Applied Animal Behaviour Science 69 Ž2000. 265–273
www.elsevier.comrlocaterapplanim
The vocal expression of feeding motivation and
frustration in the domestic laying hen,
Gallus gallus domesticus
Patrick H. Zimmerman a,) , Paul Koene a , Jan A.R.A.M. van Hooff
a
b
b
Ethology Group, Wageningen UniÕersity, P.O. Box 338, 6700 AH, Wageningen, Netherlands
Project Group, Ethology and Socio-ecology, P.O. Box 80086, 3508 TB Utrecht, Netherlands
Accepted 14 April 2000
Abstract
Thwarting of feeding behaviour in the laying hen results in an increase in stereotyped pacing,
displacement preening, and the gakel-call. These behaviours therefore reflect the frustration
arousal caused by the thwarting of feeding behaviour. This raises the question whether the level of
frustration also varies with the intensity of the motivation to perform the thwarted behaviour. This
study investigated the relationship between the intensity of the motivation and level of frustration
on the one hand and the gakel-call on the other hand. In Experiment 1, the strength of the
motivation to feed was varied by thwarting hens in their feeding behaviour in an operant
procedure after different durations of food deprivation Ž0, 8, 23 and 47 h.. Trend analysis showed
that with increasing hunger state, an increasing number of gakel-calls was given. No effect of
treatments on temporal characteristics of the gakel-call was found. In Experiment 2, the level of
frustration was varied by reducing or increasing the duration of access to food for food-deprived
hens compared to the duration of access during training. It was assumed that a shorter duration of
access to food compared to training would elicit frustration, which in turn would affect the
performance of behaviours indicative of thwarting. However, we found neither a relation between
the number of gakel-calls nor the temporal features of the gakel-call and the duration of access to
food. Possibly, the differences between treatments were not large enough to induce differences in
frustration level. Also, other factors that might have influenced the motivation are discussed.
q 2000 Elsevier Science B.V. All rights reserved.
Keywords: Chicken welfare; Motivation; Frustration; Feeding; Vocalisation
)
Corresponding author. Tel.: q31-317-483926; fax: q31-317-485006.
E-mail address: patrick.zimmerman@etho.vh.wau.nl ŽP.H. Zimmerman..
0168-1591r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 8 - 1 5 9 1 Ž 0 0 . 0 0 1 3 6 - 2
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P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 265–273
1. Introduction
In laying hens, it has been found that thwarting of feeding behaviour is expressed
through a specific vocalisation, the gakel-call ŽZimmerman and Koene, 1998.. A
gakel-call typically consists of a whining, elongated note, followed by a variable number
of short notes. Thwarting of feeding behaviour is also known to elicit escape behaviours,
an indication of the aversiveness of the situation, and subsequent stereotyped pacing
ŽDuncan and Wood-Gush, 1972a,b.. It is, however, not known whether the intensity of
thwarting and the strength of the thwarted motivation to feed are reflected in the number
of gakel-calls and temporal characteristics of this call.
The first aim of this study is to investigate whether a change in motivation to feed,
induced by different durations of food deprivation, affects the gakel-call which is given
in response to the thwarting of feeding behaviour.
Besides deprivation, the incentive value of a reward is another determinant of
motivation. According to Amsel Ž1992. frustration is ‘‘an aversive state that results from
non-reward, reduced reward or delayed reward in the presence of a history of reward’’.
This aversive state might affect the behaviours reflecting the frustration arousal resulting
from the thwarting of feeding behaviour. In this way, the level of frustration might be
reflected in the number of gakel-calls and other temporal characteristics of this call. So,
a second experiment was done to examine the relation between frustration and the
gakel-call.
In conclusion, we investigated the following research questions: is an increasing
duration of deprivation as a measure of increasing motivation to feed reflected in an
increasing number of gakel-calls during thwarting of feeding behaviour? Does an
increased motivation to feed result in a change in mean length and number of elements
per gakel-call? Furthermore, is an increasing intensity of frustration expressed in a
higher number of gakel-calls and a change in mean length and number of elements per
gakel-call?
