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Stereotyped behaviour, adjunctive drinking and the feeding periods of tethered sows
Anita. Behav., 1984, 32, 1059-1067
STEREOTYPED BEHAVIOLrR, ADJUNCTIVE DRINKING AND THE FEEDING PERIODS OF TETHERED SOWS BY J. R U S H E N *
Animal Behaviour Unit, Psychology Department, University of Queensland, St. Lucia, Queensland, 4067, Australia Abstract. The behaviour of 25 tethered sows in an intensive piggery was observed for 1 h before and 1 h after the delivery of food to determine if behavioural stereotypies appeared as adjunctive behaviours. The different components of behavioaral stereotypies were found to have different associations with the feeding period. Head-waving, bar-biting, and rubbing the snout against the cage were most common before feeding, and were shown particularly by the older sows. Manipulating the drinker and, for some sows, rubbing were most common after. There was some evidence of polydipsia. Vacuum chewing, playing with the chain, and aggressive behaviours, however, did not appear to be associated with the feeding period. The last two behaviours occurred only rarely. Seven sows showed stereotyped sequences of rapid rubbing or rapid drinking after the detivery of food, and these sows showed more excitement before food was delivered. Rooting was common for the full hour after all food had been consumed, and occurred in conjunction with long duration drinking. I suggest that the occurrence of adjunctive drinking by sows results from the persistence of feeding motivation, perhaps because concentrated food does not provide sufficient stomach distension, combined with the knowledge that food will definitely not be forthcoming. Stereotyped sequences of behaviour may be a means of reducing the arousal generated by the expectation of food. Vestergaard 1981). These are most apparent in confined sows kept in stalls or tethers (Jensen 1980; Vestergaard 1981; Blackshaw & McVeigh, 1984). The occurrence of such behaviours has been used as an argument that the welfare of the animals is being disregarded in intensive husbandry systems, and their occurrence may be useftll in making behavioural assessments of the environments being designed for animals (Dawkins 1980; Duncan 1980). However, before this can be accomplished, the causal factors underlying these behaviours need to be more fully understood. Kiley-Worthington (1977) provides a brief review of the broad range of explanations that have been proposed for the occurrence of these behaviours. The addition of novel objects into an animal's cage has been found to reduce the occurrence of stereotypies shown by chimpanzees (Berkson 1967), mandrills (Yanofsky & Markowitz 1978), and canaries (Keiper 1969). However, environmental disturbances may actually increase their occurrence (Fentress 1976; Broom 1981). Stereotypies in pigs can be inhibited from occurring by the addition of straw (Fraser 1975) or sterilized earth (Wood-Gush & Beilharz 1983), which may indicate boredom or a lack of adequate sensory stimulation. Since the stereotypies of chickens can be induced by placing them in a frustrating situation (Duncan
Stereotyped behaviours are relatively invariant sequences of motor acts, repeated frequently, and having little apparent goal (Keiper 1969; Kiley-Worthington 1977; Dawkins 1980). These occur in a wide range of species in a wide range of behavioural contexts, and are often suspected of indicating some underlying pathology or welfare problem. A broad distinction can be drawn between stereotypies that result from social deprivation and abnormal rearing conditions and which are relatively stable in the face of a change of environment, and 'cage stereotypies' that are more dependent upon the immediate environment for their occurrence (Ridley & Baker 1982). Wild animals that are caged show a variety of movement stereotypies such as backward and forward pacing. These can be considered as indicating faults in the design of the environment, such as lack of space or a lack of suitable opportunities for a variety of activities (Hediger 1950; Meyer-Holzapfel 1968). Intensively-housed pigs exhibit a wide range of stereotyped and other unusual behaviours, such as biting or nosing of the bars of the pen, pulling on chains, head-waving, and high frequency 'vacuum' chewing (Fraser 1975; *Present address: School of Agriculture and Forestry, University of Melbourne, Parkville 3052, Victoria, Australia.
1059
1060
ANIMAL
BEHAVIOUR,
& Wood-Gush 1972) they may reflect the frustration of natural behaviour patterns in artificial environments, as occurs for tethered sows (Jensen 1980). However, Palya & Zacny (1980) have argued against explanations that invoke 'global' problems such as boredom on the grounds that many observed stereotypies ( i n pigeons) are associated with feeding periods and so may be forms of adjunctive behaviour, resulting from food being delivered on a fixed schedule (Staddon 1977). Stereotyped chain pulling can be induced in young pigs by placing them on a fixed-interval food-delivery schedule (Dantzer & Mormede 1981, 1983), suggesting that this behaviour is the porcine equivalent of the excessive drinking (polydypsia) often seen in rats when kept on similar food-delivery schedules. Jensen (1980) found that the naturally occurring stereotypies were most frequent an hour after feeding, suggesting that the occurrence of such behaviour in commercial piggeries results from the fact that food is typically delivered on a fixed-interval schedule. However, Fraser (1975) found stereotypies to occur most frequently before feed periods, and it seems that different forms of behaviour may be found before and after feeding (Blackshaw & McVeigh, 1984). Most animals show a variety of stereotypies, and not all may result from the same causal factors (Keiper 1969). Adjunctive and schedule-induced behaviours can be classified into 'terminal responses' that occur immediately prior to the delivery of food, 'interim responses' that occur immediately after food delivery, and 'facultative behaviours' that occur in the intermediate period (Staddon & Simmelhag 1971; Staddon 1977). Possibly the different types of stereotypies shown by pigs represent these different types of behaviour.
Methods Subjects Observations were made at the Pig Unit of the University of Queensland farm at Pinjarra Hills, Brisbane. This is an intensive, specific pathogen-free piggery, run on a commercial basis although its primary function is for teaching and research. The main building is a 56 m • 14 m metal-framed 'Big Dutchman' shed with a concrete floor, ventilated by natural air circulation through open side shutters and ceiling vents. It is composed of four sections:
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a research section, a mating section, a tethering section and a growing section. The 55 large white x landrace cross sows are placed in farrowing crates for 3-4 weeks until weaning, then mated and penned in stalls besides the boars for approximately 6 weeks. They are then moved to tethering crates for the remainder of the gestation period of up to 120 days. The tethering section (11 m • 14 m) has 44 tethering crates in four rows and contains, at any one time, 25-30 sows on average. The sows are tethered by the neck by a 65-cm chain to the base of the tethering crates. A food trough runs along the front of the crates, and food is provided twice a day at 0800-0830 hours and 14001430 hours, in the form of pellets. Delivery is made by a single worker pushing the food trolley around the entire piggery. Water is continuously available through a single push-operated nipple placed approximately 2 cm above the top of the food trough. Observations were made of the behaviour of 25 tethered sows. These pigs were not selected on any particular basis, except that they were in tethers at the time of the study. Sows showing marked stereotypies were deliberately included in the sample. The sows had a mean age of 26 months (sD=10.59), a mean parity of 3.08 (range 1-8) and had been in the tethering crates for an average of 67.08 days (sD=24.35).
