ANIMAL BEHAVIOUR, 1999, 58, 307–319
Article No. anbe.1999.1143, available online at http://www.idealibrary.com on
Chicken food calls are functionally referential
CHRISTOPHER S. EVANS & LINDA EVANS
Animal Behaviour Laboratory, Department of Psychology, Macquarie University
(Received 16 June 1998; initial acceptance 10 September 1998;
final acceptance 5 April 1999; MS. number: 5920)
Male chickens, Gallus gallus domesticus, usually produce characteristic ‘food’ calls upon discovering edible
objects, and are more likely to do so in the presence of a hen. Food calling is thus dependent upon food
and modulated by social context, which is consistent with the idea that hens respond because they
anticipate a feeding opportunity. An alternative model suggests that female behaviour is not mediated by
the predicted presence of food but rather by social information, such as a low probability of male
aggression. We conducted two playback experiments to explore the type of information encoded in
food-associated vocal signals. Isolated hens were played recorded food calls and we compared their
responses with those evoked by ground alarm calls (which have similar acoustic characteristics) and by
contact calls (which are produced under similar social circumstances). Hens responded to food call
playbacks by fixating downwards with the frontal binocular field. This anticipatory feeding movement
was specific to food calls and did not occur in either of the control conditions. Food calls also affected
looking downwards selectively. There were no differences between the call types in their effects on social
behaviour, such as approach and contact calling, nor were there differences in the nonspecific effects of
sound playback, such as orienting towards the loudspeaker or increased locomotor activity. Chicken food
calls appear to provide conspecifics with information about the presence of food. This property has not
hitherto been demonstrated in any natural system of animal acoustic signals.

Food-associated vocalizations have also been of interest
for research addressing proximate questions, especially
efforts to understand the meaning of animal signals.
Some food calls may have properties like those of the
highly specific alarm calls described in birds (Evans et al.
1993a) and monkeys (Seyfarth et al. 1980; Macedonia
1990) and may provide information sufficient to evoke
anticipatory feeding behaviour from conspecifics. If so,
such food calls would be ‘functionally referential’ (Marler
et al. 1992; Evans 1997; Hauser 1997).
An alternative possibility is suggested by the role of
social factors in controlling the production of food calls.
For example, in house sparrows, Passer domesticus, the
rate of ‘chirrup’ calls is maximal when food is discovered
by an isolated individual and falls as group size increases
(Elgar 1986). Similarly, nonterritorial ravens, Corvus
corax, produce ‘yells’ only once a threshold number of
other birds are present (Heinrich 1988). Social effects of
this kind complicate substantially attempts to understand
call meaning. In at least some systems, it seems likely that
calls given after the discovery of food encode information
not about feeding opportunities, but rather about
attributes of the sender such as social status (Clark &
Wrangham 1994) or subsequent behaviour (Boinski &
Campbell 1996). In such cases, the calls could be considered to have ‘behavioural referents’ (Smith 1977, 1981,
Many animals produce distinctive vocal signals when
they discover food. This behaviour has been described in
several species of primates (e.g. Dittus 1984; Elowson
et al. 1991; Hauser & Marler 1993; Vankrunkelsven et al.
1996) and birds, particularly the galliformes (Williams
et al. 1968; Stokes 1971; Sherry 1977; Marler et al.
1986a, b; Collias 1987; Evans & Marler 1994). In natural
social interactions, companions typically respond to
food-associated calls by approaching rapidly (Dittus 1984;
Marler et al. 1986b; Heinrich 1988), although this is
not invariably true (Boinski & Campbell 1996). It is likely
that recruiting conspecifics benefits callers because of
more effective antipredator vigilance (Elgar 1986) or an
enhanced ability to defend a rich and ephemeral food
source (Heinrich 1988). In other systems, calling males
may attract conspecific females, which are then courted
(Marler et al. 1986a). Observations of this kind suggest
that production of food calls may have important functional consequences, although we are not aware of any
direct measurements of the relationship between food
calling and fitness.
Correspondence: C. S. Evans, Department of Psychology, Macquarie
University, Sydney, NSW 2109, Australia (email: chris@galliform.
bhs.mq.edu.au).
0003–3472/99/080307+13 $30.00/0
1999 The Association for the Study of Animal Behaviour
307

1999 The Association for the Study of Animal Behaviour
308
ANIMAL BEHAVIOUR, 58, 2
1991) but it is clearly not necessary to postulate an
external referent such as food to explain either signal
production or receiver response.
Male chickens produce distinctive pulsatile sounds
when they discover food (Collias & Joos 1953; Konishi
1963; Kruijt 1964; Marler et al. 1986a; Evans &
Marler 1994). Isolated males call at an appreciable rate,
but hens potentiate call production, particularly if they
are unfamiliar, while calling is completely suppressed in
the presence of a rival male (Marler et al. 1986b). Call
rate is positively correlated both with food quality
(Marler et al. 1986a) and with the rate at which males
perform an instrumental task to obtain access to food
(Evans & Marler 1994), suggesting that the temporal
patterning of calls reflects some aspect of a male’s motivational state. Calling males often perform ‘tidbitting’
displays in which fragments of food are picked up and
dropped repeatedly, with highly stereotyped vertical
movements of the head and neck. Hens reliably
approach calling males and take the food item either
from the substrate or directly from between the male’s
mandibles.
