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.     

Tufted titmouse (Baeolophus bicolor) calling and risk-sensitive foraging in the face of threat

Individuals often produce alarm or mobbing calls when they detect a threat such as a predator. Little is known about whether such calling is affected by the facial orientation of a potential threat, however. We tested for an effect of facial orientation of a potential threat on tufted titmice, Baeolophus bicolor, a songbird that uses chick-a-dee calls in a variety of social contexts. In two studies, a human observer wore an animal mask that either faced or faced away from the focal bird(s). In Study 1, focal birds were individual titmice captured in a walk-in trap, and the observer stood near the trapped bird. In Study 2, focal birds were titmouse flocks utilizing a feeding station and the observer stood near the station. In both studies, calling behavior was affected by mask orientation. In Study 2, foraging and agonistic behavior were also affected. Titmice can therefore perceive the facial orientation of a potential threat, and this perception affects different behavioral systems, including calling. Our results indicate sensitivity of titmice to the facial orientation of a potential predator in two quite different motivational contexts. This work suggests the possibility of strategic signaling by prey species depending upon the perceptual space of a detected predator.     

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.     

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.     

Responses of urban crows to con- and hetero-specific alarm calls in predator and non-predator zoo enclosures

Urban animals and birds in particular are able to cope with diverse novel threats in a city environment such as avoiding novel, unfamiliar predators. Predator avoidance often includes alarm signals that can be used also by hetero-specifics, which is mainly the case in mixed-species flocks. It can also occur when species do not form flocks but co-occur together. In this study we tested whether urban crows use alarm calls of conspecifics and hetero-specifics (jackdaws, Corvus monedula) differently in a predator and a non-predator context with partly novel and unfamiliar zoo animal species. Birds were tested at the Tiergarten Schönbrunn in the city of Vienna by playing back con- and hetero-specific alarm calls and control stimuli (great tit song and no stimuli) at predator (wolf, polar bear) and non-predator (eland antelope and cranes, peccaries) enclosures. We recorded responses of crows as the percentage of birds flying away after hearing the playback (out of those present before the playback) and as the number of vocalizations given by the present birds. A significantly higher percentage of crows flew away after hearing either con- or hetero-specific alarm calls, but it did not significantly differ between the predator and the non-predator context. Crows treated jackdaw calls just as crow calls, indicating that they make proper use of hetero-specific alarm calls. Responding similarly in both contexts may suggest that the crows were uncertain about the threat a particular zoo animal represents and were generally cautious. In the predator context, however, a high percentage of crows also flew away upon hearing the great tit control song which suggests that they may still evaluate those species which occasionally killed crows as more dangerous and respond to any conspicuous sound.     

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.     

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.     

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.     

Are shy people reluctant to ask for help?

Examined the help-seeking behaviors of shy and not-shy men and women. In Study 1, Ss worked on an impossible task in the presence of a male or female confederate whom they were told had just successfully completed the task. Shy Ss asked for help no less frequently than did not-shy Ss overall, but they did seek help less frequently from opposite-sex confederates than from same-sex confederates. In Study 2, shy and not-shy men and women were required to call a man and a woman and ask them to complete a questionnaire. All respondents agreed to return the questionnaire. However, when shy Ss (compared with not-shy Ss) called opposite-sex respondents, fewer of the questionnaires were actually returned. When making their calls, shy Ss sounded somewhat less warm and confident than did not-shy Ss, and they also spoke less fluently. Fluency, in turn, predicted response rate for the shy subjects calling respondents of the opposite sex.     

Male vocal competition is dynamic and strongly affected by social contexts in music frogs

