Calling and vigilance in california ground squirrels: a test of the tonic communication hypothesis

Owings & Hennessy (1984) proposed that repetitive calling by ground squirrels, i.e. long bouts of calling wherein the same vocalization is uttered repeatedly, might act as a tonic signal to promote vigilance in perceivers. This idea was tested by comparing the effect of naturally occurring repetitive and nonrepetitive calls on the behaviour of California ground squirrels, Spermophilus beecheyi. Both types of calls increased the amount of time spent vigilant by perceivers, especially in bipedal postures. More time was spent vigilant after repetitive than non-repetitive calls, thus supporting the tonic communication hypothesis. However, longer bouts of repetitive calling did not promote proportionately increased vigilance over that evoked by shorter calls. In fact, the reverse was true and the increase in vigilance to repetitive calls began to wane during the later stages of a calling bout. Repetitive calling may represent a case of ‘persuasion’, in which the signaller continues signalling in an attempt to maintain some state in resistant perceivers.     

Antipredator behaviour and predator recognition in Belding's ground squirrels

This study evaluates whether Belding's ground squirrels (Spermophilus beldingi) recognize predators under natural conditions. I observed these squirrels for 300 h during two consecutive summers, during which I described 1029 aerial and terrestrial interactions, including 299 interactions with animals known to prey on squirrels. Squirrels responded differentially to predators and non-predators, to predators that hunt differently, and to contextually different interactions with the same predator. Responses shown in encounters with predators included Trill and Chirp vocalizing, upright Posting, crouching, running to burrow entrances, entering burrows, Approaching or chasing predators, and doubling-back on pursuing predators. Ground squirrels appear to adjust their antipredator behaviour depending on the amount and kind of danger they face during an encounter.     

Premating Behavior in the Subgenus Limia (Pisces: Poeciliidae): Sexual Selection and the Evolution of Courtship

A three-year field-study of Richardson's ground squirrels was conducted to assess whether alarm calling functions to warn close relatives (“kin selection” hypothesis) or manipulate conspecifics (a “selfish” hypothesis). S. richardsonii had distinct calls for terrestrial and aerial predators, and the responses of squirrels varied appropriately according to the context of calls, implying that calling conveyed correct information concerning the nature of the danger. Alarm calling elicited by naturally occurring encounters with potential predators during 454 h of observation, and by a thrown frisbee in 70 experimental trials, was not equally probable for all age/sex classes. Squirrels were most likely to call when they had offspring or siblings nearby, which is supportive of the hypothesis that alarm calling is maintained by kin selection. Adult males, residing in the vicinity of either their probable progeny or their nonlittermate half-siblings, were the most likely age/sex class to call during the lactation period when young were below ground and were most vulnerable. I conclude that alarm calling by Richardson's ground squirrels is nepotistic rather than manipulative.     

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

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

Predator‐Associated Vocalizations in North American Red Squirrels (Tamiasciurus hudsonicus): To Whom are Alarm Calls Addressed and How do They Function?

Alarm vocalizations produced by prey species encountering predators can serve a variety of functions. North American red squirrels are a small-bodied mammal popularly known for producing loud, conspicuous alarm calls, but functional accounts of calling in this species are few and contradictory. We conducted research over a 3-yr period on a sample of 47 marked red squirrels in the foothills of the Canadian Rockies. We recorded the production of alarm calls during encounters with natural predators and in a series of simulated predator experiments. We tested for variation in call production patterns consistent with three traditional hypotheses concerning the conspecific warning functions of alarm calling: namely that they serve as warnings to kin, to potential mates, or to territorial neighbors with which callers have an established relationship. Patterns of calling did not provide clear support for any of these hypothesized functions. We consider several possible qualifications to our results. We also consider the possibility that conspicuous calls given by red squirrels during encounters with predators are directed at the predators themselves and function to announce their detection and possibly deter them. This possibility is consistent with additional life-history features of red squirrels including that they are a relatively solitary and territorial, food-hoarding species that produces the same conspicuous vocalizations in response to other squirrels intruding on their territory to steal cones. An important corollary of this account is that red squirrel alarm calls probably do not entail referentially specific messages about different types of predator, as proposed previously.     

