Anim. Behav., 1988,36,1533-1540

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

W. J. LOUGHRY* & COLLEEN M. McDONOUGHt*Ethology Program, Department of Zoology, University of Tennessee, Knoxville, TN 37996, U.S.A.

tAnimal Behavior Graduate Group, Division of Environmental Studies, University of California, Davis,CA 95616, U.S.A.

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

Schleidt (1973) first proposed a possible 'tonic'function for some aspects of animal signallingbehaviour. These tonic signals were hypothesizedto modify the behaviour of perceivers over anextended period of time rather than producingsome immediate and short-lived behavioural res-ponse. For example, Schneider et al. (1986) haveproposed that the vibration dance of the honeybee,Apis mellifera, acts tonically to regulate foragingactivity within the hive.

Owings & Hennessy (1984) applied Schleidt'shypothesis to some instances of calling in groundsquirrels. Many ground squirrels utter the samevocalization repeatedly in long, rhythmic bouts ofcalling (e.g. Balph & Balph 1966; Waring 1966,1970; Melchior 1971; Barash 1973; Betts 1976;Matocha 1977; Smith et al. 1977; Taulman 1977;Koeppl et al. 1978; Owings & Virgina 1978;Robinson 1981; Leger et al. 1984). These calls areoften heard during or in the aftermath of anencounter with a predator (e.g. Owings et al. 1986).Owings & Hennessy (1984) proposed that theserepetitive calls might act tonically to promotevigilance in perceivers, the signaller thus obtaininglookouts for detecting the predator should itreturn. There is anecdotal evidence that someground squirrel calls may function in this manner(e.g. Betts 1976; Smith et al. 1977), but thehypothesis has not yet been tested rigorously.

We attempted to test this tonic communicationhypothesis by examining the repetitive calling ofCalifornia ground squirrels, Spermophilus bee-cheyi. California ground squirrels utter both non-repetitive chatters and repetitive chatter-chatsduring and after encounters with mammalianpredators (Owings & Virginia 1978; Leger et al.1980; Owings & Leger 1980; Owi~gs et al. 1986).Owings et al. (1986) argued that non-repetitivechatters served primarily a warning function sincethey occurred early in an encounter, and thatrepetitive calling might serve some other functionsince these calls were acting on individuals that hadalready been alerted. They hypothesized that re-petitive calling might function to maintain visualvigilance in perceivers and thus produce lookoutsin case the predator should return.

Several predictions can be made in order to testthis tonic function of repetitive calling. First,repetitive calling should elicit more persistent orsustained vigilance than that evoked by non-repetitive calls alone. In other words, vigilance inresponse to non-repetitive calls should decay whilethe additional calling during repetitive calls shouldmaintain higher levels of vigilance. Second, onemight also predict that longer bouts or higher ratesof repetitive calling would produce more prolongedincreases in the vigilance of perceivers (cf. Harris etal. 1983). Finally, longer bouts of repetitive calling

1533

1534 Animal Behaviour, 36. 5

might also prevent a decay in vigilance, so thatperceivers would have lower levels of vigilance aftercompletion of a short call bout than during thelater stages of a long bout. In this paper, we testthese predictions and present data on the effect ofeach type of call on the behaviour of perceivers.

METHODS

The study was conducted on a population ofCalifornia ground squirrels located in an aban-doned walnut orchard at Camp Ohlone, SunolRegional Wilderness, Alameda County, Califor-nia. This population has been studied continuouslysince 1982 and a general description of the studysite and methods are published elsewhere (e.g.Trulio et al. 1986).

Squirrels were observed 2 days each week begin-ning 11April and ending 27June 1987,fora total of172 h of observation. Half of the observation daysoccurred prior to the first emergence of pups(young of the year) from their natal burrows.

During observations, a Uher 4400 tape-recorderwas kept running at a tape speed of 4,7 cm/s inorder to record any vocalizations that occurred.These tapes were analysed subsequently to obtaininformation on the duration, number of calls andcall rate in each recorded bout of calling. Some callscould not be analysed due to high levels ofbackground noise, although it was usually at leastpossible to obtain information on call duration.

