Hornbills can distinguish between primate alarm calls

Some mammals distinguish between and respond appropriately to the alarm calls of other mammal and bird species. However, the ability of birds to distinguish between mammal alarm calls has not been investigated. Diana monkeys (Cercopithecus diana) produce different alarm calls to two predators: crowned eagles (Stephanoaetus coronatus) and leopards (Panthera pardus). Yellow-casqued hornbills (Ceratogymna elata) are vulnerable to predation by crowned eagles but are not preyed on by leopards and might therefore be expected to respond to the Diana monkey eagle alarm call but not to the leopard alarm call. We compared responses of hornbills to playback of eagle shrieks, leopard growls, Diana monkey eagle alarm calls and Diana monkey leopard alarm calls and found that they distinguished appropriately between the two predator vocalizations as well as between the two Diana monkey alarm calls. We discuss possible mechanisms leading to these responses.     

Threat-Related Acoustical Differences in Alarm Calls by Wild Bonnet Macaques (Macaca radiata) Elicited by Python and Leopard Models

Wild and urban bonnet macaques (Macaca radiata) were studied in southern India to record alarm calls during presentations of realistic models of spotted and dark leopards (Panthera pardus) and an Indian python (Python molurus). Recordings of alarm calls were made from members of four forest troops at feeding stations who observed brief and prolonged presentations of fully exposed spotted and dark leopard morphs and partially concealed views of the spotted morph. Four different forest troops were presented a slowly moving python near feeding stations. Two predator‐inexperienced urban troops from the city of Bangalore were presented either the spotted leopard morph briefly or the python. Analyses of alarm calls revealed differences in acoustic structure, such as a lower harmonic to noise ratio, which can be interpreted as reflecting the level of perceived threat rather than predator type. Noisy alarm calls likely indicate high states of physiological arousal that might provide eavesdropping troop members with information useful for assessing the urgency of the predatory threat. Lack of alarm‐call distinctiveness characterizing predator type is complemented by explicit contextual information in which alarm calling to leopards never occurred on the ground whereas nearly all initial python‐elicited alarm calls were made by individuals on the ground monitoring the python. The alarm calls of Bangalore monkeys distinguished the leopard and python models, with the latter engendering the noisiest calls and immediate flight to trees. Such flight is unnecessary with the python and suggests that, without appropriate experience with pythons, bonnet macaques adopt less predator specific refuge‐seeking behavior.     

Interspecies semantic communication in two forest primates

West African Diana monkeys (Cercopithecus diana) and Campbell's monkeys (Cercopithecus campbelli) frequently form mixed-species associations. Males of both species produce acoustically distinct alarm calls to crowned eagles (Stephanoaetus coronalus) and leopards (Panthera pardus), two of their main predators. Field playback experiments were conducted to investigate whether Diana monkeys respond to Campbell's alarm calls and whether they understand the calls' semantic content. Diana monkeys responded to playback of Campbell's leopard or eagle alarm calls as though the original predator were present. In a second experiment, Diana monkeys were primed with either Campbell's eagle or leopard alarm calls and then subsequently probed with the vocalizations of a crowned eagle or a leopard. Results showed that monkeys used the semantic information conveyed by the Campbell's alarm calls to predict the presence of a predator. The data are consistent with the hypothesis that non-human primates are able to use acoustic signals of diverse origin as labels for underlying mental representations.     

Male blue monkeys alarm call in response to danger experienced by others

Male blue monkeys (Cercopithecus mitis stuhlmanni) of Budongo Forest, Uganda, produce two acoustically distinct alarm calls: hacks to crowned eagles (Stephanoaetus coronatus) and pyows to leopards (Panthera pardus) and a range of other disturbances. In playback experiments, males responded to leopard growls exclusively with a series of pyows and to eagle shrieks predominantly with hacks. Responses to playbacks of these alarm call series matched the responses to the corresponding predators, suggesting that the calls conveyed something about the nature of the threat. When responding to a series of hacks, indicating an eagle, males responded predominately with hacks, but produced significantly more calls if their group members were close to the playback stimulus than far away, regardless of their own position. When responding to a series of pyows, indicating a range of disturbances, males responded with pyows, but call rates were independent of the distance of other group members. The results suggest that males took into account the degree of danger experienced by other group members.     