Laboratory experiments have shown that production of
food calls is dependent upon the presence of food and
that, although calling is enhanced by the presence of a
hen, it is entirely independent of courtship display (Evans
& Marler 1994). These highly specific production conditions are consistent with the idea that food calls are
functionally referential, but they do not require such an
interpretation because the responses of females could be
mediated by the nonvocal behaviour of males, or even by
visual cues from the food item itself. Recent theoretical
papers on referential signalling have stressed that a compelling argument requires studies of both production
and perception, the latter establishing that information
encoded in the signal is sufficient to evoke appropriate
responses from conspecific receivers, even in the absence
of contextual cues provided by the nonvocal behavioural
correlates of signalling (Macedonia & Evans 1993; Evans
& Marler 1995; Evans 1997). Experimental analyses of the
responses evoked by food calls are relatively rare; most
previous work has concentrated on the circumstances
of call production (Williams et al. 1968; Stokes 1971;
Sherry 1977; Dittus 1984; Marler et al. 1986a, b; Collias
1987; Elowson et al. 1991; Evans & Marler 1994;
Vankrunkelsven et al. 1996). Although playback experiments have shown that food calls are potent stimuli for
attracting conspecifics (Elgar 1986; Heinrich 1988), published accounts do not show that approach involves
anticipatory feeding behaviour. There is consequently no
strong evidence that any of the food-associated vocalizations that have so far been described is functionally
referential.
In the present study we explored further the information content of chicken food calls to determine whether
these signals meet the criteria for functional reference.
We conducted two playback experiments assessing the
responses of isolated hens to recorded food calls and
matched control stimuli, in the absence of any other cues
to the presence of food. In the first experiment, we
presented food calls and ground alarm calls, which are
both short pulsatile sounds that are produced in long
bouts. They are acoustically similar but have very different eliciting conditions (food and terrestrial predators,
respectively). The second experiment compared the
effects of food and contact calls, which are acoustically
distinct, but are produced under similar social circumstances. We wished to conduct a direct test of the suggestion that food calls do not provide information about
feeding opportunities, but rather facilitate the formation
of social aggregations by predicting a low probability of
aggression by the sender (Smith 1991). Contact calls
and food calls are both given during affiliative social
interactions, so if these sounds have only behavioural
referents then we would expect the responses of the hens
to be similar.
We conducted frame-by-frame analyses of test session
video recordings to determine whether the call types
presented had different effects on feeding behaviour.
These data were then compared with analyses of social
responses characteristic of interactions with conspecific
companions, and also with measures of the nonspecific
effects of acoustic stimulation such as orienting and
changes in general activity. Our goal was to determine
whether food calls evoked specific feeding responses, as
would be predicted if these sounds are functionally referential, and to establish whether such responses were (1)
unique to food calls, and (2) separable from the more
general effects of vocal signals given by a simulated
companion.
EXPERIMENT 1
Methods
Subjects
We used 22 adult golden Sebright bantam hens. This
ornamental strain was selected because they have not
been subjected to intense artificial selection for rapid
growth or egg production. Comparisons of call structure
suggest that there are no differences between Sebrights
and red junglefowl, Gallus gallus spadiceus, from which all
domesticated strains have been derived.
Birds were housed indoors in a large (59 m2.45 m
high) room with windows on three sides admitting
natural light. Additional light was provided by overhead
incandescent lamps on a diurnal 12:12 h light:dark
cycle (lights on at 0730 hours). Room temperature
was 22C. Each female was maintained, with a single
male, in a cage measuring 1.01.0 m and 0.53 m high.
All cages were fitted with wooden perches and had
a deep layer of bedding material (shredded paper)
on the floor to facilitate the expression of natural
behaviour such as nest construction and dustbathing.
Food (Gordon Specialty Feeds laying ration, Sydney,
Australia) and water were continuously available.
Birds were given a mineral and vitamin supplement
(Ioford NF; Marshall Speciality Bird Supplies, Sydney,
Australia) twice weekly and chopped fresh vegetables
(lettuce, spinach, corn, potatoes, carrots) or fruit (apple)
every morning.
EVANS & EVANS: CHICKEN FOOD CALLS
Test apparatus
Experiments were conducted in a sound-attenuating
chamber, measuring 2.382.38 m and 2.15 m high
(Amplisilence S.p.a., Robassomero, Italy), which was
lined with 10-cm ‘Sonex’ foam baffles (Illbruck Inc.,
Minneapolis, U.S.A.) on the side walls and 15-cm baffles
on the ceiling to prevent reverberation. Each subject was
confined in a wood-framed wire cage, measuring
1.220.42 m and 0.55 m high, in the centre of the floor.
The cage floor was covered with artificial grass mats to
reduce movement noise and to provide a surface across
which the hens could move comfortably. Opaque black
fabric was hung over the wire at both ends of the cage to
eliminate visual cues to the location of the loudspeaker.
To observe hens continuously during testing, we used a
Panasonic WV-CL320 video camera, which was mounted
at floor level in the chamber perpendicular to the long
axis of the cage, together with a Sony 1450QM colour
monitor. A Panasonic WJ-810 time–date generator was
used to overlay a ‘stopwatch’ display over the bottom of
the video display for timing test sessions. All tests were
videorecorded using a Panasonic AG-7750 VHS-format
deck. Vocalizations produced by hens were recorded with
a Realistic model 33-1070 microphone on one ‘hi-fi’
video soundtrack, while comments by the experimenter
were recorded on the other.
