Distinct Alarm Calls Research Articles

The vocal repertoire of an African colobine, Colobus angolensis ruwenzorii: a multi-level society compared to congeners in stable groups

Abstract Vocal behaviour offers a window into understanding the social life and evolution of animals. Colobine monkeys show great interspecific and interpopulation variation in their social organization and behaviour. Recent research has shown that Rwenzori Angolan colobus (Colobus angolensis ruwenzorii) differ substantially from other black-and-white colobus in forming a multi-level society. No previous research has been conducted on the communication of C. a. ruwenzorii, but the social complexity hypothesis for communication suggests that more complex societies should evolve more complex communication repertoires. Our objective was to catalogue the vocal repertoire of C. a. ruwenzorii at Nabugabo, Uganda, and to compare it with the data available on congeners regarding intergroup tolerance, vocal repertoire size, and acoustic and behavioural features of vocal communication. Vocalizations were subject to spectrographic and behavioural analysis, and a descriptive analysis of each vocalization type was made. The influence of a few environmental and social factors on calling rates was also examined. We describe five vocalizations (i.e., the snort, roar, squeak, scream and pok) and one non-vocal signal (i.e., the tongue click) in this subspecies and their contexts. Distinct alarm calls are made for dogs, and these are given more often near the edge of the forest where humans frequent. We did not find that C. a. ruwenzorii showed a greater vocal repertoire than C. guereza or C. polykomos, which do not live in multi-level societies. Further, preliminary data do not indicate greater calling rates in larger core units of C. a. ruwenzorii compared to smaller units. These findings support the view that these primates’ vocalizations tend to be relatively conserved despite large differences in social organization.

On the -oo Suffix of Campbell’s Monkeys

Ouattara et al. (2009a,b) make the novel claim that Campbell’s monkey alarm calls demonstrate a simple pattern of linguistic morphology. The authors observe that there are at least two distinct alarm calls (called krak and hok) that are used in two different predatory contexts, and that each may be followed by a low frequency sound (called -oo) that alters the meaning of both calls in predictable ways, allowing contexts with reduced level of threat. In light of these facts, -oo is analyzed as a meaning-bearing, combinatorial unit. However, the claim that a non-human communication system has a combinatorial system (however primitive) is rare in the literature (see x5 for related patterns), and, indeed, is antithetical to certain claims that structural hierarchy is unique to human language (e.g., Bolhuis et al. 2014). Moreover, it has been noted (Schlenker et al. 2014) that there is redundancy between the apparent semantic contribution of -oo and the semantic contribution of a variety of other signal manipulations (e.g. calling rate) that are easiest to explain via non-compositional mechanisms. These facts warrant particular caution when evaluating the pattern as a possible counterexample to generalizations about human language. Thus, in this squib, we examine the compositional hypothesis further. As counterpoint, we consider a class of more conservative hypotheses in which -oo does not itself bear meaning, but instead arises as the side effect of other articulatory processes that noncompositionally affect call meaning. Key to such hypotheses is the premise that -oo is articulatorily parasitic on another phonetic process. A major contribution of this squib is thus phonetic: considering the acoustic properties of -oo, we conclude that complex calls (krakoo and hokoo) are produced with a two pulses of a single breath-group. Critically, the production of these complex calls requires an additional articulatory gesture and thus an increase in articulatory effort. An increase in articulatory effort would not be expected on an analysis in which -oo arises as a phonetic side effect; we accordingly reject these alternate hypotheses, thus strengthening the robustness of the combinatorial analysis.

Alarm calls of a cooperative bird are referential and elicit context-specific antipredator behavior

In a world where predators use an array of hunting strategies, prey must adapt their escape responses accordingly or be eaten. The ability of prey to convey information on predator type or its location to other members of social groups has received minimum attention in research regarding avian acoustic communication. Using an array of practical approaches, we present novel evidence that a social bird species possesses 2 distinct alarm calls for aerial versus terrestrial predators that can inform others of both the type of predator and its likely location.

Social familiarity affects Diana monkey (Cercopithecus diana diana) alarm call responses in habitat-specific ways.

