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. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Predation affects alarm call usage in female Diana monkeys (Cercopithecus diana diana)

Diana monkeys produce acoustically distinct calls to a number of external events, including different types of predators. In a previous study, we found population-wide differences in male alarm call production in Taï Forest, Ivory Coast, and on Tiwai Island, Sierra Leone, mostly likely originating from differences in predator experience. In Taï Forest, leopards (Panthera pardus) are common but on Tiwai Island they have been absent for decades, while the predation pressure from crowned eagles (Stephanoaetus coronatus) has been similar. To further evaluate the impact of predator experience, we here analyse the vocal behaviour of female Diana monkeys in both habitats. Female Diana monkeys produce predator-specific alarm calls, alert calls and contact calls in response to predators, suggesting that their calls serve in a broader range of functions compared to males. Results showed that females produced the same call types at both sites, despite the differences in predator fauna. Regarding call usage, leopard alarm calls were extremely rare on Tiwai Island, but not in Taï Forest, whereas we found no differences in eagle alarm call production. When comparing response latencies, Tiwai females were slower to respond to both predators compared to Taï females. Finally, we found no habitat-specific acoustic differences in the alert and predator-specific alarm calls, but significant differences in frequency-based parameters of contact calls. Overall, our results suggest that ontogenetic experience can affect primate vocal behaviour in both usage and acoustic structure but that the way in which particular call types are affected may be closely linked to function.     

Production and perception of situationally variable alarm calls in wild tufted capuchin monkeys (Cebus apella nigritus)

Many mammalian and avian species produce conspicuous vocalizations upon encountering a predator, but vary their calling based on risk urgency and/or predator type. Calls falling into the latter category are termed “functionally referential” if they also elicit predator-appropriate reactions in listeners. Functionally referential alarm calling has been well documented in a number of Old World monkeys and lemurs, but evidence among Neotropical primates is limited. This study investigates the alarm call system of tufted capuchin monkeys (Cebus apella nigritus) by examining responses to predator and snake decoys encountered at various distances (reflecting differences in risk urgency). Observations in natural situations were conducted to determine if predator-associated calls were given in additional contexts. Results indicate the use of three call types. “Barks” are elicited exclusively by aerial threats, but the call most commonly given to terrestrial threats (the “hiccup”) is given in nonpredatory contexts. The rate in which this latter call is produced reflects risk urgency. Playbacks of these two call types indicate that each elicits appropriate antipredator behaviors. The third call type, the “peep,” seems to be specific to terrestrial threats, but it is unknown if the call elicits predator-specific responses. “Barks” are thus functionally referential aerial predator calls, while “hiccups” are better seen as generalized disturbance calls which reflect risk urgency. Further evidence is needed to draw conclusions regarding the “peep.” These results add to the evidence that functionally referential aerial predator alarm calls are ubiquitous in primates, but that noncatarrhine primates use generalized disturbance calls in response to terrestrial threats.     

Anti-predator behavior of group-living Malagasy primates: mixed evidence for a referential alarm call system

Many mammals warn conspecifics with alarm calls about detected predators. These alarm calls are either functionally referential, urgency based, or they can have multiple functions, including predator deterrence. The taxonomic distribution of these alarm call systems is uneven, with primates providing the best-known examples for a functionally referential system and rodents most examples of an urgency-based system. Reports of different alarm call systems in lemurid primates prompted us to examine the anti-predator behavior of two additional lemur species. In an experimental field study we exposed adult redfronted lemurs (Eulemur fulvus rufus) and white sifakas (Propithecus verreauxi verreauxi) to playbacks of vocalizations of their main aerial and terrestrial predators, as well as to their own alarm calls given in response to the presentation of these predators. We scored the subjects' immediate behavioral responses, including alarm calls, from video recordings made during the first minute following a playback. We found that both species gave specific alarm calls only in response to raptor playbacks and the corresponding alarm calls, whereas calls given in response to carnivores and the corresponding alarm calls were also observed in other situations characterized by high arousal. Other behavioral responses, such as gaze and escape directions, corresponded to the hunting strategies of the two predator classes, suggesting that the corresponding vocalizations were categorized correctly. These two lemur species, which represent different families, have therefore independently evolved a mixed alarm call system, characterized by functionally referential calls for diurnal raptors, but not for carnivores. Electronic supplementary material to this paper can be obtained by using the Springer LINK server located at http://dx.doi.org/10.1007/s00265-001-0436-0 Electronic Publication     