Calls selected for use as playback stimuli were digitized
using the built-in A/D converter in a Macintosh Quadra
840AV computer (44.1 kHz; 16 bits) and edited using
commercial programs (Canary 1.2.1, Cornell Bioacoustics
Laboratory; SoundEdit 16, MacroMedia Inc., San
Francisco, U.S.A.). Digitized sound files were then transferred to an Amiga 4000 computer. Stimuli were played
using AD516 D/A hardware (44.1 kHz; 16 bits) and Studio
16 software (SunRize Industries, Campbell, CA, U.S.A.),
which allowed us to adjust the amplitude of each
stimulus individually and to trigger presentations with a
keypress. This latter feature made it straightforward to
synchronize acoustic stimuli with the timebase displayed
on the video monitor, so that behavioural responses
could be scored ‘blind’ (see below). Sounds were presented using a Nagra DSM loudspeaker/amplifier. Call
amplitude was standardized at 70 dB(A) peak, measured
in the centre of the test cage, using a Realistic model 3050
sound level meter.
Playback stimuli
We obtained recordings of male food calls and ground
alarm calls from an archival collection accumulated from
laboratory experiments conducted over the last decade.
Food calls were originally elicited by delivery of three
45-mg Noyes pigeon pellets to birds that were keypecking
for food reinforcement (Evans & Marler 1994). Ground
alarm calls were evoked by a life-sized moving image of a
racoon, Procyon lotor, presented on a video monitor (Evans
et al. 1993a). Original recordings were made with a
Realistic 33-1070 microphone and either a Sony TC-D5M
cassette tape recorder or a Nagra IV reel-to-reel recorder.
The physical characteristics of chicken vocalizations
vary, probably because of both individual differences
between callers and changes in motivational state (Evans
et al. 1993a; Evans & Marler 1994; Evans 1997). We tried
to incorporate some of this acoustic variability when
selecting the set of playback sounds. We first eliminated
all recordings with a low signal-to-noise ratio. In tests
with predator stimuli, this occurred when the male’s
movement away from the video monitor caused broadband clicks synchronous with ground alarm calls. Similarly, many of the recordings from tests with food
contained loud pecking noises that partially masked the
male’s food calling. The remaining call bouts were then
digitized and examined in detail using fast Fourier transform (FFT)-based spectrograms generated by Canary
1.2.1. Our goal was to identify long uninterrupted trains
of calls that could be assembled to create finished stimuli
with minimal editing. Three males produced continuous
food calls for at least 20 s. We removed other sounds (e.g.
brief contact calling by hens) by substituting a precisely
matched period of background noise, selected from intervals between calls. We used zero-crossing points in the
amplitude–time waveform to define the beginning and
end of these segments to avoid the introduction of
artefacts. Each of the edited food call bouts was then
iterated twice to create a 60-s stimulus (Fig. 1a). Ground
alarm call stimuli were also created by iterating 20-s
samples of calls, which were selected from the period
during which the predator stimulus was visible and calling was most sustained (Fig. 1b). Each of the six stimulus
exemplars was contributed by a different male. We
matched food call and ground alarm call exemplars as
closely as possible for temporal characteristics by pairing
stimuli with similar numbers of total calls. The resulting
stimulus set reproduced natural variation in call rate, but
the mean number of calls in the three stimuli of each type
and the mean call rate were identical (Table 1).
Design and Test Procedure
We used a within-subjects design in which every bird
experienced all stimulus conditions, in separate test sessions. Each of the 22 subject hens was first randomly
assigned one of the three matched pairs of calls, with the
constraint that either seven or eight hens receive each
stimulus set. They were then randomly assigned a stimulus sequence (food call–ground alarm call or ground
alarm call–food call). Hens were subsequently retested,
with different call exemplars, in the reverse order from
their first test. Order effects were thus controlled for both
by randomizing across the whole group of subjects and by
counterbalancing within subject. To avoid side biases, we
alternated loudspeaker position from one end of the cage
to the other, ensuring that each hen heard half of the
playbacks from each location.
Prior to the first test day, we allowed hens to adapt to
the test situation by placing them in the test chamber for
three 15-min intervals, separated by a minimum of 24 h,
without any stimulus presentation.
Tests were begun by placing the hen in the centre of the
test cage. The stimulus sound was presented 15 min later.
Videorecordings were made of a period extending from
2 min prestimulus until 3 min poststimulus. Playback
tests for each hen were separated by a minimum of 24 h.
309
310
ANIMAL BEHAVIOUR, 58, 2
Figure 1. Spectrograms of representative short sections from one pair of stimulus exemplars played back in experiment 1. (a) Food calls; (b)
ground alarm calls. Sampling rate 44.1 kHz, 512 point FFT (frequency resolution 350 Hz), grey scale represents an amplitude range of 40 dB.
Analysis of videorecorded responses
We selected five behavioural measures to characterize
fully the hens’ responses to call playbacks. These were
divided into anticipatory feeding behaviour (close inspection of the substrate), social responses (approach and
contact calling) and nonspecific effects of acoustic stimuli
(changes in locomotor activity and orienting towards the
loudspeaker). All of the analyses were done ‘blind’, that is,
by a rater unaware both of the call type that the hen had
received in a given trial and of the location of the
loudspeaker. We measured behaviour for 60 s prior to the
stimulus playback to obtain baseline rates for each of
the assays, during the playback, and for 60 s after the
playback.
