Applied Animal Behaviour Science 90 (2005) 351–364
www.elsevier.com/locate/applanim
The short-term effects of increasing meal frequency
on stereotypic behaviour of stabled horses
Jonathan J. Coopera,*, Natalie Mcalla,
Sharon Johnsona, H.P.B. Davidsonb
a
Department of Biological Sciences, Animal Behaviour, Cognition and Welfare Research Group,
University of Lincoln, Riseholme Park, Riseholme, Lincoln LN2 2LG, UK
b
Equine Studies Group, WALTHAM Centre for Pet Nutrition, Waltham on the Wolds, Leicestershire, UK
Accepted 12 August 2004
Available online 14 October 2004
Abstract
In this study, we investigated the effect of increasing the number of meals of concentrate (whilst
maintaining the same daily intake) on the behaviour of stabled horses with particular reference to
stereotypic activities. The study was carried out on a working equestrian yard with stables for up to 50
horses. A pilot study was used to record incidence of stereotypic behaviour and to select subjects for
the main study. In this, the behaviour of 30 warm-blooded horses was recorded during their morning
(08:30 h) and afternoon (16:30 h) concentrate feeds. Whilst there was a low incidence of stereotypic
behaviour (5.6% of scans) in the population, they were more commonly observed in the afternoon
(7.1%) than the morning observations (4.2%; P < 0.05). The higher incidence in the afternoon
observation appeared to be related to the lower availability of high fibre forage during the afternoon
meal. In the main study nine horses were fed their normal ration of concentrate divided between two,
four or six equally sized meals. Their behaviour was compared with seven control horses, which
received two meals per day throughout the trial. As the number of meals increased, the treatment
horses showed a decrease in oral stereotypies (P < 0.01), but an increase in weaving (P < 0.05) and
nodding (P < 0.01) prior to feeding. The control group increased weaving, nodding and oral
stereotypies (all P < 0.05) as their yard-mates received more meals. Consequently there was an
overall increase in incidence of stereotypy in both treatment and control horses with the increase in
meal frequency. The study, therefore, suggests that dividing the stabled horses’ concentrate ration
into a number of smaller meals may be an effective means of reducing oral stereotypies, but that
* Corresponding author. Tel.: +44 1522 895276.
E-mail address: [email protected] (J.J. Cooper).
0168-1591/$ – see front matter # 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2004.08.005
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J.J. Cooper et al. / Applied Animal Behaviour Science 90 (2005) 351–364
pre-feeding stereotypies may persist and that the practise may increase the frequency of stereotypic
behaviour on unfed horses in visual contact.
# 2004 Elsevier B.V. All rights reserved.
Keywords: Stabled horses; Meal frequency; Concentrate feeding; Stereotypic behaviour
1. Introduction
In the stabled horse, a number of lines of evidence link stereotypic patterns of behaviour
such as weaving and crib-biting with feeding regime (Cooper and Mason, 1998; Nicol,
1999). Firstly, the feeding of high energy, low fibre concentrated feeds without access to
high fibre forage has been associated with a higher incidence of stereotypic activities in
both epidemiological studies (McGreevy et al., 1995; Nicol, 1999) and experimental
studies (Gillham et al., 1994; Johnson et al., 1998). Secondly, the initiation of bouts of
stereotypic behaviour has been associated with feeding time. Weaving, for example, has
been found commonly to occur prior to receiving a concentrated feed (e.g. Cooper et al.,
2000), whilst oral stereotypies have been described as a common post-prandial activity in
horses with little fibre (e.g. McGreevy and Nicol, 1998).
This relationship between feeding and stereotypic activities can be explained in terms of
control of feeding behaviour, conditioning or a combination of the two (Mason, 1991;
Rushen et al., 1993; Lawrence and Terlouw, 1993; Cooper and Mason, 1998). Before
feeding, the animal may perform species typical foraging or pre-feeding actions, such as
rooting in pigs (Rushen et al., 1993) or locomotion in mink (Mason, 1991). These may
persist in the captive animal’s behavioural repertoire if the feed fails to provide the
necessary consummatory stimuli that would be experienced under natural conditions
(Hughes and Duncan, 1988). Alternatively, the activities may become exaggerated within
the animal’s behavioural repertoire if they are apparently rewarded by food (Savory and
Mann, 1999; Mason and Mendl, 1997).
