Squirrel Alarm Research Articles

Call-specific patterns of neural activation in auditory processing of Richardson's ground squirrel alarm calls.

IntroductionRichardson's ground squirrels use alarm calls to warn conspecifics about potential predatory threats. Chirp calls typically indicate high levels of threat from airborne predators, while whistle calls are associated with lower levels of threat from terrestrial predators. These types of calls primarily elicit escape behaviors and increased vigilance in receivers, respectively. While much is known about the neural mechanisms involved in the production of vocalizations, less is known about the mechanisms important for the perception of alarm calls by receivers, and whether changes in perceived risk are associated with unique patterns of neuronal activation. Thus, to determine whether alarm calls associated with different levels of predation risk result in differential neuronal activation, we used immunohistochemistry to identify and quantify c‐Fos immunopositive cells in brain regions important in stress, fear, danger, and reward, following alarm call reception.MethodsWe exposed 29 female Richardson's ground squirrels (10 control, 10 whistle receivers, and 9 chirp receivers) to playbacks of whistles, chirps, or a no‐vocalization control. We then assessed neuronal activation via c‐Fos immunohistochemistry in 12 brain regions.ResultsGround squirrels receiving high‐threat “chirp” vocalizations had reduced neuronal activation in the medial amygdala and superior colliculus compared with controls. It is likely that changes in activity in these brain regions serve to alter the balance between approach and avoidance in turn promoting escape behaviors.ConclusionsThus, we conclude that in Richardson's ground squirrels, these brain regions are important for the perception of risk resulting from receiving alarm calls and allow for appropriate behavioral responses by receivers.

Can California Ground Squirrels Reduce Predation Risk to Burrowing Owls?

In northern California, USA, western Burrowing Owls (Athene cunicularia) use burrows in active California ground squirrel (Otospermophilus beecheyi) colonies for nesting and protection. Ground squirrels have well-developed, anti-predator alarm-calling behavior, but the potential benefits of such alarm calling to Burrowing Owls have not been examined. The objective of this study was to assess the rate and types of predator interactions experienced by Burrowing Owls and the extent to which they may benefit from alarm calls given by California ground squirrels. We studied interactions of California ground squirrels and Burrowing Owls at Moffett Federal Airfield in urban Santa Clara County, California, during two Burrowing Owl breeding seasons, in 2012 and 2013, using cameras and direct observations. We detected 177 approaches by predators, four of which resulted in predation events on owls. The rate of predator approach during diurnal periods, as determined by direct observation, was 0.93/hr. Ground squirrels called in response to predator approaches before owls did 66% of the time, which was approximately proportional to the abundance of ground squirrels and Burrowing Owls. When squirrels called first, an estimated 75% of owls exhibited alert responses, including alarm calling, running to the burrow, and scanning, indicating that owls benefited from ground squirrel alarm calls in response to approaching predators. Our research suggests that healthy ground squirrel populations may provide important predator alert services to Burrowing Owls, especially in the context of increasing populations of urban predator species.

Anthropogenic noise alters dwarf mongoose responses to heterospecific alarm calls

Anthropogenic noise is an evolutionarily novel and widespread pollutant in both terrestrial and aquatic habitats. Despite increasing evidence that the additional noise generated by human activities can affect vocal communication, the majority of research has focused on the use of conspecific acoustic information, especially sexual signals. Many animals are known to eavesdrop on the alarm calls produced by other species, enhancing their likelihood of avoiding predation, but how this use of heterospecific information is affected by anthropogenic noise has received little empirical attention. Here, we use two field-based playback experiments on a habituated wild population of dwarf mongooses (Helogale parvula) to determine how anthropogenic noise influences the response of foragers to heterospecific alarm calls. We begin by demonstrating that dwarf mongooses respond appropriately to the alarm calls of sympatric chacma baboons (Papio ursinus) and tree squirrels (Paraxerus cepapi); fleeing only to the latter. We then show that mongoose foragers are less likely to exhibit this flee response to tree squirrel alarm calls during road-noise playback compared to ambient-sound playback. One explanation for the change in response is that noise-induced distraction or stress result in maladaptive behaviour. However, further analysis revealed that road-noise playback results in increased vigilance and that mongooses showing the greatest vigilance increase are those that do not subsequently exhibit a flee response to the alarm call. These individuals may therefore be acting appropriately: if the greater gathering of personal information indicates the absence of an actual predator despite an alarm call, the need to undertake costly fleeing behaviour can be avoided. Either way, our study indicates the potential for anthropogenic noise to interfere with the use of acoustic information from other species, and suggests the importance of considering how heterospecific networks are affected by this global pollutant.