Predation increases acoustic complexity in primate alarm calls

According to most accounts, alarm calling in non-human primates is a biologically hardwired behaviour with signallers having little control over the acoustic structure of their calls. In this study, we compared the alarm calling behaviour of two adjacent populations of Diana monkeys at Taï forest (Ivory Coast) and Tiwai Island (Sierra Leone), which differ significantly in predation pressure. At Taï, monkeys regularly interact with two major predators, crowned eagles and leopards, while at Tiwai, monkeys are only hunted by crowned eagles. We monitored the alarm call responses of adult male Diana monkeys to acoustic predator models. We found no site-specific differences in the types of calls given to eagles, leopards and general disturbances, but there were consistent differences in how callers assembled calls into sequences. At Tiwai, males responded to leopards and general disturbances in the same way, while at Taï, males discriminated by giving call sequences that differed in the number of component calls. Responses to eagles were identical at both sites. We concluded that Diana monkeys are predisposed to use their repertoire in context-specific ways, but that ontogenetic experience determines how individual calls are assembled into meaningful sequences.     

Semantic Differences in Sifaka (Propithecus verreauxi) Alarm Calls: A Reflection of Genetic or Cultural Variants?

In this study, we compared the usage of alarm calls and anti‐predator strategies between a captive and a wild lemur population. The wild lemur population was studied earlier in Western Madagascar ( Fichtel & Kappeler 2002 ). The captive population was studied in outdoor enclosures of the Duke University Primate Center. Alarm calls and anti‐predator behavior were elicited by conducting experiments with both vocal and visual dummies. We scored the subjects’ immediate behavioral responses, including alarm calls, from video recordings made during the experiments. In principle, both populations have a mixed alarm call system with functionally referential alarm calls for aerial predators and general alarm calls for terrestrial and aerial predators and for situations associated with high arousal, such as group encounters. Although wild and captive sifakas exhibit the same alarm call system and use the same alarm call types, we discovered striking differences in the usage and perception of some of the alarm calls. We argue that these differences indicate either an evolutionary drift in the meaning of these calls or reflect cultural variation. The latter possibility is consistent with our understanding of the ontogeny of call usage and comprehension.     

Causal knowledge of predators' behaviour in wild Diana monkeys

Wild Diana monkeys, Cercopithecus diana, of Ta? forest, Ivory Coast, are preyed upon by leopards, Panthera pardus, and chimpanzees, Pan troglodytes. These two predators differ in their main hunting tactic and Diana monkeys attempt to avoid predation with two distinct antipredator strategies: conspicuous alarm-calling behaviour to leopards and silent, cryptic behaviour to chimpanzees. However, the Diana monkeys' choice of the appropriate antipredator strategy is complicated by the fact that chimpanzees themselves also fall prey to leopards. Chimpanzees give loud and conspicuous alarm screams when they detect a leopard. When these chimpanzees' leopard alarm calls were played back to different groups of Diana monkeys, in about half of the cases recipients switched from a chimp-specific cryptic response to a leopard-specific conspicuous response, suggesting that some individuals assumed the presence of a leopard. Groups whose home range was in the core area of the resident chimpanzee community were more likely to respond this way than more peripheral groups, indicating between-group differences in semantic knowledge. In a follow-up experiment, the monkeys' understanding of the chimpanzee alarm calls was further assessed with a prime-probe technique. Monkeys were primed with chimpanzee alarm calls and then, 5 min later, tested with leopard growls to see whether they were able to anticipate the presence of a leopard. Results were consistent with the hypothesis that monkeys responding cryptically to chimpanzee alarm calls did so because they were not able to understand the calls' meaning. Data are discussed with respect to three possible cognitive mechanisms, associative learning, specialized learning programmes, and causal reasoning, that could have led to causal knowledge in some individuals but not others. Copyright 2000 The Association for the Study of Animal Behaviour.     