Procedure A Sony Betamax SLF1E portable colour video recorder was set up with the camera placed 12 rain front of the sows. Two or three sows were filmed simultaneously. Recording commenced 1-1.5 h before the afternoon feed period, and continued for 3 h. To minimize the noted effect of external disturbance on the occurrence of stereotypies (Fentress 1976; Broom 1981), the observer left as soon as recording commenced, and only natural lighting was used. The video recordings of the two half-hour periods prior to the food delivery, and the two half-hour periods subsequent to feeding were scored for the occurrence of each of the behaviours described below, using a portable, multichannel event recorder (Pamment & Stephens 1981). The observation periods subsequent to feeding were taken as beginning 15 rain after the delivery of food, thus allowing adequate time for all of the food in the trough to be consumed. The data from the event recorder were fed (via an audio cassette interface) into a PerkinElmer 3210 computer, where the total frequency
RUSHEN: STEREOTYPED BEHAVIOUR OF PIGS of occurrence, and the total duration of each behaviour was computed. The following behaviours, including the basic body position of the sows, and the main behavioural components of the stereotypies were scored. (1) Body position: standing, sitting or lying. (2) Rooting: this included any nosing or licking the base of the food trough or the floor. Rooting was not scored if the drinker was activated even if the snout was in the food trough. (3) Chomping or 'vacuum chewing' (Vestergaard 1981): this included any chewing movement which did not involve an object in the mouth. This often occurred in bouts, and each individual instance where the sow visibly opened her mouth was recorded. (4) Rubbing: this category included the rubbing of any part of the head against the bars of the crate (except the drinker and the tethering chain) or the food trough. In actual fact, all observed instances of rubbing involved the snout, particularly the nose. As rubbing often occurred in bouts of rapid back and forth movement, only the occurrence of each bout was scored. (5) Bar-biting; this included any instance where some part of the tethering crate, excluding the chain or the drinker, was taken into the sow's mouth, whether or not chewing movements occurred. Each individual instance of bar biting was scored. (6) Drinking: this was scored when the sow activated the water nipple in any way, and therefore need not imply the actual consumption of water. This was necessary because sows develop unique methods of drinking, some holding the nipple open with the base of the snout while water is drunk out of the food trough. Only in some cases can the consumption of water be observed. (7) Any manipulation of the tethering chain using the snout or the mouth. (8) Head-waving (Fraser 1975): because of the difficulty of clearly separating the different types of head movement, this category comprised any horizontal head movement where the head is moved at least three-quarters of the width of the crate in a single movement. (9) Aggressive behaviour. Results
Each sow was scored according to the frequency of occurrence of chomping, bar-biting, and drinking, and the frequency of bouts of rubbing
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(per min), and the amount of time spent in each behaviour (percentage of total time) during each of the four periods. Chomping, head-waving, and aggressive behaviour occurred too rapidly to allow accurate measures of duration to be reliably made. Unfortunately, owing to various factors such as low light intensity and the sows' propensity to keep the mouth in or behind the trough, it was possible to score the frequency of chomping for only 16 sows in the two periods prior to feeding, and for only 11 sows in the two periods after feeding. For all measures, the distribution of scores exhibited a marked positive skew, with a large number of scores being zero. To overcome this problem, the scores were subjected to a logarithmic transformation (Winer 1971). One way repeated-measures analysis of variance tests were used to determine if the occurrence of the behaviours differed between the four periods. The results are shown in Table I. Sows spent a greater period of time lying down prior to feeding than after feeding, and a greater percentage of time rooting in the feed trough or on the floor after feeding (Fig. 1). Both the frequency and duration of bar-biting, and the frequency of head-waving were highest prior to feeding, particularly in the period immediately prior to feeding (Fig. 2). The movement of the food trolley around the piggery caused a great deal of excitement throughout the entire piggery, and bar-biting and head-waving were most frequent in the period from when this movement began until the sow actually received its food. Table I. Results of Analysis of Variance to Determine if the Occurrence of Each Behavinur Differed in the Four Time Periods*
Behaviour Lying down--duration Rooting--duration Chomping--frequency Rubbing--frequency Rubbing--duration Bar biting--frequency Bar biting--duration Drinking--frequency Drinking--duration Chain frequency Chain--duration Headwaving--frequency Aggression frequency
df
F
P
3,72 3.72 3,30 3,72 3,72 3,72 3,72 3,72 3,72 3,72 3,72 3,72 3,72
4.31 3.09 2.39 2.91 2.10 9.83 16.91 7.36 10.98 0.20 0.10 25.12 1.79
<0.01 <0.01 NS <0.05 NS <0.001 <0.001 <0.001 <0.001 Ns NS <0.001 Ns
*Periods 1 and 2 are the two half-hour periods before feeding and periods 3 and 4 are the two half-hour periods after.
ANIMAL
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BEHAVIOUR,
The frequency and duration of drinking were highest after feeding (Fig. 3). In some cases there was evidence ofpolydipsia. Two sows spent over 50 ~ of the hour after feeding manipulating the drinker, while a further five sows spent over 20 ~ of this time drinking. The frequency and duration of rubbing differed only slightly between the time periods. However, this was complicated by four sows who exhibited a very high frequency (J?=13.66/min) and duration (J?= 42.64 ~) of rubbing in the periods after feeding. The comparable figures for the remaining 21 sows are: frequency (J~= 0.26/min), and duration ()?= 0.69 ~). This rubbing tended to
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occur in stereotyped sequences. When these four sows were removed from the analysis both the frequency of rubbing (F= 14.50, df=3,60 P < 0.001), and the duration of rubbing (F= 5.66, df=3,60, P<0.001) differed between the time periods, with both measures being highest in the period immediately prior to feeding (Fig. 4). The measures of occurrence of playing with the chain, chomping, and aggressive behaviour D R I N K I N G (DURATICI~
DRINKING ( F R E Q U E N C Y )
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1.5
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6r
z
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I I
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40
1
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a
0.5
a
2
3
4
1
2
3
4
PERIOD
20
2
3
4
1
2
3
PERIOD
J
Fig. 3. Average percentage of total time spent drinking and average frequency of drinking during each of the four periods. Periods 1 and 2 are the two half-hour periods before food delivery and periods 3 and 4 are the two halfhour periods after.
1,5
Fig. 1. Average percentage of total time spent lying down and rooting during each of the four periods. Periods 1 and 2 are the two half-hour periods before food delivery and periods 3 and 4 are the two half-hour periods after.
RUBBING
RUBBING
(DURATION)
(FREQUENCY)
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.J
I BAR-BITING
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HEAD WAVING
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I 1 2 3 4
1 2 3 4
1
34
2
1
2
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4
PERIOD
PERIOD
Fig. 2. Average percentage of total time spent barbiting, and average frequency of bar-biting and headwaving during each of the four periods. Periods 1 and 2 are the two half-hour periods before food delivery and periods 3 and 4 are the two half-hour periods after.