Male Diana monkeys produce loud and acoustically distinct alarm calls to leopards and eagles that propagate over long distances, much beyond the immediate group. Calling is often contagious, with neighbouring males responding to each other’s calls, indicating that harem males communicate both to local group members and distant competitors. Here, we tested whether male Diana monkeys responding to each other’s alarm calls discriminated familiar from unfamiliar callers in two populations in Taï Forest (Ivory Coast) and on Tiwai Island (Sierra Leone). At both sites, we found specific acoustic markers in male alarm call responses that discriminated familiar from unfamiliar callers, but response patterns were site-specific. On Tiwai Island, males responded to familiar males’ eagle alarms with ‘standard’ eagle alarm calls, whereas unfamiliar males triggered acoustically atypical eagle alarms. The opposite was found in Taï Forest where males responded to unfamiliar males’ eagle alarm calls with ‘standard’ eagle alarms, and with atypical eagle alarms to familiar males’ calls. Moreover, only Taï, but not Tiwai, males also marked familiarity with the caller in their leopard-induced alarms. We concluded that male Diana monkeys encode not only predator type but also signaller familiarity in their alarm calls, although in population-specific ways. We explain these inter-site differences in vocal behaviour in terms of differences in predation pressure and population density. We discuss the adaptive function and implications of this behaviour for the origins of acoustic flexibility in primate communication.

Rates of signal evolution are associated with the nature of interspecific communication

Some signals vary greatly, whereas others are remarkably similar across distantly related species. Here, we ask how the suite of receivers and information communicated correlates with signal evolution by comparing 2 different signals across the same set of species. Within the Old World leaf warblers (Phylloscopidae), each species utters 2 acoustically distinct alarm calls. The first, termed a call, is used in interactions with conspecifics as a well as during confrontations with predators and nest-parasitic cuckoos. The second, termed a call, is primarily used in the presence of nest-parasitic cuckoos. The rasp call precedes aggressive attacks on cuckoos and attracts surrounding heterospecifics that are also potential hosts. The general call attracts a wide range of species threatened by predators, including those that are not cuckoo hosts. Acoustic features of general calls evolve >5x faster than rasp calls. We argue that rasp calls show strong stasis because they have a restricted function as aggressive antiparasite signals, whereas multiple contexts and receivers have promoted divergence in general calls. These results support the idea that variation in the suite of receivers is a powerful force affecting signal evolution.

Living in a landscape of fear: the impact of predation, resource availability and habitat structure on primate range use

Spatial variation in predation risk generates a ‘landscape of fear’, with prey animals modifying their distribution and behaviour in response to this variable predation risk. In systems comprising multiple predators and prey species, a key challenge is distinguishing the independent effects of different predator guilds on prey responses. We exploited the acoustically distinct alarm calls of samango monkeys, Cercopithecus mitis erythrarchus, to create a predator-specific landscape of fear from eagles to assess its impact on space use within mixed regressive–spatial regressive models incorporating data on resource distribution and structural characteristics of the environment. The landscape of fear from eagles was the most significant determinant of samango range use, with no effect of resource availability. The monkeys also selected areas of their range with higher canopies and higher understory visibility, behaviour consistent with further minimizing risk of predation. These results contrast with those of vervet monkeys, Chlorocebus aethiops pygerythrus, at the same site for which the landscapes of fear from leopards and baboons were the most significant determinants of space use. While highlighting that predation risk is a key driver of primate behaviour in this population, the landscapes of fear experienced by samango monkeys and vervet monkeys appear to differ despite exposure to identical predator guilds. This emphasizes the importance of distinguishing between the risk effects of different predators in understanding prey ecology, but also that closely related prey species may respond to these predator-specific risks in different ways.

