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.     

Tawny owl vocal activity is constrained by predation risk

The vocal behaviour of birds may be influenced by many factors, including the risk of being detected by a predator. In Doñana Protected Area, the tawny owl co‐exists alongside its intraguild predator, the eagle owl Bubo bubo. We considered four scenarios to study the vocal behaviour of tawny owls at dusk by analysing: A) the calling rate of all males in 29 sites; B) the calling rate at dusk of males living within the home range of the intraguild predator; C) the calling rate of males living within the home range of the intraguild predator between 60 and 90 min after sunset; and D) the duration of male vocal bouts in visits where eagle owls have called. In scenario A we found that only the number of conspecific males affected the calling rate of tawny owls. In scenario B we observed that the presence of an eagle owl calling constrained the calling rate of the intraguild prey. In scenario C we found that this effect seemed mostly associated to a contemporaneous detection of the intraguild predator’s calls. Finally, in scenario D we found no significant effects on bout duration. These results seem to indicate that tawny owls use their intraguild predator’s calls as a cue to assess predation risk, and then adjust their vocal behaviour in order to minimize predation risk by a predator that may locate its prey by its vocalizations.     

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.     

Is Alarm Calling Risky? Marmots Avoid Calling from Risky Places

Alarm calling is common in many species. A prevalent assumption is that calling puts the vocalizing individual at increased risk of predation. If calling is indeed costly, we need special explanations for its evolution and maintenance. In some, but not all species, callers vocalize away from safety and thus may be exposed to an increased risk of predation. However, for species that emit bouts with one or a few calls, it is often difficult to identify the caller and find the precise location where a call was produced. We analyzed the spatial dynamics of yellow-bellied marmot (Marmota flaviventris) alarm calling using an acoustic localization system to determine the location from which calls were emitted. Marmots almost always called from positions close to the safety of their burrows, and, if they produced more than one alarm call, tended to end their calling bouts closer to safety than they started them. These results suggest that for this species, potential increased predation risk from alarm calling is greatly mitigated and indeed calling may have limited predation costs.     

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.     

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.     

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.     

Kea Nestor notabilis mothers produce nest-specific calls with low amplitude and high entropy

Vocal behaviour of nesting altricial birds is subject to selection pressure from several sources. Offspring beg to attract parents’ attention, thus increasing the chances of being fed, but also increasing the chances of being detected by predators. Research on passerines has shown that parents may reduce the risk of nest predation by alarm calling to warn nestlings to be quiet, and by producing food calls which solicit begging when parents are present to defend the nestlings. Both nestlings and parents may reduce the risk of predator detection by producing calls of low amplitude and high entropy which are acoustically difficult to locate. Although extensive research has been undertaken on nesting passerine vocalizations, little is known about parrots in this regard, and studies are needed to determine whether parrots show similar adaptations. We investigated the calling behaviour of Kea Nestor notabilis mothers during the nesting period to determine whether maternal vocalizations were adapted in a way that could increase the chance of brood success. A microphone was installed inside the nest to record calls produced both inside the nest and in the direct vicinity. Our prediction was that calls outside the nest would be easy to locate and could function as alarm calls to alert conspecifics or distract the predator, whereas calls inside the nest would be difficult to locate and could serve to communicate with nestlings without alerting predators. Our results accorded with these predictions. Calls produced outside the nest were loud and tonal, and corresponded to previously described Kea alarm calls. Calls produced inside the nest, however, were high-entropy and low-amplitude calls, and formed a distinct structural category. We thus provide the first evidence that a parrot species has a vocal category for communication inside the nest, and that calls within this category are structured in a way that could reduce the risk of nest predation.     

Verreaux's eagles (Aquila verreauxi) as potential predators of hamadryas baboons (Papio hamadryas hamadryas) in Eritrea

In this paper we describe for the first time encounters of Verreaux's eagle (Aquila verreauxi) with hamadryas baboons (Papio hamadryas hamadryas) in the central highlands of Eritrea (15° 22′ N, 38° 58′ E, 2300 m). During 12 h of observation on 4 days, we observed four encounters of Verreaux's eagles with baboons, of which three can be classified as possible attacks. The baboons always responded with alarm calls. In three cases some immatures rushed to adult group members and clung to them, particularly to the adult male. Adult males threatened the eagle, and the whole group did not flee. The response of baboons towards smaller raptors like tawny eagles (Aquila rapax) and black kites (Milvus migrans) was very different. The adult baboons gave no alarm barks but scanned the raptors. The permanent presence of a pair of Verreaux's eagles in the home range of the baboons may represent a considerable predation pressure, at least for immature baboons. Am. J. Primatol. 47:61–66, 1999. © 1999 Wiley‐Liss, Inc.     

