silent tidbitting in male fowl, gallus gallus: a referential visual … · and domm, 1943)...

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INTRODUCTIONFundamental to any analysis of signal function is the issue of receiverresponse specificity. Signals produced solely in a particular contextcan allow receivers to identify the eliciting event, such as thediscovery of food or the sudden appearance of a predator. In manycases, this predictive relationship allows adaptive decision making[e.g. food searching or flight (Evans, 1997; Hauser, 1997)]. Signalsthat evoke such highly specific receiver responses in the absenceof contextual cues are considered functionally referential (Evans,1997). Previous research has demonstrated the existence of acoustic(Evans et al., 1993a; Evans and Evans, 1999; Seyfarth and Cheney,1990) and visual (Gould and Gould, 1988) referential signals andthese now appear to be taxonomically widespread, occurring inspecies as diverse as non-human primates (e.g. Di Bitetti, 2003;Macedonia, 1990; Seyfarth et al., 1980), birds (Bugnyar et al., 2001;Evans et al., 1993a; Evans and Evans, 2007), suricates (Manser,2001) and social insects (von Frisch, 1993).

Some of the same species that produce referential signals alsohave multimodal communication. The honeybee, Apis mellifera,waggle dance encodes the direction, distance and profitability of afood source (von Frisch, 1974; Gould and Gould, 1988). Duringthe waggle dance, the direction of the wagging run indicates thedirection of food. This visual display is accompanied by vibratorybursts, the duration of which is correlated with the distance to food.The combined display is hence an example of multimodal referentialcommunication.

Multimodal communication has two putative benefits: ensuringthat the intended receiver perceives the signal, and maximizinginformation content (Hebets and Papaj, 2005; Partan and Marler,1999; Partan and Marler, 2005; Rowe, 1999). Redundant or ‘backup’

signals (Johnstone, 1996; Zuk et al., 1993) convey the sameinformation through each modality, thereby increasing the likelihoodof signal detection in a noisy environment. By contrast,nonredundant or ‘multiple message’ displays (Johnstone, 1996;Møller and Pomiankowski, 1993; Zuk et al., 1993) transmit differentinformation via each channel, potentially increasing the rate ofinformation transfer (Candolin, 2003; Partan and Marler, 1999;Partan and Marler, 2005). If one component of a redundantmultimodal display is functionally referential, then the othercomponent might be expected to elicit a similarly specific receiverresponse when produced independently. However, this predictionhas never been experimentally tested.

We focus here on the visual component of a food-related audio-visual multimodal display produced by fowl (tidbitting). Theacoustic component of this display (food calling) consists of seriesof pulsatile, cluck-like sounds (Marler et al., 1986a; Stokes andWilliams, 1971), which are known to be functionally referential.Audio playbacks are sufficient to evoke substrate-search responses,in the absence of other cues (Evans and Evans, 1999), and thebehavior of the hens is mediated specifically by the expectation offinding food (Evans and Evans, 2007).

Under natural conditions, discovery of a palatable item by a malein the presence of a hen reliably elicits the multimodal tidbittingdisplay (Evans and Marler, 1994; Marler et al., 1986a; Marler etal., 1986b; Stokes and Williams, 1971). This performance oftenentices one or more hens to approach the tidbitting male and food-search near him, sometimes taking the food item directly from hismandibles (Gyger and Marler, 1988; Marler et al., 1986a; Marleret al., 1986b). In this hierarchically structured system, hens preferto mate with males that provide food (Pizzari, 2003) and, in the

The Journal of Experimental Biology 212, 835-842Published by The Company of Biologists 2009doi:10.1242/jeb.023572

Silent tidbitting in male fowl, Gallus gallus: a referential visual signal with multiplefunctions

Carolynn L. Smith* and Christopher S. EvansCentre for the Integrative Study of Animal Behaviour, Department of Brain, Behaviour and Evolution, Macquarie University, Sydney,

NSW, 2109, Australia*Author for correspondence (e-mail: [email protected])