Looking downwards. Our choice of this response
measure was based upon observations of natural foraging behaviour, together with some well-documented
Table 1. Temporal characteristics of calls used as playback stimuli in
experiment 1
Food calls
Exemplar
pair
1
2
3
Mean
Ground alarm calls
Number
of pulses
Rate
(pulses/s)
Number
of pulses
Rate
(pulses/s)
186
228
249
221
3.10
3.80
4.15
3.68
201
207
255
221
3.35
3.45
4.25
3.68
characteristics of the chicken visual system. Chickens
have laterally placed eyes which provide a very large
visual field, but limited binocular vision. In addition,
they have ramped corneas with a varying radius of curvature (Miles 1972) so that the frontal visual field is focused
for short distances and the lateral field for longer distances (Rogers & Andrew 1989; Rogers 1995). Chickens
consequently fixate objects such as approaching companions or predators by turning the head abruptly to one
side and using one eye (Andrew & Dharmaretnam 1993;
Evans et al. 1993a). Frontal fixation tends to be restricted
to contexts in which close inspection is necessary, such as
searching for small food items once a target area has been
selected (Andrew & Dharmaretnam 1993) and the recognition of social companions and artificial visual stimuli
(Dawkins 1995, 1996; Dawkins & Woodington 1997).
Studies of eye use in several species of birds have consistently concluded that close binocular fixation immediately precedes pecking at a food item (e.g. Friedman 1975;
Bischof 1988; Bloch et al. 1988). We went through test
session videotapes frame-by-frame (temporal resolution
40 ms) and measured the total time that each hen spent
looking at the substrate with the binocular field (head
pitched downwards by >45). Visual inspection of this
kind was often accompanied by movements of the head
and neck so as to bring the beak close to the floor (Fig. 2),
and occasionally by pecking. Head movements that
ended with preening behaviour, which was usually
directed towards the feet and legs, were excluded.
Location and activity. To score location and movement of the hen from test session videotapes, we used
EVANS & EVANS: CHICKEN FOOD CALLS
playback loudspeaker in each trial, and converted the raw
scores into time spent close to the loudspeaker (same side)
or away from it (opposite side). We also used the event
recorder software to measure the amount of locomotor
activity occurring in each test. Only movements of the
legs and feet that had the effect of displacing the
whole of the bird’s body were counted; occasional foot
movements that accompanied scratching or preening
were excluded.
Facing the loudspeaker and contact calling. To characterize orientation of the head and vocal behaviour, we
used a 1/0 scoring technique based upon a 15-s sampling
interval (Martin & Bateson 1993). Head position was
measured from still video frames corresponding to the
sample period and categorized as facing left or facing
right; frames in which the hen was facing either
directly towards or directly away from the camera were
assigned to a null category. Isolated hens often produce
contact calls, which can be either soft pulsatile sounds or
long tonal elements (‘singing’; Collias 1987). The temporal pattern of such calls is irregular and they are thus
unlikely to be detected reliably by instantaneous sampling. We measured contact calling by scoring whether
these vocalizations had occurred in the preceding 15-s
interval.
Results
Figure 2. Still images from a test session video recording illustrating
the effects of food call playback. Frame (a) is just prior to stimulus
onset. Frames (b–e) depict the hen’s behaviour during the 60-s
sound presentation. Note the repeated downward movements of
the head and neck, with close inspection of the substrate. Frame (f)
is immediately after the stimulus. In this trial, the loudspeaker was
concealed behind a screen at the right-hand end of the cage.
the Noldus event recorder software (Noldus Inc.,
Wageningen, The Netherlands) running on a PowerMacintosh 7500/100 computer. For purposes of this
analysis, we divided the image of the test cage in half and
simply recorded whether the hen was on the left or the
right side. When hens moved from one side of the cage to
the other, we scored a transition as their heads crossed
the centre line. Once scoring had been completed, we
matched up the event recorder records with our test
protocol, so that we could determine the location of the
Playbacks of both call types evoked a startle-like
response at stimulus onset in almost all cases. Activities
such as feeding or preening were interrupted and birds
tended to orient towards the loudspeaker. After this
initial reaction, the effects of food call and ground alarm
call playback were quite different. Food calls elicited
anticipatory feeding behaviour (looking downwards and
pecking at the substrate), both during the stimulus and in
the poststimulus period, while ground alarm calls did not.
Both types of call evoked social responses such as contact
calling, together with a small increase in locomotor
activity, although birds did not consistently approach the
loudspeaker.
Prior to analysis, we averaged the scores obtained from
each bird in the two tests with each call type. Inspection
of these data revealed that there was considerable individual variation in measures such as looking downwards,
locomotor activity and contact calling. Since we were
principally concerned not with the absolute frequencies
of these behaviours but with changes caused by sound
playback, we calculated difference scores for the stimulus
and poststimulus periods by subtracting each bird’s
average prestimulus score. To ensure that the five
response measures were as comparable as possible, we
transformed all of the data in this way and then performed repeated measures ANOVAs for each assay with
factors for stimulus type (food call or ground alarm call)
and time (stimulus and poststimulus intervals). If a significant treatment effect was obtained, then further comparisons were conducted with paired t tests (Carmer &
Swanson 1973).