Functionally Referential Alarm Calls in Tamarins (Saguinus fuscicollis and Saguinus mystax) – Evidence from Playback Experiments

Studies on primate vocalisation have revealed different types of alarm call systems ranging from graded signals based on response urgency to functionally referential alarm calls that elicit predator‐specific reactions. In addition, alarm call systems that include both highly specific and other more unspecific calls have been reported. There has been consistent discussion on the possible factors leading to the evolution of different alarm call systems, among which is the need of qualitatively different escape strategies. We studied the alarm calls of free‐ranging saddleback and moustached tamarins (Saguinus fuscicollis and Saguinus mystax) in northeast Peru. Both species have predator‐specific alarm calls and show specific non‐vocal reactions. In response to aerial predators, they look upwards and quickly move downwards, while in response to terrestrial predators, they look downwards and sometimes approach the predator. We conducted playback experiments to test if the predator‐specific reactions could be elicited in the absence of the predator by the tamarins’ alarm calls alone. We found that in response to aerial alarm call playbacks the subjects looked significantly longer upwards, and in response to terrestrial alarm call playbacks they looked significantly longer downwards. Thus, the tamarins reacted as if external referents, i.e. information about the predator type or the appropriate reaction, were encoded in the acoustic features of the calls. In addition, we found no differences in the responses of S. fuscicollis and S. mystax whether the alarm call stimulus was produced by a conspecific or a heterospecific caller. Furthermore, it seems that S. fuscicollis terrestrial alarm calls were less specific than either S. mystax terrestrial predator alarms or either species’ aerial predator alarms, but because of the small sample size it is difficult to draw a final conclusion.     

Persistence of Alarm-Call Behaviour in the Absence of Predators: A Comparison Between Wild and Captive-Born Meerkats (Suricata Suricatta)

Performing correct anti‐predator behaviour is crucial for prey to survive. But, are such abilities lost in species or populations living in predator‐free environments? How individuals respond to the loss of predators has been shown to depend on factors such as the degree to which anti‐predator behaviour relies on experience, the type of cues evoking the behaviour, the cost of expressing the behaviour and the number of generations under which relaxed selection has taken place. Here we investigated whether captive‐born populations of meerkats (Suricata suricatta) used the same repertoire of alarm calls previously documented in wild populations and whether captive animals, as wild ones, could recognize potential predators through olfactory cues. We found that all alarm calls that have been documented in the wild also occurred in captivity and were given in broadly similar contexts. Furthermore, without prior experience of odours from predators, captive meerkats seemed to distinguish between faeces of potential predators (carnivores) and non‐predators (herbivores). Despite slight structural differences, the alarm calls given in response to the faeces largely resembled those recorded in similar contexts in the wild. These results from captive populations suggest that direct, physical interaction with predators is not necessary for meerkats to perform correct anti‐predator behaviour in terms of alarm‐call usage and olfactory predator recognition. Such behaviour may have been retained in captivity because relatively little experience seems necessary for correct performance in the wild and/or because of the recency of relaxed selection on these populations.     

Leopard predation and primate evolution

Although predation is an important driving force of natural selection its effects on primate evolution are still not well understood, mainly because little is known about the hunting behaviour of the primates' various predators. Here, we present data on the hunting behaviour of the leopard (Panthera pardus), a major primate predator in the Tai; forest of Ivory Coast and elsewhere. Radio-tracking data showed that forest leopards primarily hunt for monkeys on the ground during the day. Faecal analyses confirmed that primates accounted for a large proportion of the leopards' diet and revealed in detail the predation pressure exerted on the eight different monkey and one chimpanzee species. We related the species-specific predation rates to various morphological, behavioural and demographic traits that are usually considered adaptations to predation (body size, group size, group composition, reproductive behaviour, and use of forest strata). Leopard predation was most reliably associated with density, suggesting that leopards hunt primates according to abundance. Contrary to predictions, leopard predation rates were not negatively, but positively, related to body size, group size and the number of males per group, suggesting that predation by leopards did not drive the evolution of these traits in the predicted way. We discuss these findings in light of some recent experimental data and suggest that the principal effect of leopard predation has been on primates' cognitive evolution.     