Accepted 6 January 2009

SUMMARYWith the notable exception of bee dances, there are no established examples of multimodal referential signals. The food calls ofmale fowl, Gallus gallus, are functionally referential and the acoustic component of a multimodal display. However, the specificityof the receiver’s response to the visual component (tidbitting) has never been tested. Here we provide the first detailed analysisof tidbitting, and test the hypothesis that these characteristic movements are functionally referential. We conducted a playbackexperiment with five high-definition video stimuli: Silent tidbit, Matched-frequency motion in the opposite direction, Silent crows,Inactive male and Empty cage. Females searched for food more during Silent tidbitting than under any other condition,suggesting that this visual display specifically predicts the presence of food and hence has similar functional properties to foodcalls. Silent tidbitting was also singularly effective at evoking approach and close inspection, which may enhance signalmemorability. These social responses suggest that the visual component of the display has the unique function of triggeringassessment of signaler identity and quality as a potential mate. The acoustic and visual components are hence redundant as afood signal, but synergistic when additional functions are considered. These findings emphasize the perceptual complexity ofmultimodal displays and provide the first demonstration of multimodal referential signaling in a vertebrate.

Key words: multimodal communication, visual displays, food calls, referential signals.

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presence of a hen, dominant males respond to a subordinate’s foodcalling and tidbitting display with overt aggression, often chasinghim away from the food and then food calling themselves (Stokesand Williams, 1972). On occasions, subordinate males alter thesignal by producing only the visual component, suppressing the call.Experimental playbacks demonstrate that these unimodal displaysstill attract hens to the silently tidbitting male (Smith and Evans,2008).

In contrast to these detailed analyses of food calling, the visualdisplay has only been described in general terms. Davis and Domm(Davis and Domm, 1943) characterized tidbitting as a repeated,rhythmic motion of the head and neck, including repeated pickingup and dropping of the food item. Wood-Gush’s (Wood-Gush, 1954)description was similarly brief and he treated the two displaycomponents as a single action, whereas Davis and Domm (Davisand Domm, 1943) recognized that these often occur separately andtreated them as distinct. Stokes and Williams (Stokes and Williams,1971) provided the most detailed overview of the tidbitting display,although they did not quantify the specific motions performed ordetermine if there was any consistency to the sequence order. Manyvisual displays are stereotyped (Wiley, 1983) and include an alertingcomponent, which engages the attention of the intended receiver(Fleishman, 1988; Rowe, 1999) thereby improving signaldetectability in noisy environments. A more precise analysis of thestructure of the tidbitting display is an essential prerequisite forfurther study of signal design.

We have previously shown (Smith and Evans, 2008) that thevisual display elicits similar overall levels of food searching to themultimodal display and the acoustic component alone. However,the multimodal and visual display evoke higher levels of inspection– a conspecific recognition behavior (Dawkins, 1995; Guhl andOrtman, 1953) – than the audio alone. Hence the acoustic and visualcomponents of male tidbitting can be classified as perceptuallyredundant (sensu Partan and Marler, 1999) with regard to food searchduration. However, the additional social response suggests that thevisual display has an additional function.

These findings are consistent with the idea that the visual displaymight be a food-related signal with response specificity comparableto that of food calls, in which case tidbitting would have the unusualproperty of being a multimodal signal in which the components ineach modality were functionally referential. However, there areseveral possible alternative explanations for the hen’s food searchresponse. These include a release from vigilance in the presence ofan alert companion (Artiss and Martin, 1995) or a general increasein foraging in response to any male movement.

In this study, we tested the specificity of hen responses totidbitting motion. First, we classified the most common movementsand described their typical order over the course of the tidbittingdisplay. We gave males food items in the presence of an unfamiliarhen and scored the types of motor pattern produced and theprobability of transitions between them. This defined the grossstructure of the visual display and tested whether the temporalsequence was constrained. Results also informed the design of theplaybacks that followed.