Comparative evaluation of three sampling methods to estimate detection probability of American red squirrels (Tamiasciurus hudsonicus)

Measuring changes in species distribution and understanding factors influencing site occupancy are recurring goals in wildlife studies. Imperfect detection of species hinders such studies, resulting in the underestimation of the number of sites occupied by the species of interest. American red squirrels (Tamiasciurus hudsonicus) are sampled traditionally with live-traps that require substantial resources to deploy and monitor. Here, we assessed whether auditory methods yield similar detection probabilities. We compared the detection probability of American red squirrels in boreal forest using point counts, playback counts, and live-trapping. Over the summer of 2014, we conducted three trapping sessions in 60 sites within black spruce forests of northwestern Quebec, Canada. We also conducted 10 min point counts in the same sites, together with playback counts using recordings of American red squirrel alarm and territorial calls. Using dynamic occupancy models to analyse three primary periods, all composed of three secondary periods, we found that the detection probability of squirrels from point counts was as high as with live-trapping. Our results thus highlight the value of the point count method in measuring American red squirrel occupancy.

Gray squirrel alarm call composition differs in response to simulated aerial versus terrestrial predator attacks

Eastern gray squirrels use three acoustically distinct vocalizations, namely kuks, quaas and moans, in their alarm calling bouts. Although moans are highly specific to aerial threats, kuks and quaas show no clear association with either terrestrial or aerial predator type when simply examining their presence or absence in an entire bout of vocal signaling. Here we examine the relationship between alarm call composition (the presence and rate of kuks, quaas and moans) and the type of stimulus eliciting the alarm call (aerial or terrestrial). When the first 30 sec or second 30 sec of calling is examined, the presence of kuks, quaas (only used in the second 30-sec period), and moans are all associated with stimulus type. Kuks and quaas are usually used in response to terrestrial stimuli and moans are used exclusively in response to aerial stimuli. The relationship between call composition and stimulus is even stronger when considering the rate of calls. In the first 60 sec of calling, all three vocalizations differ in rate depending on threat type, with more kuks and more quaas elicited by terrestrial than aerial stimuli, while moans are not produced at all with terrestrial stimuli. Overall rates of calling, combining all three vocalization types, also differed by stimulus type. The median number of vocalizations in the first 60 sec of calling bouts elicited by terrestrial threats was nearly 3 times greater than in calling bouts elicited by aerial threats. The alarm calls of gray squirrels are predator-specific, containing significant information on whether a threat is aerial or terrestrial. Further, the rate of each vocalization type in the initial 60 sec of calling bouts provides more information than does only the presence or absence of each vocalization type.