Fig. 4. Average percentage of total time spent rubbing and average frequency of rubbing during each of the four periods. Periods 1 and 2 are the two half hour periods before food delivery and periods 3 and 4 and the two half hour periods after. The results from four sows which rubbed very frequently after feeding have been omitted.
RUSHEN:
STEREOTYPED
did not differ between the four time periods. Playing with the chain did not occur very frequently ()~=0.36/min) and did not involve much of the animals' time (_~---2.63 ~). Chomping occurred at an average rate o f 30.73 per rain. (N = 11), while the highest rate recorded was 81 bites per min in the half hour immediately after feeding. Only 69 instances of aggressive behaviour were seen during the 50 h of observation. To test the extent that the measures of frequency and duration of the behaviours were interrelated and stable across the feeding period, product-moment correlations (r) were calculated for each pair of measures in periods 2 and 3. Correlations were also calculated between these measures and the age, parity, and time in the tether of each of the sows. Measures of frequency and duration were significantly correlated for all behaviours. The age of the sow was correlated with the frequency of head-waving (r---0.61, P<0.01), the frequency of bar biting (r=0.68, P<0.01), and the duration of bar biting (r = 0.55, P < 0.01) in period 2. Parity was also significantly correlated with all of these but the correlations were smaller. The f r e q u e n c y of head-waving in period 2 was correlated with the frequency (r=0.59, P<0.01) and duration (r=0.57, P < 0 . 0 1 ) of bar-biting in period 2. Both the frequency of head-waving (r=0.45, P<0.05), and the frequency of bar-biting (r=0.61, P < 0 . 0 1 ) in period 2 were correlated with the frequency of drinking in period 3, but not with the duration of drinking. The only measures that were stable across the feeding period were the frequency (r---0.57, P<0.01) and duration (r=0.63, P = 0 . 0 1 ) of rubbing, and the frequency of playing with the chain (r=0.74, P < 0.01). The three activities in which sows spent a substantial amount of time after feeding were drinking, rubbing and rooting on the floor or in the feed trough. To examine more clearly the associations between the duration of these behaviours, the amount of time each sow spent in each activity during period 3 was plotted against the amount of time spent in the remaining two activities (Fig. 5). In general, sows that spent appreciable amounts of time rubbing against the bars of the cage spent almost zero time manipulating the drinker or rooting. In contrast, the majority of the sows that spent a large amount of time manipulating the drinker, also spent an appreciable
BEHAVIOUR
OF PIGS
1063
2ot
20
'
',; T S M E
o
ROGTENG
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\
_fIR
I 12o m a
' Q
-
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,om % TIM. r
.
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,
, 80
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lOO
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e
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so
iso
-~"oo
ROOTING
Fig. 5 Time spent in each activity by each sow during the half hour immediately after feeding; (a) percentage of time spent drinking versus percentage of time spent rooting; (b) percentage of time spent rubbing versus percentage of time spent drinking; (c) percentage of time spent rubbing versus percentage of time spent rooting.
1064
ANIMAL BEHAVIOUR,
amount of time rooting. The three exceptions to this are interesting. These sows spent an average of 41 ~ of the time drinking, yet less than 1 of the time rooting. However, the drinks taken were very frequent and of short duration, averaging 31 drinks per min. The remaining 6 sows that spent over 20 ~ of the time drinking, averaged only 1.7 drinks per min. Furthermore these rapid drinks tended to occur in fairly stereotyped sequences. During the period after feeding then, seven sows showed marked stereotypies, involving rubbing and manipulation of the drinker. The particular sequences were unique to each sow and appeared to be stable over several weeks. Multiple discriminant analysis was used to determine if these seven sows could be distinguished from the remaining 18 sows by the type of behaviour shown during the period immediately prior to feed delivery. Despite the small sample sizes some statistically significant differences were found. The two groups did not differ in terms of age, parity, or time in the tether. The sows showing stereotyped behaviour showed a higher frequency of head-waving (F=9.19, dr=l,23, P<0.01) and rubbing (F=8.36, df= 1,23, P<0.01) in period 2. They also showed a slightly higher frequency of bar-biting but this difference failed to reach significance (F=3.97, df= 1,23, P = 0.055). Discussion One point that clearly emerges from this study is that the different types of behaviours found in stereotypies have different associations with the feeding periods, supporting the findings of Blackshaw & McVeigh (t984). Global counts of such behaviour achieved by lumping all types may be obscuring important relationships. Rubbing the snout against the bars, manipulating the drinker, bar-biting, and head-waving were clearly adjunctive behaviours, associated with the feeding period. These could be classified as either terminal responses (bar-biting, rubbing, and head-waving) that occurred immediately prior to the delivery of food, or interim responses that occurred immediately after food delivery. Interim responses involved either long duration drinking combined with rooting, rapid short duration drinking, or rapid rubbing. The last two behaviours tended to occur in stereotyped sequences. Vacuum chewing and playing with the chain however, appeared to occur with equal frequency before and after feeding.