311
ANIMAL BEHAVIOUR, 58, 2
12
8
Food calls
Ground alarm calls
8
6
4
2
0
4
0
–4
–8
–12
–16
–2
Prestimulus
Stimulus
–20
Poststimulus
Figure 3. Mean±SE frequency of looking downwards in experiment
1. Scores for the stimulus and poststimulus periods have been
expressed relative to the mean frequency for each bird measured in
the 60-s prestimulus baseline period (dashed line). See text for
details. The prestimulus value has been plotted to facilitate assessment of the rate of change in this measure over successive 60-s
periods. Points displaced slightly for clarity.
Looking downwards
The probability of hens fixating the substrate was
increased markedly during food call playbacks, and this
change persisted into the 60-s poststimulus period (Fig.
3). In contrast, playback of ground alarm calls had almost
no effect on this measure; mean scores were comparable
to those obtained in the prestimulus baseline period (Fig.
3). These differences in the effects of the two call types
were reflected in significant ANOVA main effects for
both stimulus type (F1,21 =11.76, P=0.0025) and time
(F1,21 =5.19, P=0.033), together with a nonsignificant
interaction term (F1,21 =1.85, P=0.189). Subsequent pairwise comparisons revealed that food calls evoked significantly more looking downwards than ground alarm calls
both during the stimulus presentations (t21 =4.09,
P=0.0005) and in the poststimulus period (t21 =2.24,
P=0.036).
Social behaviour
The hens tended to move away from the concealed
loudspeaker during playbacks, regardless of stimulus type.
They continued to do so after food call presentations,
but not after ground alarm calls (Fig. 4a). The main
effect for stimulus type in this analysis approached statistical significance (F1,21 =4.03, P=0.058), but both the
main effect for time and the timestimulus type interaction were clearly nonsignificant (larger F1,21 =1.02,
P=0.323).
Both call types elicited increased contact calling, and
this continued into the poststimulus period (Fig. 4b), but
none of the comparisons in this analysis approached
statistical significance (largest F1,21 =1.27, P=0.272).
1.0
(b)
0.8
Contact calling (samples)
–4
Food calls
Ground alarm calls
(a)
Time spent on speaker side (s)
10
Looking downwards (s)
312
0.6
0.4
0.2
0.0
–0.2
Prestimulus
Stimulus
Poststimulus
Figure 4. Social responses evoked by food calls and ground alarm
calls. (a) Mean±SE time spent on the same side of the test cage as
the loudspeaker. (b) Mean±SE number of 15-s samples in which
contact calling occurred. Scores are expressed relative to prestimulus
baseline rates.
Nonspecific responses
Hens turned to face the loudspeaker more often during
playbacks, although this was a relatively small and transient effect (Fig. 5a). Locomotor activity was increased by
sound playback, and this was more noticeable in food call
trials, both during stimulus presentations and afterwards
(Fig. 5b). There were, however, no significant main effects
or interactions in either of the ANOVAs performed on
these data (largest F1,21 =2.20, P=0.153).
Discussion
Hens responded to playback of food calls with an
increased frequency of looking downwards, often fixating
the substrate closely in the same way as birds searching
for small particles of food (Figs 2, 3). This response was
EVANS & EVANS: CHICKEN FOOD CALLS
1.0
(a)
Food calls
Ground alarm calls
Facing speaker (samples)
0.8
0.6
0.4
0.2
0.0
–0.2
–0.4
8
(b)
Food calls and ground alarm calls share several structural characteristics, but they are produced under very
different circumstances. Food calls are given by males
when they discover food or stimuli that reliably predict
the presence of food, particularly when hens are present
(Marler et al. 1986b; Evans & Marler 1994). In contrast,
ground alarm calls are elicited by approaching terrestrial
predators (Gyger et al. 1987; Evans et al. 1993a) and are
produced at similar rates regardless of social context
(Evans 1997). The call types presented in experiment 1
thus differed both in characteristics of the eliciting
stimuli and in the nonvocal behaviour of senders. Food
calls and ground alarm calls are probably also associated
with quite distinct affective responses, although there
have been no studies of the physiological changes that
accompany call production. Therefore the responses
obtained with playbacks may be mediated not by properties of the physical stimuli that originally elicited the
sounds (food versus predators), but rather by one of the
other correlates of signal production, such as the opportunity for social interaction with the caller (Smith 1991).
Experiment 2 was designed to assess this possibility.
6
EXPERIMENT 2
Movement (s)
4
Our aim in this experiment was to compare the responses
evoked by food calls with those associated with contact
calls, another vocalization that is characteristic of nonaggressive interactions. Individual birds that have been
removed from a social group often produce bouts of
contact calling, and males and females separated by a
wire barrier sometimes exchange calls in an antiphonal
pattern (C. S. Evans, unpublished data). Contact calls are
thus well matched to food calls in behavioural correlates,
although their acoustic properties are quite different.
2
0
–2
–4
–6
Prestimulus
Stimulus
Poststimulus
Figure 5. Nonspecific effects of food calls and ground alarm calls. (a)
Mean±SE number of instantaneous samples in which hens were
oriented towards the loudspeaker. (b) Mean±SE duration of
locomotor activity. Scores are expressed relative to prestimulus
baseline rates.
not evoked by ground alarm calls (Fig. 3), even
though these sounds have similar acoustic characteristics
and were delivered at a matched amplitude level.