Hidden Markov models of eastern gray squirrel (Sciurus carolinensis) alarm calls

Eastern gray squirrels produce alarm calls—vocalizations used in the presence of danger that influence the behavior of some receivers. This influence is possible because the alarm calls’ rate, duration, and structure contain information about the threat and the caller. Gray squirrels’ mix of different structural call types (kuks and quaas) could contain information on potential internal influences within the squirrel. Hidden Markov models (HMMs) are ideal tools to investigate whether hidden states explain the frequencies of kuks versus quaas throughout an alarm call sequence. In this study, we compare the ability of an iid (independent and identically distributed) model and two- to six-state HMMs to represent observed sequences of kukking, quaaing, and periods of silence. Audio recordings of 44 gray squirrels were collected and the first 30 s of each alarm call sequence was coded based on spectrograms. A number of HMMs were fitted, and the overall fit of the observed sequences to each model was assessed using Akaike’s Information Criterion (AIC) and Bayesian Information Criterion (BIC), and Monte Carlo methods. The five-state HMM fit the observed call frequencies better than the other models, suggesting that the squirrels’ alarm calling sequences are influenced by a more complex temporal sequencing of acoustic units.

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

AbstractIn 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.

Alarm Calls of California Ground Squirrels (Spermophilus beecheyi)

California ground squirrel alarm vocalizations were recorded in field and laboratory, and sonagraphically analysed. The contexts of both naturally occurring and experimentally elicited calls were noted in the field. The components of this graded system are chatters, chats and whistles. Chatters and chats are often elicited by terrestrial predators, whistles commonly by low flying raptors. Whistles are more commonly associated with cryptic behavior and flight than chatter-chats, but both call types usually elicit bipedal alert postures. These calls grade along a number of dimensions which may signal redundantly the level of excitation of the caller. We propose that the chatter-chat calls of highly aroused squirrels are composed of more and longer notes, occur at a higher rate, are less noisy and contain more frequency modulation. Whistles, however, are single-note calls that contain no frequency modulation, even though they are emitted by highly aroused squirrels and are long and noise free. Preliminary data suggest that: 1) chats are easier for a human ♀ to localize than whistles; 2) elevation of the head, by adopting bipedal postures and mounting promontories, enhances the audibility of alarms.

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

AbstractAlarm 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.

Short-Term and Long-Term Individuality in Speckled Ground Squirrel Alarm Calls

Apart from the alerting function of alarm calls, selection may favor cues that help individuals to distinguish between reliable and unreliable callers. However, this mechanism for selective response to real and false alarms may act only if the individual characteristics of the call are stable at least for some time. Here we test this implicit assumption for the caller’s reliability hypothesis, studying individuality of alarm calls in a colony of free-living, individually marked speckled ground squirrels (Spermophilus suslicus). We recorded each of 20 study animals 4 times during repeated captures when calling from a live trap toward a human, with spans of 1 day, 2 weeks, and 1 year from the 1st capture. Ten alarm call notes per animal per capture were analyzed. Individual alarm call notes showed high similarity within captures but differed strongly between captures. Both multivariate analysis of variance and discriminant function analysis showed that vocal individuality decreased rapidly with an increase of the time span between recordings. However, vocal individuality always remained higher than expected random value. Examination of our data suggests that alarm calls are unstable, which contradicts the caller reliability hypothesis, because its implicit assumption of stable individual identity is not fulfilled. However, short-term stability still may be sufficient to ensure short-term individual recognition between kin and neighbors. Also, even if the alarm calls change structurally, because group members meet up daily, they can update their knowledge of the call structure of individuals, and this would likely allow them to distinguish between reliable and unreliable individuals.

Signaler and Receiver Ages Do Not Affect Responses to Richardson's Ground Squirrel Alarm Calls

Abstract Alarm calls alert receivers to the presence and/or nature of a predatory threat. Studies of alarm communication in Richardson's ground squirrels (Spermophilus richardsonii) have focused on juvenile signalers and receivers; however, adult and juvenile receivers may tailor their response to alarm calls based on different underlying signal parameters and attend differentially to alarm calls broadcast by adult versus juvenile signalers. To examine the potential influence of signaler and receiver age on the perception of response urgency, we presented free-living juvenile and adult S. richardsonii with alarm calls produced by juveniles and adults. Behavioral responses of call recipients were videotaped and analyzed to determine the influence of signaler and receiver age-class. No differences in vigilance response after juvenile- and adult-produced calls were detected for either adult or juvenile receivers. At the proximate level, the absence of any detectable difference in the acoustic attributes of j...