The Sound of Danger: Threat Sensitivity to Predator Vocalizations,Alarm Calls,and Novelty in Gulls

The threat sensitivity hypothesis predicts that organisms will evaluate the relative danger of and respond differentially to varying degrees of predation threat. Doing so allows potential prey to balance the costs and benefits of anti-predator behaviors. Threat sensitivity has undergone limited testing in the auditory modality, and the relative threat level of auditory cues from different sources is difficult to infer across populations when variables such as background risk and experience are not properly controlled. We experimentally exposed a single population of two sympatric gull species to auditory stimuli representing a range of potential threats in order to compare the relative threat of heterospecific alarm calls, conspecific alarms calls, predator vocalizations, and novel auditory cues. Gulls were able to discriminate among a diverse set of threat indicators and respond in a graded manner commensurate with the level of threat. Vocalizations of two potential predators, the human voice and bald eagle call, differed in their threat level compared to each other and to alarm calls. Conspecific alarm calls were more threatening than heterospecfic alarm calls to the larger great black-backed gull, but the smaller herring gull weighed both equally. A novel cue elicited a response intermediate between known threats and a known non-threat in herring gulls, but not great black-backed gulls. Our results show that the relative threat level of auditory cues from different sources is highly species-dependent, and that caution should be exercised when comparing graded and threshold threat sensitive responses.     

A community-level evaluation of the impact of prey behavioural and ecological characteristics on predator diet composition

Although predation avoidance is the most commonly invoked explanation for vertebrate social evolution, there is little evidence that individuals in larger groups experience lower predation rates than those in small groups. We compare the morphological and behavioural traits of mammal prey species in the Taï forest, Ivory Coast, with the diet preferences of three of their non-human predators: leopards, chimpanzees and African crowned eagles. Individual predators show marked differences in their predation rates on prey species of different body sizes, but clear patterns with prey behaviour were apparent only when differences in prey habitat use were incorporated into the analyses. Leopard predation rates are highest for terrestrial species living in smaller groups, whereas eagle predation rates are negatively correlated with group size only among arboreal prey. When prey predation rates are summed over all three predators, terrestrial species incur higher predation rates than arboreal species and, within both categories, predation rates decline with increasing prey group size and decreasing density of groups in the habitat. These results reveal that it is necessary to consider anti-predator strategies in the context of a dynamic behavioural interaction between predators and prey.     

Effect of alarm calling by male Red‐winged Blackbirds on nestling begging and female provisioning behavior

ABSTRACT Nestling begging and parental provisioning can attract nest predators and reduce reproductive success, so parents and their offspring might be expected to respond adaptively by minimizing predator‐attracting cues when predators threaten nests. Male Red‐winged Blackbirds (Agelaius phoeniceus) are well known for their antipredator alarm calls that contain information about the approach of potential nest predators. We examined the begging behavior of nestlings and the provisioning behavior of females in response to antipredator alarm calls of males to test the adaptive response hypothesis. Playback experiments provided no evidence that alarm calls function to switch off vocal begging; nestlings were equally likely to beg vocally during playback and control periods. Video recordings showed that male alarm calling had no significant effect on inappropriate vocal begging (in the absence of an adult), but significantly reduced the incidence of spontaneous calling (in the absence of begging). Adult females responded to male antipredator alarm calls by delaying their provisioning visits. In addition, although having no significant effect on use of nest‐arriving calls by females, male alarm calling significantly reduced their use of nest‐leaving calls. We conclude that nestling and female Red‐winged Blackbirds respond to male alarm calls in ways that might reduce the risk of predation, but nestlings beg vocally when females arrive to feed them, regardless of male alarm calling, perhaps to avoid a competitive disadvantage with broodmates.     