Thus in the horse, activities such as pawing, door kicking or weaving may initially arise
as anticipatory, appetitive activities and then become a conditioned response to feeding
time with repeated delivery of their meal shortly following their performance (Cooper and
McGreevy, 2002). Following feeding, particularly if this involved a nutritionally
inadequate meal, then feeding or foraging behaviour may persist (Terlouw et al., 1993;
Haskell et al., 1996; Savory and Mann, 1999) and in the absence of appropriate means of
expression, animals may direct this to apparently inappropriate substrates. In the stable
environment this may mean re-direction of feeding behaviour to fittings, to wood-chewing
(Haenlein et al., 1966; Krzak et al., 1991) or to crib-biting (McGreevy and Nicol, 1998) in
horses with limited access to alternative forages (Cooper and Mason, 1998). Re-directed
feeding activities may also become exaggerated, repetitive activities through reinforcement, if as some authors argue they are rewarding. This may be because they have general
rewarding properties associated with coping with an adverse environment (e.g. Broom and
Johnson, 1983) or because they address a specific adverse response to the feeding of
concentrates (Lawrence and Terlouw, 1993; Nicol et al., 2002).
J.J. Cooper et al. / Applied Animal Behaviour Science 90 (2005) 351–364
353
Elucidation of the role of motivation and conditioning on the ontogeny of stereotypic
patterns of behaviour requires careful experimental investigation over the period of the
activity’s development (e.g. Waters et al., 2002). As the two behavioural mechanisms may
have synergistic actions (Hughes and Duncan, 1988; Lawrence and Terlouw, 1993), and
many stereotypic activities appear to become emancipated from their original causes over
time (Cooper et al., 1996), it is often difficult to predict the effect of changes in husbandry
practice on the incidence of these behaviours (Mason, 1991). It has, however, been argued
that husbandry regimes that are sensitive to the biological background of the animal may
reduce the incidence of stereotypic behaviours (Mason and Mendl, 1997; Cooper and
McGreevy, 2002).
Horses are naturally trickle feeders and eat for 16–18 h per day (Davidson and Harris,
2002; Goodwin, 2002). If concentrated feeding is deemed to be a necessary component of a
horse’s management (for example, to maintain energy intake and therefore condition in
performance horses), then spreading the delivery of feed over a longer time frame may
reduce the incidence of stereotypies or other problems associated with concentrated feeds
(Tinker et al., 1997; Nicol et al., 2002). Dividing the concentrate ration into many smaller
meals may be one approach to achieving this. Firstly, with shorter gaps between meals the
horse’s feeding motivation may be lower at the time of delivery of each meal. Consequently
the horse may be less likely to perform exaggerated anticipatory activities prior to feeding.
In addition, each individual small meal may be better able to satisfy the horse’s feeding
motivation than a smaller number of interspersed large meals. In which case, feeding
motivation may not persist following consumption of the concentrate and be less likely to
be re-directed into oral stereotypies. Alternatively, the horses’ response to feeding may be
independent of its feeding motivation, for example a conditioned response to feeding time
or emancipated from its original causal factors. Under these circumstances, the horse may
persist with a similar amount of stereotypic behaviour before and after each meal. Finally,
more frequent feeding may strengthen the conditioned association between stereotypy and
feeding. Consequently, there may be an increase in the frequency of these activities
particularly prior to feeding.
This study investigated these possible outcomes by comparing the incidence of
stereotypic behaviour in stabled horses on a conventional feeding regime of two meals per
day with horses on more frequent feeding regimes. The project was carried out on a
working equestrian yard where up to 50 horses could be observed. A pilot study was first
carried out on 30 stabled horses to identify suitable horses for the main trial. From this
population nine horses were selected for treatments where they were observed for 6 h per
day on various feeding regimes. In addition nine control horses were selected to sample the
behaviour of horses on the same yard that were not exposed to the altered feeding regimes.