Functional morphology of Richardson's ground squirrel, Spermophilus richardsonii, alarm calls: the meaning of chirps, whistles and chucks

Repetitive alarm vocalizations of Richardson's ground squirrels vary in terms of the acoustic structure of their primary syllables and the inclusion of brief, lower-amplitude, frequency-modulated trailing elements we term ‘chucks.’ Chucks are included in calls of both males and females and increase in prevalence with the proximity of the caller to the alarm-evoking stimulus. Furthermore, chuck presence is not independent of primary syllable type: chucks follow primary syllables that have constant frequency and diminishing amplitude (‘whistle’), but do not trail primary syllables with diminishing frequency and nondescending amplitude spectra (‘chirps’). Playbacks to free-living squirrels of repeated alarm calls having whistle- or chirp-like primary syllables factorially combined with chuck presence or absence revealed that chirp-like syllables elicited greater vigilance from call recipients during signal propagation. The addition of chucks to the end of primary syllables of either type, however, increased initial vigilance duration and the proportion of time devoted to vigilance during and after signal reception. Chucks thus promote increased and lasting vigilance on the part of call recipients. Beyond enhancing vigilance, however, the inclusion of frequency-modulated chucks and chirps facilitates the orientation of receivers to the signaller. Multiple acoustic parameters of Richardson's ground squirrel alarm vocalizations thus interact to communicate information regarding several aspects of a predator encounter. Receivers use this information to their advantage, affording greater attention to calls that would be more readily located by predators, and hence are more costly for signallers to produce.

Individual acoustic variation in Belding's ground squirrel alarm chirps in the High Sierra Nevada.

The acoustic structure of calls within call types can vary as function of individual identity, sex, and social group membership and is important in kin and social group recognition. Belding’s ground squirrels (Spermophilus beldingi) produce alarm chirps that function in predator avoidance but little is known about the acoustic variability of these alarm chirps. The purpose of this preliminary study was to analyze the acoustic structure of alarm chirps with respect to individual differences (e.g., signature information) from eight Belding’s ground squirrels from four different lakes in the High Sierra Nevada. Results demonstrate that alarm chirps are individually distinctive, and that acoustic similarity among individuals may correspond to genetic similarity and thus dispersal patterns in this species. These data suggest, on a preliminary basis, that the acoustic structure of calls might be used as a bioacoustic tool for tracking individuals, dispersal, and other population dynamics in Belding’s ground squirrels, and perhaps other vocal species.

Yellow-bellied marmot and golden-mantled ground squirrel responses to heterospecific alarm calls

When two species have predators in common, animals might be able to obtain important information about predation risk from the alarm calls produced by the other species. The behavioural responses of adult yellow-bellied marmots, Marmota flaviventris, and golden-mantled ground squirrels, Spermophilus lateralis, to conspecific and heterospecific alarm calls were studied to determine whether interspecific call recognition occurs in sympatric species that rarely interact. In a crossed design, marmot and squirrel alarm calls were broadcast to individuals of both species, using the song of a sympatric bird as a control. Individuals of both species responded similarly to conspecific and heterospecific anti-predator calls, and distinguished both types of alarms from the bird song. These results indicate that both marmots and squirrels recognized not only their own species' anti-predator vocalizations, but also the alarm calls of another species, and that these vocalizations were discriminated from an equally loud non-threatening sound. These findings suggest that researchers ought to think broadly when considering the sources of information available to animals in their natural environment. Copyright 1998 The Association for the Study of Animal Behaviour Copyright 1998 The Association for the Study of Animal Behaviour.