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Although aggressive behaviour has been induced as an interim activity by placing pigeons on a feeding schedule (Staddon 1977) there is little evidence that aggression in pigs is related to the feeding periods. However, this may be due to the fact that aggression is a fairly uncommon behaviour in confined sows and that aggression in acquainted pigs is not elicited by frustration (Arnone & Dantzer 1980). Of course, the discovery that some behaviours are associated with the feed period does not necessarily imply that they are schedule induced (Roper 1978). This can only be demonstrated by adequate experimental manipulation of the feeding schedule. However, the fact that adjunctive drinking in rats has been shown unequivocally to be schedule induced (Roper 1978), and the evidence of some polydipsia (excessive drinking) in these sows, does support this interpretation. The most plausible account of the terminal responses of rats and pigeons is that they are classically conditioned responses (Schwartz & Gamzu 1977; Staddon 1977). In this piggery, the movement of the food trolley causes considerable excitement in the animals, and it is during this period that bar-biting, nose rubbing, and head-waving occur most rapidly. Although the feeding schedule is not strictly a fixedinterval one, the range of feeding times is sufficiently narrow for the pigs to show considerable expectation as feeding time approaches. Any movement or sudden disturbance can provoke outbursts of these behaviours. This conditioning interpretation is supported by the finding that older pigs, which had the most experience with the feeding schedules, showed the greatest amount of the terminal responses. Schwartz & Gamzu (1977) argue that the particular types of behaviour shown as terminal responses on feeding and drinking schedules are components of the behaviour used in feeding and drinking respectively. The bar-biting and nosing seen in the pigs may be components of rooting that have become classically conditioned by the movement of the trolley. However, head-waving also occurs yet this is not a component of feeding in pigs. In addition, the actual topography of the behaviours is different from that of rooting and feeding movements. During bar-biting, the bar is taken deep into the sow's mouth, and the head is often moved rapidly to one side. Chewing movements, although they do occur, are by no means invariably present. The rubbing movements are rapid, and
RUSFIEN: STEREOTYPEDBEHAVIOUROF PIGS do not resemble the strong, slow nosing used in rooting. Finally, the behaviours are not directed to the actual 'conditioned stimulus', i.e. the trolley, as is the case in the studies reviewed by Schwartz & Gamzu (1977), but rather to the bars of the cage. As the food trolley moves around the piggery, the behaviour of the sows suggests that they are attempting to approach it. The sows often tread in the food trough and thrust the head through the bars of the cage. The terminal responses may be frustration responses resulting from the restraint of the sows by the tethering crate. This may explain why the occurrence of these behaviours increases with the degree of restraint of the animals (Jensen 1980; Vestergaard 1981). Barbiting also occurs just before defaecation or urination (Fraser 1975), which Vestergaard (1981) takes as further evidence of frustration. A more appropriate view of terminal responses is that it is general food motivation that becomes classically conditioned rather than specific terminal behaviours (Bindra 1974), which then result from the restraint imposed. The variety of explanations of the interim behaviours are far less satisfactory, none being able to account for all the properties of these behaviours (Staddon 1977; Roper 1980, 1981). Our understanding of interim behaviours comes mainly from studies of adjunctive drinking in rats or pigeons. The explanations often invoke specific thirst motivation (Roper t981). However, since such drinking takes time to learn (Staddon 1977) and is relatively insensitive to conditioned taste aversions (Hyson et al. 1981) it is unlikely to be post-prandial. The fact that other behaviours besides drinking can occur as interim activities also argues against this interpretation. Indeed the causal factors associated with feeding behaviour would seem to be of more relevance. Since adjunctive drinking does not occur when food is delivered on a truly random interval (Millenson et al. 1977), and since it can also be elicited by stimuli that signal the absence of food (Minor & Coulter 1982), it appears to result from the fact that when food is delivered on a schedule the consumption of the food signals a period of definite food absence. A common explanation is that the interim period, marked by the absence of the causal factors responsible for feeding, is a period during which alternative behaviours such as drinking, that are normally inhibited by feeding, can be
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safely performed (Staddon & Simmelhag 1971; Falk 1977; Staddon 1977; Rachlin 1982). However, this disinhibition theory does not account for the exaggerated nature of the drinking (Roper 1980). Furthermore, the long duration interim drinking for these pigs was accompanied by continued rooting behaviour, suggesting that interim drinking occurs in the presence rather than the absence of continued feeding motivation. Stereotyped chain pulling by pigs (Dantzer & Mormede 1981, 1983), and adjunctive drinking and wood chewing by rats (Roper & Crossland 1982) are facilitated by periods of prior food deprivation. In general, adjunctive drinking is typically seen in laboratory animals that have been deprived of food. Two mechanisms could explain this persistence of feeding behaviour. Firstly, feeding may involve positive feedback resulting in the persistence of food motivation, and feed-related behaviours (Toates 1980). In natural conditions the pig spends some 6-7 h in feeding and foraging (Signoret et al. 1975), while in intensive conditions the highly concentrated food is consumed in less than 10 min. Secondly, although the nutrient value of the concentrated food is not in doubt, there remains the question of whether it provides sufficient stomach bulk since stomach distension does play some role in switching off feeding (Bolles 1975; Toates 1980). Adding nonnutritive chopped straw to food does increase the amount of time the pigs spend lying down (Fraser 1975), the duration of which was actually reduced after feeding. This persistence of feeding motivation in the absence of any food, and the strong probability that food will not be forthcoming, may provide the crucial factors for the occurrence of long duration interim drinking, particularly where, due to the method of housing, the animals are forced into continued proximity to the area now devoid of food. However, for a number of pigs the post-food periods were not marked by persistent rooting. These pigs showed rapid drinking or rapid rubbing combined in stereotyped sequences, rather than prolonged drinking. That alternative interim behaviours can be exhibited is an interesting problem. The reduction in the occurrence of stereotypies that results from placing extra material such as straw into the environment has often been interpreted as indicating that stereotypies are a reaction to boredom. However, it is possible that the activities generated are simply alternative interim behaviours.
1066
ANIMAL
BEHAVIOUR,
A number of factors may affect the particular type of behaviour shown. The types of interim behaviour shown by rats is affected by the duration of the intervals between food deliveries (Roper 1978). However, the structure of the environment may also be an important factor. By placing young pigs on a fixed-interval food-delivery schedule, Dantzer & Mormede (1981, 1983) were able to induce interim chain pulling, but not drinking, arguing that for pigs, drinking was low on the 'hierarchy of needs'. However, the present study found far more interim drinking, while chain pulling did not appear to be related to food delivery. A more satisfactory explanation would involve the relative spatial position of the objects. In the Dantzer & Mormede study, the chain was hanging directly above the food trough, while in the pens in this study the tether chain was attached below the food trough, and to play with it the sow had to remove her head from the trough. However, the drinking nozzle was placed directly above the trough, and the sows could operate the drinker with the base of their snouts while keeping the mouth in the trough. The type of interim behaviour chosen by pigs also depends on the degree of arousal experienced while awaiting the delivery of food. In this piggery, a key factor appears to be the delay between the beginning of the movement of the food trolley, and when each pig actually receives food. It is during this period that intense excitement is evident, and the pigs that show the greatest amount of activity prior to the food delivery were most likely also to exhibit stereotyped behaviour after the food had finished. The reasons for the stereotypy are not clear. The delivery of reinforcement often leads to the d~velopment of stereotyped sequences of behav1our before the actual behaviour that is being reinforced (Schwartz 1980). However, if this were the factor responsible for these stereotypies then these behaviours should have been most apparent in the period before the delivery of food, which was not the case. These behaviours should have been most apparent in the pre-feed period, which was not the case. Stereotyped sequences tended to occur where behaviours were being performed rapidly, and this may be the crucial variable (Fentress 1976). As the nose and the mouth were the main body parts involved, this would result in considerable tactiIe sensory input. For pain sensations, a high degree of sensory activation actually results in a decrease in the number of signals reaching
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the brain (Melzack & Wall 1983). Possibly a similar 'gating' mechanism may exist whereby general arousal produced by the expectation of food delivery is reduced by high sensory input. There is a variety of evidence that the performmance of stereotypies can serve to regulate the level of arousal (Berkson 1967; Broom 1981). There is also evidence that the time periods associated with interim behaviours are aversive (Staddon 1977), so the causal factors present may not so much result in the production of specific behaviours but simply result in stress. The interim behaviours themselves may be learned means of coping with this stress, representing one of the animal's hierarchy of stress responses (McBride 1980). Both adjunctive drinking by rats (Brett & Levine 1979), and stereotyped chain pulling by pigs (Dantzer & Mormede 1981, 1983) appear to result in a reduction in plasma corticosteroid levels. Although the observed reduction in physiological stress measures as a result of behaviour may serve to define that behaviour as a 'coping strategy' (Levine et al. 1978) the question remains as to just how complete this coping is. In addition, it is not clear whether the animals that do not show stereotypies are not coping or are simply not stressed. Individual differences in the occurrence of these stereotypies need to be related to individual differences in the stress measures. Acknowledgments This research was partly funded by an Australian Pig Industries Research Commission grant to Professor G. McBride. I am very grateful to Mr B. Wilson and Mr J. McVeigh for providing facilities at the University of Queensland farm, Judith Blackshaw and John McVeigh for kindly providing me with a copy of their unpublished manuscript, Carol Petherick for helpful discussions, Peter Pamment and Fred Foenander for computing and technical assistance, and especially to Glen McBride for help at all stages of the research.