When a repetitive or non-repetitive calloccurred, we immediately selected a squirrel otherthan the caller and began a focal-animal sample ofthat individual (Altmann 1974). If another callerbegan calling before the first caller had stopped, weabandoned data collection. We avoided biasing ourdata towards conspicuously vigilant squirrels byeither selecting the animal closest to the caller or,more often, pre-selecting an individual prior to anycalling. Individuals were selected so as to providean approximately equal sample of all age/sexclasses (Loughry & McDonough, unpublisheddata). Focal samples were collected only when theelicitor of the call was unknown. This was done toavoid confounding vigilance produced by callingwith that elicited by the disturbance itself. Weassumed that calls for which we did not know thecause were also perceived as such by the squirrels,thus making the methodology a form of naturalplayback experiment (e.g. Robinson 1981). This

mayor may not have been a valid assumptiondepending on how much information about theeliciting situation was potentially extractable fromthe calls (e.g. Leger et al. 1980; Owings & Leger1980).

Focal samples centred on whether the animalwas vigilant. Vigilance is defined here as includingany instance in which the squirrel was stationaryand its head was at or above a horizontal planepassing through its shoulders. We distinguishedbetween bipedal and quadrupedal forms of vigi-lance, hypothesizing that bipedal vigilance wouldbe more important in detecting or monitoringpredators and thus more likely to be influenced byrepetitive calling. The time of onset and termi-nation of each bout of vigilance was recorded andthe percentage of time spent in bipedal and quad-rupedal vigilance was then calculated. Focal sam-ples were continued for the duration of the call andfor 5 min after the end of the call. Control sampleswere then obtained for the focal animal after atleast 15 min had elapsed in which no callingoccurred. These control samples were taken for thesame length of time as during the call or for aminimum of 5 min for calls of short duration. Notall individuals could be relocated and observed on

the day the call was uttered. When this happened,the control sample was taken at the same time ofday during the next observation session.

The focal animal's vigilance may have beeninfluenced by the number of other squirrels andtheir distance from the focal individual (Loughry &McDonough, unpublished data). Howeyer, wefound no evidence that the distributions of thesevariables were different for repetitive versus non-repetitive calls, or for calls versus control periods,so they do not influence the comparisons madehere. Vigilance in California ground squirrels canalso vary with microhabitat location (Leger et al.1983), but no attempt was made to control for this.In part this was because the focal squirrels usuallymoved through large areas of the colony duringsampling (both during calls and control periods),thus removing any bias from remaining in aparticular microhabitat location.

Data on vigilance were calculated as the percent-age of time spent in either quadrupedal or bipedalvigilance. These percentages were arcsine trans-formed prior to analysis. The data for individualswho were sampled more than once for a particulartype of call were pooled for each individual and theaverage values were used in analyses. Matched-

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pairs t-tests were used to investigate the effect ofrepetitive and non-repetitive calling on vigilance.Unpaired t-tests were used to compare repetitiveand non-repetitive calling with one another. Alltests are two-tailed.

RESULTS

We first examine the effects of non-repetitive andrepetitive calls on vigilance separately and then testthe predictions of the tonic communicationhypothesis.

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Non-repetitiveCalls

All non-repetitive calls were chatter vocaliza-tions. California ground squirrels also give non-repetitive 'whistles' to avian predators (Owings &Virginia 1978; Leger et aI. 1979), but we did notrecord any of these, since raptors are rare in theorchard. Non-repetitive calls usually consisted of asingle chatter lasting less than I s, although boutsof up to fivechatters lasting almost 2 min were alsorecorded (X = 1.74 calls per bout, durationrange= < 1-110 s, N = 36).

After hearing a chatter, squirrels significantlyincreased the percentage of time they spent vigilantand this increase was largely due to an increase inthe time squirrels spent bipedally vigilant (Fig. 1).Matched-pairs t-tests revealed significant differ-ences between post-call and control periods for

total (t=2'07, P<0'03), total bipedal (t=3'05,P<0'003) and total quadrupedal (t=2'19,P < 0.02) vigilance. In all cases, df = 31. In fact, thepercentage of time spent in quadrupedal vigilancedeclined during this time (Fig. I), suggesting thatsquirrels may make some trade-off in the timeallocated to different forms of vigilance.