Letters to the Editor

LETTERS TO THE EDITOR Dear Sir: Mazin B. Qumsiyeh (Spring 1990 issue) has portrayed passionately and pessimistically some of the heated controversies in modern evolutionary biology. Although they are sweetly reasonable compared to the nastiness of Bishop WiIberforce toward Darwin and Thomas Huxley, Qumsiyeh worries that when scientific positions are held with "acid conviction" they may retard scientific progress. But such worry is foundless. The argument over cladistics versus phenetics is not frivolous; it strikes at the very heart of the central question of evolution—the descent of modern species from ancient ones. It is essential that systematists face the issue squarely. The debate over human sociobiology is classical, stretching back for centuries. For biologists interested in understanding Homo sapiens sapkns, no question is more important or fundamental than the relative contributions of culture and heredity and their interaction. There often lies at the bottom of these debates the problem of imprecise definition of terms. There has been, for example, a public argument over whether parental care should be classed as altruistic [1—4]. However, as Wilson [5, p. 117] points out, "Self-sacrifice for the benefit of offspring is altruism in the conventional but not in the strict genetic sense, because individual fitness is measured by the number of surviving offspring." (emphasis added) Scientific terms must be strict and precise and since altruism in evolutionary theory is a genetic question, the genetic sense must be used, never the conventional. (Even though Wilson himself reverts to the conventional meaning a few pages later.) The failure to define terms precisely and to consistently follow that definition leads to confusion and unproductive debate. Older sciences do not have this problem. In mechanics, the term "velocity" means the time rate ofchange ofposition of a body in reference to a specified direction; it never means simply speed. I am sanguine that as the young science of biology matures, terms will be used more precisely, and useless debate will disappear. REFERENCES 1.Dunford, C. Kin selection for ground squirrel alarm calls. Am. Nat. 111:782-785, 1977. 2.Sherman, P. Nepotism and the evolution of alarm calls. Science 197:1246-1253, 1977. 3.Shields, W. M. Ground squirrel alarm calls: nepotism or parental care. Am. Nat. 116:599-603, 1980. Permission to reprint a letter printed in this section may be obtained only from the author. Perspectives in Biology and Medicine, 34, 3 ¦ Spring 1991 467 4.Brown, J. L. Cooperation—a biologist's dilemma. In Advances in the Study ofBehavior, edited by J. S. Rosenblatt, R. A. Hinde, C. Beer, and M. C. Busnel. New York: Academic Press, 1982. 5.Wilson, E. O. Sociobiology. Cambridge, Mass.: Belknap, 1975. Leonard Hersher College of Medkine State University ofNew York Syracuse, New York 13210 Dear Sir: In a recent assay (Spring 1990 issue), I discussed the development and factors affecting resolution (or lack of resolution) of controversies in evolutionary biology . I used three examples to illustrate recent heated controversies in this field: the designation of subspecies names, the philosophy of systematics, and the influence of sociobiology. My conclusion is that, in some situations, lack of proper data combined with a biased attention to the extremes of any controversy produce heated arguments that sometimes border on being personal and political . I suggested a more "peaceful" approach which involves encouraging more data collection combined with less dogma. Such an approach would be conducive to further research and stimulation of new ideas and would encourage new students of biology to pursue research in evolution. The letter by Dr. Hersher raises two issues. First, he states that discussions such as cladistics versus phenetics are "not frivolous" in biology. I stated in my assay that these controversies are fundamental but that the heated discussions between the extremes of each view may be too excessive, bordering on the political and personal debate and occupying countless pages ofjournal space. I also stated that this level was reached in some evolutionary controversies of which I cited three examples. Again, Hersher implies that I stated that discussions are not good for evolutionary biology and that all discussions lead to heated controversies. His comment, as well as the statement about Bishop Wilberforce, is either because he did...

Ground Squirrel Alarm Calls: Nepotism or Parental Care?

