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.     

Adaptive differences in response to two types of parental alarm call in altricial nestlings

Vertebrate alarm calls can contain information about the type of predator and the degree of danger, but young animals often respond to alarm calls differently from adults. The distinct behaviour of young may reflect an imperfect stage in the gradual development of the adult response, or a response adapted to specific risks faced by young. In this study, we tested whether nestling white-browed scrubwrens, Sericornis frontalis, responded to different alarm calls according to their specific risks of predation. As predators on the ground pose a danger to scrubwren nestlings, whereas flying predators do not, we predicted that they would respond to ground alarm calls but not to aerial alarm calls. In a field playback experiment, we tested the response of young to aerial and ground alarm calls, each presented in a shorter (less urgent) and longer (more urgent) form. We found that both 5- and 11-day-old nestlings responded to ground alarm calls, and did so more strongly to the more urgent playback. By contrast, the response to aerial alarm calls started to develop only towards the end of the nestling stage. Thus, scrubwren nestlings can distinguish between different types of alarm calls and react more strongly to calls warning of a predator posing greater danger, appropriate to the nestling stage of development. Furthermore, they use the length of ground alarm calls as an indicator of the degree of danger.     

Age Differences in the Responses to Adult and Juvenile Alarm Calls by Bonnet Macaques (Macaca radiata)

This study examined the differential responses to alarm calls from juvenile and adult wild bonnet macaques ( Macaca radiata ) in two parks in southern India. Field studies of several mammalian species have reported that the alarm vocalizations of immature individuals are often treated by perceivers as less provocative than those of adults. This study documents such differences in response using field-recorded playbacks of juvenile and adult alarm vocalizations. To validate the use of playback vocalizations as proxies of natural calls, we compared the responses of bonnet macaques to playbacks of alarm vocalizations with responses engendered by natural alarm vocalizations. We found that the frequency of flight, latency to flee, and the frequency of scanning to vocalization playbacks and natural vocalizations were comparable, thus supporting the use of playbacks to compare the effects of adult and juvenile calls. Our results showed that adult alarm calls were more provocative than juvenile alarm calls, inducing greater frequencies of flight with faster reaction times. Conversely, juvenile alarm calls were more likely to engender scanning by adults, a result interpreted as reflecting the lack of reliability of juvenile calls. Finally, we found age differences in flight behavior to juvenile alarm calls and to playbacks of motorcycle engine sounds, with juveniles and subadults more likely to flee than adults after hearing such sounds. These findings might reflect an increased vulnerability to predators or a lack of experience in young bonnet macaques.     

Ontogeny of conspecific and heterospecific alarm call recognition in wild Verreaux's sifakas (Propithecus verreauxi verreauxi)

The production of vocalizations in nonhuman primates is predominantly innate, whereas learning influences the usage and comprehension of vocalizations. In this study, I examined the development of alarm call recognition in free-ranging infant Verreaux's sifakas. Specifically, I investigated their ability to recognize conspecific alarm calls as well as those of sympatric redfronted lemurs (Eulemur fulvus rufus) in Kirindy forest, western Madagascar. Both species have functionally referential alarm calls for aerial predators and give general alarm calls for both aerial and general predators and also other kinds of threats, such as intergroup encounters with conspecifics. I conducted playback experiments with members of two birth cohorts (nine and ten individuals) to determine the age at which infant Verreaux's sifakas discriminate between conspecific alarm calls, heterospecific alarm calls, and non-alarm vocalizations (parrot song). Most 3-4 months old infants fled toward adults after hearing any playback stimuli, whereas 4-5-month-old infants did so only after presentation of alarm calls. Moreover, all infants of these age classes showed a longer latency to flee after the parrot song indicating their emerging ability to discriminate between alarm calls and non-alarm stimuli. At an age of about 6 months, infants switched from fleeing toward adults to performing adult-like escape responses after presentation of conspecific and heterospecific alarm calls. Thus, the ability to discriminate between alarm from non-alarm stimuli precedes the appearance of adult-like responses. The transition to adult-like escape behavior was coincident with the physical independence of infants from their mothers.     

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.     