Male–male vocal competition in anuran species is critical for mating success; however, it is also highly time-consuming, energetically demanding and likely to increase predation risks. Thus, we hypothesized that changes in the social context would cause male vocal competition to change in real time in order to minimize the costs and maximize the benefits of competition. To test this hypothesis, we assessed the effect of repeating playbacks of either white noise (WN) or male advertisement calls on male call production in the Emei music frog (Babina daunchina), a species in which males build mud-retuse burrows and call from within these nests. Previous studies have shown that calls produced from inside burrows are highly sexually attractive (HSA) to females while those produced outside nests are of low sexual attractiveness (LSA). Results showed that most subjects called responsively after the end of WN playbacks but before the onset of conspecific call stimuli although call numbers were similar, indicating that while males adjusted competitive patterns according to the biological significance of signals, their competitive motivation did not change. Furthermore, these data indicate that the frogs had evolved the ability of interval timing. Moreover, when the inter-stimulus interval (ISI) between playbacks was varied, the subjects preferentially competed with HSA calls when the ISI was short (<4 s) but responded equally to HSA and LSA calls if the ISI was long (≥4 s), suggesting that males allocate competitive efforts depending on both the perceived sexual attractiveness of rivals and the time available for calling. Notably, approximately two-thirds of male calls occurred in response to HSA calls, a preference rate comparable to that previously found for females in phonotaxis experiments and consistent with the idea that the mechanisms underlying both the male’s competitive responses to rivals and the female’s preferences toward potential mates coevolved under the same selective pressure.     

Do responses of galliform birds vary adaptively with predator size?

Past studies of galliform anti-predator behavior show that they discriminate between aerial and ground predators, producing distinctive, functionally referential vocalizations to each class. Within the category of aerial predators, however, studies using overhead models, video images and observations of natural encounters with birds of prey report little evidence that galliforms discriminate between different raptor species. This pattern suggests that the aerial alarm response may be triggered by general features of objects moving in the air. To test whether these birds are also sensitive to more detailed differences between raptor species, adult chickens with young were presented with variously sized trained raptors (small, intermediate, large) under controlled conditions. In response to the small hawk, there was a decline in anti-predator aggression and in aerial alarm calling as the young grew older and less vulnerable to attack by a hawk of this size. During the same developmental period, responses to the largest hawk, which posed the smallest threat to the young at all stages, did not change; there were intermediate changes at this time in response to the middle-sized hawk. Thus the anti-predator behavior of the adult birds varied in an adaptive fashion, changing as a function of both chick age and risk. We discuss these results in light of current issues concerning the cognitive mechanisms underlying alarm calling behavior in animals.     

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.     

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.     

Vaginal scent marking: effects on ultrasonic calling and attraction of male golden hamsters

Male hamsters were tested for their responses to areas that had been scent marked by intact or vaginectomized females to determine the effects of naturally deposited vaginal secretions on male behavior. In the first experiment males produced more ultrasonic courtship calls when investigating areas marked by intact females than areas scented by vaginectomized females, demonstrating that vaginal marks facilitate such calling. In a wind-tunnel preference test situation in which scent-marked alleys and clean alleys served as sources of odor, males approached the scented alley first if it had been freshly marked by intact females but not if it had been scented by vaginectomized females or other males. Thus, the odors of vaginal marks are sufficient to attract males over short distances. After males entered these alleys they showed a preference for odors of both intact and vaginectomized females over no odors, but still spent significantly more time investigating the odors of intact females than those of vaginectomized females. These experiments indicate that vaginal secretions are one of the primary cues that elicit male courtship calling, and the small quantities of vaginal secretions deposited by females in vaginal marks are sufficient to elicit ultrasonic calling and attract males over short distances. Thus it is likely that vaginal scent marking and ultrasonic calling by females interact to facilitate attraction and location of mates during courtship.     

Social facilitation as a function of the mere presence of others

According to R. B. Zajonc's (1965) drive theory of social facilitation, the mere presence of others increases arousal and, thereby, the frequency of dominant responses (i.e., responses with the greatest habit strength). In the present experiment, U.S. undergraduates performed a stimulus discrimination task under 1 of 2 conditions: in the presence of another individual (audience) or alone. The mere presence condition was designed to make it difficult for the participants to attend directly to the audience. The task was designed to minimize the likelihood that the specific response (numerical preference) would be attributable to a desire to respond appropriately to the audience. There was a significant difference in the mean number of dominant responses between the participants in the audience condition and those in the alone condition. The results provide support for Zajonc's mere presence drive theory of social facilitation.     