Previous articleNext article No AccessNotes and CommentsGround Squirrel Alarm Calls: Nepotism or Parental Care?William M. ShieldsWilliam M. Shields Search for more articles by this author PDFPDF PLUS Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The American Naturalist Volume 116, Number 4Oct., 1980 Published for The American Society of Naturalists Article DOIhttps://doi.org/10.1086/283651 Views: 12Total views on this site Citations: 20Citations are reported from Crossref Copyright 1980 The University of ChicagoPDF download Crossref reports the following articles citing this article:Brandon C. Wheeler Selfish or altruistic? An analysis of alarm call function in wild capuchin monkeys, Cebus apella nigritus, Animal Behaviour 76, no.55 (Nov 2008): 1465–1475.https://doi.org/10.1016/j.anbehav.2008.06.023Warren G. Holmes The Development and Function of Nepotism, (Jan 2001): 281–316.https://doi.org/10.1007/978-1-4615-1209-7_8DANIEL T BLUMSTEIN, KENNETH B ARMITAGE Why do yellow-bellied marmots call?, Animal Behaviour 56, no.44 (Oct 1998): 1053–1055.https://doi.org/10.1006/anbe.1998.0875MARK E HAUBER, PAUL W SHERMAN Nepotism and marmot alarm calling, Animal Behaviour 56, no.44 (Oct 1998): 1049–1052.https://doi.org/10.1006/anbe.1998.0876Douglas P. Chivers, R. Jan F. Smith Chemical alarm signalling in aquatic predator-prey systems: A review and prospectus, Écoscience 5, no.33 (Mar 2016): 338–352.https://doi.org/10.1080/11956860.1998.11682471 Daniel T. Blumstein and Kenneth B. Armitage Does Sociality Drive the Evolution of Communicative Complexity? A Comparative Test with Ground‐Dwelling Sciurid Alarm Calls Blumstein & Armitage, The American Naturalist 150, no.22 (Jul 2015): 179–200.https://doi.org/10.1086/286062DANIEL T. BLUMSTEIN, JEFF STEINMETZ, KENNETH B. ARMITAGE, JANICE C. DANIEL Alarm calling in yellow-bellied marmots: II. The importance of direct fitness, Animal Behaviour 53, no.11 (Jan 1997): 173–184.https://doi.org/10.1006/anbe.1996.0286R. Bruce MacWhirter Vocal and Escape Responses of Columbian Ground Squirrels to Simulated Terrestrial and Aerial Predator Attacks, Ethology 91, no.44 (Apr 2010): 311–325.https://doi.org/10.1111/j.1439-0310.1992.tb00872.xP. Gouat, J. Ggouat Les Sequences De Remplacement Chez Ctenodactylus gundi: Competition Ou Cooperation?, Behavioural Processes 18, no.1-31-3 (Jan 1989): 107–118.https://doi.org/10.1016/S0376-6357(89)80009-9Paul W. Sherman The levels of analysis, Animal Behaviour 36, no.22 (Apr 1988): 616–619.https://doi.org/10.1016/S0003-3472(88)80039-3C.N. Slobodchikoff, William M. Shields ECOLOGICAL TRADE-OFFS AND SOCIAL BEHAVIOR, (Jan 1988): 3–10.https://doi.org/10.1016/B978-0-12-648780-0.50005-0Kenneth B. Armitage Social dynamics of mammals: Reproductive success, kinship and individual fitness, Trends in Ecology & Evolution 2, no.99 (Sep 1987): 279–284.https://doi.org/10.1016/0169-5347(87)90037-1Bruce Waldman Mechanisms of kin recognition, Journal of Theoretical Biology 128, no.22 (Sep 1987): 159–185.https://doi.org/10.1016/S0022-5193(87)80167-4Paul W. Sherman Alarm calls of Belding's ground squirrels to aerial predators: nepotism or self-preservation?, Behavioral Ecology and Sociobiology 17, no.44 (Oct 1985): 313–323.https://doi.org/10.1007/BF00293209William M. Shields Barn swallow mobbing: Self-defence, collateral kin defence, group defence, or parental care?, Animal Behaviour 32, no.11 (Feb 1984): 132–148.https://doi.org/10.1016/S0003-3472(84)80331-0John L. Hoogland Nepotism and alarm calling in the black-tailed prairie dog (Cynomys ludovicianus), Animal Behaviour 31, no.22 (May 1983): 472–479.https://doi.org/10.1016/S0003-3472(83)80068-2Jerram L. Brown Cooperation—A Biologist's Dilemma, (Jan 1983): 1–37.https://doi.org/10.1016/S0065-3454(08)60284-3Ian G. McLean The association of female kin in the arctic ground squirrel Spermophilus parryii, Behavioral Ecology and Sociobiology 10, no.22 (Apr 1982): 91–99.https://doi.org/10.1007/BF00300168Jerram L. Brown BEHAVIORAL ECOLOGY FOR SOPHOMORES, Evolution 36, no.22 (May 2017): 421–422.https://doi.org/10.1111/j.1558-5646.1982.tb05063.xPaul W. Sherman Kinship, demography, and belding's ground squirrel nepotism, Behavioral Ecology and Sociobiology 8, no.44 (Jul 1981): 251–259.https://doi.org/10.1007/BF00299523