The hearing of an avian predator and its avian prey

Summary Auditory tuning curves of a small songbird, the great tit (Parus major), and of its principal avian predator, the European sparrowhawk (Accipiter nisus), were determined by an operant positive reinforcement conditioning procedure, using the method of constant stimuli. Thresholds were measured by the criterion of a 50% correct response and a d of 1.5 for intra- and interspecific comparison, respectively. The best frequency of both species was 2 kHz, the hawk being 6.5 dB SPL more sensitive than the tit. Although the high-frequency cutoff was very similar in both species, at 8 kHz the great tit was about 30 dB more sensitive than the sparrowhawk. The hearing abilities of the prey and its predator are discussed with reference to the acoustic alarm communication of great tits confronted with sparrowhawks. Two alarm calls lie in the frequency range of the best hearing of both the hawk and the tits: the mobbing call and a call given in response to a nearby hawk when fleeing from it. In contrast, the seeet call, an alarm call given mainly in response to distant flying sparrowhawks, can only be heard well by the tit. The implications of these results for hypotheses concerning the evolution of alarm calls in small songbirds are discussed.     

Predator-specific alarm calls in Campbell's monkeys, Cercopithecus campbelli

One of the most prominent behavioural features of many forest primates are the loud calls given by the adult males. Early observational studies repeatedly postulated that these calls function in intragroup spacing or intergroup avoidance. More recent field experiments with Diana monkeys (Cercopithecus diana) of Taï Forest, Ivory Coast, have clearly shown that loud male calls function as predator alarm calls because calls reliably (1) label different predator classes and (2) convey semantic information about the predator type present. Here, I test the alarm call hypothesis another primate, the Campbell's monkey (C. campbelli). Like Diana monkeys, male Campbell's monkeys produce conspicuous loud calls to crowned hawk eagles (Stephanoaetus coronatus) and leopards (Panthera pardus), two of their main predators. Playback experiments showed that monkeys responded to the predator category represented by the different playback stimuli, regardless of whether they consisted of (1) vocalisations of the actual predators (crowned hawk eagle shrieks or leopard growls), (2) alarm calls to crowned hawk eagles or leopards given by other male Campbell's monkeys or (3) alarm calls to crowned hawk eagles or leopards given by sympatric male Diana monkeys. These experiments provide further evidence that non-human primates have evolved the cognitive capacity to produce and respond to referential labels for external events.     

Do yellow-bellied marmots respond to predator vocalizations?

We conducted four experiments to determine whether yellow-bellied marmots, Marmota flaviventris, discriminate among predator vocalizations, and if so, whether the recognition mechanism is learned or experience-independent. First, we broadcast to marmots the social sounds of coyotes, Canis latrans, wolves, Canis lupus, and golden eagles, Aquila chrysaetos, as well as conspecific alarm calls. Coyotes and eagles are extant predators at our study site, while wolves have been absent since the mid-1930s. In three follow-up experiments, we reversed the eagle call and presented marmots with forward and reverse calls to control for response to general properties of call structure rather than those specifically associated with eagles, we tested for novelty by comparing responses to familiar and unfamiliar birds, and we tested for the duration of predator sounds by comparing a wolf howl (that was much longer than the coyote in the first experiment) with a long coyote howl of equal duration to the original wolf. Marmots suppressed foraging and increased looking most after presentation of the conspecific alarm call and least after that of the coyote in the first experiment, with moderate responses to wolf and eagle calls. Marmots responded more to the forward eagle call than the reverse call, a finding consistent with a recognition template. Marmots did not differentiate vocalizations from the novel and familiar birds, suggesting that novelty itself did not explain our results. Furthermore, marmots did not differentiate between a wolf howl and a coyote howl of equal duration, suggesting that the duration of the vocalizations played a role in the marmots’ response. Our results show that marmots may respond to predators based solely on acoustic stimuli. The response to currently novel wolf calls suggests that they have an experience-independent ability to identify certain predators acoustically. Marmots’ response to predator vocalizations is not unexpected because 25 of 30 species in which acoustic predator discrimination has been studied have a demonstrated ability to respond selectively to cues from their predators.     