The effect of food calls on looking downwards was
specific. Social behaviour such as increased contact calling (Fig. 4b) was evoked by both call types, although
hens did not reliably approach the loudspeaker (Fig. 4a).
Similarly, both call types elicited orienting responses
(Fig. 5a) and increased activity (Fig. 5b). These
comparisons allow us to exclude the possibility that
changes in the probability of looking downwards
were simply part of a suite of responses that would be
evoked by playback of any repeated pulsatile sound,
perhaps as a correlate of increased activity levels,
as has been shown in several species of mammals
(McConnell 1991).
Methods
Subjects
We used 22 adult golden Sebright bantam hens, all of
which had been subjects in the first series of playback
tests. The minimum interval between the last test of
experiment 1 and the first test of experiment 2 was 10
weeks.
Test apparatus
Digitized sounds were played back using the built-in
D/A hardware in a Macintosh Quadra 840AV computer
(44.1 kHz; 16 bits), controlled by DeckII software
(MacroMedia Inc.). Equipment was otherwise identical
with that used in the first series of playback tests.
Playback stimuli
Recordings of contact calls from previous studies were
screened in the same way as the ground alarm calls and
food calls used in experiment 1. Periods of contact calling
are often quite brief and these sounds are characteristically produced at a rather low amplitude. Most recordings
had to be excluded from consideration either because
they contained only very brief bouts of calling or because
313
ANIMAL BEHAVIOUR, 58, 2
8
(a)
6
4
Frequency (kHz)
314
2
0
8
(b)
6
4
2
0
0.5 s
Figure 6. Spectrograms of representative short sections from one pair of stimulus exemplars played back in experiment 2. (a) Food calls;
(b) contact calls. Sampling rate 44.1 kHz, 512 point FFT (frequency resolution 350 Hz), grey scale represents an amplitude range of 40 dB.
the signal-to-noise ratio was substantially lower than
that of food calls. We selected representative contact
call bouts from two males. To ensure that the stimuli
presented would not differ in their degree of novelty,
we also selected two new food call recordings, neither
of which had contributed material for playback in
experiment 1.
We wished to create two matched pairs of stimulus
exemplars. While food calls are relatively consistent in
structure (Fig. 6a), contact calls are quite variable, particularly in pulse duration. Bouts of contact calling often
begin and end with relatively brief elements, with much
longer calls in between (Fig. 6b). It was therefore impractical to match the total number of pulses, as we had in the
previous experiment. We chose instead to equate as
closely as possible the total duration of sound within
stimulus pairs. Bouts of food calling were edited by
isolating trains of calls that had a summed pulse duration
approximating that of contact call bouts. We were careful
to select only naturally occurring trains of calls, placing
all of the edit points during the unusually long intercall
intervals that separate consecutive call bouts. Edited
sounds were then iterated to create 60-s stimuli in the
same way as in experiment 1. Intervals between repetitions of each sound file were adjusted so that all of the
stimuli began and ended at precisely the same point.
The completed stimulus sets reproduced characteristic
differences in temporal pattern between food calls and
contact calls, together with some of the individual variation in call rate, but the total duration of sound in each
of the paired stimuli was similar (Table 2).
Design and test procedure
We used the same within-subjects counterbalanced
design and experimental protocol as in the first series of
tests.
Results
The effects of playback closely paralleled those
obtained in experiment 1. Both types of call elicited
contact calling and orienting towards the loudspeaker,
but only food calls increased the probability of looking
downwards. There was very little change in overall levels
of activity and there was no clear tendency for hens to
approach the loudspeaker. We analysed the data in the
same way as in experiment 1, using the average of the two
scores from each hen for each response measure,
Table 2. Temporal characteristics of calls used as playback stimuli in
experiment 2
Food calls
Exemplar
pair
1
2
Mean
Contact calls
Number
of pulses
Total
duration
(s)
Number
of pulses
Total
duration
(s)
135
216
175.5
13.30
13.55
13.43
42
27
34.5
13.29
13.71
13.50
EVANS & EVANS: CHICKEN FOOD CALLS
12
8
Food calls
Contact calls
8
6
4
2
0
4
0
–4
–8
–12
–16
–2
–4
Food calls
Contact calls
(a)
Time spent on speaker side (s)
Looking downwards (s)
10
Prestimulus
Stimulus
–20
Poststimulus
Figure 7. Mean±SE frequency of looking downwards in experiment
2. Scores are expressed relative to prestimulus baseline rates.
1.0
(b)
Looking downwards
Hens spent more time fixating the substrate during
food call playbacks than in the prestimulus period (Fig. 7)
and the magnitude of this effect was comparable with
that obtained in experiment 1 (compare Figs 7 and 3).
After the food call presentations, the frequency of looking
downwards returned rapidly to baseline levels. Playback
of contact calls had no effect on looking downwards
(Fig. 7). An ANOVA comparing the responses evoked by
the two call types revealed significant main effects
for both stimulus (F1,21 =5.013, P=0.036) and time
(F1,21 =5.00, P=0.036), together with a significant stimulus typetime interaction (F1,21 =10.46, P=0.004). Subsequent pairwise comparisons reveal that food calls evoked
significantly more looking downwards than contact calls
during stimulus presentations (t21 =2.95, P=0.008), but
not in the poststimulus period (t21 =0.91, P=0.373).
