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.     

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.     

Audience effects on alarm calling in chickens (Gallus gallus)

The male domestic chicken (Gallus gallus) has been found to modulate the production of vocal signals in response to the presence or absence of a suitable audience. We investigated effects on alarm calling by presenting overhead predator models to cockerels in the presence of a variety of social companions. The production of aerial predator calls in response to hawk silhouettes varied with the presence or absence of a member of the same species. The kinds of audience investigated included the mate, unfamiliar females, other females and males with which subjects had had prior visual and auditory contact, and broody hens with and without young. Domestic chicks, unrelated to the subjects, were almost as effective an audience as conspecific adults. A member of another species, however, failed to potentiate alarm-call production. The subjects gave more alarm calls when they were in the presence of either a male or a female audience than when they were alone. By manipulating the visibility of overhead predator models to the subjects and to the audience, we showed that the subjects were not cued by alarm and escape behaviors of the audience. Comparisons with food calling indicate that, in deciding whether to emit a signal in response to the appropriate referent (e.g., food or predators), chickens respond to subtle differences in the nature of the audience with behaviors that vary from one communicative context to another.     

Internal and external factors modulate food-calling in domestic hens

Two series of experiments investigated factors affecting utterance of food calls in the domestic hen, Gallus domesticus. The first series of experiments tested the effect of food preference and the hen’s internal state on the utterance of food calls. Different food types were presented first singly and then in a choice test to 20 hens, first when hens were laying, and then when they were maternal. The second series of experiments tested the effect of hunger level on the utterance of food calls in laying hens, and maternal hens with or without chicks. These two series of experiments showed that laying hens and maternal hens showed a similar marked preference for certain types of food, but laying hens very rarely emitted food calls, in contrast to maternal hens. This shows the effect of the bird’s psychophysiological state on her tendency to emit food calls. The more a maternal hen preferred a food type, the more food calls she emitted. This was observed from the beginning of a test in single-food tests as well as in choice tests. Hunger level positively affected food-call production under certain feeding conditions in maternal hens, but not in laying hens. When maternal hens were tested in the absence of their chicks, utterance of food calls was more sustained than in the presence of chicks. Received: 14 May 1998 / Accepted after revision: 11 October 1998     

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.     

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.     

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.     

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.     

Inverted-U shape relationship between cortisol and learning in ground squirrels

Adrenal hormones regulate glucose levels, responses to unpredictable stressors and modulate cognition. Glucocorticoids can have an inverted-U shape relationship with cognition, as very low or high levels impair, whereas moderate elevations facilitate, acquisition and retention of memories. To date these relationships have been tested with humans and rodents in laboratory settings rather than with wild animals in biologically relevant contexts. This study examined whether the elevated cortisol observed in juvenile Belding’s ground squirrels (Spermophilus beldingi) at natal emergence might promote both acquisition of adaptive responses to this species’ two alarm calls warning of predators and memory of the spatial configuration of mothers’ territories. Both experimentally increased and decreased basal cortisol levels interfere with acquisition and retention of an association between a warning call and the appropriate response compared with naturally occurring moderately elevated cortisol. Further, decreased cortisol impairs learning of a novel, complex spatial maze. Thus in the field the brief elevation of cortisol at emergence might facilitate acquisition of spatial memory of a three-dimensional environment and responses to alarm calls during a sensitive period of learning. This novel demonstration of the inverted-U shape function in a wild animal suggests that natural selection has favored a hormonal profile facilitating rapid acquisition of important survival behaviors.     

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.     

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...     

Functional referents and acoustic similarity revisited: the case of Barbary macaque alarm calls

Barbary macaques (Macaca sylvanus) utter "shrill barks" in response to disturbances in their surroundings. In some cases, the majority of group members react by running away or climbing up a tree. In many other instances, however, group members show no overt reaction to these calls. We conducted a series of playback experiments to identify the factors underlying subjects' responses. We presented calls given in response to dogs that had elicited escape responses and calls that had failed to do so. We also presented calls given in response to snakes and to the observer approaching the sleeping-trees at night. An acoustic analysis of the calls presented in the playback experiments (electronic supplementary material, audioclip S1) revealed significant differences among calls given in response to dogs, the observer approaching at night, and snakes. However, the analysis did not detect any differences between calls given in response to dogs that were related to whether or not they had elicited escape responses in the first place. Correspondingly, after playback of calls given in response to dogs, we observed no difference in subjects' responses in relation to whether or not the calls had initially elicited escape responses. Subjects showed startle or escape responses significantly more often after playbacks of calls given in response to dogs than after calls given in response to observers. Playbacks of calls given in response to snakes failed to elicit specific responses such as standing bipedally or scanning the grass. Although these findings may imply that responses depend on the external referent, they also indicate that there is no clear-cut relationship between the information available to the listeners and their subsequent responses. This insight forces us to extend current approaches to identifying the meaning of animal signals. Accepted after revision: 15 May 2001 Electronic Publication     

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

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

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.     