2. Pilot study
A pilot study was carried out on 30 horses that were housed on the Caythorpe Court
Equestrian Yard, Lincolnshire School of Agriculture, University of Lincoln. The majority
of these horses were bedded with straw (20), though eight horses had paper bedding and
two horses were housed on shavings. All horses were housed in conventional stables, which
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measured 12 ft 12 ft with a single conventional half-door entrance. Observations were
carried out on Saturdays and Sundays when the yard was less busy than on weekdays and
the routine more fixed. On these days horses were fed fresh forage (1.5–4.0 kg of haylage)
and their morning feed (2 kg of feed in a bucket made up of 1 kg soaked sugar beet pulp,
0.5 kg chopped hay/straw and 0.5 kg of a commercial pelleted feed) between 08:20 and
08:30 h and were exercised between 10:00 and 12:00 h. During the early afternoon there
was little activity on the yard and horses received their afternoon feed (2 kg of sugar beet,
chopped hay/straw and pelleted concentrate) between 16:20 and 16:30 h and a further
ration of fresh haylage (same amount as in morning) at 17:00 h (Table 1). On weekdays
when horses received more work, there was an additional feed of 1 kg of the sugar beet,
chopped hay, concentrate mix at 12:30 h.
The horses were observed from 08:00 to 09:00 h and from 16:00 to 17:00 h on both the
Saturday and Sunday of a single weekend. During this time yard staff and students carried
out normal day to day yard management. Each horse was scanned once every 2 min (30
scans per observation) and on each scan its behaviour was recorded according to a simple
ethogram of 16 mutually exclusive categories of behaviour (Table 2). These covered
general activity, feeding and other ingestive behaviour, stereotypic behaviour and other
activities. Specific forms of oral stereotypy (e.g. wood-chewing, crib-biting, wall-licking)
were rare and sometimes difficult to consistently differentiate. Consequently all incidences
of stereotypic oral activities were added together for analysis.
2.1. Analysis
Data for each activity were converted to proportion of scans, then analysed using
parametric statistics following angular transformation. The effects of day (Saturday versus
Sunday) and time of day (morning versus afternoon) were analysed using a repeated
measure ANOVA blocking data by individual horse. The effects of bedding type (straw,
paper, shavings) was analysed using a one-way ANOVA on the average proportions for
each horse over the four observations. Data is presented as percentage of scans in the results
for clarity.
2.2. Results of pilot study
Horses tended to be active in the hour around feeding time. They spent most scans
standing alert (38.6% of scans), with eating concentrate (14.9%), eating haylage (14.2%)
and bedding directed activity (22.0%) also commonly observed. Horses were only
recorded engaged in stereotypic activities in 5.6% of scans of which oral stereotypies were
Table 1
Typical events during observation periods in pilot study
Morning observation
Afternoon observation
8:00
8:20
8:40
9:00
16:00 Start afternoon observation
16:20 Staff on yard: feeding begins
Start morning observation
Staff on yard: feeding begins
Haylage added
Turning out begins
17:00 Haylage added
J.J. Cooper et al. / Applied Animal Behaviour Science 90 (2005) 351–364
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Table 2
Categories of activity used in pilot and main studies
Category
Definition
Stand alert
Standing with eyes open and ears pricked. Attention may appear to be directed at observer,
yard staff, other horses or other aspects of social or physical environment
Stand doze
Standing but not appearing to pay attention to surroundings. Typically eyes
shut or half-closed, ears not erect
Lie
Lying recumbent or sternally
Locomotion
Moving from one location in stable to another. Not overtly repetitive (see Box walking)
Feed
Eating concentrate
Hay
Eating haylage
Bedding
Sniffing, nosing or eating bedding
Drink
Drinking from water bucket
Weave
Repetitive lateral (swinging) movement of head, typically but not always whilst held above
stable half-door. May also involve swaying of fore-body, and lifting of fore legs
Nod
Repetitive vertical movement of head, typically but not always whilst held above stable door
Oral
Repetitive oral activities without overt nutritional function, such as sham chewing, tongue
stereotypy
rolling, biting or grasping stable fittings or repeated licking of stable fittings
Box walk
Repeatedly moving between two locations in stable or walking a route around the stable
Door kick/paw Kicking stable door (or other fittings), stamping or scraping foot on stable floor
Other
Any activity not covered by the above (e.g. urination)
most common (2.1%), followed by nodding (1.9%) and weaving (1.3%). Door kicking or
pawing was rarely observed (0.3% of scans) and horses spent little time on standing
inactive (2.4%), locomotion (1.1%), drinking (0.3%) and other activities (0.8%) during the
observation periods.
There was an effect of time of day on the percentage of scans spent standing alert, eating
haylage, bedding directed behaviour and on oral stereotypy (Table 3). Horses spent less scans
eating haylage in the afternoon observation than in the morning and more scans engaged in
bedding directed activities (Fig. 1). Horses also spent more scans on oral stereotypies in the
afternoon than the morning though there was no significant difference in the scans engaged in
weaving or nodding (Fig. 2). There were no other differences in behaviour between morning
and afternoon feeds and the day of observation had no effect on any activity.