REFERENCES Arnone, J. & Dantzer, R. 1980. Does frustration induce aggression in pigs? AppI. Anim. Ethot., 6, 351-362. Berkson, G. 1967. Abnormal stereotyped acts. In: Comparative Psychopathology (Ed. by J. Zubin & H. F. Hunt), pp. 76-94. New York: Grune & Stratton. Bindra, D. 1974. A motivational view of learning, performance, and behaviour modification. Psychol. Rev., 81, 199-213. Blackshaw, J. K. & McVeigh, J. F. 1984. The behaviour of sows and gilts; housed in stalls, tethers and groups. In: Welfare and Pig Production: Proceed-
R U S H E N : STEREOTYPED BEHAVIOUR OF PIGS
ings of the Australian Society of Animal Production 15th Biennial Conference, Armidale, N.S.W. (Ed. by J. A. A. Gardner), pp. 83-85. Sydney: Pergamon Prsss. Bolles, R. C. 1975. Theory of Motivation. New York: Harper & Row. Brett, L. P. & Levine, S. 1979. Schedule-induced polydipsia suppresses pituitary adrenal activity in rats. J. comp. physiol. PsyehoI., 93, 946-956. Broom, D. M. 1981. The Biology of Behaviour. Cambridge: Cambridge University Press. Dantzer, R. & Mormede, P. 1981. Pituitary-adrenal consequences of adjunctive activities in pigs. Horm. Behav., 15, 386-395. Dantzer, R. & Mormede, P. 1983. De-arousal properties of stereotyped behaviour: evidence from pituitaryadrenal correlates in pigs. Appl. Anita. Ethol., 10, 233-244. Dawkins, M. 1980. Animal Suffering. New York: Chapman & Hall. Duncan, I. J. H. 1980. Can scientific research help in assessment of animal welfare? I n : Behaviour in Relation to Reproduction, Management and Welfare of Farm Animals (Ed. by M. WodzickaTomaszewska, T. N. Edey & J. J. Lynch), pp. 87-92. Armidale, New South Wales: University of New England. Duncan, I. J. H. & Wood-Gush, D. G. M. 1972. An analysis of displacement preening in domestic fowl. Anita. Behav., 20, 68-71. Falk, J. L. 1977. The origin and flmctions of adjunctive behaviour. Anita. Learn. Behav., 5, 325-335. Fentress, J. C. 1976. Dynamic boundaries of patterned behaviour: interaction and self organization. In: GrowingPoints in Ethology (Ed. by P. P. G. Bateson & R. A. Hinde), pp. 135-169. Cambridge: Cambridge University Press. Fraser, D. 1975. The effect of straw on the behaviour of sows in tether stalls. Anita. Prod., 21, 59-68. Hediger, H. 1950. Wild Animals in Captivity. London: Butterworths. Hyson, R. L., Sickel, J. L., Kulkosky, P. J. & Riley, A. L. 1981. The insensitivity of schedule-induced polydipsia to conditioned taste aversions: effect of amount consumed during conditioning. Anim. Learn. Behav., 9, 281-286. Jensen, P. 1980. The effect of confinement on the behaviour of dry sows--an ethological study. Uppsala: Faculty of Veterinary Medicine, Swedish University of Agricultural Sciences. Keiper, R. R. 1969. Causal factors of stereotypies in caged birds. Anita. Behav., 17, 114-119. Kiley-Worthington, M. 1977. Behavioural Problems of Farm Animals. London: Oriel Press. Levine, S., Weinberg, J. & Ursin, H. 1978. Definition of the coping process and statement of the problem. In: Psychobiology of Stress: A Study of Coping Men (Ed. by H. Ursin & S. Levine), pp. 3-21. New York: Academic Press. McBride, G. 1980. Adaptation and welfare at the mananimal interface. In: Behaviour in Relation to Reproduction, Management and Welfare of Farm Animals (Ed. by M. Wodzicka-Tomaszewska, T. N. Edey, & J. J. Lynch), pp. 195-198. Armidale, New South Wales: University of New England. Melzack, R. & Wall, P. 1983. The Challenge of Pain. Harmondsworth, Middx: Penguin. Meyer-Holzapfel, M. 1968. Abnormal behaviour in zoo animals. In: Abnormal Behaviour in Animals (Ed. by M. W. Fox), pp. 476-484. London: W. B. Saunders.
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Millenson, J. R., Allen, R. B. & Pinker, S. 1977. Adjunctive drinking during variable and random-interval food reinforcement schedules. Anita. Learn. Behav., 5, 285-290. Minor, T. R. & Coulter, X. 1982. Associative and postprandial control of schedule induced drinking: implications for the study of interim behaviour. Anita. Learn. Behav., 10, 455-464. Palya, W. L. & Zacny, J. P. 1980. Stereotyped adjunctive pecking by caged pigeons. Anita. Learn. Behav., 8, 293-303. Pamment, P. & Stephens, J. B. 1981. A multicharmel, multiobserver portable event recorder. Behav. Res. 2r lnstrum., 13, 732-734. Rachlin, H. 1982. Absolute and relative consumption space. Nebraska Syrup. Motiv., 29, 129-167. Ridley, R. M. & Baker, H. F. 1982. Stereotypy in monkeys and humans. Psychol. Med., 12, 61-72. Roper, T. J. 1978. Diversity and substitutability of adjunctive activities under fixed-interval schedules of food reinforcement. J. exp. Anal. Behav., 30, 83-96. Roper, T. J. 1980. 'Induced' behaviour as evidence of nonspecifie motivational effects. In: Analysis of MotivationalProcesses (Ed. by F. N. Toates & T. R. Halliday), pp. 221-228. London: Academic Press. Roper, T. J. 1981. What is meant by the term 'scheduleinduced' and how general is schedule induction. Anim. Learn. Behav., 9, 433-440. Roper, T. J. & Crossland, G. 1982. Schedule-induced wood-chewing in rats and its dependence on body weight. Anita. Learn. Behav., 10, 65-71. Schwartz, B. 1980. Development of complex, stereotyped behaviour in pigeons. J. exp. Anal. Behav., 33, 153-166. Schwartz, B. & Gamzu, E. 1977. Pavlovian control of operant behaviour. In: Handbook of Operant Behaviour (Ed. by W. K. Honig & J. E. R. Staddon), pp. 53-97. Englewood Cliffs, N. J.: Prentice Hail. Signoret, J. P., Baldwin, B. A., Fraser, D. & Hafez, E. S. E. 1975. The behaviour of swine. In: The Behaviour of Domestic Animals (Ed. by E. S. E. Hafez), pp. 295-329. London: Balli~re Tindall. Staddon, J. E. R. 1977. Schedule induced behaviour. In: Handbook of Operant Behaviour (Ed. by W. K. Honig & J. E. R. Staddon), pp. 125-152. Englewood Cliffs, N. J. : Prentice Hall. Staddon, J. E. R. & Simmelhag, V. L. 1971. The 'superstition' experiment: a reexamination of its implications for the principles of adaptive behaviour. Psyehol. Rev., 78, 3-43. Toates, F. M. 1980. Animal Behaviour: A Systems Approach. New York: John Wiley. Vestergaard, K. 1981. Influence of fixation on the behaviour of sows. In: The Welfare of Pigs (Ed. by W. Sybesma), pp. 16-30. The Hague: Martinus Nijhoff. Winer, B. J. 1971. Statistical Principles in Experimental Design. Sydney: McGraw-Hill Kogakusha. Wood-Gush, D. G. M. & Beilharz, R. G. 1983. The enrichment of a bare environment for animals in confined conditions. AppL Anita. Ethol., 10, 209-218. Yanofsky, R. & Markowitz, H. 1978. Changes in general behaviour of two mandrills (Papio sphinx) concomitant with behavioural testing in the zoo. Psyehol. Rec., 28, 369-373.
