Vocal and Escape Responses of Columbian Ground Squirrels to Simulated Terrestrial and Aerial Predator Attacks

Most ground-dwelling sciurids emit nonrepetitive and repetitive calls in response to predators. In this study, I simulated terrestrial (badger Taxidea taxus) and aerial (flying disc) predator attacks to elicit escape and vocal responses in Columbian ground squirrels (Spermophilus columbianus). In response to the badger, ground squirrels often ran, but rarely to a burrow, and were most likely to give nonrepetitive calls before running or without running; rarely did they enter burrows. Ground squirrels in direct line of the flying disc (i.e., “target” squirrels under “attack”), ran to, and into, the nearest escape burrow and rarely gave a nonrepetitive call. Squirrels distant from the flying disc often called, usually while running or after assuming an upright posture at the nearest burrow. These results suggest that ground squirrels incur little cost when calling in response to aerial predators. Nonrepetitive and repetitive calling in response to the badger and flying disc did not differ significantly among age-sex classes; however, parous females were more likely than nonparous females to give both types of calls in response to the badger. Nonparous females either with or without close nondescendant kin rarely called in response to the badger. Thus, there was no indication that females exposed to the badger behaved nepotistically toward close kin other than their juvenile offspring. Nonrepetitive calling in response to the badger apparently functions primarily to warn vulnerable offspring and, hence, is a component of maternal investment. Although the occurrence of antipredator calling in response to the flying disc did not vary significantly among parity-kin classes, there was evidence that adult and yearling females were more likely to emit repetitive, and to a lesser extent, nonrepetitive calls, if close nondescendant kin were in the colony. I conclude that indirect fitness benefits, that is, kin selection, probably contributes to the maintenance of antipredator calling in response to aerial predators.     

Adult Richardson's Ground Squirrels (Spermophilus richardsonii) Ignore Rate Changes in Juvenile Alarm Calls: Age‐Differential Response Urgency Perception?

Juvenile Richardson's ground squirrels (RGS; Spermophilus richardsonii) communicate response urgency by modulating the rate of syllable production in repetitive alarm calls, although longer call bouts do not promote more pronounced or longer‐lasting (tonic) vigilance in juvenile call recipients. We exposed free‐living adult RGS to playbacks of alarm calls differing in rate and length to determine whether adult receivers respond to the same alarm parameters as juveniles. Adult squirrels did not respond differentially to differences in call rate or length, suggesting that adult RGS do not attend to call rate as do juveniles. This difference in response may be attributable to a developmental change in the perceptual mechanisms by which individuals extract information regarding response urgency, but could also be a product of adult receivers devaluing information encoded in alarm calls emitted by relatively inexperienced juvenile signalers.     

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.     

Monotony and the Information Content of Richardson's Ground Squirrel (Spermophilus richardsonii) Repeated calls: Tonic Communication or Signal Certainty?

The repetition of elements within an alarm signal is commonly thought to ensure that receivers have detected that signal, or to promote residual vigilance in light of the dangerous circumstances prompting the signal's initial production (tonic communication). Beyond alerting others and maintaining that state of alertness, however, repetitive signal elements may be parsed so as to encode information about the nature of potential threats. To determine how call length and variation in intersyllable latency might prove informative in the repetitive alarm vocalizations of Richardson's ground squirrels (Spermophilus richardsonii), we conducted a field‐based playback experiment quantifying antipredator responses to manipulated alarm calls. Free‐living juvenile squirrels were exposed to playbacks of 12 syllable (long) and six syllable (short) calls with a constant (monotonous) or changing (variable) call rate. The length of calls had no significant effect on the behaviour of call recipients during and immediately after call production; however, call recipients showed greater vigilance after the playback of monotonous calls than after variable calls. The absence of a call length effect is not consistent with tonic communication in the strict sense; rather, enhanced responsiveness to monotonous relative to variable calls suggests that multiple syllables, and the emergent patterns of intersyllable latency, communicate information about response urgency or the distance to a predatory threat. Only monotonous calls convey those aspects with any certainty on the part of the signaller and hence are selectively attended to by receivers.     

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.     

