and engagement (mutual face directedness) during vocal communication. We also assessed the impact of directed cues and engagement on social interactions by coding the behaviour of social partners before, during and after a vocalisation, and examining whether they contingently changed their behaviour in response to the vocalisation if it was directed or if engagement occurred. We found that face directed vocalisations showed a general increase during ontogeny and we observed call-type dependent effects of age for mutual face directedness. Only face directed vocalisations were significantly predictive of behavioural responses in social partners. We conclude that like young humans, young chimpanzees routinely exhibit directed behaviours and engagement during vocal communication. This social competency improves during ontogeny and benefits individuals by increasing the chances of eliciting behavioural responses from social partners. Directedness and engagement likely provide a foundation for language phylogenetically, as well as ontogenetically.

Research Highlights

• We show that directedness and engagement routinely occur during early chimpanzee vocalisations.
• Directedness increases throughout chimpanzee vocal ontogeny, similar to human infants.
• Directedness enhances social partner responsiveness, demonstrating a direct benefit to this style of communication.
• Directedness and engagement could provide a route towards language phylogenetically as well as ontogenetically.

     

Responses of white-faced capuchins (Cebus capucinus) to naturalistic and experimentally presented food-associated calls

In the context of foraging, many animal species produce specific calls that attract others. Researchers hypothesize that these vocalizations function to inform others about food; however, few studies have investigated whether food-associated calls alone are sufficient to cause individuals to respond as if they have been informed about food. Playback experiments on white-faced capuchins (Cebus capucinus) investigated whether listeners could infer the presence of food merely by hearing food-associated calls. Recipients looked significantly longer toward the call source and approached the speaker more often after hearing food-associated calls, as compared with control calls. Because these responses are not indicative of feeding, it is unclear whether listeners associated the calls with food. Nonetheless, these responses, specific to food-associated calls, may increase individuals' chances of finding food.     

Rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) remember agency information from past events and integrate this knowledge with spatial and temporal features in working memory

The purpose of the present study was to examine whether rhesus monkeys remember information about their own agency—along with spatial, temporal and contextual properties—from a previously experienced event. In Experiment 1, rhesus monkeys (n = 4) used symbols to reliably indicate whether they had performed or observed an event on a computer screen. In Experiment 2, naïve and experienced monkeys (n = 8) reported agency information when stringent controls for perceptual and proprioceptive cues were included. In Experiment 3, five of the monkeys completed a task in which they reported agency information along with spatial and temporal features of events. Two monkeys performed this agency discrimination when they could not anticipate which memory test they would receive. There was also evidence that these features were integrated in memory. Implications of this research are discussed in relation to working memory, episodic memory and self-awareness in nonhuman animals.     

Learning, memorizing and apparent forgetting of chemical cues from new predators by Iberian green frog tadpoles

Many antipredator adaptations are induced by the prey’s ability to recognize chemical cues from predators. However, predator recognition often requires learning by prey individuals. Iberian green frog tadpoles (Pelophylax perezi) have the ability to learn new potential predators. Here, we tested the memory capabilities of Iberian green frog tadpoles. We conditioned tadpoles with chemicals cues from a non-predatory fish in conjunction with conspecific alarm cues, and examined whether tadpoles retained their conditioned response (reduction of activity level). We found that conditioned tadpoles reduced their activity levels in subsequent exposures to the non-predatory fish cues alone. Tadpoles were able to remember this association and reduced movement rate at least for 9 days after. The ability to learn and memorize potential predators may be especially important for the survivorship of prey species that are likely to find a high variety of predators. However, after those 9 days, there was a lack of response to the non-predatory fish cues alone in the absence of reinforcement. This could be explained if tadpoles behave according to the threat-sensitive predator avoidance hypothesis, and the perceived risk to the learning cue diminished over time, or it could be due to an apparent forgetting process to avoid non-adaptative responses to chemical cues of non-dangerous species that were randomly paired with alarm cues. Thus, this study demonstrates that green frog tadpoles in the absence of reinforcement remember the chemical cues of a learned predator only for a limited time that may be adaptative in a threat-sensitive context.     

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.     

The response of guide dogs and pet dogs (Canis Familiaris) to cues of human referential communication (pointing and gaze)

The study raises the question of whether guide dogs and pet dogs are expected to differ in response to cues of referential communication given by their owners; especially since guide dogs grow up among sighted humans, and while living with their blind owners, they still have interactions with several sighted people. Guide dogs and pet dogs were required to respond to point, point and gaze, gaze and control cues of referential communication given by their owners. Results indicate that the two groups of dogs do not differ from each other, revealing that the visual status of the owner is not a factor in the use of cues of referential communication. Both groups of dogs have higher frequencies of performance and faster latencies for the point and the point and gaze cues as compared to gaze cue only. However, responses to control cues are below chance performance for the guide dogs, whereas the pet dogs perform at chance. The below chance performance of the guide dogs may be explained by a tendency among them to go and stand by the owner. The study indicates that both groups of dogs respond similarly in normal daily dyadic interaction with their owners and the lower comprehension of the human gaze may be a less salient cue among dogs in comparison to the pointing gesture.     

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.