Alarm Calls of Marmosets (Callithrix geoffroyi) to Snakes and Perched Raptors

Communication about the presence of predators is an important benefit of group living. Critical information about the nature of danger can be conveyed through referential alarm calls. Raptors pose a significant predatory threat to callitrichid species. Unlike a raptor in flight, a perched raptor cannot attack suddenly at great speed, and it can be monitored from a safe distance. In this sense a perched bird may pose a threat more similar to that of a terrestrial predator such as a snake. Here we compare predatory contexts by addressing these two questions: 1) Do marmosets produce acoustically distinct alarm calls to snake models and perched raptor models? 2) Do the visual responses of the marmosets to the playbacks of perched raptor–elicited calls differ from those given to the playbacks of calls given in response to snakes? We recorded alarm calls from two groups of outdoor-housed Geoffroy’s marmosets (Callithrix geoffroyi) in response to predator models. Later, we played back stimuli created from these recordings to the marmosets and scored their gaze direction. Results show that calls given to models of perched raptors are acoustically distinct from those given to models of snakes. Further, the relative number of upward to downward looks while listening to the playbacks of perched raptor–elicited calls was significantly greater than it was for snake-elicited calls. Reactions to airborne raptors are known to elicit freezing or rapid flight, neither of which occurred in response to our playbacks. Our data suggest a greater complexity in the alarm call repertoire of marmosets than previously demonstrated.

Male blue monkey alarm calls encode predator type and distance

There is considerable controversy about what is encoded when primates produce alarm calls to an external event. Results are often compatible with multiple explanations, such as differences in a caller's perceived level of threat, direction of attack or category of predator. Using acoustic predator models, we investigated how male blue monkeys', Cercopithecus mitis stuhlmani , alarm calls were affected by predator type, distance, and elevation. We found that individuals produced two types of acoustically distinct alarm calls, ‘pyows’ and ‘hacks’. Males produced these calls in predator-specific ways, but call rates were also affected by the distance and location of the predator. We discuss these findings in relation to the different predator hunting techniques and two common antipredator strategies pursued by monkeys, predator deterrence and conspecific warning.

Eavesdropping of woodchucks (Marmota monax) and eastern chipmunks (Tamias striatus) on heterospecific alarm calls

Individuals of 1 species might obtain information by eavesdropping on calls produced by a syntopic species. Intercepting alarm calls allows the eavesdropper to respond with antipredator behavior without the need to produce its own call, which might attract the attention of a predator. We examined eavesdropping on heterospecific alarm calls by nonsocial eastern chipmunks (Tamias striatus) and woodchucks (Marmota monax), which live in the same community, share some predators, are solitary, and produce distinct alarm calls. If these 2 species recognize heterospecific alarm calls, we should see antipredator behaviors similar to those displayed upon hearing a conspecific’s alarm call. We broadcast single alarm calls of woodchucks, eastern chipmunks, and American crows (Corvus brachyrhynchos) to individuals of the first 2 species, using the territorial song of the syntopic male black-capped chickadee (Poecile atricapillus) as a control. Woodchucks became more vigilant after hearing both conspecific and heterospecific alarm calls compared with controls; however, they spent more time vigilant in response to conspecific alarm calls compared to heterospecific alarm calls. Thus, woodchucks apparently can recognize heterospecific alarm calls, but they appear to process conspecific and heterospecific calls differently. Eastern chipmunks responded to heterospecific alarm calls, but sample sizes were small and the results not definitive. Our results suggest that nonsocial mammals might benefit from eavesdropping on heterospecifics.

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.

The irrelevance of individual discrimination in meerkat alarm calls

Individual discrimination is an important element in the evolution of social behaviour and is particularly important in social living species which show intense intragroup interactions. Numerous previous studies, particularly with nonhuman primates, ground squirrels and marmots, demonstrate the widespread ability of various species to signal and perceive individual identity from vocalizations. The function of individually different alarm calls is thought to assist in the detection of unreliable individuals. This would allow individuals to optimize the benefits of antipredator behaviour by self-assessing the relative predation risk, and responding selectively to reliable callers. In this study we investigated whether meerkats, Suricata suricatta, a social mongoose, discriminated among alarm callers individually, and adjusted their response accordingly. Several parameters of the acoustic structure of meerkat alarm calls were measured and analysed with multivariate statistics. Within groups, the 10-fold cross-validation of a multinomial regression yielded, on average, 90% correct assignment. This strongly suggests that meerkats have individually distinct alarm calls. With a habituation–dishabituation playback experiment, we then tested whether meerkats use this information to discriminate between individual callers. Receivers did not distinguish between different individuals in the playback experiments. In meerkats, unreliable callers appear to be uncommon, and the cost of being predated might exceed the costs of responding to an unreliable caller, thus rendering a reliability-based discrimination mechanism unnecessary. Although meerkat alarm calls contain information on individual identity, this information does not appear to be important to the receivers in this context.