Age differences and developmental trends in alarm peep responses by squirrel monkeys (Saimiri sciureus)

Alarm calls can code for different classes of predators or different types of predatory threat. Acoustic information can also encode the urgency of threat through variations in acoustic features within specific alarm call types. Squirrel monkeys (Saimiri sciureus) produce an alarm call, known as the alarm peep, in highly threatening situations. Infant squirrel monkeys appear to have an innate predisposition to respond to alarm peeps but require experience to associate alarm peeps with the appropriate type of predatory threat [Herzog & Hopf, American Journal of Primatology 7:99-106, 1984]. Little is known about age-related differences in the type or frequency of response to alarm peeps, or the development of alarm peep response in infants. The purpose of this study was to test experimentally the response strategies of different age classes of squirrel monkey to the playback of alarm peeps that were produced by infants, juveniles, or adults. Results suggest that infants, juveniles, and female subadults respond more frequently to alarm peeps than do adult females. Infant squirrel monkeys showed different behavioral strategies in response to alarm peeps as a function of age. Adult females differentiate between infant and adult alarm peeps by responding more frequently to the alarm peeps of adult females. These data demonstrate that squirrel monkeys use acoustic information to discern when to respond to the alarm peeps from conspecifics, and that infants gradually develop an adult-like response to alarm peeps over the first year of development.     

Singing in the Face of Danger: the Anomalous Type II Vocalization of the Splendid Fairy-Wren

Males of certain species of fairy-wrens (Aves: Maluridae) emit a unique vocalization, the Type II vocalization, in response to the calls of potential predators. We conducted field observations and playback experiments to identify the contexts in which the Type II vocalization is emitted by splendid fairy-wren ( Malurus splendens ) males, and to examine social and genetic factors that influence its occurrence. In field observations and controlled playback experiments, Type II vocalizations were elicited most consistently by calls of the predatory gray butcherbird ( Cracticus torquatus ). Some vocalizations from other avian species also elicited Type II vocalizations, and the majority of these were vocalizations from avian predators. Splendid fairy-wrens are cooperative breeders, and males that responded with Type II vocalizations to playbacks of butcherbird calls tended to be primary rather than secondary males, had larger cloacal protuberances, and were older than those that did not respond. In addition, secondary males that were sons of resident females were more likely than non-sons to respond with a Type II vocalization. In another playback experiment, females responded similarly to the Type I song and Type II vocalizations of their mates. Although the Type II vocalization is emitted primarily in response to predator calls, it is inconsistent with an alarm call explanation. Patterns of reproductive success among Type II calling males suggest that it does not function as an honest signal of male quality. At present, the function of the vocalization remains anomalous, but indirect fitness benefits may play a role in its explanation.     

Eavesdropping on the Neighbourhood: Collared Pika (Ochotona collaris) Responses to Playback Calls of Conspecifics and Heterospecifics

The acoustic environment, composed in part by the vocalizations of sympatric animals, is a major source of information and can be used to fine-tune behavioural decisions. Active assessment of alarm calls within and between mammal species is not fully understood. We explored the behavioural responses of collared pikas to con- and heterospecific vocalizations, in order to determine whether they selectively attend to these calls. Pikas increased their vigilance after playback of alarm calls of heterospecific mammals (marmots and ground squirrels), but responded most strongly to conspecific calls. While responses to playback calls of their own, of neighbours and of a stranger did not differ, pikas did discriminate between individual callers in a habituation-discrimination experiment. The ability to make use of information from different sources in their acoustic environment likely facilitates pikas' behavioural decisions that affect foraging, predator avoidance and nepotism.     

Mule deer (Odocoileus hemionus) respond to yellow‐bellied marmot (Marmota flaviventris) alarm calls