We then conducted an experiment to test perceptual processing.Stimuli were designed to evaluate a range of motions, with varyinglevels of spatiotemporal similarity to normal tidbitting. Hens wereshown high-definition videos of a male performing four differentmovement patterns and control footage of an empty cage. We thenanalyzed video recordings of the hens’ food searching and socialbehavioral responses. If the visual display were functionallyreferential, we would predict an increase in the food searching

behavior specific to normal tidbitting, such that responses to thisplayback would be greater than those to any other type of motionand to the empty cage control.

MATERIALS AND METHODSSubjects

Male and female golden Sebright bantam fowl, Gallus gallus(Linnaeus 1758), were the subjects for both experiments. Thebehavior of this strain closely resembles that of the ancestral form,the red junglefowl, Gallus gallus (Collias and Joos, 1953; Collias,1987; Andersson et al., 2001; Schütz and Jensen, 2001) from whichall domesticated strains have been derived (Fumihito et al., 1994;Fumihito et al., 1996). In particular, Sebrights have not beensubjected to artificial selection for rapid growth or egg production.

Birds were housed in 1.0m�1.0m�0.6m (length � width �height) cages in a climate-controlled room maintained at 22°C ona 12h:12h day:night cycle and given ad libitum access to high-protein food (Gordon Specialty Feeds, Sydney, Australia) and waterin their home cages. Twenty-five males participated in experimentI, which measured the structure of tidbitting. Each male was housedwith a single female. Twenty-four different hens participated inexperiment II, which tested specificity of response. These hens werehouse in same-sex pairs.

Recordings for creation of playback stimuli and behavioraltesting were conducted in a sound-attenuating chamber (AmpisilenceS.p.a., Roberssomero, Italy 2.38m�2.38m�2.15m), which waslined with 10cm ‘Sonex’ foam baffles (Illbruck, Minneapolis, USA)on the side walls and 15cm baffles on the ceiling to preventreverberation.

Experiment I: tidbitting performanceTest apparatus

During each trial, the male was confined to a steel-framed wire cage(0.60m�0.45m�0.86m), which had an audience hen cage ofsimilar size abutting the left side wall and a food dispenser on theopposite wall (for details, see Evans and Evans, 1999). Wemonitored tests via a Sony 1450QM color monitor, connected to aPanasonic WV-CL320 video camera in the sound chamber. APanasonic WJ-810 time-date generator provided a ‘stopwatch’ atthe bottom of the video display for timing test sessions. All testswere video recorded using a Panasonic AG-7750 VHS-format deck.

Design and test procedureMales were placed in the test cage for 15min each on threeconsecutive days to habituate them to the test environment. Weplaced each male’s cage-mate in the adjoining audience cage duringthese sessions to facilitate habituation. No food was presented.

On the fourth day, the male was again placed in the test cage,but with an unfamiliar hen in the audience cage. Unfamiliar henswere used as audience because males are most likely to display foran unfamiliar female, although the performance does not differ basedon familiarity (C.S.E., unpublished). After a 5min delay, whichallowed the male to settle after handling, the food dispenser wasactivated, delivering five corn kernels onto the floor of his cage.

Analysis of head movementsWe recorded the type of movement and position of the male’s headin space in every video frame (PAL standard; 40ms time interval).Movements fell naturally into three discrete classes, which we codedas follows: ‘twitch’ (Fig.1A): a rapid horizontal side-to-side motionof the head with the neck held fully upright; ‘short bob’ (Fig.1B):abrupt vertical movement of the head from a fully upright position

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to a point halfway above the floor, returning to the upright position;and ‘long bob’ (Fig.1C): vertical movement of the head, plungingthrough the full arc toward the floor, often picking up the food itemwith the mandibles, and ending with the head in the upright position.We recorded all transitions between these motor patterns andcalculated mean probabilities, which were then summarized in akinematic plot (Lehner, 1979). Results of this analysis informed thedesign of the experiment II stimuli.

Experiment II: female response to visual tidbitting displayTest apparatus

The test apparatus consisted of a 106cm Sony high-definition flatpanel plasma display (resolution 1080 by 1960 pixels), mounted atfloor level next to a 1.2m�0.30m�0.5m cage with a remote-controlled wire door 0.4m from one end. Previous research hasdemonstrated the hens can recognize the movements of conspecifics

on video screens (McQuoid and Galef, 1993) and that videoplayback evokes natural anti-predator and social responses (Evansand Marler, 1991; Evans et al., 1993a; Evans et al., 1993b). TheHDV format used in this study provides an approximately four-foldincrease in resolution over standard-definition digital video and hassuccessfully been used in multimodal playbacks with hens (Smithand Evans, 2008).