A forest monkey’s alarm call series to predator models

Some non-human primates produce acoustically distinct alarm calls to different predators, such as eagles or leopards. Recipients respond to these calls as if they have seen the actual predator, which has led to the notion of functionally referential alarm calls. However, in a previous study with free-ranging putty-nosed monkeys (Cercopithecus nictitans martini), we demonstrated that callers produced two acoustically distinct alarm calls to eagle shrieks and leopard growls, but both alarm calls were given to both predators. We can think of two basic explanations for this surprising result, a methodological and theoretical one. Firstly, acoustic predator models may not always be suitable to test alarm call behaviour in primates, sometimes causing uncharacteristic behaviour. Secondly, referential alarm calling may not be a universal feature of primate alarm call systems. Considering the methodological and theoretical importance of these possibilities, we conducted a follow-up study using life-sized leopard, eagle, and human models on the same population and compared the resulting vocal responses to those given to acoustic predator models. We compared the alarm call series given to each of these predator model types and found a considerable degree of consistency suggesting that the mode of presentation did not affect anti-predator calling strategies. However, evidence for audience effects on calling behaviour was inconclusive. While it appears that predator class is reliably encoded by different call series types irrespective of the mode of presentation, observations of these same call series given in non-predatory contexts indicate that predator class is unlikely to be the relevant organising principle underlying the alarm-calling behaviour in this species. We conclude by offering an alternative, non-referential, account of the alarm-calling system exhibited by this species.

What’s in a name? The vervet predator calls and the limits of the Washburnian synthesis

After the Second World War, a renaissance in field primatology took place in the United States under the aegis of the ‘new physical anthropology’. Its leader, Sherwood Washburn, envisioned a science uniting studies of hominid fossils with Darwinian population genetics, experimental functional anatomy, and field observation of non-human primates and human hunter–gatherers. Thanks to Washburn’s stimulus, his colleague at Berkeley, the bird ethologist Peter Marler, took up the study of the natural communicative behaviour of apes and monkeys. When Marler’s first primatological student, Thomas Struhsaker, reported in the mid-1960s that the vervet monkeys of Amboseli, Kenya, give acoustically distinct alarm calls to different predators, and respond to alarm calls as if to the sight of those predators, a debate broke out over whether the vervet calls thus function as names, translating as ‘leopard’, ‘eagle’ and ‘python’. Washburn and his students argued that no matter what the behavioural evidence, vervet calls could not be predator names, since monkeys had been shown to lack the neuroanatomical basis of naming. This controversy thus reveals, first, the persistence of older patterns of disciplinary allegiance within the new, synthetic physical anthropology; and second, the impotence of adaptationist Darwinism — common to both sides of the debate — as a force for unity.