2. Experiment 1
2.1. Materials and methods
2.1.1. Animals and apparatus
Sixteen non-naive hens, eight Brown Warrens and eight White Leghorn, from a
previous experiment ŽZimmerman and Koene, 1998. were used. In this earlier experiment, the hens had been conditioned in a classical and operant procedure and after that,
had been subjected to both a control and extinction session in a food context. In the
present experiment, the hens were housed individually in cages Ž139 = 50 = 50 cm.
containing a nest and a dust box. Food Žcommercial poultry mash. and water were
available ad libitum outside the experimental treatments. The light period fell between
4:00 AM and 8:00 PM.
A Skinnerbox was located in a sound-attenuated room next to the room where the
hens were housed. This Skinnerbox was operated through a personal computer standing
in the same room.
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 265–273
267
2.1.2. Experimental procedure
All hens were habituated to the Skinnerbox and the experimental environment during
a total of 45 min on 3 consecutive days. Next, the hens were deprived of food for
approximately 8 h and subjected to a number of sessions in which the instrumental
response of key pecking was shaped. After the shaping sessions, the hens were deprived
of food for 23 h and subjected to a series of 15-min conditioning sessions. In such a
session, a trial started with an interval of 35 " 10 s, then a light was lit for 10 s during
which a hen could peck a key to make a food magazine come within reach and eat for 5
s. A training session consisted of approximately 20 trials. All hens were subjected to one
training session a day. A hen was considered to be trained sufficiently when she pecked
the key and fed in all trials during three consecutive sessions.
After training, the 16 hens were subdivided in four groups and all hens in each group
were subjected to an extinction session after the following durations of food deprivation:
0 Žtreatment Dep0., 8 ŽDep8., 23 ŽDep23. and 47 ŽDep47. h. The treatments were
assigned to the groups in a balanced way. In an extinction session, the food magazine
was presented with a Plexiglas cover. Thus, the hens were thwarted in their feeding
behaviour. For every hen, one extinction session was run per day. Between extinction
sessions, hens were subjected to a training session in which they received a food reward
in each trial to prevent a carry-over effect of one treatment on the subsequent on. The
training and extinction sessions were carried out in the afternoon after the hens had laid
their egg.
During the extinction sessions, vocalisations were recorded on videotape using an
external microphone ŽBandridge BMC 660. and a videorecorder ŽPanasonic AG-6200..
From the videotape, the gakel-calls were digitised with the Signal w software program
ŽEngineering Design, 1992.. From those recorded gakel-calls that contained no
background noise the mean duration, the mean number of notes and the mean length of
the first four notes were determined with the Signal w software program.
2.1.3. Statistical analysis
A repeated measurements analysis was used in the GLM-procedure in the SAS w
statistical programme ŽSAS Institute, 1989. with strain, group, and treatment as factors.
A square-root transformation on the number of gakel-calls was used to reach normality.
A polynomial contrast was made to take into account the quantitative values of the
treatments of deprivation. Furthermore, a trend analysis was done to test whether a
linear or quadratic relation existed between the duration of deprivation and the number
of gakel-calls.
The effect of strain, group, and treatment on mean duration and number of notes per
gakel-call were determined in a repeated measures analysis in SAS.
3. Results
No effect of strain or group on the number of gakel-calls was found. There was a
significant effect of duration of deprivation Ž F1,14 s 12.21, P - 0.001. on the number of
gakel-calls. In treatment Dep47, the hens gave significantly more gakel-calls than in
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Fig. 1. Mean number of gakel-calls Žmean"SEM. in the treatments Dep0, Dep8, Dep23 and Dep47. Different
letters indicate significant differences between treatments below the 0.05 level.
treatments Dep8 Ž P - 0.05. and Dep0 Ž P - 0.001. ŽFig. 1.. Trend analysis revealed a
significant positive relationship between the duration of food deprivation and the
number of gakel-calls; this concerned both the linear Ž F1,14 s 26.31, P - 0.001. and
quadratic component Ž F1,14 s 6.13, P - 0.05..