Chick-a-dee call variation in the context of “flying” avian predator stimuli: a field study of Carolina chickadees (<Emphasis Type="Italic">Poecile carolinensis</Emphasis>)

Chick-a-dee calls function in social organization in Poecile (chickadee) species. Recent field and aviary studies have found that variation in chick-a-dee calls relates to the type or proximity of avian predator, or level of threat. Earlier studies on calls in the context of predator stimuli have typically used stationary and perched predator models. For chickadees and other small songbirds, more frequently detected and more dangerous avian predatory stimuli are flying predators. In the present study, we tested whether simulated flying avian predator and control models influenced chick-a-dee calling behavior of wild Carolina chickadees, Poecile carolinensis. At 20 independent field sites, chickadee subjects were presented with wooden models that were painted to resemble either a predatory sharp-shinned hawk (Accipiter striatus) or a blue jay (Cyanocitta cristata) and that were made to “fly” down a zip line near a feeding station chickadees were using. The note composition of chick-a-dee calls was affected by both the flight of stimuli and type of model. Call variation in this flying predator context suggests interesting similarities and differences with experimental findings with congeners. Finally, increased production of certain notes to the flying of both model types provides support for a “Better Safe than Sorry” strategy. When costs of alarm calling are low but costs of discriminating potentially serious threats may be extremely high, individuals should err on the side of caution, and alarm call to any potentially threatening stimulus.     

The squirrel that cried wolf: reliability detection by juvenile Richardson's ground squirrels (Spermophilus richardsonii)

Where alarm signals function to warn others of the presence of threat, variation is likely to exist in the reliability of alarm signalers. Some signalers, with too low a threshold of excitation, will issue false alarms and should be ignored if potential alarm recipients are to maximize energy gains. We exposed juvenile Richardson's ground squirrels to reliable signalers, whose alarm calls were paired with the presentation of a predator model, and unreliable signalers, whose alarm calls were played when no potential predator was present. Call recipients discriminated among individual alarm callers, and reduced responsiveness to callers that had been unreliable. Thus, like primates, squirrels are capable of forming a concept of reliability by associating an individual's identity with that individual's past performance.     

The alarm call system of wild black-fronted titi monkeys, <Emphasis Type="Italic">Callicebus nigrifrons</Emphasis>

Upon encountering predators, many animals produce specific vocalisations that alert others and sometimes dissuade the predators from hunting. Callicebus monkeys are known for their large vocal repertoire, but little is known about the function and meaning of most call types. We recorded a large number of natural predator responses from five different groups of black-fronted titi monkeys in their Atlantic forest habitat in South Eastern Brazil. When detecting predatory threats, adult group members responded with call sequences that initially consisted of two brief, high-pitched calls with distinct frequency contours. Call A was mainly given to raptors but also to predatory capuchin monkeys and other threats within the canopy, while call B was given to predatory or non-predatory disturbances on the ground. In later parts of the sequences, we also recorded a high-pitched unmodulated call C and various low-pitched loud calls. Results therefore suggest that calls A and B provide listeners with rapid and reliable information about the general classes of danger experienced by the caller, while obtaining more specific information through other call types and combinations and behavioural responses. We discuss these findings in relation to current evolutionary theory of primate communication.     

Ontogenetic changes in alarm-call production and usage in meerkats (<Emphasis Type="Italic">Suricata suricatta</Emphasis>): adaptations or constraints?