Decisions about the overall layout of the test setup were informedby the well-described properties of the fowl visual system. Hensrecognize conspecifics using close binocular inspection of the otherbird’s head and neck region (Guhl and Ortman, 1953), but they aremyopic in the frontal field and so unable to determine individualidentity from distances greater than 30cm (Dawkins, 1995; Dawkins,1996; Dawkins and Woodington, 1997). We hence positioned theend of the test cage 30cm from the plasma display, a distance atwhich a hen should attempt social recognition by fixating on thescreen. Note that this spatial separation was also sufficient to preventhens from resolving individual pixels, with a concomitant loss ofverisimilitude. The long axis of the cage was perpendicular to theplasma display and the remote-controlled door was at the end farthestfrom it.

Stimulus designWe used a 3-CCD high-definition video camera (Sony HDR-FX1)to make high-definition (1920�1080 lines) video recordings of 12male fowl, Gallus gallus, performing the tidbitting display. Duringrecording, the video signal was monitored on the plasma displaylater employed for playbacks, allowing us to adjust the camera zoomso that the image of the male was precisely life-sized. Males wereconfined in a 0.60m�0.45m�0.86m wire cage, 0.8m from thecamera. The audience hen was held in a separate cage, approximately30cm from that of the male. After a 10min acclimation period, fourmealworms were delivered from a remote-controlled food hoppermounted above the male’s cage. This usually evoked tidbitting andfood calling from the male.

We selected four males using the same criteria as in our previousstudy (Smith and Evans, 2008). Raw footage was then edited usingFinal Cut Pro 5.1 (Apple Computer) to create five stimuli from eachmale, each of 15min duration. These consisted of an empty cagefor the first 5min, to allow the hen to settle, followed by 5min ofa male standing alone, which provided a baseline measurement forfood searching in the company of a vigilant companion, then 60sof one of the five test sequences, followed by 4min of empty cage.Each successive phase of the test stimuli began and ended with a0.5s fade transition to avoid evoking a startle response. The first10min and the last 4min of every trial were hence identical acrossevery condition. Only the 60 s test sequence differed acrossconditions.

Test sequences were designed systematically to assess thespecificity of female responses to male display movements. Thefive stimuli were Silent tidbitting (normal signal), Matched-frequency motion in the opposite direction, Silent crows, Inactivemale and Empty cage. Decisions about design of the stimuli wereinformed by the results of experiment I, as detailed below.

Silent tidbittingSilent tidbitting consisted of the male performing the full naturaldisplay, including twitches, short bobs and long bobs (Fig.1).

Matched-frequency motion in the opposite directionAnalysis of the tibitting movements (experiment I) revealed that themajority (77%) of the movements during a typical tidbitting display

Initial/final position Midpoint of movement

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Fig. 1. Classification of tidbitting movements. (A) Twitch: side-to-sidehorizontal movement of the head with the neck upright; (B) short bob:vertical movement of the head from a fully upright position, stoppingabruptly when approximately horizontal; and (C) long bob: verticalmovement of the head from upright through a full arc towards the floor.This often includes seizing the food item between the mandibles. The smallwhite object on the floor is a chicken dropping.


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include a rapid downward sweep and return upward of the head andneck. To test whether this characteristic, rapid, vertical movementwas a crucial signal component, independent of temporal pattern, wecreated stimuli with Matched-frequency motion in the oppositedirection. Each of the Silent tidbitting exemplars was used as atemplate; we edited spontaneous crowing of the same male so thateach upward extension of the neck during the crowing motioncorresponded to one of the long, downward sweeping motions in theSilent tidbitting sequence (Fig.2A,B). Matched pairs of completedstimuli contained movement sequences with similar timing andamplitude of displacement in the vertical plane (range 19–22movements) but in opposite directions.