Situational Specificity in Alpine-marmot Alarm Communication

We studied the degree to which alpine marmot (Marmota marmota L.) alarm calls function as communication about specific external stimuli. Alpine marmots emit variable alarm calls when they encounter humans, dogs, and several species of aerial predators. The first part of the study involved observations and manipulations designed to document contextual variation in alarm calls. Alarm calls varied along several acoustic parameters, but only along one that we examined, the number of notes per call, was significantly correlated with the type of external stimulus. Marmots were more likely to emit single-note alarm calls as their first or only call in response to an aerial stimulus, and multiple-note alarm calls when first calling to a terrestrial stimulus. This relationship was not without exceptions; there was considerable variation in the number of notes they emitted to both aerial and terrestrial stimuli, and a single stimulus type — humans — elicited a wide range of acoustic responses. The second part of the study involved playing back three types of alarm calls to marmots and observing their responses. Marmots did not have overtly different responses to the three types of played-back alarm calls. Our results are consistent with the hypotheses that: 1. Alarm calls do not refer to specific external stimuli; 2. Alarm calls function to communicate the degree of risk a caller experiences; and 3. Alarm calls require additional contextual cues to be properly interpreted by conspecifics.     

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.     

Brief communication: Plio‐Pleistocene eagle predation on fossil cercopithecids from the Humpata Plateau,southern Angola

Recent studies suggest a large raptor such as the crowned eagle (Stephanaoetus coronatus) was responsible for collecting at least a portion of the primate fauna from the South African fossil site of Taung, including its lone hominin specimen. This taphonomic signature at Taung is currently regarded as a unique and, most likely, isolated case in primate and human evolution. However, the activities of large, carnivorous birds should also be detectable at other primate fossil localities in Africa if raptors have been a strong selective force throughout primate evolution. Over the last 60 years, a collection of extinct cercopithecids has been assembled from several cave breccias on the Humpata Plateau in southern Angola. The material, dated near the Plio‐Pleistocene boundary, includes an assortment of craniodental and postcranial remains variably assigned to Papio (Dinopithecus) cf. quadratirostris, Parapapio, Cercopithecoides, and Theropithecus. We compare the Angolan and Taung material to remains of extant primates killed by crowned eagles in the Ivory Coast's Tai National Park. Our analysis indicates that the size distribution and composition of fauna from the localities is quite similar and that there are striking consistencies in damage to the crania from each site. The absence of large bodied (>20 kg) primates and other mammalian taxa at the Taung hominin locality and Tai, and their rarity in Angola, combined with the strong likelihood that raptor nests were positioned near fissure openings at both fossil localities, provides additional support for eagle involvement. On the basis of this evidence, we conclude that at least some of the Angolan cercopithecids were most likely raptor prey and hypothesize that raptor predation has been a strong and perhaps underappreciated selective force during the course of primate evolution. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

Conspicuous calling near cryptic nests: a review of hypotheses and a field study on white‐browed scrubwrens

Predation is an important source of nest mortality in many bird species and calling near the nest can increase this risk, yet adults of many species regularly vocalize near their nests. Some of these calls serve clearly adaptive functions, such as alarm or provisioning calls. However, many species also give conspicuous ‘contact’ calls near the nest, which is puzzling because the function of these calls is unclear, and they might attract predators. Most studies of parental vocalizations near nests have focused on specific vocalizations and single hypotheses, yet there is a diversity of vocalization types and potential functions. We review the literature on the diversity and possible function of parental vocalizations near the nest, and then investigate the puzzle of conspicuous contact calling near nests by white‐browed scrubwrens Sericornis frontalis. In scrubwrens, ‘chip‐zz’ contact calls were almost always used when adults approached nests, and when they approached one another or changed location. Call composition also changed: the proportion of ‘chip’ elements increased as callers approached the nest or other adults. Neither adult sex nor nestling age affected calling. Thus, chip‐zz calls appear to be used as ongoing signals to other group members of the caller's activity and location, particularly relative to the nest. Nestlings appeared to use the calls as cues of adult arrival, and increased calling as adults approached nests. Further, adults called less after a predator was on the territory, suggesting that parents may be able to reduce the risk of chip‐zz calls betraying nest location, or possibly use the absence of calling as a signal of danger. This study thus demonstrates that calling near nests could inform both adults and nestlings about the caller's behaviour, and could serve multiple functions. Future studies will need to experimentally test these functions, as well as the other hypotheses reviewed here.     