(Received 12 September 1983; revised 23 November 1983; MS. number: 2439)
STEREOTYPED BEHAVIOLrR, ADJUNCTIVE DRINKING AND THE FEEDING PERIODS OF TETHERED SOWS BY J. R U S H E N *
Animal Behaviour Unit, Psychology Department, University of Queensland, St. Lucia, Queensland, 4067, Australia Abstract. The behaviour of 25 tethered sows in an intensive piggery was observed for 1 h before and 1 h after the delivery of food to determine if behavioural stereotypies appeared as adjunctive behaviours. The different components of behavioaral stereotypies were found to have different associations with the feeding period. Head-waving, bar-biting, and rubbing the snout against the cage were most common before feeding, and were shown particularly by the older sows. Manipulating the drinker and, for some sows, rubbing were most common after. There was some evidence of polydipsia. Vacuum chewing, playing with the chain, and aggressive behaviours, however, did not appear to be associated with the feeding period. The last two behaviours occurred only rarely. Seven sows showed stereotyped sequences of rapid rubbing or rapid drinking after the detivery of food, and these sows showed more excitement before food was delivered. Rooting was common for the full hour after all food had been consumed, and occurred in conjunction with long duration drinking. I suggest that the occurrence of adjunctive drinking by sows results from the persistence of feeding motivation, perhaps because concentrated food does not provide sufficient stomach distension, combined with the knowledge that food will definitely not be forthcoming. Stereotyped sequences of behaviour may be a means of reducing the arousal generated by the expectation of food. Vestergaard 1981). These are most apparent in confined sows kept in stalls or tethers (Jensen 1980; Vestergaard 1981; Blackshaw & McVeigh, 1984). The occurrence of such behaviours has been used as an argument that the welfare of the animals is being disregarded in intensive husbandry systems, and their occurrence may be useftll in making behavioural assessments of the environments being designed for animals (Dawkins 1980; Duncan 1980). However, before this can be accomplished, the causal factors underlying these behaviours need to be more fully understood. Kiley-Worthington (1977) provides a brief review of the broad range of explanations that have been proposed for the occurrence of these behaviours. The addition of novel objects into an animal's cage has been found to reduce the occurrence of stereotypies shown by chimpanzees (Berkson 1967), mandrills (Yanofsky & Markowitz 1978), and canaries (Keiper 1969). However, environmental disturbances may actually increase their occurrence (Fentress 1976; Broom 1981). Stereotypies in pigs can be inhibited from occurring by the addition of straw (Fraser 1975) or sterilized earth (Wood-Gush & Beilharz 1983), which may indicate boredom or a lack of adequate sensory stimulation. Since the stereotypies of chickens can be induced by placing them in a frustrating situation (Duncan
Stereotyped behaviours are relatively invariant sequences of motor acts, repeated frequently, and having little apparent goal (Keiper 1969; Kiley-Worthington 1977; Dawkins 1980). These occur in a wide range of species in a wide range of behavioural contexts, and are often suspected of indicating some underlying pathology or welfare problem. A broad distinction can be drawn between stereotypies that result from social deprivation and abnormal rearing conditions and which are relatively stable in the face of a change of environment, and 'cage stereotypies' that are more dependent upon the immediate environment for their occurrence (Ridley & Baker 1982). Wild animals that are caged show a variety of movement stereotypies such as backward and forward pacing. These can be considered as indicating faults in the design of the environment, such as lack of space or a lack of suitable opportunities for a variety of activities (Hediger 1950; Meyer-Holzapfel 1968). Intensively-housed pigs exhibit a wide range of stereotyped and other unusual behaviours, such as biting or nosing of the bars of the pen, pulling on chains, head-waving, and high frequency 'vacuum' chewing (Fraser 1975; *Present address: School of Agriculture and Forestry, University of Melbourne, Parkville 3052, Victoria, Australia.
1059
1060
ANIMAL
BEHAVIOUR,
& Wood-Gush 1972) they may reflect the frustration of natural behaviour patterns in artificial environments, as occurs for tethered sows (Jensen 1980). However, Palya & Zacny (1980) have argued against explanations that invoke 'global' problems such as boredom on the grounds that many observed stereotypies ( i n pigeons) are associated with feeding periods and so may be forms of adjunctive behaviour, resulting from food being delivered on a fixed schedule (Staddon 1977). Stereotyped chain pulling can be induced in young pigs by placing them on a fixed-interval food-delivery schedule (Dantzer & Mormede 1981, 1983), suggesting that this behaviour is the porcine equivalent of the excessive drinking (polydypsia) often seen in rats when kept on similar food-delivery schedules. Jensen (1980) found that the naturally occurring stereotypies were most frequent an hour after feeding, suggesting that the occurrence of such behaviour in commercial piggeries results from the fact that food is typically delivered on a fixed-interval schedule. However, Fraser (1975) found stereotypies to occur most frequently before feed periods, and it seems that different forms of behaviour may be found before and after feeding (Blackshaw & McVeigh, 1984). Most animals show a variety of stereotypies, and not all may result from the same causal factors (Keiper 1969). Adjunctive and schedule-induced behaviours can be classified into 'terminal responses' that occur immediately prior to the delivery of food, 'interim responses' that occur immediately after food delivery, and 'facultative behaviours' that occur in the intermediate period (Staddon & Simmelhag 1971; Staddon 1977). Possibly the different types of stereotypies shown by pigs represent these different types of behaviour.