However, the impact of a chatter was not longlasting. We split the 5-min post-call period into twohalves and examined vigilance in each half. FigureI shows that the increase in bipedal vigilance wasonly apparent during the first half of the post-callperiod. Indeed, the percentage of time spent inbipedal vigilance was significantly higher in the firsthalf than in the second half of the post-call period(t=2'67, df=28, P<0'02). Bipedal vigilance dur-ing the second half of the post-call period was onlymarginally different from that observed duringcontrol observations (t= 1,64, df=27, P<0'06).Focal squirrels spent more time bipedally thanquadrupedally vigilant during the first half of thepost-call period (t=3'02, df=30, P<O'OI), but bythe second half they spent equ.alamounts of time ineach type of vigilance (t= 1'36, df=28, P<0'19,this was also the case during control periods,t=0'59, df=80 for quadrupedal versus bipedalvigilance).

In sum, non-repetitive chatters did increasevigilance, largely by increasing the proportion oftime perceivers spent bipedally vigilant. This effectlasted for only a few minutes before perceiversreturned to baseline levels of visual vigilance.

1536 Animal Behaviour, 36, 5

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Repetitive Calls

Repetitive calls were usually initiated by one ormore chatter vocalizations, followed by a variablenumber of rythmically uttered single-note 'chats'(Owings & Virginia 1978).The inclusion of a seriesof chats distinguished repetitive from non-repeti-tive calls and no repetitive calling bout consistedsolely of chatters. Repetitive calling bouts werelong (X duration=394'5 s, range=21-1462 s,N = 56) and contained a large number of vocaliza-tions (X number of calls per bout = 264'9,range = 6-1596, N = 49). The rate of calling withina bout was faster initially and declined as the boutprogressed (call rate during the first half of the boutversus overall call rate, paired t=5.22, df=34,P<O'OOOI,means=0'70 versus 0.55 callsjs, res-pectively). Also, bouts oflonger duration tended tohave higher overall rates of calling (Pearson'sr=0'65, N=43, P<O'OI).

Repetitive calling did increase vigilance over thatobserved during control periods. Figure 2a showsthat total vigilance during a repetitive call bout wassignificantly different from that observed bothduring the control (t=5.81, df=46, P<O'OOOI)and during the 5-min post-call periods (t = 3.39,df=43, P< 0'001). Total vigilance was also signifi-cantly higher during the 5 min after the call thanduring the control period (t=2.43, df=42,

P < 0'01, see Fig. 2a). As Fig. 2b demonstrates, thisincreased vigilance during repetitive calling wasdue to an increase in the percentage of time spentbipedal during the first half of the bout (time spentbipedal in first versus second half t=4'34, df=49,P < 0.000I). By the second half of a call bout,bipedal vigilance had declined to post-call levels(t=0.50, df=43), but was still significantly greaterthan control levels (t = 2,67, df = 46, P < 0'02). Thiseffect seems independent of the duration of calling.We split repetitive calls into two groups: those withdurations shorter (X duration = 184 s) and longer(X duration=654 s) than the median (350 s).Separate examination of these short and longrepetitive calls showed the same pattern of declinein bipedal vigilance from the first to the second halfof a calling bout (P<0'004 in both cases). Thiseffect may be due to the fact that in both short andlong calling bouts, the rate of calling declined as thebout progressed (call rate in the first half of thebout versus overall call rate), though for short callbouts this difference was not significant (t= 1,74,df=lO, P<0.12).