Individuals may obtain valuable information about the presence of predators by listening to heterospecific alarm signals. Most playback studies have demonstrated that similarly sized and taxonomically related species may respond to the calls of each other, but less work has been carried out to define these factors influence responsiveness to alarm signals. In theory, individuals should respond to calls from any species that provide information about the presence of important predators, regardless of body size or taxonomic relationship. However, size is often associated with vulnerability. Coyotes (Canis latrans) in the Rocky Mountains prey upon both mule deer (Odocoileus hemionus) and yellow‐bellied marmots (Marmota flaviventris), which differ considerably in size, alarm vocalizations, and antipredator behavior. We conducted a playback experiment to see whether deer discriminated between marmot alarm calls and the non‐alarm song of a common sympatric bird. We found that deer increased vigilance significantly more after hearing broadcast marmot alarm calls compared with the bird song. Interestingly, deer that were studied within 0.5 km of homes showed significantly greater discrimination than those studied farther from humans. Our results suggest relative size differences do not prevent interspecific communication and that common predators should generally drive the evolution of the ability to learn to respond to meaningful risk cues. As long as two species share a predator, it should benefit the other to respond to its alarm calls.     

From nestling calls to fledgling silence: adaptive timing of change in response to aerial alarm calls

Young birds and mammals are extremely vulnerable to predators and so should benefit from responding to parental alarm calls warning of danger. However, young often respond differently from adults. This difference may reflect: (i) an imperfect stage in the gradual development of adult behaviour or (ii) an adaptation to different vulnerability. Altricial birds provide an excellent model to test for adaptive changes with age in response to alarm calls, because fledglings are vulnerable to a different range of predators than nestlings. For example, a flying hawk is irrelevant to a nestling in a enclosed nest, but is dangerous to that individual once it has left the nest, so we predict that young develop a response to aerial alarm calls to coincide with fledging. Supporting our prediction, recently fledged white-browed scrubwrens, Sericornis frontalis, fell silent immediately after playback of their parents' aerial alarm call, whereas nestlings continued to calling despite hearing the playback. Young scrubwrens are therefore exquisitely adapted to the changing risks faced during development.     

Dual Function of Chip Calls Depending on Changing Call Rate Related to Risk Level in Territorial Pairs of White‐Eared Ground‐Sparrows

Different mechanisms have been proposed for encoding information into vocalizations: variation of frequency or temporal characteristics, variation in the rate of vocalization production, and use of different vocalization types. We analyze the effect of rate variation on the dual function of chip calls (contact and alarm) produced by White‐eared Ground‐sparrows (Melozone leucotis). We conducted an acoustic playback experiment where we played back 1 min of four chip call rates (12, 36, 60, 84 calls/min). We measured the response of territorial pairs using behavioral responses, and fine structural features of calls produced in response to those playbacks. White‐eared Ground‐sparrows showed more intense behavioral responses to higher than lower call rate playbacks. Both individuals of the pair approached the source of the playback stimulus faster, produced the first vocalization faster, produced more vocalizations, and spent more time close to the stimulus in higher call rate than in lower call rate playbacks. Frequency and duration characteristics of calls (chip and tseet) were similar in response to all call rate playbacks. Our playback experiment elicited different intensity of behavioral responses, suggesting that risk‐based information is encoded in call rate. Our results suggest that variation in the rate of chip call production serves a dual function in this species; calls are used at lower rates for pair contact and at higher rates for alarm/mobbing signals.     

Acoustic communication in the Bocon toadfish (<Emphasis Type="Italic">Amphichthys cryptocentrus</Emphasis>)

The soundscapes of many coastal habitats include vocalizations produced by species of the family Batrachoididae (toadfish and midshipman). We describe the calling and grunting behavior of male Amphichthys cryptocentrus, a tropical toadfish, and predict how these vocalizations are influenced by conspecifics. We recorded individual males, which produced broadband grunts and multi-note, harmonic “boatwhistle” calls. Grunts were either in combination with calls or stand-alone. We used a null model to test if these latter grunts were produced at random or in response to calls from conspecifics. The model supports the hypothesis that grunts were in response to calls from neighboring males, suggesting acoustic competition. Using the most conservative estimate of hearing abilities we predict that males responded to the second harmonic of neighbor’s calls (230 Hz) at amplitudes of approximately 100–125 dB re 1μPa²/Hz. We also observed that call and grunt rates increased when males were exposed to higher rates of acoustic activity from neighboring fish. Fish used grunts to respond to background calls that occurred at different amplitudes, suggesting they responded to the calls of multiple neighboring fish and not just the highest amplitude neighbor. This communication with multiple fish within hearing range suggests a communication network in which the spatial distribution of individual toadfish relative to one another will impact their vocal behavior. Thus, the density and distribution, and not just abundance, of these toadfish at a given site will influence the characteristics of the chorus and the role of this species in the local soundscape.     