Variation in and Meaning of Alarm Calls in a Social Desert Rodent Rhombomys opimus

The great gerbil (Rhombomys opimus), a social rodent that lives in family groups, emits three different alarm vocalizations in the presence of predators: a rhythmic call; a faster more intense call; and a single whistle. We tested the hypothesis that the alarm calls communicate risk of predation. We quantified the relationship between predator distance and type of alarm call via human approaches to gerbils. We also tested responses of focal adults in family groups to playback broadcasts of the different calls and controls of bird song and tape noise. Results showed that alarm calls were related to distance from a predator. Gerbils gave the rhythmic call when the predator was farthest away, the more intense call as the predator moved closer; and a short whistle when startled by a close approach of the predator. Gerbils stopped feeding and stood vigilant in a frozen alert posture in response to playbacks of all three alarm calls. They decreased non‐vigilant behavior to the alarm vocalizations more than to the controls and decreased non‐vigilant behavior significantly more in response to the intense alarm and whistle compared with the rhythmic alarm. We conclude that one function of gerbil alarm calls is to communicate response urgency to family members. The rhythmic alarm communicates danger at a distance, whereas the intense alarm and whistle signal the close approach of a predator.     

Heterospecific recognition of referential alarm calls in two species of lemur

ABSTRACT

Alarm vocalizations are a common feature of the mammalian antipredator response. The meaning and function of these calls vary between species, with some species using calls to reference-specific categories of predators. Species can also use more than just the calls of conspecifics to detect threat, ‘eavesdropping’ on other species’ signalling to avoid predation. However, the evidence to date for both referential signalling and eavesdropping within primates is limited. We investigated two sympatric populations of wild lemur, the Coquerel’s sifaka Propithecus coquereli and the common brown lemur Eulemur fulvus, presenting them with playbacks of predator calls, conspecific alarm calls and heterospecific lemur alarm calls, and recorded their behavioural responses following the playbacks. Results suggest that the Coquerel’s sifaka may have functionally referential alarm calls with high specificity for aerial predators, but there was no evidence for any referential nature of the other call investigated. Brown lemurs appear to have a mixed alarm system, with one call being specific with respect to aerial predators. The other call investigated appeared to reference terrestrial predators. However, it was also used in other contexts, so does not meet the criteria for functional reference. Both species showed evidence for heterospecific alarm call recognition, with both the Coquerel’s sifaka and the brown lemurs responding appropriately to heterospecific aerial alarm calls.     

Communication of Stimulus Size and Shape in Alarm Calls of Gunnison's Prairie Dogs, Cynomys gunnisoni

Gunnison's prairie dogs ( Cynomys gunnisoni ) emit multiple-note alarm calls to terrestrial predators that vary in acoustic structure according to the eliciting stimulus. The characteristics of the predator that are salient with respect to alarm call variation, however, are poorly understood. Although the behavior of predators has been shown to influence alarm call production in other species of ground-dwelling sciurids, the degree to which sciurid alarm calls describe physical characteristics of predators has not been addressed independently of the effects of variation in predator behavior. The effect of variation in the size and shape of the eliciting stimulus was studied by presenting silhouette models to a colony of prairie dogs and recording the alarm calls that were elicited. Discriminant function analysis on 7 variables measured from spectrograms revealed that the alarm calls differed with respect to silhouette. These results suggest that information with respect to stimulus size and shape is encoded in prairie dog alarm calls.     

The information that receivers extract from alarm calls in suricates.

Field observations and acoustic analyses have shown that suricate (Suricata suricatta) alarm calls vary in their acoustic structure depending on predator type. In this study, we tested whether receivers respond appropriately when hearing a call in the absence of a predator. Although the only way for suricates to escape from predators is to retreat to boltholes, responses to playbacks could be divided into distinct categories. The subjects responded differently to alarm calls given in response to aerial or terrestrial predators and to recruitment calls emitted in response to snakes and deposits on the ground. Suricates also showed rather distinct responses to low, medium and high urgency aerial calls. Differences in the responses were less obvious for different levels of urgency in the terrestrial and recruitment calls. Suricate receivers thus gain information about both the predator type and level of urgency from the acoustic structures of their calls.     