In many species, individuals suffer major mortality in their first year because of predation. Behaviours that facilitate successful escape are therefore under strong selection, but anti-predator skills often emerge gradually during an individual’s early development. Using long-term data and acoustic recordings of alarm calls collected during natural predator encounters, we aimed to elucidate two largely unsolved issues in anti-predator ontogeny: (1) whether incorrect predator assignment is adaptively age-appropriate, given that vulnerability often changes during development, or whether age-related differences reflect true mistakes made by immature individuals; and (2) the extent to which the development of adult-like competence in alarm-call production and usage is simply a function of maturational processes or dependent upon experience. We found that young meerkats (Suricata suricatta) were less likely to give alarm calls than adults, but alarmed more in response to non-threatening species compared to adults. However, stimuli that pose a greater threat to young than adults did not elicit more calling from young; this argues against age-related changes in vulnerability as the sole explanation for developmental changes in calling. Young in small groups, who were more likely to watch out for predators, alarmed more than less vigilant young in larger groups. Moreover, despite similarities in acoustic structure between alarm call types, calls appeared in the repertoire at different rates, and those that were associated with frequently encountered predators were produced relatively early on. These results indicate that experience is a more plausible explanation for such developmental trajectories than maturation.     

Bornean orangutan geophagy: analysis of ingested and control soils

Environmental Geochemistry and Health - Geophagy among orangutans is the most poorly documented in contrast to the knowledge of soil-eating practices of other great ape species. Observations of...     

Functional reference in an alarm signal given during nest defence: seet calls of yellow warblers denote brood-parasitic brown-headed cowbirds

Field observations and model-presentation experiments have shown that yellow warblers (Dendroica petechia) produce seet calls preferentially in response to brood-parasitic brown-headed cowbirds (Molothrus ater). In this study, we investigated whether seet calls are functionally referential alarm calls denoting cowbirds by determining whether female warblers responded appropriately to seet calls in the absence of a cowbird, whether alarm calling by warblers varied with response urgency, and how warblers in a population allopatric with cowbirds responded to cowbird and avian predator models and seet playbacks. As a control, we presented chip calls, which are elicited by nest predators as well as by non-threatening intruders, but are not strongly associated with cowbirds. Yellow warblers responded differently to playbacks of seet than chip calls. To seet playbacks, almost 60% of females gave seet calls and rushed to sit in their nests, responses typically elicited by cowbirds, whereas these responses were given infrequently in response to chip calls. Yellow warblers seet called equally in situations that simulated low, medium and high risk of parasitism, which suggests that these calls did not vary with response urgency. In a population allopatric with cowbirds, seet calls were rarely produced in response to cowbird or avian nest predator models and never to seet playbacks. These results suggest that seet calls are functionally referential signals denoting cowbirds and that cowbird parasitism was a strong selective pressure in the evolution of functional referentiality in the seet call of yellow warblers.Communicated by W.A. Searcy     

Specific targeting of host individuals by a kleptoparasitic bird

Kleptoparasitism is a tactic used to acquire food opportunistically and has been shown to provide several benefits, including greater food intake rate and the acquisition of items not normally available during self-foraging. Host individuals may differ in their ability to defend themselves against kleptoparasitic attacks and therefore identifying those host individuals that are particularly vulnerable to attack could both provide energetic benefits and increase the efficiency of kleptoparasitism as a foraging strategy. Here, we show that the kleptoparasitic fork-tailed drongo (Dicrurus adsimilis) specifically targets juveniles when following groups of cooperatively breeding pied babblers (Turdoides bicolor). Drongos give alarm calls upon sighting a predator, thus providing extra predator vigilance to foraging pied babblers. However, drongos also use alarm calls to steal food items. During kleptoparasitic attacks, drongos give false alarm calls and then swoop down to steal food items dropped by alarmed babblers. Juvenile pied babblers are particularly vulnerable to attack because they (a) spend a longer period handling prey items prior to consumption and (b) respond to alarm calls primarily by immediately moving to cover, in contrast to adults who respond by looking up and visually scanning the surrounding area. Drongos attack juvenile babblers significantly more often than adults, with attacks on juveniles more likely to result in the successful procurement of a food item. This patterns of attack suggests that drongos are able to differentiate between individuals of different age when targeting pied babblers, thus increasing the efficiency of kleptoparasitism as a foraging strategy.     