Responses to alarm calls by California ground squirrels: Effects of call structure and maternal status

1. The purposes of this study were to assess the response eliciting properties of five structural variants of the California ground squirrel alarm call system, and to compare the responsiveness of females with and without young to the vocalizations. Tape recordings of alarm calls and control sounds were played back in the field to adult female ground squirrels. The squirrels responded very little to control sounds. Following alarm calls, however, posture height and running increased; feeding, walking and non-locomotion movements decreased. None of the playbacks elicited vocalizations from the squirrels. 2. The four chatter-chat calls evoked patterns of response that were distinctly different from reactions to the whistle. The immediate running response to chatter-chats was followed quickly by upright posturing, which subsequently declined throughout the 3-min period following the call. Feeding was suppressed throughout the 3-min post-chatter-chat interval, but movement increased after initial inhibition. After the initial running response to whistles, walking was common and upright posturing was delayed until the second post-call minute. Feeding and nonlocomotion movement were initially suppressed but increased monotonically over time. We proposed that these differences were adaptively related to the fact that chatter-chats typically follow detection of terrestrial predators, whereas whistles usually signal flying raptors. 3. The responses to the four chatter-chat calls were graded in intensity, reaching higher levels in response to calls with more notes and lower noise content. The chat, a one-note call with high noise content, evoked the weakest reaction. We proposed that these two dimensions of calling (number of notes and noise content), in conjunction with several other semi-independent parameters, provide a sufficient diversity of signals to permit specification of the referent of the call (conspecific or predator) as well as the arousal level of the caller. 4. We hypothesized that kin selection was responsible for the greater responsiveness of parous than of nonparous females to the alarm calls, and we discussed some implications of this difference.

Kin Selection for Ground Squirrel Alarm Calls

Kin Selection for Ground Squirrel Alarm Calls

Characteristics of arctic ground squirrel alarm calls.

Arctic ground squirrels, Citellus undulatus, produce six distinctly different sounds. Each of these sounds may represent a signal in itself, but combinations of these acoustic elements or repetition of a single element produce additional signals. Several of these signals serve as alarm calls. One sound element consists of a short (0.05 sec) broad frequency chat while another is a longer (0.16 to 0.25 sec) descending narrow frequency whistle. Squirrels utter three-note chatter calls when approached by a ground predator, and a series of five or more chatters, which fade in intensity, is given upon the close approach of a ground predator as the squirrel escapes into a burrow. A single whistle, which resembles the alarm call of some birds, is given upon the approach of an aerial predator. This call is repeated at approximately six to eight second intervals if the predator alights near a squirrel and remains nearby.