Titi monkey call sequences vary with predator location and type

Animal alarm calls can encode information about a predator''s category, size, distance or threat level. In non-human primates, alarm calls typically refer to broad classes of disturbances, in some instances to specific predators. Here, we present the results of a field experiment with a New World primate, the black-fronted titi monkey (Callicebus nigrifrons), designed to explore the information conveyed by their alarm call system. Adults produced sequences consisting of two main alarm call types that conveyed, in different parts of the utterance, information about a predator''s type and location. In particular, sequence compositions differed depending on whether the predator was a mammalian carnivore or a raptor, and whether it was detected in a tree or on the ground. This is the first demonstration of a sequence-based alarm call system in a non-human animal that has the capacity to encode both location and type of predatory threat.     

Campbell's Monkeys Use Affixation to Alter Call Meaning

Human language has evolved on a biological substrate with phylogenetic roots deep in the primate lineage. Here, we describe a functional analogy to a common morphological process in human speech, affixation, in the alarm calls of free-ranging adult Campbell''s monkeys (Cercopithecus campbelli campbelli). We found that male alarm calls are composed of an acoustically variable stem, which can be followed by an acoustically invariable suffix. Using long-term observations and predator simulation experiments, we show that suffixation in this species functions to broaden the calls'' meaning by transforming a highly specific eagle alarm to a general arboreal disturbance call or by transforming a highly specific leopard alarm call to a general alert call. We concluded that, when referring to specific external events, non-human primates can generate meaningful acoustic variation during call production that is functionally equivalent to suffixation in human language.     

Alarm calls of wintering great tits Parus major: warning of mate,reciprocal altruism or a message to the predator?

When a predator is not an immediate threat, a prey may produce relatively loud alarm calls because the risk is low. Since such calls could nevertheless attract acoustically oriented predators, the cost of predator attraction must be outweighed by factors beneficial to the caller. In this field study we elicited low-risk alarm calls by temporarily catching wintering adult male great tits Parus major at feeders both within and outside their territories. We tested whether the alarm calls of dominant males can be explained in terms of mate warning, reciprocal altruism or notifying the predator of detection. If alarms are intended to warn mates, males accompanied by their mates should give alarm calls both within and outside home range, even if other permanent flock members are absent. If alarms are to be explained by reciprocal altruism, male great tits should give low-risk alarm calls when accompanied by permanent flock members other than mate within and not outside of the home-range. If alarm calling is a message to a predator, males should call when foraging alone. We found that male great tits gave low-risk alarm calls when accompanied by their mates, independent of feeder location. They also gave low-risk alarm calls within home ranges in the presence of other permanent flock members when mates were absent. In contrast, only a few males gave calls when foraging alone within their home ranges, or when in the company of unfamiliar great tits outside their usual home-range. The results suggest that the utterance of alarm calls may be explained as mate protection and reciprocal altruism among familiar individuals.     

Referential labelling in Diana monkeys

Animal semantic communication has received considerable theoretical and empirical attention because of its relevance to human language. Advances have been made by studies of alarm-call behaviour in nonhumans. In monkeys, for example, there is evidence that recipients have a fairly sophisticated understanding of a call's meaning; that is, the predator type usually associated with a certain alarm call. Little is known, however, about the mental mechanisms that drive call production in nonhuman primates. In some nonprimate species, it has been found that signallers do not respond to a predator's physical features but instead seem to respond to its relative threat or direction of attack. In these species, therefore, alarm calls do not denote different predator categories but simply reflect different types or levels of danger. Because different predator categories typically impose different types and degrees of threat it is entirely possible that nonhuman primates also respond to threat rather than a predator's category. This study examined how wild Diana monkeys, Cercopithecus diana, of the Ta? forest, Ivory Coast, label predation events. By altering playback stimuli and the position of a concealed speaker, I investigated whether Diana monkeys respond with acoustically different alarm calls depending on a predator's (1) distance (close versus far), (2) elevation (above versus below), or (3) category (eagle versus leopard). Analysis of male and female alarm-call behaviour showed that Diana monkeys consistently responded to predator category regardless of immediate threat or direction of attack. Data further suggested that, in addition to predator category, monkeys' alarm calls might also convey information about the predator's distance. Copyright 2000 The Association for the Study of Animal Behaviour.     