Social behaviour
Hens tended to move away from the loudspeaker during playbacks and continued to do so during the poststimulus period for both call types (Fig. 8a). Contact
calling also exceeded baseline levels, in a similar
pattern (Fig. 8b). However, none of the comparisons in
these analyses achieved statistical significance (largest
F1,21 =2.90, P=0.104).
Nonspecific responses
Hens tended to orient towards the loudspeaker during
playbacks, and the effects of food calls and contact calls
were similar (Fig. 9a). There was very little change in
levels of locomotor activity to either call type (Fig. 9b).
Neither of the ANOVAs performed on these data
0.8
Contact calling (samples)
expressed as a difference relative to the prestimulus
baseline period.
0.6
0.4
0.2
0.0
–0.2
Prestimulus
Stimulus
Poststimulus
Figure 8. Social responses evoked by food calls and contact calls.
(a) Mean±SE time spent on the same side of the test cage as
the loudspeaker. (b) Mean±SE number of 15-s samples in which
contact calling occurred. Scores are expressed relative to prestimulus
baseline rates.
produced significant differences (largest F1,21 =1.41,
P=0.249).
Discussion
Hens responded to food calls with increased binocular
fixation of the substrate (Fig. 7). This behaviour was not
evoked by contact calls, although the two stimulus types
otherwise had similar effects on social behaviour (Fig. 8),
orienting and activity (Fig. 9). These results suggest that
food calls affect feeding behaviour specifically and that
the responses of hens were not simply attributable to
the simulated presence of a nonaggressive conspecific
companion.
Although the overall pattern of responsiveness to food
calls resembled closely that obtained in experiment 1,
315
ANIMAL BEHAVIOUR, 58, 2
1.0
(a)
Food calls
Contact calls
Facing speaker (samples)
0.8
0.6
0.4
0.2
0.0
–0.2
and subjects were substantially more experienced in the
second study than in the first. It is, however, straightforward to assess whether there was a reduction in responsiveness to food call playback within an experiment, and
this should provide the most sensitive test for habituation
because the interval between playbacks of a particular
type was relatively short. In experiment 2, the duration
of looking downwards actually increased from trial 1
(mean difference scoreSD= +4.9912.83 s) to trial 2
(+7.2213.31 s), although this change was not statistically significant (t21 =1.163, P=0.258). We suggest that
the apparent difference in the effects of food call presentations between the first and second series of playbacks
is probably attributable to differences in the response
of hens to capture and handling, and also possibly to
increased familiarity with the test situation, rather than
to habituation or extinction.
–0.4
GENERAL DISCUSSION
8
(b)
6
4
Movement (s)
316
2
0
–2
–4
–6
Prestimulus
Stimulus
Poststimulus
Figure 9. Nonspecific effects of food calls and contact calls. (a)
Mean±SE number of instantaneous samples in which hens were
oriented towards the loudspeaker. (b) Mean±SE duration of
locomotor activity. Scores are expressed relative to prestimulus
baseline rates.
differences in looking downwards were apparent only
during the stimulus period (Fig. 7), rather than in both
stimulus and poststimulus periods (Fig. 3). This difference
may reflect habituation to food call playback. Alternatively, changes in responsiveness may reflect the extinction of search behaviour that was not reinforced by the
discovery of food. However, the food call exemplars
presented in experiment 2 were entirely novel, and the
interval between the first and second experiments was
several months, suggesting that habituation would not be
a likely explanation for differences in poststimulus
responses.
Statistical comparisons of the data from experiments 1
and 2 would be difficult to interpret because of the
substantial interval between the two studies. In addition,
the playbacks were conducted at different times of year,
Laboratory studies of the conditions under which male
chickens produce food calls have shown that these
sounds are reliably associated with the discovery of food
(Evans & Marler 1994). Our present results reveal that
food calls are also sufficient to elicit anticipatory feeding
behaviour in conspecific receivers. Hens reliably
increased the rate at which they inspected the substrate,
often moving their heads close to the ground as in
natural foraging behaviour, even though no food was
present.
These responses were highly specific in two ways. First,
increases in looking downwards were evoked by food
calls, but not by either ground alarm calls, which are
closely matched in acoustic characteristics (experiment
1), or by contact calls, which are produced under similar
social circumstances (experiment 2). Second, playback of
food calls affected looking downwards selectively.
Changes in looking downwards were not associated with
increases in social behaviour, such as approach and contact calling. These comparisons show that the effects of
playback are not simply an incidental correlate of social
responses, of the type that might be evoked by vocal
signals from a nonaggressive companion. We are also able
to exclude the possibility that the response to food calls is
part of a broad suite of changes in behaviour, such as
those that might be caused by overall increases in arousal,
because there were no correlated increases in orienting
and locomotor activity.
When considered together with earlier studies of food
call production (Evans & Marler 1994), our results lead us
to conclude that chicken food calls are functionally
referential. We believe that this is the first such demonstration in any natural system of food-associated vocal
signals.
The effects of food call playback cannot readily be
accommodated by the theoretical position that this
vocalization has exclusively behavioural referents (Smith
1991). Such a model implies that food calls affect the
behaviour of conspecific receivers solely by predicting
aspects of the sender’s subsequent behaviour, particularly
a low probability of aggression. If this were so, then we
EVANS & EVANS: CHICKEN FOOD CALLS
would expect the response to food calls to covary with
other aspects of social behaviour such as approach and
contact calling, and we would expect the effects of food
call playback and contact call playback to be similar.