A significant effect of treatment Ž F3,11 s 3.09, P - 0.05; Fig. 2a. on the mean
duration of a gakel-call was found. It was not possible to carryout trend analysis for the
mean duration per gakel-call, because of the small number of hens Ž N s 11. that
produced gakel-calls of sufficient sound quality. A post-hoc test showed that in
treatment Dep0, the mean duration per gakel-call was significantly longer than in
treatment Dep47. A significant effect of treatment Ž F3,11 s 3.34, P - 0.05; Fig. 2b. was
also found on the mean number of notes per gakel-call. A post-hoc test showed that the
gakel-calls in treatment Dep23 consisted of more notes than in treatment Dep0.
No significant correlation ŽSpearman rank correlation. was found between mean
length and number of notes per gakel-call.
4. Experiment 2
4.1. Materials and methods
4.1.1. Animals and apparatus
For this experiment, 20 naive ISA Brown hens of 22 weeks of age were used. They
were housed individually in the same cages as the hens in Experiment 1. When not
stated otherwise, food mash and water were available ad libitum. The light period fell
between 4:00 AM and 8:00 PM.
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 265–273
269
Fig. 2. Mean duration per gakel-call wŽa.; mean"SEMx and the mean number of notes per gakel-call Žb. in the
treatments Dep0, Dep8, Dep23 and Dep47. Different letters indicate statistically significant differences
between treatments below the 0.05 level.
4.1.2. Experimental procedure
All hens were subjected to the same schedule of habituation and training as the hens
in Experiment 1 with the following exception that in Experiment 2, the hens were
allowed access to a 10-s food reward unlike the 5-s food reward provided in Experiment
1.
After training, the hens were subdivided in four groups. Two hens were left out of the
test because they failed to acquire the operant task. All hens of each group were
subjected to four conditioning sessions, which differed in the duration of access to food:
0 ŽFood0., 3 ŽFood3., 10 ŽFood10. and 30 s ŽFood30.. The order in which the hens were
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P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 265–273
subjected to the four sessions differed between groups. In the Food0 treatment, the food
magazine came within reach for 10 s but was covered with Plexiglas. The assumption
was that treatments Food0 and Food3 would induce frustration, because of the reduction
in reward ŽAmsel, 1992., whereas treatment Food10 would create no frustration
compared to the training. Treatment Food30 was assumed to be a bonus.
The hens were subjected to one test session each day. Test sessions were carried out
after 2:00 PM after all hens had laid their egg. Between test days, hens were subjected to
a training session to prevent an effect of a treatment on the subsequent one.
Vocalisations were recorded on videotape. Gakel-calls were digitised with the
Signal w software programme ŽEngineering Design, 1992.. Again, from those recorded
gakel-calls of good sound quality, the mean duration and mean number of elements per
gakel-call were calculated.
4.1.3. Statistical analysis
For each bird, the mean number of gakel-calls per intertrial interval was calculated in
order to correct the mean number of gakel-calls for the different number of trials in the
different treatments. Since the test session in all treatments had the same duration and
the same intertrial interval and because the duration of the food rewards differed
between treatments, this meant that the mean number of trials also differed between
treatments.
The procedure used in the Food0 treatment unintentionally introduced an inequality
with the other frustration treatment Food3. The mean length of intertrial intervals in both
Food0 and Food3 treatment was the same. However, by presenting a covered feeder
during 10 s in treatment Food0 the intertrial period, in which the food magazine was
inaccessible, was actually extended for 10 s compared to treatment Food3. It was
Fig. 3. Mean number of intertrial gakel-calls Žmean"SEM. in the treatments Food0, Food3, Food10 and
Food30. Different letters indicate significant differences between treatments below the 0.05 level.
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 265–273
271
Table 1
Mean duration and mean number of notes per gakel-call Žmean"SEM. in the treatments Food0, Food3,
Food10 and Food30
Mean duration Žms.
Mean number of notes
Food0
Food3
Food10
Food30
849"71
1.3"0.1
939"64
1.4"0.1
1020"96
1.4"0.1
848"45
1.4"0.1
decided then to compare treatment Food0 with Food10 and, concerning the varying
motivation to feed, make the comparison between treatments Food3, Food10, and
Food30.