Squirrels spent approximately the same percent-age of time in quadrupedal vigilance during andafter calling as during the control period, althoughthere was a significant decline from the first to thesecond half of the post-call period (t= 1,68, df=40,P < 0'05, Fig. 2b). It was only during the first half ofa repetitive call bout that squirrels spent more timebipedally than quadrupedally vigilant (t = 4'12,df=49, P<O'OOOI).For the rest of the bout andthroughout the post-call period, squirrels spentapproximately equal percentages of time in eachform of vigilance and this was also true of controlperiods (see above and Fig. 2b, note also thatcontrol levels of vigilance did not differ for repeti-tive and non-repetitive calls, compare Figs I and 2).These findings did not change when short and longbouts were examined separately.

These data indicate that repetitive calling doesincrease visual vigilance in perceivers, but that thiseffect diminishes as the bout progresses. Given theseemingly limited impact of repetitive calling, itcould be argued that either (I) the repetitivecomponent of the call is unimportant and it isactually the initiating chatter(s) that promoteincreased vigilance, or (2) there are unmeasuredeffects of repetitive calling on perceiver behaviour.The former argument can be tested by comparingthe effects of repetitive and non-repetitive calls onperceiver vigilance. If repetitive calling acts tonic-

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Figure 3. Effect of repetitive and non-repetitive calls on percentage oftime spent vigilant by perceivers. Values representthe percentage oftime spent vigilant during the first 5 min of a repetitive calling bout and the 5 min after a non-repetitivecall. Legend is the same as in Fig. I. Only total vigilance was significantly different between call types, see text.

ally, one would predict increased vigilance torepetitive calls over that elicited by a non-repetitivecall alone.

Tests of the Tonic Hypothesis

We tested the above prediction by comparingvigilance during the 5-min post-call period forchatters with vigilance during the first 5 min of arepetitive call. If the additional cells in a repetitivecall did not have an effect on visual vigilance, thenthe values should be similar. If repetitive callingacted tonically to maintain higher levels of suchvigilance, then the values should be higher thanthose for chatters alone. The results of this analysisare presented in Fig. 3. As predicted, total vigilancein this 5-min period was increased by repetitivecalling (t=2.23, df=61, P<0'03). This was acumulative effect since neither bipedal nor quadru-pedal levels of vigilance were significantly differentbetween the two call types (although the trendswere in the appropriate direction, see Fig. 3). Theseresults represent a strong test of the tonic commu-nication hypothesis and provide support for itsprimary prediction.

Comparison of the levels of vigilance over theentire duration of a repetitive calling bout withvigilance after a chatter revealed the same pattern:bipedal and quadrupedal vigilance were not differ-ent when examined separately, but total vigilancewas marginally higher for repetitive calls (t = 1'91,

df=81, P<0'06; repetitive calls: 1'=68.9%, non-repetitive calls: 1'= 55.6%). Thus, although visualvigilance declined as a repetitive calling boutprogressed (see above), calling was not completelyfutile since it did elicit more vigilance from per-ceivers than did chatters. Additionally, absolute(rather than proportional) levels of vigilance weresignificantly related to call duration (e.g. totalbipedal vigilance during a call bout, r=0.45,N=41, P<O'OI; total vigilance during a call bout,r=0'50, N=41). Thus, longer repetitive callingbouts produced longer periods of vigilance inperceivers, but the percentage of time perceiversspent in vigilance declined as the bout progressed.

There was little support for the second predictionderived from the tonic hypothesis. Only one signifi-cant correlation of vigilance with call rate orduration was found, and this was negative (per-centage of time in quadrupedal vigilance in the firsthalf of the call bout with call rate in the first half ofthe bout, r= -0.37, N=30, P<0'O5). Recall thatwe predicted that longer calling bouts shouldpromote a prolonged increase in vigilance over thatproduced by shorter bouts, but the data do notsupport this prediction.

We attempted to test this prediction further bycomparing short and long repetitive calls (definedabove). Again, the prediction was not supported.While no comparison reached statistical signifi-cance, even the trends were in the direction op-posite that predicted. For example, both total

1538 Animal Behaviour, 36, 5

vigilance during a bout and in the post-call periodtended to be higher for short than for long calls(total vigilance during call: short = 74,5%,long=64-4%, t= 1,32, df=45, P<0'19; post-call:short=60'5%, long=44'4%, t= 1,49, df=40,P<0'14).