Multiple discontinuities in nonhuman vocal tracts – A reply

Male West African Diana monkeys (Cercopithecus diana)produce acoustically distinct alarm calls to two of their mainpredators, the crowned eagle and the leopard. The calls are re-markable in their acoustic structure for at least three reasons.First, they exhibit clear formant frequencies, a defining featureof human speech. Second, Diana monkeys are able to modifythe basic structure of these formants by creating formant tran-sitions. In leopard alarm calls, the first formant describesa transition of approximately 150 Hz, while the transition ofthe second one is about 200 Hz. In striking contrast, the twoformants remain relatively constant in eagle alarm calls (Riedeand Zuberbu¨hler, 2003a,b). Experiments have shown that theseacoustic differences have semantic value to recipients (Zuber-bu¨hler, 2003). Third, the first and second formants in Dianamonkeys’ alarm calls are in close proximity, a feature not nor-mally observed in animal vocalizations. We propose that thisformant proximity is the result of a discontinuity (or ‘non-uni-formity’) along the monkey’s vocal tract.In a previous paper (Riede et al., 2005), we sought to un-derstand the production mechanisms of the Diana monkeyvocal system using a computer modelling technique, basedon anatomical data. Lieberman (2006) has challenged a num-ber of our findings. His concerns relate to the possibility oftongue movements, pharyngeal constrictions, and the posi-tion of the larynx. Additionally, the technique of derivingvocal tract area functions from lateral x-rays is criticized.We would like to respond to these criticisms by first sum-marizing our main point, the notion of non-uniform vocaltracts in nonhumans, before responding in detail to Lieber-man’s critique.How do Diana monkeys achieve vocal flexibility?When an acoustic wave propagates in a cavity, such as avocal tract, boundary effects determine the acoustic structureof the signal. The acoustic impedance of the cavity (Z) isnot constant over the cross section of the cavity but relatesto air density (r), speed of sound (c), and area of the cross sec-tion (A) according to Eq. (1).Z ¼r cAð1ÞThe last factor (i.e., a change in the cross section area) ismost relevant in this context. We suggested that the formantpatterns observed in Diana monkey alarm calls are the likelyresult of an area change in the vocal tract caused by an artic-ulatory movement and permanent presence of a constriction(Riede et al., 2005). A uniform vocal tract, in contrast, canonly generate equally spaced formant frequencies withoutany transitions. Using phonetic terminology, a uniform vocaltract takes a ‘‘neutral configuration’’ which produces a ‘‘neu-tral sound’’ (Laver, 1994), as for example observed in thegrunts of chacma baboons (reviewed in Riede et al., 2005).However, some vocalizations, including human speech sounds,dog growls, or rhesus monkey coo calls, deviate from this pat-tern (Riede and Fitch, 1999; Table 1 of this reply). Diana mon-key alarm calls are another good example of such deviationfrom the ‘‘equal formant distance pattern,’’strongly suggestingthat their vocal tract is non-uniform (i.e., constricted some-where along its length between vocal folds and lips) duringvocal production (Riede and Zuberbu¨hler, 2003b; Fig. 1 inRiede et al., 2005).Additionally, Diana monkeys are able to change the contourof these formants when responding to leopards by creating for-mant transitions. To account for the transitions, we predicted

The responses of black-casqued hornbills to predator vocalisations and primate alarm calls

AbstractBlack-casqued hornbills (Ceratogymna atrata) forage in small flocks in the tropical forests of West Africa, often in the vicinity of primate groups, including Diana and Campbell's monkeys (Cercopithecus diana, C. campbelli). Previous work has shown that these monkey species produce acoustically distinct alarm calls to crowned eagles (Stephanoaetus coronatus) and leopards (Panthera pardus), two of their main predators. Black-casqued hornbills are highly vulnerable to crowned eagles, but not leopards, suggesting that individuals may respond differently to these two predators. We analysed the vocal response of these birds to field playbacks conducted on different monkey species in Taï National Park, Ivory Coast. We tested six stimuli, three of which related to the presence of a crowned eagle (eagle shrieks, Diana and Campbell's eagle alarm calls) and three to the presence of a leopard (leopard growls, Diana and Campbell's leopard alarm calls). Results showed that hornbills consistently distinguished between eagle- and leopard-related stimuli, suggesting that birds attended to the predator class associated with the various stimuli. Second, within eagle-related stimuli, hornbills responded more strongly to the actual predator vocalizations than the associated alarm calls. One interpretation of these data is that birds were sensitive to the precision of information concerning the location of the eagle. We discuss these results in light of previous data on hornbill behaviour and cognitive capacities.

Meaning and emotion in animal vocalizations.