Table 3
The percentage of scans (mean and S.E.) on standing active, feeding and stereotypic activities during the morning
and afternoon feeds on the pilot study
Activity
Morning
Afternoon
F, P
Standing alert
Concentrate
Haylage
Bedding
Weave
Nod
Oral
Total stereotypy
35.2
16.3
22.7
14.5
1.1
1.6
1.2
4.2
42.2
13.5
5.7
29.5
1.5
2.2
3.0
7.1
1.22 ns
1.01 ns
35.3***
20.7***
0.13 ns
0.37 ns
4.76*
4.46*
*
p <0.05
p <0.001
***
(4.0)
(1.3)
(3.8)
(3.0)
(0.7)
(0.9)
(1.0)
(1.5)
(4.8)
(1.8)
(2.8)
(3.7)
(0.5)
(1.1)
(1.2)
(1.8)
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Fig. 1. The percentage of scans (mean S.E.) engaged in standing alert, eating concentrate (feeding), eating
haylage and in bedding directed behaviour by 30 horses during morning and afternoon meals on weekend days.
There were also significant differences in the behaviour of horses on different bedding
types. Horses on shavings (2.7% of scans) and paper (2.4% of scans) tended to show more
oral stereotypies than horses on straw bedding (1.2% of scans: F2,27 = 3.82, P < 0.05).
There was, however, no difference in the incidence of bedding directed behaviour between
bedding types and no other effects of bedding on the horses’ behaviour.
Fig. 2. The percentage of scans (mean S.E.) engaged in weaving, nodding and oral stereotypic behaviour by 30
horses during morning and afternoon meals on weekend days.
J.J. Cooper et al. / Applied Animal Behaviour Science 90 (2005) 351–364
357
2.3. Discussion and conclusion of pilot study
The principle findings of the pilot study were that there was a difference in incidence
of eating haylage, bedding directed activities and oral stereotypy between the two
meal times and an effect of bedding type on oral stereotypy. The effect of observation
period could be due to a number of factors such as simply the time of day, the time
since rest/turning out or the level of human activity on the yard, though the yard activity
was broadly similar between the two observations. One management factor that did differ
considerably between the two observations was the presence of forage in the stable, as
during the morning feed horses consistently received their haylage within 10–20 min of
the concentrate, whereas in the afternoon horses often received haylage 40 min following
concentrate feeding. As a consequence, following the morning presentation of
concentrate horses had free access to haylage, whereas in the afternoon many horses
had limited access to forage during the observation period. This may not only explain the
low incidence of haylage eating during the afternoon but also the higher incidence of
bedding directed activities during the afternoon. This in turn may represent the
perseverance of foraging motivation following a concentrate meal (Goodwin et al.,
2002) and is consistent with other studies relating persistent oral activities including
stereotypy to redirection of feeding motivation in horses with low availability of forage
(Willard et al., 1977; Krzak et al., 1991; Johnson et al., 1998; McGreevy and Nicol,
1998).
Our findings also support those of other studies of the relationship between stereotypy
and bedding, which indicate that stereotypies are less common in horses bedded on straw
relative to paper or shavings (McGreevy et al., 1995; Mills et al., 2000). It must, however,
be noted that in the current study the horses had already been allocated their bedding types
for health (e.g. dust allergies) or other management reasons (e.g. so-called ‘‘bed-eaters’’).
So this was not a true test of the effect of bedding on stereotypy, and other potential
behavioural effects of bedding type, such as incidence of bedding directed behaviour might
have been masked by these management decisions.
3. Main study
3.1. Subjects
For the main part of the study we chose 18 horses from the pilot study. These had to be
available for observation over a 6-week period and maintained on broadly similar feeding,
exercise and husbandry routines prior to the main study. Half the horses were allocated to
the treatment group, which were to receive the same quantity of concentrated feed in a
larger number of meals and half the horses were allocated to the control group who had no
change to their feeding regime. Treatment and control horses were selected to control for
breed, bedding type and type of stereotypy. Comparison of the two groups using data from
the pilot study revealed that there was no difference in their behaviour prior to the main
study.