A final prediction from the tonic hypothesis canbe made if one assumes that repetitive calling actsto retard the rate of decay in perceiver vigilance. Ifso, then the percentage of time spent in vigilanceshould be greater in the later stages of a long callingbout than in the post-call period of a short bout.We attempted to test this by comparing vigilance inthe second half of long calling bouts with vigilancein the post-calling period of short bouts. Again,there was no support for this prediction (bipedal,quadrupedal and total vigilance, P<O'77, df=47in all cases).

DISCUSSION

In total, the results presented here partially supportthe tonic communication hypothesis for repetitivecalling by California ground squirrels. Both repeti-tive and non-repetitive calling increased the per-centage of time perceivers spent visually vigilant,but repetitive calling maintained this increase invigilance for a longer period of time. However,repetitive call bouts were only effective at maintain-ing high levels of such vigilance in perceivers overthe first half of the bout's duration. Indeed,increased call duration did not lead to an increasein the percentage of time perceivers spent vigilant(see also Harris et al. 1983). Long repetitive callbouts may have been less effectivethan shorter onesat maintaining proportionately high levels of vigi-lance in perceivers, but long calling bouts were notcompletely futile since they did produce higherabsolute levels of vigilance than did short bouts.These findings indicate that, while better than non-repetitive calls, there may be some limit to theeffectiveness of repetitive calling at maintainingvisual vigilance.

This constraint may arise from the conflict ofinterest between signaller and perceiver inherent inmany communicatory systems (Dawkins & Krebs1978; Morton 1982; Krebs & Dawkins 1984;Owings & Hennessy 1984; Mark11985; Owings &Loughry 1985). Repetitive calling is a time-con-suming activity; some bouts lasted more than 20min and we observed one to go on for more than an

hour. Recall that, in this study, only calls for whichthe elicitor was presumably unknown were used.Thus, perceivers of these call bouts could poten-tially have spent considerable amounts of timescanning for a disturbance that did not exist or wasof uncertain significance. It is clearly in the bestinterests of a perceiver to scan the environment atthe onset of a call, but it seems reasonable toassume that willingness to maintain this activitywill decline as calling continues and nothing hap-pens. The particular 'giving up' time will probablydepend on the constraints imposed on the timebudget of an individual. For instance, one mightpredict that adult females with vulnerable youngmight remain vigilant longer (e.g. Leger & Owings1978). Recently emerged pups face an interestingtrade-off in that they are probably more vulnerableindividuals and so should remain vigilant for a longtime, but they also need to feed in order to put onthe weight necessary for successful overwintering(e.g. Murie & Boag 1984). Of course, some activi-ties are not fully incompatible with vigilance. It wascommon to observe squirrels begin feeding whilestill remaining bipedal and scanning the surround-ings (see also Devenport 1986).

Repetitive calling by California ground squirrelsmay represent a form of 'persuasion' (Dawkins &Krebs 1978; Krebs & Dawkins 1984), whereinsignallers attempt to maintain or induce, byrepeated signalling, some outcome in perceivers.Chatter vocalizations, either alone or as initiatorsof a repetitive calling bout, seem effective intemporarily increasing vigilance in perceivers.Repetitive calling might then be necessary topersuade perceivers to remain vigilant for longerthan they otherwise would if a non-repetitive callhad been used. The effectiveness of this persuasionis then constrained by the interests of the particularperceiver. Thus, longer repetitive call bouts maybecome less effective than shorter ones (see above).The mechanism for this loss of effectiveness mightbe some form of habituation. California groundsquirrels may be able to circumvent this constraintand induce longer periods of vigilance by insertingnon-repetitive calls intermittently into a repetitivecalling bout (see also Beletsky et al. 1986).We haveobserved this on a few occasions and it seemed toincrease the vigilance of perceiving squirrels,although the effect was usually short-lived. Alter-natively, a signaller might increase the rate ofrepetitive calling in an attempt to maintain vigi-lance during long call bouts (e.g. Morton & Shalter

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1977). Although we found no positive correlationbetween call rate and vigilance, we did not attemptto correlate vigilance with changes in call rate. Itwas our impression that sudden increases in callrate evoked temporary increases in vigilance byconspecifics. Thus, in order to remain an effectivepersuader within a repetitive calling bout, sig-nallers may have to vary their signalling output (ineffect, dishabituating perceivers). The effectivenessof such a strategy would then also be imbeddedwithin longer time-scale constraints such as thesignaller's past history of reliability with perceivers(Cheney & Seyfarth 1988).