The More the Scarier: Adult Richardson's Ground Squirrels (Spermophilus richardsonii) Assess Response Urgency Via the Number of Alarm Signallers

Richardson’s ground squirrels (RGS) produce alarm calls that warn conspecifics of potential predators. We presented free‐living adult and juvenile RGS with playbacks of repetitive alarm calls from one vs. two juvenile callers broadcast sequentially through two spatially separated loudspeakers. Adult RGS spent a greater proportion of time vigilant in response to two vs. one calling squirrel, whereas juvenile RGS did not respond differentially to two vs. one caller. Apparently then, the relative inexperience of juvenile RGS with alarm calls and the context in which such calls are emitted precludes their enumeration of alarm callers. Taken together with our earlier finding that adult but not juvenile RGS ignore information regarding response urgency encoded in the rate of juvenile produced repetitive calls, our present results suggest a developmental shift in response‐urgency perception. Adult RGS selectively extract information regarding response urgency via discrimination of the number of callers, ignoring less reliable information encoded in the rate of repetitive calls issued by inexperienced juvenile signallers.     

Avoiding predators at night: antipredator strategies in red-tailed sportive lemurs (Lepilemur ruficaudatus)

Although about one-third of all primate species are nocturnal, their antipredator behavior has rarely been studied directly. Crypsis and a solitary lifestyle have traditionally been considered to be the main adaptive antipredator strategies of nocturnal primates. However, a number of recent studies have revealed that nocturnal primates are not as cryptic and solitary as previously suggested. Thus, the antipredator strategies available for diurnal primates that rely on early detection and warning of approaching predators may also be available to nocturnal species. In order to shed additional light on the antipredator strategies of nocturnal primates, I studied pair-living red-tailed sportive lemurs (Lepilemur ruficaudatus) in Western Madagascar. In an experimental field study I exposed adult sportive lemurs that lived in pairs and had offspring to playbacks of vocalizations of their main aerial and terrestrial predators, as well as to their own mobbing calls (barks) given in response to disturbances at their tree holes. I documented the subjects' immediate behavioral responses, including alarm calls, during the first minute following a playback. The sportive lemurs did not give alarm calls in response to predator call playbacks or to playbacks with barks. Other behavioral responses, such as gaze and escape directions, corresponded to the hunting strategies of the two classes of predators, suggesting that the corresponding vocalizations were correctly categorized. In response to barks, they scanned the ground and fled. Because barks do not indicate any specific threats, they are presumably general alarm calls. Thus, sportive lemurs do not rely on early warning of acoustically simulated predators; rather, they show adaptive escape strategies and use general alarm calls that are primarily directed toward the predator but may also serve to warn kin and pair-partners.     

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.     

Nepotistic alarm calling in the Siberian jay, Perisoreus infaustus

From a life history perspective, parents have an incentive to protect their reproductive investment, and so may provide care even after their offspring are independent. Such prolonged parental care could lead to postponed dispersal of the offspring and thereby facilitate the formation of kin groups. We tested whether alpha birds in Siberian jays protected their independent, retained offspring by giving alarm calls during simulated predator attacks. We compared the responses to predator attacks simulated by flying a hawk model over a dyad of birds on a feeder for dyads composed of an alpha bird and either a relative or a nonrelative. Alpha females were nepotistic in their alarm-calling behaviour, in that they called more frequently when accompanied by their retained offspring than by unrelated immigrants, but alpha males called indiscriminately. This difference in alarm calling could reflect dominance relationships in Siberian jay groups, because the presence of immigrants may be less costly to alpha males, but alpha females are more vulnerable to competition from immigrants. Alarm calls were usually given during escape, when both individuals in the dyad had left the feeding site. However, results of a playback experiment suggest that alarm calls conveyed information about danger and incited an immediate escape reaction. Our results indicate that alarm calling can be nepotistic, and that factors other than kinship influence alarm-calling behaviour. Nepotistic antipredator behaviours are benefits that offspring can gain only in their natal territory. Hence, in the absence of preferential treatment by their parents, offspring may be more likely to disperse and kin groups are prevented from forming.     