Interspecific attraction to the mobbing calls of black-capped chickadees (Parus atricapillus)

The species and number of birds attracted to playbacks of mobbing calls and song of the black-capped chickadee, Parus atricapillus, were compared. The chickadee vocalizations were played at abandoned chickadee nests, and the numbers and species of other birds that approached the speaker were tallied. Few non-chickadees were observed in the area when the song was played. That significantly more birds approached the speaker and displayed mobbing behavior during the mobbing call playback suggests that black-capped chickadee mobbing vocalizations carry meaning for at least ten other avian species. This finding supports the idea that species subjected to the same predators in an area may benefit by recognizing each others’ predator calls. This recognition may be facilitated by the similar structure of different species’ mobbing calls and also a learned association of another species’ call with the presence of a predator. Received: 23 March 1995 /Accepted after revision: 28 October 1995     

Variation in behavioral and hormonal responses of adult male gray-cheeked mangabeys (<Emphasis Type="Italic">Lophocebus albigena</Emphasis>) to crowned eagles (<Emphasis Type="Italic">Stephanoaetus coronatus</Emphasis>) in Kibale National Park,Uganda

Intensive study of arboreal forest-dwelling primates and their predators in Africa is increasingly revealing that crowned eagles (Stephanoaetus coronatus) are major predators of primates. Gray-cheeked mangabeys (Lophocebus albigena) are overrepresented in the diets of crowned eagles in Kibale National Park, Uganda, and adult male mangabeys are represented more than females. We focused on the behavior of adult male gray-cheeked mangabeys living in social groups in Kibale National Park (1) to clarify the interactions between mangabeys and eagles that might put adult males at greater risk and (2) to better understand individual variation in behavioral responses to predators. Adult male mangabeys in five groups responded to observer-confirmed presence of crowned eagles 88 times over a 13-month period. While all males gave alarm calls, only the highest-ranking male in each of four groups chased eagles. These males had elevated levels of fecal cortisol metabolites in the days immediately after they engaged in active defense, suggesting that they perceived such behavior as risky. In the one group where male ranks were unstable and there were no infants, no male was observed to chase eagles. We suggest that males pursue the dangerous tactic of chasing eagles only when they are likely to have offspring in the group. Males in larger groups also spent less time alarm calling to crowned eagles (from first to last call in a group), and our observations confirmed that the duration of their alarm calls was related to eagle presence. Thus, eagles spent less time around larger mangabey groups. Alarm calling by adult male mangabeys may signal to this ambush predator that it has been detected and should move on.     

Chick-a-dee call syntax,social context,and season affect vocal responses of Carolina chickadees (<Emphasis Type="Italic">Poecile carolinensis</Emphasis>)

Chick-a-dee calls in many chickadee (Poecile) species are common vocal signals used in a diversity of social contacts. The calls consist of four notes, A, B, C, and D, which follow simple rules of syntax (note ordering and composition) to generate many unique call types. We used field playbacks with Carolina chickadees, P. carolinensis, to ask whether violations of a syntactical rule affected their vocal responses. We show that chickadee responses to typical calls (e.g. AAAACCCC and CCCCDDDD) differ from responses to atypical calls (e.g. CACACACA and DCDCDCDC) depending on playback note composition, season, and social context (presence of heterospecifics). In the fall/winter, playbacks of typical calls with A and C notes elicited the greatest number of A and B notes in chick-a-dee call responses and typical calls with D notes elicited the greatest number of C notes, when in the presence of heterospecifics. In contrast, the corresponding atypical calls did not elicit similar responses. This suggests communicative significance is lost in calls that violate a rule of syntax in the fall/winter. In the spring, neither chickadee feebeefeebay song rate nor chick-a-dee calls responses differed by playback type. We suggest that call syntax is less salient for mated pairs in the spring than it is for fall/winter flocks that rely more on conspecific communication for foraging success and flock cohesion. This study represents the first experimental evidence that chickadees attend to both note composition and ordering in chick-a-dee calls.Communicated by W.A. Searcy     

Limited geographic variation in the acoustic structure of and responses to adult male alarm barks of African green monkeys