Methods Subjects Observations were made at the Pig Unit of the University of Queensland farm at Pinjarra Hills, Brisbane. This is an intensive, specific pathogen-free piggery, run on a commercial basis although its primary function is for teaching and research. The main building is a 56 m • 14 m metal-framed 'Big Dutchman' shed with a concrete floor, ventilated by natural air circulation through open side shutters and ceiling vents. It is composed of four sections:
32, 4
a research section, a mating section, a tethering section and a growing section. The 55 large white x landrace cross sows are placed in farrowing crates for 3-4 weeks until weaning, then mated and penned in stalls besides the boars for approximately 6 weeks. They are then moved to tethering crates for the remainder of the gestation period of up to 120 days. The tethering section (11 m • 14 m) has 44 tethering crates in four rows and contains, at any one time, 25-30 sows on average. The sows are tethered by the neck by a 65-cm chain to the base of the tethering crates. A food trough runs along the front of the crates, and food is provided twice a day at 0800-0830 hours and 14001430 hours, in the form of pellets. Delivery is made by a single worker pushing the food trolley around the entire piggery. Water is continuously available through a single push-operated nipple placed approximately 2 cm above the top of the food trough. Observations were made of the behaviour of 25 tethered sows. These pigs were not selected on any particular basis, except that they were in tethers at the time of the study. Sows showing marked stereotypies were deliberately included in the sample. The sows had a mean age of 26 months (sD=10.59), a mean parity of 3.08 (range 1-8) and had been in the tethering crates for an average of 67.08 days (sD=24.35).
Procedure A Sony Betamax SLF1E portable colour video recorder was set up with the camera placed 12 rain front of the sows. Two or three sows were filmed simultaneously. Recording commenced 1-1.5 h before the afternoon feed period, and continued for 3 h. To minimize the noted effect of external disturbance on the occurrence of stereotypies (Fentress 1976; Broom 1981), the observer left as soon as recording commenced, and only natural lighting was used. The video recordings of the two half-hour periods prior to the food delivery, and the two half-hour periods subsequent to feeding were scored for the occurrence of each of the behaviours described below, using a portable, multichannel event recorder (Pamment & Stephens 1981). The observation periods subsequent to feeding were taken as beginning 15 rain after the delivery of food, thus allowing adequate time for all of the food in the trough to be consumed. The data from the event recorder were fed (via an audio cassette interface) into a PerkinElmer 3210 computer, where the total frequency
RUSHEN: STEREOTYPED BEHAVIOUR OF PIGS of occurrence, and the total duration of each behaviour was computed. The following behaviours, including the basic body position of the sows, and the main behavioural components of the stereotypies were scored. (1) Body position: standing, sitting or lying. (2) Rooting: this included any nosing or licking the base of the food trough or the floor. Rooting was not scored if the drinker was activated even if the snout was in the food trough. (3) Chomping or 'vacuum chewing' (Vestergaard 1981): this included any chewing movement which did not involve an object in the mouth. This often occurred in bouts, and each individual instance where the sow visibly opened her mouth was recorded. (4) Rubbing: this category included the rubbing of any part of the head against the bars of the crate (except the drinker and the tethering chain) or the food trough. In actual fact, all observed instances of rubbing involved the snout, particularly the nose. As rubbing often occurred in bouts of rapid back and forth movement, only the occurrence of each bout was scored. (5) Bar-biting; this included any instance where some part of the tethering crate, excluding the chain or the drinker, was taken into the sow's mouth, whether or not chewing movements occurred. Each individual instance of bar biting was scored. (6) Drinking: this was scored when the sow activated the water nipple in any way, and therefore need not imply the actual consumption of water. This was necessary because sows develop unique methods of drinking, some holding the nipple open with the base of the snout while water is drunk out of the food trough. Only in some cases can the consumption of water be observed. (7) Any manipulation of the tethering chain using the snout or the mouth. (8) Head-waving (Fraser 1975): because of the difficulty of clearly separating the different types of head movement, this category comprised any horizontal head movement where the head is moved at least three-quarters of the width of the crate in a single movement. (9) Aggressive behaviour. Results
Each sow was scored according to the frequency of occurrence of chomping, bar-biting, and drinking, and the frequency of bouts of rubbing
1061
(per min), and the amount of time spent in each behaviour (percentage of total time) during each of the four periods. Chomping, head-waving, and aggressive behaviour occurred too rapidly to allow accurate measures of duration to be reliably made. Unfortunately, owing to various factors such as low light intensity and the sows' propensity to keep the mouth in or behind the trough, it was possible to score the frequency of chomping for only 16 sows in the two periods prior to feeding, and for only 11 sows in the two periods after feeding. For all measures, the distribution of scores exhibited a marked positive skew, with a large number of scores being zero. To overcome this problem, the scores were subjected to a logarithmic transformation (Winer 1971). One way repeated-measures analysis of variance tests were used to determine if the occurrence of the behaviours differed between the four periods. The results are shown in Table I. Sows spent a greater period of time lying down prior to feeding than after feeding, and a greater percentage of time rooting in the feed trough or on the floor after feeding (Fig. 1). Both the frequency and duration of bar-biting, and the frequency of head-waving were highest prior to feeding, particularly in the period immediately prior to feeding (Fig. 2). The movement of the food trolley around the piggery caused a great deal of excitement throughout the entire piggery, and bar-biting and head-waving were most frequent in the period from when this movement began until the sow actually received its food. Table I. Results of Analysis of Variance to Determine if the Occurrence of Each Behavinur Differed in the Four Time Periods*
Behaviour Lying down--duration Rooting--duration Chomping--frequency Rubbing--frequency Rubbing--duration Bar biting--frequency Bar biting--duration Drinking--frequency Drinking--duration Chain frequency Chain--duration Headwaving--frequency Aggression frequency
df
F
P
3,72 3.72 3,30 3,72 3,72 3,72 3,72 3,72 3,72 3,72 3,72 3,72 3,72
4.31 3.09 2.39 2.91 2.10 9.83 16.91 7.36 10.98 0.20 0.10 25.12 1.79
<0.01 <0.01 NS <0.05 NS <0.001 <0.001 <0.001 <0.001 Ns NS <0.001 Ns
*Periods 1 and 2 are the two half-hour periods before feeding and periods 3 and 4 are the two half-hour periods after.