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3.2. Treatment group
The nine treatment horses were to be exposed to the regime of similar quantity of feed
per day but divided into more meals. The horses first received their daily 4 kg ration as two
conventional 2 kg meals at 10:30 and 16:30 over two successive weekend days. Two weeks
later they received their full ration as four equally sized 1 kg meals at 10:30, 12:30, 14:30
and 16:30 on two consecutive weekend days. After a further two weeks they received their
full ration as six equally sized 0.66 kg meals at 10:30, 11:30, 12:30, 14:30, 15:30 and
16:30, again over two successive weekend days. In addition to feeding times, treatment
horses were turned out or exercised between 08:00 and 10:00 in the morning and received
their rations of haylage at 10:00 and 17:00. On days between observations the horses
received the same husbandry as all other horses on the yard (see Section 2). Table 4
summarises the meals times and yard activity of the treatment horses.
3.3. Control group
A further nine horses from the yard with no change in their own management were also
observed to record the effect of the additional meals on the rest of the yard. These horses
received their normal 2 kg allowance of concentrate at 8:30 and 16:30 and haylage at 8:30
and 17:00. If they were exercised or turned out this was usually between 10:00 and 12:00 in
the morning. After the first weekend of observations, two control horses were required for
other purposes, which affected their meal times. These were therefore removed from the
study and their data not used in analysis.
3.4. Data collection and analysis
The ethogram from the pilot study was again used and all horses were observed over six
time periods on each test day. These were 10:00–11:00, 11:00–12:00, 12:00–13:00, 14:00–
15:00, 15:00–16:00 and 16:00–17:00 (Table 4). There was little difference in yard activity
at these times between Saturdays and Sundays except afternoon yard duties usually began
at 16:00 on Saturdays and at 15:00 on Sundays. During observation periods the behaviour
of each horse was scan sampled once every 2 min for 60 min (i.e. 30 scans per observation
period). The total number of scans of each activity was calculated for the whole day and
this was converted to proportion of scans then angular transformed for analysis using
parametric ANOVA. Data from treatment and control horses were analysed separately to
investigate the effect of meal frequency on the behaviour of the two groups.
Table 4
The six observation periods showing yard husbandry and treatment feeding during the trial
Observation period 10:00–11:00 11:00–12:00 12:00–13:00 14:00–15:00 15:00–16:00
16:00–17:00
Yard activity
Busy
Busy
Quiet
Quiet
Quiet (Saturday), Busy
busy (Sunday)
Two meals
Four meals
Six meals
X
X
X
X
X
X
X
X
X
X
X
X
J.J. Cooper et al. / Applied Animal Behaviour Science 90 (2005) 351–364
359
Table 5
The percentage of scans engaged in standing active, feeding activities and stereotypic activities by the treatment
and control horses during the three weekends of the trial
Treatment
Active
SA
Feed
Hay
Bed
Weave
Nod
Oral
Kick
SS
Control
2
4
6
F
2
4
6
F
36.5
5.7
13.6
27.6
0.27
0.49
0.63
0.23
1.62
29.8
7.8
18.0
22.4
0.72
0.81
0.28
0.20
2.21
31.7
8.7
25.4
23.0
1.29
1.73
0.26
0.10
3.38
2.35
16.5***
15.3***
3.07*
3.89*
5.38**
3.64*
0.55
3.58*
36.6
4.6
12.3
29.6
0.29
0.96
0.56
0.30
2.11
31.7
4.0
17.6
25.4
1.03
1.73
1.16
0.22
4.14
36.3
6.0
14.3
28.3
1.32
3.32
1.42
0.30
6.36
2.78
2.82
2.30
2.58
3.78*
6.32**
4.70**
0.21
5.55**
*
p <0.05
p <0.01
***
p <0.001
**
4. Results
Horses spent much of the observation period standing alert (32.3% of scans), standing
dozing (10.9%), eating concentrate (7.0%), eating haylage (17.4%) or in bedding directed
behaviour (25.9%). Stereotypy only occupied 3.25% of scans, of which weaving made up
0.82%, nodding 1.50% and oral stereotypies 0.72% of scans. In addition a small number of
scans of door kicking or floor pawing were also observed (0.21%), though box walking and
wind sucking were not observed.
Fig. 3. The incidence of weaving, nodding and oral stereotypic behaviour in treatment and control horses when
treatment horses are fed two meals per day.
