Perceptual specificity in the alarm calls of Gunnison's prairie dogs

Gunnison's prairie dogs have a complex alarm communication system. We show that the escape responses of prairie dogs to naturally occurring live predators differed depending upon the species of predator. We also show that playbacks of alarm calls that were elicited originally by the live predators produced the same escape responses as the live predators themselves. The escape responses fell into two qualitatively different categories: running to the burrow and diving inside for hawks and humans, and standing upright outside the burrow for coyotes and dogs. Within these two categories there were differences in response. For hawks, only the prairie dogs that were in the direct flight path of a stooping red-tailed hawk ran to their burrows and dove inside, while for humans and human alarm call playbacks there was a colony-wide running to the burrows and diving inside. For coyotes and coyote alarm call playbacks there was a colony-wide running to the burrows and standing alert at the burrow rims, while for domestic dogs and playbacks of alarm calls for domestic dogs the prairie dogs assumed an alert posture wherever they were feeding, but did not run to their burrows. These responses to both the live predators and to predator-elicited alarm calls suggest that the alarm calls of Gunnison's prairie dogs contain meaningful referential information about the categories of predators that approach a colony of prairie dogs.     

A fuzzy-neural system for identification of species-specific alarm calls of Gunnison's prairie dogs

In this study we describe the design and application of an automated classification system that utilizes artificial intelligence to corroborate the finding that Gunnison's prairie dogs have different alarm calls for different species of predators. This corroboration is strong because it utilizes an entirely different analysis technique than that used in the original research by Slobodchikoff et al. [Slobodchikoff, C.N., Fischer, C., Shapiro, J., 1986. Predator-specific alarm calls of prairie dogs. Am. Zool. 26, 557] or in subsequent study done by Slobodchikoff et al. [Slobodchikoff, C.N., Kiriazis, J., Fischer, C., Creef, E., 1991. Semantic information distinguishing individual predators in the alarm calls of Gunnison's prairie dogs. Anim. Behav. 42, 713-719]. The study described here also is more completely automated than earlier study in this area. This automation allowed a large volume of field data to be processed where all measurements of relevant parameters were performed through software control. Previous study processed a smaller data set and utilized manual measurement techniques. The new classification system, which combines fuzzy logic and an artificial neural network, classified alarm calls correctly according to the eliciting predator species, achieving accuracy levels ranging from 78.6 to 96.3% on raw field data digitized with low quality audio equipment.     

Bird calls: just emotional displays or something more?

Two widely held assumptions about the sounds of birds and other animals are (1) they are impulsive and involuntary, and cannot be controlled, and (2) they are based only on emotion, apparently because the stimuli eliciting them are thought to be very generalized. The validity of these assumptions has been tested in studies of the alarm calling and food calling behavior of domestic chickens. Videotapes of aerial and ground predators–a hawk overhead and a raccoon on the ground–were effective in eliciting the two major classes of alarm calls. The frequency of aerial alarm calling was strongly affected by presence or absence of a companion, while other aspects of antipredator behavior were unchanged. This so-called "audience effect" on calling is not found with the ground predator call, apparently because this call is addressed to the predator as well as companions. The rules for audience effects are different again with food calling. Evidently calling is not completely impulsive, but can be controlled. By varying the attributes of digitized video images of predators we have shown that stimuli eliciting the aerial predator alarm call are quite specific, encoding different information than the ground predator call. Playback experiments demonstrate that another chicken can decode this information, and react adaptively. Although emotion is undoubtedly involved in bird calling, we conclude that simple emotion-based models of bird calls are inadequate as the sole basis for explaining the vocal behavior of birds.     

Bird calls: just emotional displays or something more?

Two widely held assumptions about the sounds of birds and other animals are (1) they are impulsive and involuntary, and cannot be controlled, and (2) they are based only on emotion, apparently because the stimuli eliciting them are thought to be very generalized. The validity of these assumptions has been tested in studies of the alarm calling and food calling behavior of domestic chickens. Videotapes of aerial and ground predators–a hawk overhead and a raccoon on the ground–were effective in eliciting the two major classes of alarm calls. The frequency of aerial alarm calling was strongly affected by presence or absence of a companion, while other aspects of antipredator behavior were unchanged. This so-called "audience effect" on calling is not found with the ground predator call, apparently because this call is addressed to the predator as well as companions. The rules for audience effects are different again with food calling. Evidently calling is not completely impulsive, but can be controlled. By varying the attributes of digitized video images of predators we have shown that stimuli eliciting the aerial predator alarm call are quite specific, encoding different information than the ground predator call. Playback experiments demonstrate that another chicken can decode this information, and react adaptively. Although emotion is undoubtedly involved in bird calling, we conclude that simple emotion-based models of bird calls are inadequate as the sole basis for explaining the vocal behavior of birds.     