Silent crowsTo assess the role of movement frequency, we created exemplars ofSilent crows, in which the male performed four upward neckextensions with 12s of resting behavior between them; therebycreating a stimulus with a fivefold reduction in the frequency ofmovements compared to the Silent tidbitting and Matched-frequencymotion stimuli. Crowing was chosen as the motor pattern for thesetwo stimuli because it has a similar duration and distance ofdisplacement to the long bob motor pattern in tidbitting. It is also anatural motion performed spontaneously by males. Unlike the acousticcomponent of crowing, which has a well-established territorialfunction (Miller, 1978), there is no evidence that the accompanyingmovement has specific social salience in the absence of vocalizations.

Inactive maleTo test the effect of an alert companion, we created the Inactivemale playbacks, in which the male maintained a stationary alertposture, with occasional spontaneous side-to-side head movements,appearing to scan horizontally around the cage, but without anyvertical displacement of the head.

Empty cageThe Empty cage video was identical to the other stimuli in everyrespect, except that the male was absent. We standardized the five

test sequences for several parameters that seemed likely to influencehen responses. To prevent potential interactions between food callsand the motor patterns, which were the focus of the study, allplaybacks were silent. Mealworms appeared and remained on thevideo screen during all five 60s test sequences to control for thepresence of a preferred food item. Finally, to reduce the possibilityof social facilitation of food search caused by observation of afeeding companion (Zajonc, 1965; McQuoid and Galef, 1993), themales were not shown consuming the mealworms. Results fromexperiment I revealed no obligatory transitions between the threemotor patterns (Fig.3), suggesting that temporal sequence is unlikelyto be an important aspect of display structure; hence we did notmanipulate transition patterns in experiment II.

Test procedureHens were individually placed in the test cage for four 15minperiods, at intervals of 48h, to acclimate them to the apparatus andsound chamber. At the start of each session, the wire door was closedand the hen was confined to the end section of the cage, preventingher from approaching the plasma display. During each session thewire door was remotely released once and the empty cage video,without mealworms, played on the plasma screen. By the fourthacclimation session, all hens readily emerged and walked the lengthof the cage after the door opened and none exhibited signs ofdisturbance such as wing-flapping or crouching.

We used a within-subjects design in which each hen was firstassigned one of the four male exemplars and then a unique randomsequence of the five treatments (test sequences). To ensure that thevideo male was unfamiliar to the hen, we applied the constraint thatshe should have had no social contact with the real male for at leastsix months prior to the experiment. Hens were tested at the sametime of day to minimize diel variation in behavior. The inter-trialinterval was 48h. Each trial began with the hen behind the closedwire door in the section of the cage farthest from the plasma screen.This standardized the hen’s minimum distance from the video maleat the beginning of the 60s stimulus. For the first 10min, the doorremained closed while the empty cage and then the male video


A

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Crow

Fig. 2. Images of Silent tidbitting (A) and Matched motion (B) stimuli. Each long bob in the Silent tidbitting exemplar was paired with a crow by the samemale in the Matched motion exemplar.



played. The test sequence (i.e. one of the four movement types orEmpty cage control) then began and the remote control door wasopened, allowing the hen to approach the video male.

We monitored the tests using a CCD camera (Panasonic WV-CL320) connected to a Sony color monitor (Sony PVM-1450QM).The video output was converted into MPEG-2 format using a Miglia-EvolutionTV and saved for later analysis. Behaviors of interest werescored using JWatcher Video 1.0 (Blumstein et al., 2006), whichreads the time-code of the video file to permit single-frameresolution. We measured the duration of food searching, which ischaracterized by distinctive close binocular fixation of the substrate(Evans and Evans, 1999; Evans and Evans, 2007) and two socialresponses: time spent in close proximity to video male, indicatedby approach to within 0.1m of the end of the cage closest to thescreen, and inspection behavior, which was characterized by thehen stretching her neck towards the flat panel monitor at the height

of the male’s head, exactly as hens scrutinize other flock members(Guhl and Ortman, 1953).