Neither of these predictions was supported.
We do not, however, wish to imply that food calls
might not allow receivers to anticipate the sender’s subsequent behaviour. Rather, we suggest that referential
signals are likely to encode several different kinds of
information, predicting the presence of a particular class
of eliciting stimuli while also revealing aspects of the
sender’s nonvocal response, together with affective
changes synchronous with call production (Evans &
Marler 1995). The challenge for future analyses of signal
structure will be to identify the acoustic vehicles for each
of these ‘messages’, and to determine the degree to which
they are separate (Evans & Marler 1995; Evans 1997). It
will also be important to determine whether there is an
obligatory relationship between information identifying
the class of eliciting stimuli and that which reflects sender
behaviour. For example, it is easy to imagine systems in
which one type of information (e.g. discovery of
food) might be more or less reliable than another (e.g.
preparedness to share the food item).
Playback of food calls was not sufficient to elicit
approach responses from hens (cf. van Kampen 1994).
Indeed, there was a nonsignificant tendency for hens to
withdraw from the vicinity of the playback speaker in
experiment 1. Possibly, this was an avoidance response
evoked by the calls of an unfamiliar male (Wood-Gush
1956; McBride et al. 1969). There is thus a clear contrast
between the effects of presenting the food calls in isolation and the results of earlier experiments describing
the behaviour of hens in the presence of a live foodcalling male (Marler et al. 1986a). Under such circumstances, hens consistently approached the males and took
the food item from them. This difference may simply be
an artefact of the playback arrangements employed. For
example, the cage confining the hen might have been too
small to facilitate expression of an approach response
because a hen in the centre of the floor would have been
relatively close (0.61 m) to the speaker at sound onset.
However, reliable approach responses have been demonstrated with a similar spatial separation between a live
calling male and subject hen (0.90 m; Marler et al. 1986a).
We think it more likely that the approach behaviour of
hens is mediated by visual cues from the male such as the
characteristic tidbitting display, and perhaps by other
aspects of morphology known to be particularly salient to
conspecific females (e.g. Zuk 1991).
There is clearly the potential for visual information to
act synergistically with that encoded in the acoustic
signal to affect female behaviour (Evans 1997). Recent
video playback experiments have shown that chickens
can recognize the feeding movements of conspecifics and
discriminate these from other types of motor activity
(McQuoid & Galef 1993). Similarly, hens are sensitive to
the upright threat posture of a companion when presented on a video display (D’Eath & Dawkins 1996). It
may therefore be possible to explore systematically the
interaction between food calls and the tidbitting display
by means of video playback experiments in which visual
and acoustic information is manipulated independently
(e.g. Evans & Marler 1991). It will also be necessary
to study the nonvocal behaviour of males during
call production because it is currently difficult to
determine whether tidbitting should be categorized as a
contextual cue that potentially modulates the effects
of a vocal signal (e.g. Leger 1993), or whether these
movements should be considered as a visual signal in
their own right.
Studies of antipredator behaviour reveal that chickens
have two qualitatively distinct types of alarm call, one
evoked by terrestrial predators and the other by aerial
predators (Gyger et al. 1987; Evans et al. 1993a). The
stimulus characteristics necessary for eliciting aerial alarm
calls are now understood in some detail (Evans et al.
1993b) and playback experiments show that both types of
signal are sufficient to evoke responses appropriate for
dealing with the type of predator that had originally
elicited them. Chickens thus have at least three functionally referential vocal signals, encoding information about
their two principal classes of predator and about the
discovery of food.
Each of these call types evokes characteristic changes in
the way in which the birds monitor their environment.
Both aerial alarm calls and ground alarm calls increase the
rate of horizontal scanning but aerial alarm calls also
evoke looking upwards, which the birds do by rolling
their head to fixate with the lateral field of one eye. In the
present study, food calls evoked close examination of the
substrate with the frontal binocular field. There is a clear
relationship between these behavioural responses and
characteristics of the chicken visual system. Chickens
have two anatomically separate visual pathways from the
optic nerve to the forebrain. The thalamofugal visual
system sends projections to nuclei in the thalamus and
thence to the hyperstriatum dorsale, whereas the tectofugal visual system consists of projections through the
optic tectum to the nucleus rotundus and then to
the ectostriatum (Shimizu & Karten 1993; Rogers 1995).
The thalamofugal system handles input only from the
lateral visual fields, while the tectofugal system processes
information from both lateral and binocular fields
(Rogers 1996). Aerial alarm calls and food calls thus
engage the chicken visual system in quite distinct ways.
While aerial alarm call playback stimulates search with
the lateral field, involving both pathways, food call playback elicits binocular fixation, involving only the tectofugal pathway. This comparison invites exploration of
the relationships between natural vocal signals and visual
information processing.
Acknowledgments
We thank W. McTegg and N. Lambert for bird care and Dr
R. Marshall for veterinary support. We are also grateful to
Professor L. Rogers and Drs C. D. Blaha, K. C. Cheng and
J. M. Macedonia for commenting on the manuscript. This
research was supported by a grant to C.S.E. from the
Australian Research Council.
317
318
ANIMAL BEHAVIOUR, 58, 2
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