Begging to differ: scrubwren nestlings beg to alarm calls and vocalize when parents are absent

Nestling birds face a dilemma: they can increase parental provisioning by begging more intensively, but by doing so may also increase their risk of predation. Nestlings could deal with this dilemma by reducing begging intensity after parents have warned them of a nearby predator. We therefore tested experimentally whether nestling scrubwrens, Sericornis frontalis, increase begging intensity with hunger but reduce it after adult alarm calls. Single 5- and 8-day-old nestlings were temporarily taken into the laboratory for playback experiments. Over a 90-min period of food deprivation we simulated parental visits every 10 min by playing back adult feeding calls. Hungrier nestlings begged louder and longer to simulated parental visits, but contrary to expectation did not beg less if they had previously heard playback of alarm calls, and even begged to the alarm calls themselves. The results were similar for both ‘mobbing’ and ‘flee’ alarm calls. Nestlings also gave distinctive calls in the 10-min interval between simulated parental visits, and the number of these calls increased with hunger and after playback of alarm calls. We suggest that nestlings acquire the ability to respond appropriately to alarm calls late in the nestling period and that therefore parents might be selected to avoid alarm calling when defending young nestlings.Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Development of infant baboons' responses to graded bark variants.

We studied the development of infant baboons' (Papio cynocephalus ursinus) responses to conspecific 'barks' in a free-ranging population in the Okavango Delta, Botswana. These barks grade from tonal, harmonically rich calls into calls with a more noisy, harsh structure. Typically, tonal variants are given when the signaller is at risk of losing contact with the group or a particular individual ('contact barks'), whereas harsh variants are given in response to predators ('alarm barks'). We conducted focal observations and playback experiments in which we presented variants of barks recorded from resident adult females. By six months of age, infants reliably discriminated between typical alarm and contact barks and they responded more strongly to intermediate alarm calls than to typical contact barks. Infants of six months and older also recognized their mothers by voice. The ability to discriminate between different call variants developed with increasing age. At two and a half months of age, infants failed to respond at all, whereas at four months they responded irrespective of the call type that was presented. At six months, infants showed adult-like responses by responding strongly to alarm barks but ignoring contact barks. We concluded that infants gradually learn to attach the appropriate meaning to alarm and contact barks.     

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.     

Two Novel Vocalizations Are Used by Veeries (Catharus fuscescens) during Agonistic Interactions

Avian vocalizations are common examples of the complex signals used by animals to negotiate during agonistic interactions. In this study, we used two playback experiments to identify agonistic signals in a songbird species with several acoustically complex songs and calls, the veery. In the first experiment, we compared veery singing behavior in response to simulated territorial intrusions including playback of three variations of veery song: 1) song alone as a control, 2) songs with added whisper calls, and 3) songs with introductory notes removed. In the second experiment, we used multimodal stimuli including songs, whisper calls and songs with introductory notes removed, along with a robotic veery mount. Focal males readily responded to all of the playback stimuli, approached the speaker and/or robotic mount, and vocalized. Male veeries gave more whisper calls, and sang more songs without the introductory note in response to all types of playback. However, veeries responded similarly to all types of stimuli presented, and they failed to physically attack the robotic mount. These results indicate that rival veeries use two different types of novel vocalizations: whisper calls and songs lacking the introductory note as agonistic signals, but do not allow us to discern the specific functions of these two vocalizations.     