Primate vocal production and the riddle of language evolution

Trying to uncover the roots of human speech and language has been the premier motivation to study the signalling behaviour of nonhuman primates for several decades. Focussing on the question of whether we find evidence for linguistic reference in the production of nonhuman primate vocalizations, I will first discuss how the criteria used to diagnose referential signalling have changed over time, and will then turn to the paradigmatic case of semantic communication in animals, the alarm calls of vervet monkeys, Chlorocebus pygerythrus. A recent in-depth analysis of the original material revealed that, while the alarm calls could be well distinguished, calls of similar structure were also used in within- and between-group aggression. This finding is difficult to reconcile with the idea that calls denote objects in the environment. Furthermore, nonhuman primates show only minimal signs of vocal production learning, one key prerequisite for conventionalized and symbolic communication. In addition, the structure of calls in different populations or closely related species is highly conserved. In conclusion, any continuity between nonhuman primate and human communication appears to be found at the level of the processing of signals. Why and how the ancestors of our own species one day began to talk to each other continues to be an enigma. Future research should focus on changes in the neural structure supporting volitional control over vocalizations, the gene networks associated with vocal production, and the developmental processes involved in the integration of production and perception of vocalizations.     

Friend or foe? The role of latent inhibition in predator and non-predator labelling by coral reef fishes

In communities of high biodiversity, the ability to distinguish predators from non-predators is crucial for prey success. Learning often plays a vital role in the ability to distinguish species that are threatening from those that are not. Many prey animals learn to recognise predators based on a single conditioning event whereby they are exposed to the unknown predator at the same time as alarm cues released from injured conspecifics. The remarkable efficiency of such learning means that recognition mistakes may occur if prey inadvertently learn that a species is a predator when it is not. Latent inhibition is a means by which prey that are pre-exposed to an unknown species in the absence of negative reinforcement can learn that the unknown animal is likely not a threat. Learning through latent inhibition should be conservative because mistakenly identifying predators as non-predators can have fatal consequences. In this study, we demonstrated that a common coral reef fish, lemon damselfish, Pomacentrus moluccensis can learn to recognise a predator as non-threatening through latent inhibition. Furthermore, we showed that we could override the latent inhibition effect by conditioning the prey to recognise the predator numerous times. Our results highlight the ability of prey fish to continually update the information regarding the threat posed by other fishes in their vicinity.     

Emotion,controllability and orientation towards stress as correlates of children’s coping with interpersonal stress

Guided by the motivational theory of coping (Skinner and Zimmer-Gembeck in Ann Rev Psychol 58:119–144. doi:10.1146/annurev.psych.58.110405.085705, 2007), we investigated children’s anticipated coping with three different stressful events (bullying, parental argument, parent–child verbal conflict), and examined whether their reliance on challenge coping responses versus threat coping responses could be accounted for by emotional reactions (including feelings of sadness, anger and fear), perceived controllability, and orientation or interest in the stressor. In addition, we examined parents’ reports of their children’s temperamental traits as correlates of coping. In random order followed by a positive stimulus, children (N = 206, age 8–12 years) watched each of the three stressful events, and reported their emotions, perceived control, orientation and coping after each one. As anticipated, results indicated that controllability was associated with more challenge coping (a composite of adaptive/approach coping responses such as problem solving and support seeking) and less threat coping (a composite of maladaptive/withdrawal coping responses such as helplessness and escape). In general, feelings of sadness were more strongly associated with challenge coping, whereas fear and anger especially related to more threat coping. Greater orientation towards the stressor was particularly predictive of more challenge coping, but also was associated with more threat coping in response to parent stressors. These associations were significant, even after controlling for temperament (negative reactivity, task persistence, withdrawal, and activity), which was generally unrelated to children’s coping. Other combinations of coping responses were also examined.     

The “who designed the designer?” objection to design arguments

One of the most commonly-raised objections to the design argument is the so-called “who designed the designer?” objection, which charges that any designer invoked to explain complexity in the universe will feature complexity of its own, and thus require explanation in terms of design. There are two distinct versions of this objection in the contemporary literature, with it being couched in terms of: (1) Complexity of designer: a designer exhibits complexity, which calls for explanation in terms of design; (2) Complexity of ideas: a designer’s ideas exhibit complexity, which calls for explanation in terms of design. To each of these versions of the objection there corresponds various responses from proponents of design. These proponents adopt a very particular strategy when crafting their responses: they argue that the objection can be neutralised simply by appealing to one or more of God’s attributes. In this paper I argue that this strategy is inapt, and unable to yield a successful response to either version of the objection. I also argue that a more promising way of tackling the objections is to identify their own peculiar weaknesses, for once these are exposed the objections cease to be a credible threat to the design hypothesis.     

Maternal hen calls modulate memory formation in the day-old chick: the role of noradrenaline

Facilitation of memory for discriminative learning in young chicks is enhanced following exposure to a synthesized rhythmic auditory stimulus. Increased arousal, mediated by noradrenergic activation, is believed to underlie this effect. In this report we examine whether ethologically relevant rhythmic auditory stimuli produce the same noradrenaline-mediated memory enhancement in neonate chicks (Gallus gallus domesticus). Maternal hen attraction calls which contained a rhythmic pattern were found to facilitate retention. Intracerebral injection of noradrenaline or the beta(2)-adrenergic antagonist propranolol demonstrated that this enhancement is likely to be mediated by noradrenergic activation of central beta(2)-noradrenergic receptors. In contrast, a rhythmic alarm call inhibited retention. Subcutaneous injection of the alpha(1)-adrenergic antagonist prazosin revealed that this impairment may be due to higher arousal levels resulting in activation of alpha(1)-noradrenergic receptors. It is concluded that the maternal hen calls of domestic chickens can influence the memory ability of the offspring via noradrenaline release in the brain. The current data suggest that call meaning and rhythmicity interact to yield the appropriate levels of beta(2)-adrenergic activation required to facilitate retention for a discriminative task.