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There had been no overall difference in behaviour of the treatment and control horses
in the pilot study or in the first week of observation when both received two meals per
day, but differences in behaviour were apparent as meal frequency was increased in the
treatment horses (Table 5). In these horses there was an increase in time spent feeding and
eating haylage with more meals per day and a decrease in bedding directed behaviour.
There was also a decline in oral stereotypies (P < 0.05) with the number of meals, but an
increase in weaving (P < 0.05) and nodding (P < 0.01). Door kicking/pawing was not
affected by meal frequency and overall there was an increase in stereotypic behaviour
with number of meals. In the control population, the meal frequency had no effect on any
non-stereotypic activity (Table 5). There was, however, an increase in weaving, nodding
and oral stereotypic behaviours and consequently the total time performing stereotypy
(P < 0.01).
Figs. 3–5 shows in more detail the incidence of stereotypic behaviour in the control and
treatment horses in each observation period. With two meals per day the majority of
stereotypy in both control and treatment horses is seen around the treatment horses’
feeding time between 10:00 and 11:00 and between 16:00 and 17:00 (Fig. 1). Stereotypy is
rarely scanned during the rest of the day. With four meals per day, treatment horses show
weaving and nodding at each mealtime (Fig. 2). Oral stereotypies are also seen at each
mealtime but these are infrequent, leading to the overall decrease in oral stereotypy
compared with two meals per day (Table 5). Control horses show peaks in weaving,
nodding and oral stereotypies at the 10:30, 12:30, 14:30 mealtimes, even though they are
not actually fed, in addition to their own 16:30 feed delivery. These associations between
stereotypic behaviour and mealtimes are also seen with six meals (Fig. 3). The treatment
horses again show a high incidence of weaving and nodding with each meal, but a lower
incidence of oral stereotypic behaviour. Control horses again perform weaving,
nodding and oral stereotypy at a high rate each time the treatment horses are fed (Figs.
4 and 5).
Fig. 4. The incidence of weaving, nodding and oral stereotypic behaviour in treatment and control horses when
treatment horses are fed four meals per day.
J.J. Cooper et al. / Applied Animal Behaviour Science 90 (2005) 351–364
361
Fig. 5. The incidence of weaving, nodding and oral stereotypic behaviour in treatment and control horses when
treatment horses are fed six meals per day.
5. Discussion
Increasing meal frequency affected the behaviour of treatment horses in a number of
positive ways with a decrease in oral stereotypy and more time taken to eat their ration of
concentrate. Oral stereotypic behaviours have been associated with gut dysfunction
including colic (Hillyer et al., 2002), ulceration (Nicol et al., 2002) and low pH (Willard et
al., 1977), whilst slowing rate of ingestion of concentrates may reduce these problems
(Davidson and Harris, 2002). There were also more scans of eating haylage and less scans
on bedding directed behaviour, an activity that is considered undesirable by some horse
owners (McBride and Long, 2001; Goodwin et al., 2002) due to perceived risks of parasite
infection or impaction (Davidson and Harris, 2002). These changes in behaviour suggest
that with a larger number of smaller meals, there is a lower tendency to show feeding
behaviour following each meal and to re-direct this to alternative, potentially undesirable
substrates. This contrasts with the findings of studies with pigs (Haskell et al., 1996) and
broilers (Savory and Mann, 1999), which increase oral stereotypies when fed a larger
number of small meals.
In the study, unlike those involving pigs and broilers, the horses were provided with
forage in the form of haylage prior to the first morning feed, which usually lasted the horses
until early afternoon. Therefore, if the horses continue to be motivated to eat following a
meal of concentrates, they will eat haylage whilst it is available rather than re-direct their
feeding behaviour to less suitable substrates. This explanation is consistent with the
findings of the pilot study and with other studies investigating the effect of provision of
forage on diet selection (Goodwin et al., 2002) and stereotypic behaviour (Willard et al.,
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1977; McGreevy et al., 1995; McGreevy and Nicol, 1998; Johnson et al., 1998). It also
points to a simple practical measure to reduce oral stereotypic behaviour in stabled horses,
namely providing suitable high fibre forage at feeding times, as concentrated feeds alone
do not provide an adequate, functional diet for horses.