The global diversity of human languages is a remarkable feature of our species, which requires a capacity for rapid vocal learning. Given that primate alarm calling systems have played an important role in the language origin debate, identifying geographic variation in primate alarm calls and understanding the underlying causal mechanisms are important steps to help uncover evolutionary precursors to language. This study investigates geographic variation in the alarm bark of the widely distributed African green monkey (Chlorocebus). To quantify geographic variation in spectral and temporal call structure, acoustic analysis was used to compare the adult male barks of green monkeys (Chlorocebus sabaeus) and two subspecies of vervet (Chlorocebus pygerythrus pygerythrus and Chlorocebus pygerythrus hilgerti). Playback experiments were also carried out to test whether adult male vervets would distinguish between the barks of own-group males, unknown conspecific males and green monkey males. Acoustic analysis showed that, whilst similar in overall structure, the barks of green monkeys could be distinguished from vervet barks with a high degree of accuracy; the barks of vervet subspecies could also be discriminated, although to a lesser degree. Males responded most strongly to unknown conspecific males’ barks, and exhibited responses typical of leopard-avoidance and territorial defence. Taken together, these findings indicate that variation in alarm calls can be best explained by phylogenetic distance, and that intra- and inter-species differences are relevant during social interactions. Moreover, barks may function as an alarm and display call, which could explain the observed sexual dimorphism in barks in this genus.     

Do echolocation calls of wild colony-living Bechstein's bats (Myotis bechsteinii) provide individual-specific signatures?

Social animals often use vocal communication signals that contain individual signatures. As bats emit echolocation calls several times per second to orient in space, these might seem ideal candidates for conveying the caller's individual identity as a free by-product. From a proximate perspective, however, coding of caller identity is hampered by the simple acoustic structure of echolocation signals, by their task-specific design and by propagation loss. We investigated the occurrence of individual signatures in echolocation calls in individually marked, free-living Bechstein's bats (Myotis bechsteinii) in a situation with defined social context in the field. The bats belonged to two different colonies, for both of which genetic data on relatedness structure was available. While our data clearly demonstrate situation specificity of call structure, the evidence for individual-specific signatures was relatively weak. We could not identify a robust and simple parameter that would convey the caller's identity despite the situation-specific call variability. Discriminant function analysis assigned calls to call sequences with good performance, but worsened drastically when tested with other sequences from the same bats. Therefore, we caution against concluding from a satisfactory discrimination performance with identical training and test sequences that individual bats can reliably be told apart by echolocation calls. At least the information contained in a single call sequence seems not to be sufficient for that purpose. Starting frequencies did give the best discrimination between individuals, and it was also this parameter that was correlated with genetic relatedness in one of our two study colonies. Echolocation calls could serve as an additional source of information for individual recognition in Bechstein's bats societies, while it is unlikely that a large number of individuals could be reliably identified in different situations based on echolocation alone.     

Age and sex influence marmot antipredator behavior during periods of heightened risk

Animals adjust their antipredator behavior according to environmental variation in risk, and to account for their ability to respond to threats. Intrinsic factors that influence an animal’s ability to respond to predators (e.g., age, body condition) should explain variation in antipredator behavior. For example, a juvenile might allocate more time to vigilance than an adult because mortality as a result of predation is often high for this age class; however, the relationship between age/vulnerability and antipredator behavior is not always clear or as predicted. We explored the influence of intrinsic factors on yellow-bellied marmot (Marmota flaviventris) antipredator behavior using data pooled from 4 years of experiments. We hypothesized that inherently vulnerable animals (e.g., young, males, and individuals in poor condition) would exhibit more antipredator behavior prior to and immediately following conspecific alarm calls. As expected, males and yearlings suppressed foraging more than females and adults following alarm call playbacks. In contrast to predictions, animals in better condition respond more than animals in below average condition. Interestingly, these intrinsic properties did not influence baseline time budgets; animals of all ages, sexes, and condition levels devoted comparable amounts of time to foraging prior to alarm calls. Our results support the hypothesis that inherent differences in vulnerability influence antipredator behavior; furthermore, it appears that a crucial, but poorly acknowledged, interaction exists between risk and state-dependence. Elevated risk may be required to reveal the workings of state-dependent behavior, and studies of antipredator behavior in a single context may draw incomplete conclusions about age- or sex-specific strategies.