Food Transfer and Development of Feeding Behavior and Food-Associated Vocalizations in Cotton-Top Tamarins

Food transfer between adults and infants is common in many marmoset and tamarin monkeys, and is often accompanied by vocalizations. We hypothesized that vocalizations by adults in a food transfer context creates an opportunity for infants to learn not only what foods are appropriate but what vocalizations are appropriate in feeding contexts. We studied the development of feeding behavior and food-associated vocalizations in 10 infant cotton-top tamarins through the first 20 wks of life. Infants obtained solid food through transfers from older group members, primarily the adult male, beginning at weeks 5–6. Both adults and infants vocalized during food transfers with adults, producing rapid sequences of the call types adults normally give when feeding. Infants were usually successful in obtaining food primarily when the adult was vocalizing. The sooner infants were active participants in food transfers, the sooner they began to feed independently. In the early weeks, infants produced a large number of vocal types during food transfers, but with increasing age there was a steady increase in the number of adult-form food calls and a reduction in other, non-food-associated calls. Infants that fed independently at an early age produced fewer non-food-associated calls by the last month of observation. Infants called at higher rates to their most preferred food. Food transfers accompanied by vocalizations may provide an opportunity for infants to learn about appropriate foods as well as the vocalizations that accompany feeding in adults, and may represent a form of 'coaching' or information donation by adults.     

Age Differences in the Response of Willow Tits (Parus montanus) to Conspecific Alarm Calls

Predation is an important mortality factor in wintering birds. To counter this, birds produce alarm calls in the presence of predators which serve to warn conspecifics. In social hierarchical bird flocks, adults survive the winter better than juveniles and therefore survival strategies probably vary with social status. This study examined the differential responses to alarm calls by free-living willow tits, Parus montanus, in dominance-structured winter flocks in Finland. To explore the age-dependent differences in response to conspecific alarm calls, a series with three alarm calls was played to focal adults and juveniles while they sat in the middle section of a spruce branch. Immediately after the playback, juvenile willow tits moved more often, flew longer distances and changed branches more often than did adults. Previous mammal studies have shown that juveniles are more likely to flee than adults after hearing conspecific alarm calls. The current study demonstrates that similar age-dependent responses to conspecific alarm calls occur in birds also. These findings reflect an increased vulnerability to predators or lack of experience of young birds.     

Alarm responses are maintained during captive rearing in chicks of endangered kaki

The maintenance of species-specific behavioural repertoires and traditions is an important but often implicit goal of conservation efforts. When captive rearing is used as a conservation practice, it becomes critical to address its possible implications for the social and behavioural traits of developing individuals. In particular, animals must retain or acquire many of their behavioural abilities to increase the likelihood of survival upon release into the wild. This study investigated the behavioural development of critically endangered kaki (black stilt: Himantopus novaezelandiae ) chicks reared without live adult conspecifics. The captive rearing programme included playbacks of adult kaki alarm calls during cleaning and handling of precocial chicks housed as groups. We used videotaped observations and playback experiments to address the following questions: do kaki chicks respond differentially to (1) familiar versus unfamiliar adult kaki alarm calls and (2) conspecific alarm versus heterospecific control vocalizations. Adult-naïve kaki chicks exhibited a varied behavioural repertoire over their early development. In multivariate analyses, when age was statistically controlled, chicks showed responses to familiar and unfamiliar alarm calls that were similar in magnitude. In contrast, following conspecific alarm calls chicks had longer average latencies to resume pre-playback activities than following heterospecific vocalizations. Although the generality of these conclusions is limited by experimental constraints stemming from working with an endangered species, the findings suggest that current management techniques produce captive-reared kaki for release into the wild that possess many of the behavioural and auditory recognition skills that are required for survival.     

Parental alarm calls suppress nestling vocalization

Evolutionary models suggest that the cost of a signal can ensure its honesty. Empirical studies of nestling begging imply that predator attraction can impose such a cost. However, parents might reduce or abolish this cost by warning young of the presence of danger. We tested, in a controlled field playback experiment, whether alarm calls cause 5-, 8- and 11-day-old nestlings of the white-browed scrubwren, Sericornis frontalis, to suppress vocalization. In this species, nestlings vocalize when parents visit the nest ('begging') and when they are absent ('non-begging'), so we measured effects on both types of vocalization. Playback of parental alarm calls suppressed non-begging vocalization almost completely but only slightly reduced begging calls during a playback of parental feeding calls that followed. The reaction of nestlings was largely independent of age. Our results suggest two reasons why experiments ignoring the role of parents probably overestimate the real cost of nestling vocalizations. Parents can warn young from a distance about the presence of danger and so suppress non-begging vocalizations that might otherwise be overheard, and a parent's presence at the nest presumably indicates when it is safe to beg.