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

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

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

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

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.     

Western Burrowing Owls (Athene cunicularia hypugaea) Eavesdrop on Alarm Calls of Black‐Tailed Prairie Dogs (Cynomys ludovicianus)

Animals sharing a common habitat can indirectly receive information about their environment by observing information exchanges between other animals, a process known as eavesdropping. Animals that use an auditory alarm calling system are an important indirect information source for eavesdropping individuals in their environments. We investigated whether Western burrowing owls (Athene cunicularia hypugaea) nesting on black‐tailed prairie dog (Cynomys ludovicianus) colonies responded to broadcasts of prairie dog alarm calls. Western burrowing owls are closely associated with black‐tailed prairie dogs in Colorado and neighboring states on the Great Plains of the United States. Prairie dog burrows in active colonies can serve as nesting sites for Western burrowing owls, and prairie dogs may act as an alternative prey source for predators, potentially decreasing the burrowing owls' risk of predation through the dilution effect. Burrowing owls nesting on prairie dog colonies may also eavesdrop on prairie dog alarm calls, enhancing their survival and nesting success on prairie dog colonies. We performed broadcast experiments with three different sounds: a prairie dog alarm call, a biological control (cattle mooing), and a non‐biological control (an airplane engine), and characterized burrowing owl responses as either alert or relaxed. For each sound stimulus, we recorded the time to first alert response to broadcast sounds (latency) and also how frequently the target burrowing owl exhibited an alert response within the first ten seconds of the broadcast (intensity). Burrowing owls reacted more quickly to the prairie dog alarm than to the biological control. They significantly increased the intensity of alert behaviors in response to broadcasts of the alarm, but did not show an increased reaction to either the biological or the non‐biological control. Our results suggest that burrowing owls nesting on prairie dog colonies eavesdrop on, and increase their alert behaviors in response to, prairie dog alarm calls.     

The Predator Deterrence Function of Primate Alarm Calls

It is generally assumed that alarm calls function in intraspecific communication, for example to warn close relatives about the presence of a predator. However, an alternative hypothesis suggests that, in some cases, signallers may also gain fitness benefits in directly communicating to the predator, for example by advertising perception and unprofitability to predators that depend on unprepared prey. In this study, we show that six monkey species in Taï forest, Ivory Coast, produce significantly more alarm calls to leopards than to chimpanzees, although both are notorious monkey predators. The conspicuously high vocalization rates to leopards had adaptive consequences for the monkeys. By following a radio-collared leopard, we found that after detection and high alarm call rates the leopard gave up its hiding location and left the group significantly faster than would be expected by chance. We discuss these data with respect to the various functional hypothesis of alarm call behaviour and conclude that the high alarm call rates to leopards are part of an anti-predator strategy in primates that may have evolved to deter predators that depend on surprise.     

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.     

Anti‐Predator Behaviour in a Nocturnal Primate,the Grey Mouse Lemur (Microcebus murinus)

Although one‐third of all primates are nocturnal, their anti‐predator behaviour has rarely been studied. Because of their small body size, in combination with their solitary and nocturnal life style, it has been suggested that they mainly rely on crypsis to evade predators. However, recent studies revealed that nocturnal primates are not generally cryptic and that they exhibit predator‐specific escape strategies as well as alarm calls. In order to add to this new body of research, we studied anti‐predator strategies of nocturnal grey mouse lemurs experimentally. In order to elicit anti‐predator behaviour and alarm calls, we conducted experiments with a carnivore‐, snake‐ and raptor model. We also conducted playback experiments with mouse lemur alarm calls to characterize their function. In response to predator models, they exhibited a combination of anti‐predator strategies: in response to carnivore and snake models, mouse lemurs monitored the predator, probably to assess the potential risk that emanates from the predator. In response to raptor models they behaved cryptically and exhibited freezing behaviour. All mouse lemurs, except one individual, did not alarm call in response to predator models. In addition, during playback experiments with alarm calls, recorded during real predator encounters, mouse lemurs did not emit alarm calls nor did they show any escape behaviour. Thus, as in other nocturnal primates/mammals, mouse lemurs do not seem to rely on routinely warning of conspecifics against nearby predators.     