There is considerable individual variation among hens in timeallocated to foraging. To increase the sensitivity of our responsemeasure, we used a difference score, adjusting responses to playbackwith a corresponding estimate of the spontaneous level of foodsearching (Evans and Evans, 1999; Evans and Evans, 2007). Thiswas calculated by measuring each hen’s total duration of foodsearching during the 60s test sequence and then subtracting abaseline estimate, which was obtained by averaging two samples:her time spent food searching during the first 60s after the videomale appeared (min6 of 15min trial period) and that during the last60s before the test playback began (min9). This approach alsofurther controlled for day-to-day variation.

Tests for overall treatment effects were conducted with repeatedmeasures ANOVAs (SPSS 15.0.6 for Windows), using maleexemplar as a blocking factor. Exemplar was never significant, soall data were pooled for further analysis. Significant differences werefurther explored using Tukey’s honestly significant difference(HSD) to conduct multiple pair-wise comparisons; this maintainedthe overall alpha level at the nominated value of 0.05.

RESULTSExperiment I

We analyzed the average frequency of each motor pattern in thetidbitting display and the transition probabilities between them(Fig.3). ‘Short bob’ and ‘long bob’ combined accounted for themajority of the movements (40% and 37%, respectively). Althoughthe individual motor patterns appear stereotyped and are readilydistinguishable, the sequences are relatively unconstrained. Overthe course of the display, males switched continually between thethree motor patterns. Transitions between ‘twitch’ and ‘short bob’were common and a ‘short bob’ was most frequently followed bya ‘long bob’ (Fig.3). Transitions between ‘long bob’ and ‘twitch’were less frequent.

Experiment IIFood search duration

Analysis of food searching duration, adjusted for baseline rate,revealed that Silent tidbitting playbacks evoked a significantly higherresponse than any of the other test sequences (Fig.4). Responses toInactive male, Silent crows and Matched motion in the opposite

Motor pattern key:

Twitch:

Short bob:

Long bob:

Fig. 3. Kinematic plot of motor pattern frequency and transition probabilitiesduring tidbitting display. Diameter of circles is proportional to the frequencyof occurrence of each motor pattern (twitch: 23%; short bob: 40%; longbob: 37%). Width of connecting bars is proportional to frequency oftransitions between the motor patterns. Bars of same shading add to 100%of transitions. Specific transition frequencies were as follows: twitch to shortbob (78.8%), to long bob (21.2%); short bob to twitch (63%), to long bob(37%); and long bob to twitch (15%), to short bob (85%).

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Fig. 4. Food search duration. Time spent food searching during 60 splaybacks (values are means ± s.e.m.). Scores adjusted forindividual baseline level (see text for details). Different lettersindicate significant differences (P<0.05) as determined by repeated-measures ANOVA, followed by post-hoc Tukey’s HSD. Inset showscharacteristic binocular close inspection of substrate during foodsearch.


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direction did not differ significantly from one another, despiteconsiderable variation in the frequency of movement depicted inthese three stimulus types. In addition, Silent crows and Matchedmotion were not significantly different from Empty cage (F4,88=9.61,P<0.0001; Tukey’s HSD, P<0.05).

Proximity to video maleWe measured approach to the video male by scoring the time eachhen spent within 0.1m of the end of the cage closest to the plasmascreen. Mauchly’s test of sphericity was significant (P<0.05), sowe applied a Huynh-Feldt correction (ε=0.85). The overall treatment(stimulus type) effect was highly significant (F3,75=7.52, P<0.001).Post-hoc tests revealed that hens spent significantly more time closeto the simulated male in the Silent tidbitting playbacks than in anyother treatment. There were no significant differences among theother four stimuli (Tukey’s HSD, P<0.05; Fig.5).

InspectionAs a complementary measure of social response, we measured theamount of time hens spent in inspection behavior (Fig.6). Mauchly’s

test of sphericity was significant (P<0.05), so we applied a Huynh-Feldt correction (ε=0.78). The overall treatment effect was highlysignificant (F3,68=40.04, P<0.001). Post-hoc tests revealed thatfemales spent significantly more time inspecting the male on theplasma screen during the Silent tidbitting sequences than in any ofthe other playbacks. None of the other treatments were significantlydifferent from one another (Tukey’s HSD, P<0.05).