Alarm call‐based discrimination between common cuckoo and Eurasian sparrowhawk in a Chinese population of great tits

Morphological resemblance of the common cuckoo Cuculus canorus to the Eurasian sparrowhawk Accipiter nisus has been regarded as an example of predator mimicry. Common hosts could distinguish parasites as the result of coevolution, while rare hosts or non‐hosts may mistake cuckoos for hawks because rare hosts or non‐hosts behave similarly when faced with these two species. Birds usually produce alarm calls in addition to showing behavioral responses when in danger. However, previous studies of identification by rare hosts or non‐hosts of sparrowhawks usually lacked experimental evidence of alarm calls. Great tits Parus major, a rare cuckoo host, perform similar behaviors and usually produce alarm calls in response to sparrowhawks and common cuckoos. Here, we tested whether great tits could distinguish common cuckoo from sparrowhawk based on analysis of their alarm calls and the effects of playback of alarm calls on conspecific behavior. Previous studies showed that great tits have a complex communication system that conveys information about predators, and they could perform different kinds of response behavior to different alarm calls. If great tits have not made the ability to distinguish between common cuckoo and sparrowhawk, then their acoustic responses to these two species and their response behaviors in playback experiments should be similar. Specimens of a common cuckoo (parasite), a sparrowhawk (predator) and an Oriental turtle dove Streptopelia orientalis (harmless control) were used to elicit and subsequently record the response behavior and alarm calls of great tits. There was no significant difference in behavioral response among great tits when exposed to the dummy of cuckoo, sparrowhawk and dove. In contrast, they differed significantly in alarm calls. Great tits produced more notes per call that contained increasing D‐type and decreasing I‐type notes when responding to sparrowhawk as compared to cuckoo or dove. In playback experiments, we found that great tits responded more strongly to great tit hawk than to great tit cuckoo or great tit dove alarm calls. Our study suggests that great tits are able to distinguish sparrowhawks from common cuckoos and convey relevant information in alarm calls by adjusting the number and combinations of notes of a single call type.     

No evidence of eavesdropping on heterospecific alarm calls by captive zebra finches recently descended from wild birds

Alarm calls are vocalisations animals give in response to predators which mainly function to alert conspecifics of danger. Studies show that numerous species eavesdrop on heterospecific calls to gain information about predator presence. Responding to heterospecific calls may be a learned or innate response, determined by whether the response occurs with or without prior exposure to the call. In this study, we investigated the presence of eavesdropping behaviour in zebra finches Taeniopygia guttata. This species is not known to possess a distinct alarm call to warn adult conspecifics of a threat, and could be relying on alarm calls of nearby heterospecifics for predator information. We used a playback experiment to expose captive zebra finches to three heterospecific sounds: an unfamiliar alarm call (from the chestnut‐rumped thornbill Acanthiza uropygialis), a familiar alarm call, and a familiar control (both from the noisy miner Manorina melanocephala). These calls were chosen to test if the birds had learnt to distinguish between the function of the two familiar calls, and if the acoustic properties of the unfamiliar alarm indicated presence of a threat to the finches. Our results showed that in response to the thornbill alarm, the birds reduced the rate of production of short calls. However, this decrease was also seen when considering both short and distance calls in response to the control sound. An increase in latency to call was also seen after the control stimulus when compared to the miner alarm. The time spent scanning increased in response to all three stimuli, but this did not differ between stimuli. There were no significant differences when considering the stimulus by time interaction for any of the three vigilance measures. Overall, no strong evidence was found to indicate that the captive zebra finches were responding to the heterospecific alarm stimuli with anti‐predator behaviour.