Does Gray Squirrel (Sciurus carolinensis) Response to Heterospecific Alarm Calls Depend on Familiarity or Acoustic Similarity?

In habitats in which multiple species are prey to the same predators, individuals can greatly benefit from recognizing information regarding predators that is provided by other species. Past studies have demonstrated that various mammals respond to familiar heterospecific alarm calls, but whether acoustic similarity to a familiar call can prompt a mammal's recognition of an unfamiliar call has yet to be shown. We presented alarm calls to free‐ranging eastern gray squirrels (Sciurus carolinensis) and recorded behavioral changes in vigilance and antipredatory response. Playbacks included alarm calls of a sympatric bird (American robin, Turdus migratorius), an allopatric bird with a call structure similar to that of the robin (common blackbird, Turdus merula), and an allopatric bird with a distinct call structure (New Holland honeyeater, Phylidonyris novaehollandiae). Squirrels responded significantly more frequently to squirrel alarm calls (positive control) than to robin song (negative control) or honeyeater calls. Squirrel response to robin and blackbird alarm calls was statistically similar to their response to squirrel alarm calls, indicating that squirrels responded to those alarm calls as if they provided information about the presence of predators. However, squirrel response to robin song was not statistically different from response to any of the other avian calls, including the robin and blackbird alarms, suggesting that squirrels neither respond to blackbird alarms as if they clearly signify danger, nor as if they clearly do not signify danger, perhaps reflecting some ambiguity in interpretation of the calls. These results suggest that squirrel responses to alarm calls are generally based on call familiarity, but that acoustic similarity of an unfamiliar allopatric call to a familiar call also can elicit antipredator behavior. The lack of response to honeyeater alarm calls also supports the hypothesis that call recognition by gray squirrels is dependent on familiarity, rather than simply detection of an acoustic feature common to alarm calls across a variety of avian species.     

Plasticity of Alarm-call Response Development in Belding's Ground Squirrels (Spermophilus beldingi, Sciuridae)

Plasticity in the alarm-call responses of Belding's ground squirrels ( Spermophilus beldingi ) may function to prepare young to respond appropriately to calls according to the predator environment and habitat in which the young develop. To examine the extent to which antipredator responses are sensitive to early rearing environments, we studied the development of behavioural responses to playbacks of alarm calls and non-alarm calls in free-living juveniles and captive juveniles housed in large outdoor enclosures. Compared with same-aged, free-living juveniles, captive juveniles were more likely to show an observable response to playbacks, exhibited more exaggerated initial responses (e.g. enter a burrow vs. freeze), and remained alert longer following playbacks. The influence of rearing history on antipredator responses was limited to responses to auditory stimuli, as the two groups of juveniles reacted similarly to fast-moving visual stimuli. The responses of free-living juveniles appeared to be more discriminating than responses of captive juveniles, particularly following playbacks of calls associated with less immediate threats.
The responses of captive and free-living mothers were similar, indicating a developmental component to the juvenile response differences observed here. Free-living juveniles developed a discrimination among alarm and non-alarm calls sooner than captive young. Response differences were evident within 1 wk of first emergence from natal burrows and persisted at least 4 wk, at around the age of natal dispersal. This suggests that early rearing history has an enduring effect on response repertoires, which may be adaptive if animals continue to inhabit the predator environment in which they developed.     

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.     

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.     

What is Communicated in the Antipredator Calls of Lemurs: Evidence from Playback Experiments with Ringtailed and Ruffed Lemurs

Two hypotheses of signal specificity in antipredator calls (“referential signalling” and “response urgency”) are discussed in light of prior research on ground squirrels and vervet monkeys. These hypotheses then are examined with data on responses of semi-captive ringtailed and ruffed lemurs to antipredator call playbacks. Although the responses of ringtailed lemurs support a referential-signalling interpretation of their antipredator calls, those of ruffed lemurs do not conform well to either hypothesis. Rather, ruffed lemur antipredator calls seem best viewed as “affective” signals that may only reflect underlying emotional/motivational states.     