DISCUSSIONStructure of the tidbitting display

The visual component of the tidbitting display is made up of threedistinct motor patterns: twitch, short bob and long bob (Fig.1).Displays are primarily composed of the short bob and long bob motorpatterns, with relatively fewer twitches (Fig.3). Over the course ofthe displays, the males continuously transitioned between the threemotor patterns. These motor pattern sequences are highly variable,with no indication of temporal stereotypy (Fig.3), suggesting thatnone of them has evolved specifically to have an alerting function(i.e. design for particular efficacy in engaging a visual grasp reflex),as in some other dynamic visual signals (Peters and Evans, 2003).

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Fig. 5. Close approach to video male. Time spent within 0.1 mof the video male during 60 s test stimulus (values are means± s.e.m.). Different letters indicate significant difference(P<0.05) as determined by repeated-measures ANOVA,followed by post-hoc Tukey’s HSD. Inset shows hen standingin region closest to plasma screen (white line added forillustration).

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Fig. 6. Inspection of video male. Time hens engaged in binocularfixation directed toward the video male during 60 s test stimulus(values are means ± s.e.m.). Different letters indicate significantdifference (P<0.05) as determined by repeated-measuresANOVA, followed by post-hoc Tukey’s HSD. Inset shows heninspecting video male.



One possible explanation for this may be that the displays containfar more motion in the vertical plane than in the horizontal. Suchsignal design should generate a large sweep area in the visual fieldof potential receivers that is robust to variation in angle of view andtherefore should be consistently conspicuous (Marr, 1982; Peterset al., 2002; Peters and Evans, 2007). A second possibility is thatthe visual display is typically accompanied by food calls, which areeasy to localize and audible over a considerable distance (Stokesand Williams, 1971), thereby relaxing selection for a specializedinitial movement. A third possibility is that the wattles, which moveconsiderably, swinging from side to side, during each type of motorpattern and produce a large proportion of the apparent motion duringthe display (C.L.S., unpublished), may so enhance detectability thatno constraint on movement sequence is necessary. Plannedexperiments will test these predictions.

Referential signalingWe tested whether the food search response evoked by visualtidbitting is specifically dependent on the spatiotemporalcharacteristics of the display, including frequency and direction. Inits most restrictive form, this hypothesis requires that hens respondsignificantly more to a silently tidbitting male than to any othermotion type. Comparisons of food-searching duration revealprecisely the predicted pattern of responses (Fig.4). It is particularlystriking that Matched control movements at the same frequency astidbitting, but in the opposite direction, were much less effective(Fig.4). This implies that the downward direction of motion is animportant component of the signal.

This experiment also demonstrates that the hens’ increased foodsearching is not simply a consequence of a decrease in vigilancecaused by the presence of an alert companion (Artiss and Martin,1995). Although the difference between the Inactive male and Emptycage is consistent with such an effect, the fourfold increase in foodsearching to the Silent tidbitting display over that recorded with theInactive male reveals an additional response specific to the tidbittingsignal (Fig.4). We conclude the food searching response to a silentlytidbitting male is not caused by a change in the foraging/vigilancetradeoff (Artiss and Martin, 1995). In addition, the increase in foodsearching response to Silent tidbitting cannot be attributed to socialfacilitation (Zajonc, 1965; McQuoid and Galef, 1993) because theplayback male was shown signaling, rather than searching thesubstrate. We conclude that the tidbitting display is sufficient toevoke foraging behavior and that responses to these movements havespecificity similar to that previously demonstrated for food calls(Evans and Evans, 1999).

Tidbitting movements. therefore have all the characteristics of afunctionally referential visual signal. When combined with foodcalling, as in the majority of displays, this constitutes the firstexperimental demonstration of multimodal referential signaling ina non-human vertebrate.