A repeated measurements analysis was used in the GLM-procedure in the SAS w
ŽSAS Institute, 1989. statistical programme with group and treatments Food0, Food3,
Food10 and Food30 as factors. Polynomial contrasts were made to take into account the
quantitative values of the food rewards. Trend analysis was carried out to investigate the
nature of the relation between intensity of frustration and number of gakel-calls.
5. Results
No significant differences between groups concerning the number of gakel-calls were
found Ž F1,14 s 1.37, P s 0.29.. When testing the number of gakel-calls in the treatments
with the similar procedures ŽFood0 and Food10. a significant difference was found
Ž F1,14 s 8.40, P - 0.05.. On average, more gakel-calls were given between trials in
treatment Food0 Žmean " SEM:1.02 " 0.1. than in treatment Food10 Ž0.73 " 0.1..
Repeated measurements analysis revealed no statistically significant differences in the
mean number of intertrial gakel-calls between treatments Food3 Ž0.78 " 0.1., Food10
Ž0.73 " 0.1., and Food30 Ž0.89 " 0.2.. A trend analysis revealed no significant relation
between these treatments and number of gakel-calls ŽFig. 3..
No statistically significant effects of group or treatment were found on either mean
duration or number of elements per gakel-call ŽTable 1.. No statistically significant
correlation ŽSpearman. existed between the mean length and number of notes per
gakel-call.
6. General discussion
The results from Experiment 1 indicate that a higher motivation to feed, induced by a
longer time of deprivation, is expressed in a higher number of gakel-calls. However,
unintentionally, an inequality between treatments might have been introduced which
could have affected the number of gakel-calls. The hens were trained on a 23-h
deprivation schedule. In treatment Dep47, the hens were put in a Skinnerbox 24 h later
than during training. The resulting frustration, caused by the delayed reward ŽAmsel,
1992., might have influenced the number of gakel-calls given in response to the
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P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 265–273
thwarting of feeding behaviour. So, in treatment Dep47, the motivation to feed might
have been affected not only by deprivation, but also by frustration induced by delayed
reward.
The relation between the intensity of frustration and the number of gakel-calls was
examined in Experiment 2. Intensity of frustration was varied by reducing or increasing
the duration of access to the food reward compared to training. A higher number of
gakel-calls was recorded when the hens had no access to food compared to 10-s access
to food. So, non-reward in a situation that previously had been rewarded resulted
in a higher number of gakel-calls, as has been found before ŽSchenk et al., 1983;
Zimmerman and Koene, 1998..
We assumed that the intensity of frustration decreased from treatment Food0, Food3,
Food10 to Food30 and that intensity of frustration was related to the expression of the
thwarting response. So, we expected the hens to give the highest number of gakel-calls
in treatment Food0 and to show a linear decrease from Food10 to Food30. We expected
treatment Food30 to produce the lowest number of gakel-calls. However, such linear
relationship between treatment and the number of gakel-calls was not found. A possible
explanation might be that the differences in the intensity of frustration in this experiment
were too small to influence the number of gakel-calls. An alternative explanation for the
lack of a difference in the number of gakel-calls between treatments Food3, Food10, and
Food30 is the phenomenon of positive feedback of feeding ŽWiepkema, 1971.. This
positive feedback of feeding, in the initial phase of a feeding bout, on the motivation to
feed may have counteracted the effect of frustration; in the longer food-access treatments, this effect might have been stronger. However, we can probably reject this
interpretation because positive feedback of feeding has never been found in the domestic
hen, at least not in chicks ŽClifton, 1979..
7. General conclusion
A higher motivation to feed, induced by a longer duration of deprivation, is expressed
in a higher number of gakel-calls in laying hens. A change in the intensity of frustration
was not found to be expressed in the number of gakel-calls. Experiments on the vocal
expression of feeding motivation in laying hens should take into account the possible
frustrative effect of food deprivation. The phenomenon of positive feedback of feeding
is also something that should be taken into account when studying the vocal expression
of frustration in adult laying hens.
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