Recognition of Predator and Competitor Calls in Nonhuman Primates and Birds: a Preliminary Report

Field playback experiments were conducted in the Kibale Forest, Uganda to determine whether three monkeys (redtail monkeys, blue monkeys, and red colobus monkeys) and one bird (great blue turaco) [1] respond with flight and/or increased vigilance to exemplars of calls given by potential predators (crowned eagle, chimpanzee) and [2] respond differently to food competitors vs. noncompetitors (black-and-white casqued hornbill, chimpanzee vs. red colobus). Because the chimpanzee is both a potential predator of all subject species and a food competitor of blue and redtail monkeys and great blue turacos, we also examined whether chimpanzee calls induced responses appropriate to potential predation or competition. Each subject species responded differentially to the calls of potential predators, competitors and noncompetitors. Thus, acoustic cues appeared sufficient for the detection of predators and competitors.     

Fatal attack on a Rylands' bald-faced saki monkey (<Emphasis Type="Italic">Pithecia rylandsi</Emphasis>) by a black-and-white hawk-eagle (<Emphasis Type="Italic">Spizaetus melanoleucus</Emphasis>)

Predation risk has played an important role in primate behavioral evolution, yet natural primate–predator interactions are rarely observed. We describe the consumption and probable predation of an adult bald-faced saki monkey (Pithecia rylandsi) by a black-and-white hawk-eagle (Spizaetus melanoleucus) at the Los Amigos Biological Station in lowland Amazonian Peru. To our knowledge, this is the first published case of a black-and-white hawk-eagle consuming any primate species. We contend that while most reported observations of successful and attempted predation by raptors involves the largest and most notorious species (i.e. the harpy eagle), smaller and lesser known species like S. melanoleucus should be considered more seriously as a predator of neotropical primates. We discuss the predation event in the context of understanding what other neotropical primates might be vulnerable to S. melanoleucus predation given its body size and hunting tactic.     

Inter- and Intraspecific Variation in the Acoustic Habitats of Three Marmot Species

Closely related species often have remarkably different vocalizations. Some of the variation in acoustic structure may result from species adapting their calls to maximize transmission through their acoustic environments. We document the relative magnitude of inter- and intraspecific variation in acoustic transmission properties of the habitats of three closely related marmot species to study the relative importance that the acoustic environment may have played in selecting for species-specific marmot alarm calls. We used spectrogram correlation to quantify the degree to which pure tones and alarm calls changed as they were broadcast through marmot home ranges to describe the acoustic habitats of golden (M. candata aurea), yellow-bellied (M. flaviventris), and alpine (M. marmota L.) marmots. Species lived in quantifiably different acoustic habitats. One analysis partitioned variation between species and between marmot social groups (nested within species). We found significant interspecific variation in the acoustic transmission fidelity of the three species' habitats and insignificant intraspecific variation between social groups. Further analysis of a larger sample of alarm calls broadcast through golden marmot social groups found significant intraspecific variation. Interspecific variation greater than intraspecific variation suggests that variable acoustic habitats may be responsible for at least some of the interspecific variation in alarm call structure. This is the first study to use spectrogram correlation to describe habitat acoustics. We discuss aspects of the method that may be useful for others seeking to quantify habitat acoustics.     

Rapid acquisition of an alarm response by a neotropical primate to a newly introduced avian predator

Predation is an important selective pressure in natural ecosystems. Among non-human primates, relatively little is known about how predators hunt primate prey and how primates acquire adaptive responses to counteract predation. In this study we took advantage of the recent reintroduction of radio-tagged harpy eagles (Harpia harpyja) to Barro Colorado Island (BCI), Panama to explore how mantled howler monkeys (Alouatta palliata), one of their primary prey, acquire anti-predator defences. Based on the observation that harpies follow their prey prior to attack, and often call during this pursuit period, we broadcast harpy eagle calls to howlers on BCI as well as to a nearby control population with no harpy predation. Although harpies have been extinct from this area for 50-100 years, results indicate that BCI howlers rapidly acquired an adaptive anti-predator response to harpy calls, while showing no response to other avian vocalizations; howlers maintained this response several months after the removal of the eagles. These results not only show that non-human primates can rapidly acquire an alarm response to a newly introduced predator, but that they can detect and identify predators on the basis of acoustic cues alone. These findings have significant implications both for the role of learning mechanisms in the evolution of prey defence and for conservation strategies, suggesting that the use of 'probing' approaches, such as auditory playbacks, may highly enhance an a priori assessment of the impact of species reintroduction.