Social responsesFor males, achieving close proximity to a hen is an important factorin mating success (Graves et al., 1985). The playback experimentreveals that tidbitting can play an important role: hens spent moretime standing close to the silent tidbitting male than they did duringany other treatment (Fig.5). This visual display was uniquelyeffective, both relative to other movements and in absolute terms;none of the other video male stimulus evoked significantly moreclose approach than the Empty cage control sequence. Hens,therefore, responded very specifically to the visual display, and notsimply to rapid motion or to the presence of a simulated companion.

It has been suggested that one of the functions of the food callingmight be to lure the intended receiver close to the signaler (Stokesand Williams, 1971) and many descriptions of multimodal tidbittinghave noted that the hen typically approaches the calling male (Colliasand Collias, 1996; Stokes and Williams, 1971; Wood-Gush, 1954).Our experimental results confirm that the visual display alone issufficient to evoke this social response.

Tidbitting may also improve memorability of both the signal andsignaler, an important aspect of visual signal design (Guilford andDawkins, 1991) that has primarily been explored in the context ofaposematic coloration (Halpin et al., 2008). Hens spentapproximately four times longer inspecting the silent tidbitting malethan any of the other male stimuli, none of which differed fromEmpty cage (Fig.6). Close inspection, as indicated by the henbinocularly fixating on the video male’s head, is hence uniquelytriggered by tidbitting. Previous research (Dawkins, 1995; Dawkins,1996; Hodos, 1993) has implicated binocular fixation with the frontalfield as a critical process in conspecific recognition and hasestablished that hens use the area around the eye to identify flockmates (Dawkins, 1996). Hens prefer males that tidbit more (Pizzari,2003; Zuk et al., 1993), so it seems likely that the inspection of themale’s head evoked by tidbitting may facilitate formation of anassociation between the appearance of a particular male andprovisioning with food. Mating does not usually occur immediatelyafter tidbitting (Stokes and Williams, 1971), so females must retainsome memory of individual male tidbitting performance forpreference subsequently to be expressed.

Although the visual and acoustic components of this multimodaldisplay are redundant (sensu Partan and Marler, 1999), with regardto predicting food availability (Smith and Evans, 2008), the visualdisplay has a synergistic effect on social responses that the soundsdo not (Evans and Evans, 1999), increasing the time spent in closeproximity and inspecting the male. This contrast presents a challengefor theoretical models of multimodal signaling, since categorizationwill be sensitive to the function(s) of interest.

Unimodal production of the tidbitting signal: functionalimplications

Short-term changes in signal structure can reduce potential costs (Ryanet al., 1982). Conspicuous signals attract predators (Bayly and Evans,2003; Roberts et al., 2007), parasites (Bernal et al., 2006) andcompetitors (Stokes and Williams, 1971). In fowl, dominant malesobtain the majority of matings (Pizzari, 2003) and are aggressivetowards subordinate males that tidbit, often displacing them and takingthe food item (Stokes and Williams, 1971). However, Johnsen et al.(Johnsen et al., 2001) observed that subordinate males were able totidbit as frequently as alphas when the subordinate male could displayout of sight of the alpha. In flocks living under naturalistic conditions,we have observed that subordinate males tidbit without perceptiblefood calling. This behavior created additional mating opportunitiesby attracting nearby hens, which approached and food searched nearhim (C.L.S., unpublished). If the silent tidbitting signal is lessconspicuous than the multimodal display, then this behavior mayreflect a tradeoff by subordinates between the benefit of attractingfemales and the social cost of increased conspicuousness to adominant male. Planned studies will test the conspicuousness ofunimodal and multimodal signals and the frequency of theiroccurrence as a function of social context.

These experiments comply with the ‘Principles of animal care’, publication No. 86-23, revised 1985, of the National Institute of Health, and the Australian Code ofPractice for the Care and Use of Animals for Scientific Purposes (NHMRC, 1997).We thank R. Miller and C. Jude for bird care, and R. Marshall for veterinary


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support. We also thank A. Taylor for assistance with the statistical analysis. Thisresearch was supported by a grant to C.S.E. from the Australian ResearchCouncil.

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