An alternative to the interpretation of repetitivecalling as persuasion might be that such callingallows perceivers to go on with their normalactivities while remaining auditorily alert with thecaller acting as a kind of sentinel (e.g. Morton &Shalter 1977). This alternative seems consistentwith the decline in visual vigilance associated withlong bouts of repetitive calling. This view wouldalso seem to predict increased visual vigilance todeviations from the established calling pattern (e.g.alterations in call rate or insertion of non-repetitiveelements). However, this view would not seem topredict the tonic effect of repetitive calling docu-mented in this paper. Indeed, one might predict theopposite effect, that visual vigilance would declineat the onset of a repetitive call and thus be less thanthat elicited by a non-repetitive call alone.

These two alternatives could be distinguishedexperimentally. The persuasion view argues thatcallers continue calling repetitively in order to gainlookouts should the predator return. The sentinelview argues that call perceivers reduce their vigi-lance and rely on the signaller to be a sentinel.Thus, the persuasion view would predict that apredator would be detected by non-calling indi-viduals earlier in trials in which calling occurredthan during non-calling trials. The sentinel viewwould predict that non-calling individuals woulddetect the approach of a predator no earlier, andpossibly later, than during non-calling controlperiods. In addition, the sentinel hypothesis wouldnot predict changes in call patterning in the absenceof changes in the eliciting situation. Remember thatthe calls under study here were apparently notevoked by the actual presence of a predator andchanges in call patterning did not appear to us to becorrelated with any obvious change in environmen-tal conditions. If callers often alter call patten in theabsence of situational changes, then the sentinel

1539

hypothesis would seem less explanatory. Finally,whether one interprets repetitive calling as persuas-ive or as the outcome of the signaller attempting toinform conspecifics about changes in the elicitingsituation, seems to us to depend on whether oneopts for an informational or non-informationalview of communicatory systems (e.g. Smith 1977;Dawkins & Krebs 1978; Green & Marler 1979;Morton 1982;Owings & Hennessy 1984;Owings &Loughry 1985). It is not clear whether empiricalinformation can resolve this larger issue.

Repetitive and non-repetitive forms of callingare ubiquitous among ground squirrels (see refer-ences in Introduction) and are probably commonamong other species as well. So far as we are aware,this is the first study to demonstrate empirically afunction for repetitive calling. It seems unlikelythat repetitive calling necessarily serves the samefunction in all other ground squirrels. Indeed,repetitive calling may not function in the same wayfor all individuals within a species. There is someevidence of age, sex and seasonal differences inindividual responsiveness to repetitive and non-repetitive calls in California ground squirrels(Leger & Owings 1978; Loughry & McDonough,unpublished data). We await further testing of thetonic communication hypothesis in other species,which will undoubtedly deepen our understandingof this form of calling.

ACKNOWLEDGMENTS

We thank Don Owings for permitting us to carryout this project at his study site. NSF grant BNS8210065 to D. H. Owings and D. F. Hennessy madethe establishment of this study site possible. Specialthanks to Marta Hersek and Diane Boellstorf forproviding help, advice and friendship in the field.Don Owings and W. J. Hamilton III graciously lentus the necessary equipment. D. W. Leger, D. H.Owings, W. J. Smith, C. T. Snowdon and ananonymous reviewer made many useful commentson an earlier version of this paper. Preparation ofthe manuscript was made possible while W.J.L.held an N.I.H. post-doctoral traineeship in Etho-logy at the University of Tennessee.

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(Received 12 November 1987; revised 22 January 1988;MS. number: A5173)