Age Differences in the Response of California Ground Squirrels (Spermophilus beecheyi) to Conspecific Alarm Calls

Juvenile California ground squirrel responses to adult alarm calls and juvenile alarm calling may be modified during development to achieve adult form. Adult conspecific chatter and whistle alarm calls were played back to juvenile and adult ground squirrels at an agricultural field site. In response to chatter playbacks, adults spent more time visually orienting to the environment and less time out of view and in covered habitats than juveniles; the converse was true in response to whistle playbacks. To test the evocativeness of juvenile calling, a subset of adult subjects received juvenile chatter and whistle playbacks. Adults spent less time out of view to juvenile call types than to adult calls, and showed more similar responses to juvenile chatters and whistles than to adult chatters and whistles. Age differences in the ground squirrel's alarm call system may reflect adjustments to changing risks during development.     

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.     

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.     

Species-specific and shared features in vocal repertoires of three Eurasian ground squirrels (genus <Emphasis Type="Italic">Spermophilus</Emphasis>)

Along to alarm calls, Eurasian ground squirrels of the genus Spermophilus also produce other call types toward potential predators and rival conspecifics. Individually identified 50 speckled (Spermophilus suslicus), 18 European (S. citellus) and 59 yellow (S. fulvus) ground squirrels were examined for interspecies differences in their vocal repertoires. A separate sample of 116 (90 adult and 26 juvenile) S. suslicus was examined for presence of ultrasound in their alarm calls. In addition, all tonal calls in all the three species were checked for presence of nonlinear phenomena. Calls were elicited by approaching animals in live-traps or near burrows; some types of vocalizations were also recorded during handling. Eight call types, three tonal and five wideband ones, were described. Vocal repertoires were remarkably similar between species, excluding the alarm calls, which were species-specific. Alarm calls with ultrasonic components were found in two individuals of S. suslicus. Concerning nonlinear phenomena, biphonation in alarm calls of S. suslicus, frequency jumps and sidebands in screams of S. citellus, frequency jumps and subharmonics in screams of S. fulvus were found. Results are discussed with literature evidence on audible and ultrasonic vocalizations in ground squirrels.     

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.     

Localization of Passerine Seeet and Mobbing Calls by Goshawks and Pygmy Owls

Goshawks and pygmy owls responded to recordings of passerine alarm calls by correctly orienting to their source. The seeet, or “aerial predator” alarm call which is generally assumed to be “non-localizable”, while it elicited fewer responses than did mobbing calls, was nevertheless accurately localized by all birds that did respond. The evolution of alarm calls is discussed in terms of efficient prey communication, following Darwin's “antithesis principle”, rather than predator selection for non-localizability.     

Experimental study of alarm calls of the oriental tit (Parus minor) toward different predators and reactions they induce in nestlings

Anti-predatory strategies of birds are diverse and may include predator-specific alarm calls. For example, oriental tit (Parus minor) parents can distinguish snakes from other predators and produce snake-specific referential vocalizations ("jar" call) when a snake poses a threat to their nest. The “jar” call has a very specific function to induce fledging of nestlings close to fledging age. This reaction ensures nestlings' survival in natural encounters with snakes that are capable of entering nest cavities and kill entire broods. Sciurid rodents, like chipmunks, may pose a similar threat to cavity-nesting birds. We explored the hypothesis that parents use the fledging-inducing alarm vocalizations in this situation, because chipmunks, like snakes, can kill the brood upon entering the nest cavity. We compared alarm calls of parents toward two predators (chipmunk and snake) who pose a similar threat to the nestlings in a nest cavity, and toward an avian predator (Eurasian jay) who cannot enter nest cavities and poses no threat to the nestlings in a nest. Our results show that the vocal responses of oriental tits were different among the three predators. This suggests that the acoustic properties of vocal responses to predators are different between predators of a similar hunting strategy (nest-cavity entering). The playback of recorded vocal responses of parents to chipmunks did not trigger the fledging of old nestlings, whereas the vocalizations toward a snake did, as shown by earlier studies. Our study suggests that the vocal response of parents does not carry information about the ability of predators to enter the nest cavity and confirms the special status of alarm calls triggered by snakes.     