Historically, a dichotomy has been drawn between the semantic communication of human language and the apparently emotional calls of animals. Current research paints a more complicated picture. Just as scientists have identified elements of human speech that reflect a speaker's emotions, field experiments have shown that the calls of many animals provide listeners with information about objects and events in the environment. Like human speech, therefore, animal vocalizations simultaneously provide others with information that is both semantic and emotional. In support of this conclusion, we review the results of field experiments on the natural vocalizations of African vervet monkeys, diana monkeys, baboons, and suricates (a South African mongoose). Vervet and diana monkeys give acoustically distinct alarm calls in response to the presence of leopards, eagles, and snakes. Each alarm call type elicits a different, adaptive response from others nearby. Field experiments demonstrate that listeners compare these vocalizations not just according to their acoustic properties but also according to the information they convey. Like monkeys, suricates give acoustically distinct alarm calls in response to different predators. Within each predator class, the calls also differ acoustically according to the signaler's perception of urgency. Like speech, therefore, suricate alarm calls convey both semantic and emotional information. The vocalizations of baboons, like those of many birds and mammals, are individually distinctive. As a result, when one baboon hears a sequence of calls exchanged between two or more individuals, the listener acquires information about social events in its group. Baboons, moreover, are skilled "eavesdroppers:" their response to different call sequences provides evidence of the sophisticated information they acquire from other individuals' vocalizations. Baboon males give loud "wahoo" calls during competitive displays. Like other vocalizations, these highly emotional calls provide listeners with information about the caller's dominance rank, age, and competitive ability. Although animal vocalizations, like human speech, simultaneously encode both semantic and emotional information, they differ from language in at least one fundamental respect. Although listeners acquire rich information from a caller's vocalization, callers do not, in the human sense, intend to provide it. Listeners acquire information as an inadvertent consequence of signaler behavior.

A syntactic rule in forest monkey communication

Syntactic rules allow a speaker to combine signals with existing meanings to create an infinite number of new meanings. Even though combinatory rules have also been found in some animal communication systems, they have never been clearly linked to concurrent changes in meaning. The present field experiment indicates that wild Diana monkeys, Cercopithecus diana, may comprehend the semantic changes caused by a combinatory rule present in the natural communication of another primate, the Campbell's monkey, C. campbelli. Campbell's males give acoustically distinct alarm calls to leopards, Panthera pardus, and crowned-hawk eagles, Stephanoaetus coronatus, and Diana monkeys respond to these calls with their own corresponding alarm calls. However, in less dangerous situations, Campbell's males emit a pair of low, resounding ‘boom’ calls before their alarm calls. Playbacks of boom-introduced Campbell's alarm calls no longer elicited alarm calls in Diana monkeys, indicating that the booms have affected the semantic specificity of the subsequent alarm calls. When the booms preceded the alarm calls of Diana monkeys, however, they were no longer effective as semantic modifiers, indicating that they are meaningful only in conjunction with Campbell's alarm calls. I discuss the implications of these findings for the evolution of syntactic abilities.

Alarm calls of Belding's ground squirrels to aerial predators: nepotism or self-preservation?

Belding's ground squirrels (Spermophilus beldingi) give acoustically distinct alarm calls to aerial and terrestrial predators. The animals typically give multiple-note trills to predatory mammals, and single-note whistles to flying hawks. During a 9-year study of free-living S. beldingi at Tioga Pass, California, the adaptive significance of the whistle call was investigated. Data were gathered on 664 ground squirrel-hawk interactions, most of which were induced by flying trained raptors over individually marked study animals of known sex and age. The sight of a flying hawk and the sound of whistles stimulated widespread calling and running to shelter by the ground squirrels (Fig. 1). Wild raptors were rarely successful at capturing the rodents once a whistle had been given, and fewer callers than noncallers were killed (Table 1). Individuals of both sexes and all ages whistled equally often (Fig. 4), and females' tendencies to whistle were not affected by the presence of relatives, including offspring (Fig. 5). The most frequent callers were animals in exposed positions: far from cover and close to the predatory bird (Table 2). Taken together the data suggest that unlike trills, which increase vulnerability to terrestrial predators (Table 1) and function to warn relatives, whistle directly benefit callers by increasing their chances of escaping from hawks.