Birds adjust acoustic directionality to beam their antipredator calls to predators and conspecifics

Animals in many vertebrate species vocalize in response to predators, but it is often unclear whether these antipredator calls function to communicate with predators, conspecifics or both. We evaluated the function of antipredator calls in 10 species of passerines by measuring the acoustic directionality of these calls in response to experimental presentations of a model predator. Acoustic directionality quantifies the radiation pattern of vocalizations and may provide evidence about the receiver of these calls. We predicted that antipredator calls would have a lower directionality if they function to communicate with surrounding conspecifics, and a higher directionality and aimed at the receiver if they function to communicate with the predator. Our results support both of these functions. Overall, the birds produce antipredator calls that have a relatively low directionality, suggesting that the calls radiate in many directions to alert conspecifics. However, birds in some species increase the directionality of their calls when facing the predator. They can even direct their calls towards the predator when facing lateral to it—effectively vocalizing sideways towards the predator. These results suggest that antipredator calls in some species are used to communicate both to conspecifics and to predators, and that birds adjust the directionality of their calls with remarkable sophistication according to the context in which they are used.     

Ultrasonic Vocalizations Emitted by Flying Squirrels

Anecdotal reports of ultrasound use by flying squirrels have existed for decades, yet there has been little detailed analysis of their vocalizations. Here we demonstrate that two species of flying squirrel emit ultrasonic vocalizations. We recorded vocalizations from northern (Glaucomys sabrinus) and southern (G. volans) flying squirrels calling in both the laboratory and at a field site in central Ontario, Canada. We demonstrate that flying squirrels produce ultrasonic emissions through recorded bursts of broadband noise and time-frequency structured frequency modulated (FM) vocalizations, some of which were purely ultrasonic. Squirrels emitted three types of ultrasonic calls in laboratory recordings and one type in the field. The variety of signals that were recorded suggest that flying squirrels may use ultrasonic vocalizations to transfer information. Thus, vocalizations may be an important, although still poorly understood, aspect of flying squirrel social biology.     

Silent katydid females are at higher risk of bat predation than acoustically signalling katydid males

Males that produce conspicuous mate attraction signals are often at high risk of predation from eavesdropping predators. Females of such species typically search for signalling males and their higher motility may also place them at risk. The relative predation risk faced by males and females in the context of mate-finding using long-distance signals has rarely been investigated. In this study, we show, using a combination of diet analysis and behavioural experiments, that katydid females, who do not produce acoustic signals, are at higher risk of predation from a major bat predator, Megaderma spasma, than calling males. Female katydids were represented in much higher numbers than males in the culled remains beneath roosts of M. spasma. Playback experiments using katydid calls revealed that male calls were approached in only about one-third of the trials overall, whereas tethered, flying katydids were always approached and attacked. Our results question the idea that necessary costs of mate-finding, including risk of predation, are higher in signalling males than in searching females.     

Calling at a cost: elevated nestling calling attracts predators to active nests

Begging by nestling birds has been used to test evolutionary models of signalling but theory has outstripped evidence. Eavesdropping predators potentially impose a cost on begging that ensures signal honesty, yet little experimental evidence exists for such a cost at active nests because the use of artificial nests, long playback bouts and absence of parents may have exaggerated costs. We broadcast short periods (1 h) of either nestling vocalizations or background noise at active white-browed scrubwren, Sericornis frontalis, nests. Nestlings called naturally during both treatments, allowing us to test whether elevated calling increases risk, a key but rarely tested assumption of evolutionary models. Predators visited nests exclusively during periods of elevated calling. Furthermore, playbacks affected neither adult visits nor nestling activity, suggesting that calling alone attracted predators. Adults gave alarm calls and nestlings usually called less when predators approached nests. Predation risk to broods is, therefore, likely to fluctuate substantially over short periods of time, depending on nestling hunger and whether adults or young have detected predators. This study confirms a present-day cost of nestling begging, demonstrates that this cost can be incurred over short periods and supports the importance of parent-offspring antipredator strategies in reducing predation risk.     

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.