To call or not to call: parents assess the vulnerability of their young before warning them about predators

Communication about predators can reveal the effects of both conspecific and heterospecific audiences on signalling strategy, providing insight into signal function and animal cognition. In species that alarm call to their young, parents face a fundamental dilemma: calling can silence noisy offspring and so make them less likely to be overheard, but can also alert predators that young are nearby. Parents could resolve this dilemma by being sensitive to the current vulnerability of offspring, and calling only when young are most at risk. Testing whether offspring vulnerability affects parental strategy has proved difficult, however, because more vulnerable broods are often also more valuable. We tested experimentally whether parent white-browed scrubwren, Sericornis frontalis, assessed brood noisiness when alarm calling near nests. When a model predator was nearby, parents gave more alarm calls when playbacks simulated noisy broods, yet brood noisiness did not affect adult calling when only a control model was present. Parents were therefore sensitive to the tradeoff between silencing young and alerting predators to the presence of nests. Our study demonstrates that receiver vulnerability can affect signalling decisions in species other than primates.     

Models for alarm call behaviour

The evolution of alarm call behaviour under individual selection is studied. Four mathematical models of increasing complexity are proposed and analysed. Theoretical conditions for the evolution of “selfish”, “mutualistic”, “altruistic” or “spiteful” alarm calls are established. The models indicate that the hypotheses of benefits of retaining group members or avoiding group detection are not sufficient to explain the evolution of alarm call behaviour, but serve as a complementary factor to facilitate its evolution in most cases. It is hypothesized that the evolution of alarm calls between non-kin should evolve probably when calls are mutualistic, mildly altruistic and there are beneficial group size effects against predation.     

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.     

Acoustic Behaviour of Birds and Mammals in the Predator Context; I. Factors Affecting the Structure of Alarm Signals. II. The Functional Significance and Evolution of Alarm Signals

I. 7 vocalizations emitted in the predator context are defined in terms of their function. The physical and physiological constraints on the evolution of the physical structure of alarm calls with respect to detectability and localizability are discussed. Detection of various calls depends on signal amplitude, environmental attenuation, signal-to-noise ratio, discrimination of the receiver against background noise, and absolute auditory sensitivity of the receiver. The combined effect of these factors is discussed for an exemplary predator-prey system, in which the hearing of both, predator and prey is known. Localizability of an alarm call is determined by its frequency, bandwidth, and possibly its amplitude relative to the auditory threshold of the receiver. Crude differentiation between localizable and non-localizable signals is not possible, and localizability of particular sounds varies between species. In some cases the question of detectability may render the problem of localizability unimportant. Besides detectability and localizability, other factors such as the acoustic background formed by the alarm calls of sympatric species and by the species' own repertoire of calls are discussed. II. Requisite conditions and available evidence for the evolution of alarm calls through individual selection and kin selection are described. Five types of alarm calls are discussed individually:

• 1 The occurrence of mobbing calls indicates that a major function of these calls is predator deterrence (“move on”), although the calls also alert other prey and promote cultural transmission of the predator's characteristics.
• 2 Alarm calls associated with evasive actions of the prey cause the predator to give up the hunt or diminish its hunting success by warning other prey, which only in some cases are closely related to the caller.
• 3 Distress calls of a seized prey either attract other prey which then mob the predator, or attract other predators, which presumably attack the first predator. In both cases the chances to escape are enhanced because the predator's attention is diverted.
• 4 Defence calls are used to threaten a predator. These calls often mimic sounds of other predators.
• 5 Distraction calls may enhance the effect of distraction display.

Although the different functions of various alarm calls are treated individually, certain of the calls may have more than one function and may be employed in nonpredator contexts as well.     

Red Squirrels (Sciurus vulgaris) Respond to Alarm Calls of Eurasian Jays (Garrulus glandarius)

Recognition of heterospecific (interspecific) alarm calls has been demonstrated in birds and mammals, but bird–mammal interactions have rarely been studied. Here, I tested the hypothesis that red squirrels (Sciurus vulgaris) are able to recognize alarm calls of a sympatric bird species, the Eurasian jay (Garrulus glandarius), and respond adequately with anti‐predator behaviour. Both animals are preyed upon by the same predators. To test whether squirrels would react to heterospecific alarm calls, I recorded squirrels behaviour during playbacks of jay alarm calls, control playbacks (territorial songs of sympatric songbirds) and during silence. Differences between the control treatment (songbirds) and silence were not significant. Seven of the 13 squirrels responded with escape after broadcasting alarm calls of jays. Further, squirrels spent less time in the patch, expressed a higher vigilance, and showed more rapid head and body movements. These results suggest that squirrels recognize heterospecific alarm vocalizations of jays and discriminate them from equally loud non‐threatening sounds.