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

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

Heterospecific recognition of referential alarm calls in two species of lemur

ABSTRACT

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

Does sociality drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls

While sociality has been hypothesized to drive the evolution of communicative complexity, the relationship remains to be formally tested. We derive a continuous measure of social complexity from demographic data and use this variable to explain variation in alarm repertoire size in ground-dwelling sciurid rodents (marmots, Marmota spp.; prairie dogs, Cynomys spp.; and ground squirrels, Spermophilus spp.). About 40% of the variation in alarm call repertoire size was explained by social complexity in the raw data set. To determine the degree to which this relationship may have been influenced by historical relationships between species, we used five different phylogenetic hypotheses to calculate phylogenetically independent contrasts. Less variation was significantly explained in contrast-based analyses, but a general positive relationship remained. Social complexity explained more variation in alarm call repertoire size in marmots, while sociality explained no variation in repertoire size in prairie dogs and no variation in phylogenetically based analyses of squirrels. In most cases, substantial variation remained unexplained by social complexity. We acknowledge that factors other than social complexity, per se, may contribute to the evolution of alarm call repertoire size in sciurid rodents, and we discuss alternative hypotheses. Our measure of social complexity could be used by other researchers to test explicit evolutionary hypotheses that involve social complexity.     

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

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

Habitat structure and alarm call dialects in Gunnison's prairie dog (Cynomys gunnisoni)

We examined the relationship between habitat structure and alarmcall characteristics in six colonies of Gunnison's prairiedogs (Cynomys gunnisoni) near Flagstaff, Arizona, before andafter a mid-summer vegetation change. We found significantdifferences in alarm call characteristics between colonies,confirming the existence of alarm call dialects. Differencesin frequency components but not temporal components of callswere associated with differences in habitat structure. Playback experiments revealed that differences in alarm call structureaffected acoustic transmission of calls through the local habitat.Thus, we identify habitat structure as one factor that maycontribute to alarm call differences between colonies of Gunnison'sprairie dogs. Relationships between call characteristics andhabitat structure changed over seasons. Playback experimentssuggested that this changing relationship could reflect a change in the purpose of the alarm call between early and late summer.Some components of alarm calls seem tailored for attenuationover short distances in the early summer but for long-distancetransmission at summer's end. These differences might arisebecause pups stay close to their natal burrows in the earlysummer and disperse throughout a colony in late summer. Alternatively, these differences in alarm call transmission between seasonscould be caused by the increase in vegetation in the mid-summer.At the end of the summer prairie dogs could be more dependenton long-distance antipredator calls to offset the loss of visibilitycaused by the increase in vegetation in the late summer.     

A method for identifying sounds used in the classification of alarm calls

In this study, we present a methodology that identifies acoustic units in Gunnison's prairie dog alarm calls and then uses those units to classify the alarm calls and bouts according to the species of predator that was present when the calls were vocalized. While traditional methods measure specific acoustic parameters in order to describe a vocalization, our method uses the variation in the internal structure of a vocalization to define possible information structures. Using a simple representation similar to that used in human speech to identify vowel sounds, a software system was developed that uses this representation to recognize acoustic units in prairie dog alarm calls. These acoustic units are then used to classify alarm calls and their associated bouts according to the species of predator that was present when the alarm calls were vocalized. Identification of bouts with up to 100% accuracy was obtained. This work represents a first step toward revealing the details of how information is encoded in a complex nonhuman communication system. Furthermore, the techniques discussed in this paper are not restricted to a database of prairie dog alarm calls. They could be applied to any animal whose vocalizations include multiple simultaneous frequencies.     

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.     

Distress Calls of Birds in a Neotropical Cloud Forest1

Distress calls are loud, harsh calls given by some species of birds when they are captured by a predator or handled by humans. We recorded the frequency of distress calls and struggling behavior in 40 species of birds captured in mist nets during the dry season in a Costa Rica cloud forest. We tested the following hypotheses proposed to explain the function of distress calls: (1) calling for help from kin or reciprocal altruists; (2) warning kin; (3) eliciting mobbing behavior; (4) startling the predator; and (5) distracting the predator through attraction of additional predators. Our results did not support the calling‐for‐help, warning kin, or mobbing hypotheses. Indeed, genera that regularly occurred with kin or in flocks were not more likely to call than non‐flocking genera. There was no relationship between calling frequency and struggling behavior as predicted by the predator startle hypothesis. Genera of larger birds tended to call more than smaller birds, providing some support for both the predator distraction hypothesis and predator startle hypotheses. Calls of higher amplitude may be more effective in startling the predator. Distress calls of larger birds may also travel greater distances than those of smaller birds, supporting the predator manipulation hypothesis, but this requires further testing.     

Titi monkey call sequences vary with predator location and type

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