There was, however, an increase in weaving and nodding in the treatment horses and an
increase in weaving, nodding and oral stereotypies in horses elsewhere on the yard. This
appears to contradict the findings of McGreevy et al. (1995) owner-based epidemiological
study of risk factors associated with equine stereotypy, where more frequent provision of
forage meals reduced the risk of stereotypic behaviour. However, the horses’ behavioural
response to provision of concentrate and provision of forage differs markedly, with a peak
in stereotypy as concentrate feeding time approaches which is not seen prior to forage
feeding times (Cooper et al., 2000). In our study, the treatment horses appeared to rapidly
learn the new feeding regimes and performed pre-feeding actions in the anticipation of
meals throughout the day (Figs. 3–5). This suggests weaving and nodding were an
anticipatory response to feeding time (Cooper and Mason, 1998; Nicol, 1999) which may
have been either learnt as a result of the feed reward or because the motivation to perform
horse’s species specific pre-feeding behaviour has not been extinguished in the stable
environment (Hughes and Duncan, 1988; Cooper and McGreevy, 2002). In this study we
made no attempt to alter pre-feeding cues (apart from time of day) and removal of these
cues may have reduced stereotypic behaviour particularly prior to feeding. This has been
achieved in dry sows, where feeding without cues effectively extinguished pre-feeding
stereotypic behaviour (Terlouw et al., 1993). Removal of overt pre-feeding cues such as
activity in the feed room may be a means of reducing stereotypy in the short-term, though
the usefulness of this approach in practise is debateable, as it may be difficult to
completely remove pre-feeding cues from working yards and because the horses with time
may learn to associate other cues with feeding and consequently persist with anticipatory
activities.
Another approach to providing horses with their concentrated feed in a larger number of
discrete meals is the use of operant foraging devices (Young et al., 1994). These devices
allow horses to work for their food and have been found to produce some desirable changes
in behaviour such as an increase in the time spent foraging (Winskill et al., 1996). Their
effect on stereotypic behaviour is, however, equivocal. There is good evidence that they
reduce pre-feeding stereotypies such as weaving (Henderson and Waran, 2001). This could
be because of the removal of cues that predict feeding time, or because the horse can
express anticipatory or appetitive feeding actions in a more meaningful way, such as
working on the device to deliver feed. The evidence that they reduce oral stereotypies is
less clear as horses, with no overall decrease in frequency compared with horses fed
conventionally (Henderson and Waran, 2001). This may be because the performance of
oral stereotypies is inherently associated with consumption of hard feed so animals are
motivated to perform the activities after each meal (Lawrence and Terlouw, 1993; Savory
and Mann, 1999). Under these circumstances, increasing mealtimes may lead to an
increase in post-feeding stereotypy, unless the individual meal-sizes are large enough to be
nutritionally satisfactory (Haskell et al., 1996) without being so large as to cause digestive
dysfunction (Tinker et al., 1997), or the horses have access to an alternative more
acceptable means of expressing feeding behaviour such as forage (Goodwin et al., 2002).
J.J. Cooper et al. / Applied Animal Behaviour Science 90 (2005) 351–364
363
The increase in weaving, nodding and oral stereotypies in the control horses appeared to
result from the visual cues of other horses being fed without the act of feeding themselves.
The timing of these activities was centred on the feeding of the treatment horses rather than
distributed across the day (Figs. 3–5), with weaving commonly preceding feeding times
and nodding and oral stereotypies performed as the treatment horses ate their meals. These
activities in the control horses may have represented a form of observational learning, such
as observational conditioning (Sweeting et al., 1985; Nicol, 1995). In time this may decline
as the association between the cues and feeding itself became extinguished. However, this
may take many exposures for horses that have been performing pre-feeding stereotypic
behaviour for long periods and is unlikely to be seen favourably by horse owners.
Furthermore, where horses are exposed to feeding cues, but not fed, then the increased
incidence of stereotypic may be an indication of behavioural frustration or conflict (Broom
and Johnson, 1983).
This study demonstrates the difficulties associated with attempting to identify and
resolve the causal factors underlying the performance of stereotypic behaviour in stabled
horses or indeed other captive animals. It suggests that reducing the amount of concentrate
fed at each meal has the potential to reduce oral stereotypy in stabled horses, but that this
may be negated by an increase in pre-feeding stereotypic behaviour if pre-feeding cues are
not removed. Furthermore, exposing stabled horses to feed cues without actually feeding
them leads to an increase in the incidence of their stereotypic activities.
Acknowledgements
We would like to thank Nicholas Locke of the University of Lincoln Equine Yard for
permission to observe the horses and Amy Richardson and Sharon Kirby for help on the
yard. The project was funded by Waltham Centre for Pet Nutrition.
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