Group-directed criticism in Indonesia: Role of message source and audience

Research in individualist cultures has shown that group members are more likely to agree with criticisms of their group when the criticisms are made by another ingroup member as opposed to an outgroup member (the intergroup sensitivity effect). However, evaluations of ingroup critics are often harsher when they take their comments to an outgroup audience. In light of research on facework and tolerance for dissent, it seems important to test whether these effects are generalizable to a collectivist culture. Indonesian Muslims ( N  = 191) received a criticism of their religion stemming either from another Muslim or a Christian, and published in either a Muslim or a Christian newspaper. Participants agreed with the comments more when they were made by an ingroup as opposed to an outgroup member. Furthermore, consistent with previous research in Australia, the effects of audience on agreement were moderated by levels of group identification. Results are discussed in relation to theory about the functional role internal critics can play in group life.     

Sensory cues that elicit ultrasonic vocalizations in female rats (Rattus norvegicus)

Female rats emit ultrasonic vocalizations during copulation. Female vocalizations are associated with darting and other proceptive behavior. In addition, females frequently call while approaching the male. A series of experiments was undertaken to determine whether female rats emit ultrasonic vocalizations in response to other rats or to their odors. Females were exposed either to bedding soiled by males or females or to devocalized conspecifics separated from the subject by a barrier. Females vocalized more to male cues than to female cues, regardless of whether the odor cues were from soiled bedding or from a devocalized conspecific. In addition, subjects vocalized more when presented with a devocalized female rather than a neutral stimulus. Furthermore, devocalized adult males, separated by a barrier, were more effective than either devocalized castrated or juvenile males in eliciting vocalizations; in turn, castrates and juveniles were more effective than neutral stimuli. Female calling was likely induced by odors from the male. In one experiment, the female subject was positioned in such a way that she could neither see or touch the stimulus male. Presentation of tape-recorded male vocalizations did not affect calling by the female. Vocalizations emitted by females in response to male odors may attract males or may facilitate subsequent copulatory behavior by the male.     

Acoustic variability and individual distinctiveness in the vocal repertoire of red-capped mangabeys (Cercocebus torquatus)

Acoustic variability and individual distinctiveness of vocal signals are expected to vary with both their communicative function and the need for individual recognition during social interactions. So far, few attempts have been made to comparatively study these features across the different call types within a species' vocal repertoire. We collected recordings of the six most common call types from 14 red-capped mangabeys (Cercocebus torquatus) to assess intra- and interindividual acoustic variability, using a range of temporal and frequency parameters. Acoustic variability was highest in contact and threat calls, intermediate in food calls, and lowest in loud and alarm calls. Individual distinctiveness was high in contact, threat, loud and alarm calls, and low in food calls. In sum, calls mediating intragroup social interactions were structurally most variable and individually most distinctive, highlighting the key role that social factors must have played in the evolution of the vocal repertoire in this species. We discuss these findings in light of existing hypotheses of acoustic variability in primate vocal behavior.     

THE FUNCTIONAL RELATIONSHIP BETWEEN ARTIFICIAL FOOD COLORS AND HYPERACTIVITY

The presence of a functional relationship between the ingestion of artificial food colors and an increase in the frequency and/or duration of selected behaviors that are representative of the hyperactive behavior syndrome was experimentally investigated. Two eight-year-old females, who had been on the Feingold K-P diet for a minimum of 11 months, were the subjects studied. The experimental design was a variation of the BAB design, with double-blind conditions. This design allowed an experimental analysis of the placebo phases as well as challenge phases. Data were obtained by trained observers on Out of Seat, On Task, and Physically Aggressive behaviors, as they occurred in the subjects' regular class setting. Results indicated (a) the existence of a functional relationship between the ingestion of artificial food colors and an increase in both the duration and frequency of hyperactive children.     

Social Facilitation as a Function of the Mere Presence of Others

Abstract

According to R. B. Zajonc's (1965) drive theory of social facilitation, the mere presence of others increases arousal and, thereby, the frequency of dominant responses (i.e., responses with the greatest habit strength). In the present experiment, U.S. undergraduates performed a stimulus discrimination task under 1 of 2 conditions: in the presence of another individual (audience) or alone. The mere presence condition was designed to make it difficult for the participants to attend directly to the audience. The task was designed to minimize the likelihood that the specific response (numerical preference) would be attributable to a desire to respond appropriately to the audience. There was a significant difference in the mean number of dominant responses between the participants in the audience condition and those in the alone condition. The results provide support for Zajonc's mere presence drive theory of social facilitation.