ANIMAL
1062
BEHAVIOUR,
The frequency and duration of drinking were highest after feeding (Fig. 3). In some cases there was evidence ofpolydipsia. Two sows spent over 50 ~ of the hour after feeding manipulating the drinker, while a further five sows spent over 20 ~ of this time drinking. The frequency and duration of rubbing differed only slightly between the time periods. However, this was complicated by four sows who exhibited a very high frequency (J?=13.66/min) and duration (J?= 42.64 ~) of rubbing in the periods after feeding. The comparable figures for the remaining 21 sows are: frequency (J~= 0.26/min), and duration ()?= 0.69 ~). This rubbing tended to
32,
4
occur in stereotyped sequences. When these four sows were removed from the analysis both the frequency of rubbing (F= 14.50, df=3,60 P < 0.001), and the duration of rubbing (F= 5.66, df=3,60, P<0.001) differed between the time periods, with both measures being highest in the period immediately prior to feeding (Fig. 4). The measures of occurrence of playing with the chain, chomping, and aggressive behaviour D R I N K I N G (DURATICI~
DRINKING ( F R E Q U E N C Y )
p-
LYING
+
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1.5
r--
6r
z
i
I I
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a
2
3
4
1
2
3
4
PERIOD
20
2
3
4
1
2
3
PERIOD
J
Fig. 3. Average percentage of total time spent drinking and average frequency of drinking during each of the four periods. Periods 1 and 2 are the two half-hour periods before food delivery and periods 3 and 4 are the two halfhour periods after.
1,5
Fig. 1. Average percentage of total time spent lying down and rooting during each of the four periods. Periods 1 and 2 are the two half-hour periods before food delivery and periods 3 and 4 are the two half-hour periods after.
RUBBING
RUBBING
(DURATION)
(FREQUENCY)
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~E P"
.J
I BAR-BITING
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+
Z
o.s
I 1 2 3 4
1 2 3 4
1
34
2
1
2
3
4
PERIOD
PERIOD
Fig. 2. Average percentage of total time spent barbiting, and average frequency of bar-biting and headwaving during each of the four periods. Periods 1 and 2 are the two half-hour periods before food delivery and periods 3 and 4 are the two half-hour periods after.
Fig. 4. Average percentage of total time spent rubbing and average frequency of rubbing during each of the four periods. Periods 1 and 2 are the two half hour periods before food delivery and periods 3 and 4 and the two half hour periods after. The results from four sows which rubbed very frequently after feeding have been omitted.
RUSHEN:
STEREOTYPED
did not differ between the four time periods. Playing with the chain did not occur very frequently ()~=0.36/min) and did not involve much of the animals' time (_~---2.63 ~). Chomping occurred at an average rate o f 30.73 per rain. (N = 11), while the highest rate recorded was 81 bites per min in the half hour immediately after feeding. Only 69 instances of aggressive behaviour were seen during the 50 h of observation. To test the extent that the measures of frequency and duration of the behaviours were interrelated and stable across the feeding period, product-moment correlations (r) were calculated for each pair of measures in periods 2 and 3. Correlations were also calculated between these measures and the age, parity, and time in the tether of each of the sows. Measures of frequency and duration were significantly correlated for all behaviours. The age of the sow was correlated with the frequency of head-waving (r---0.61, P<0.01), the frequency of bar biting (r=0.68, P<0.01), and the duration of bar biting (r = 0.55, P < 0.01) in period 2. Parity was also significantly correlated with all of these but the correlations were smaller. The f r e q u e n c y of head-waving in period 2 was correlated with the frequency (r=0.59, P<0.01) and duration (r=0.57, P < 0 . 0 1 ) of bar-biting in period 2. Both the frequency of head-waving (r=0.45, P<0.05), and the frequency of bar-biting (r=0.61, P < 0 . 0 1 ) in period 2 were correlated with the frequency of drinking in period 3, but not with the duration of drinking. The only measures that were stable across the feeding period were the frequency (r---0.57, P<0.01) and duration (r=0.63, P = 0 . 0 1 ) of rubbing, and the frequency of playing with the chain (r=0.74, P < 0.01). The three activities in which sows spent a substantial amount of time after feeding were drinking, rubbing and rooting on the floor or in the feed trough. To examine more clearly the associations between the duration of these behaviours, the amount of time each sow spent in each activity during period 3 was plotted against the amount of time spent in the remaining two activities (Fig. 5). In general, sows that spent appreciable amounts of time rubbing against the bars of the cage spent almost zero time manipulating the drinker or rooting. In contrast, the majority of the sows that spent a large amount of time manipulating the drinker, also spent an appreciable
BEHAVIOUR
OF PIGS
1063
2ot
20
'
',; T S M E
o
ROGTENG
b
\
_fIR
I 12o m a
' Q
-
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.
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,
, 80
,
lOO
__
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e
z
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,
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so
iso
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Fig. 5 Time spent in each activity by each sow during the half hour immediately after feeding; (a) percentage of time spent drinking versus percentage of time spent rooting; (b) percentage of time spent rubbing versus percentage of time spent drinking; (c) percentage of time spent rubbing versus percentage of time spent rooting.
1064
ANIMAL BEHAVIOUR,
amount of time rooting. The three exceptions to this are interesting. These sows spent an average of 41 ~ of the time drinking, yet less than 1 of the time rooting. However, the drinks taken were very frequent and of short duration, averaging 31 drinks per min. The remaining 6 sows that spent over 20 ~ of the time drinking, averaged only 1.7 drinks per min. Furthermore these rapid drinks tended to occur in fairly stereotyped sequences. During the period after feeding then, seven sows showed marked stereotypies, involving rubbing and manipulation of the drinker. The particular sequences were unique to each sow and appeared to be stable over several weeks. Multiple discriminant analysis was used to determine if these seven sows could be distinguished from the remaining 18 sows by the type of behaviour shown during the period immediately prior to feed delivery. Despite the small sample sizes some statistically significant differences were found. The two groups did not differ in terms of age, parity, or time in the tether. The sows showing stereotyped behaviour showed a higher frequency of head-waving (F=9.19, dr=l,23, P<0.01) and rubbing (F=8.36, df= 1,23, P<0.01) in period 2. They also showed a slightly higher frequency of bar-biting but this difference failed to reach significance (F=3.97, df= 1,23, P = 0.055). Discussion One point that clearly emerges from this study is that the different types of behaviours found in stereotypies have different associations with the feeding periods, supporting the findings of Blackshaw & McVeigh (t984). Global counts of such behaviour achieved by lumping all types may be obscuring important relationships. Rubbing the snout against the bars, manipulating the drinker, bar-biting, and head-waving were clearly adjunctive behaviours, associated with the feeding period. These could be classified as either terminal responses (bar-biting, rubbing, and head-waving) that occurred immediately prior to the delivery of food, or interim responses that occurred immediately after food delivery. Interim responses involved either long duration drinking combined with rooting, rapid short duration drinking, or rapid rubbing. The last two behaviours tended to occur in stereotyped sequences. Vacuum chewing and playing with the chain however, appeared to occur with equal frequency before and after feeding.
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Although aggressive behaviour has been induced as an interim activity by placing pigeons on a feeding schedule (Staddon 1977) there is little evidence that aggression in pigs is related to the feeding periods. However, this may be due to the fact that aggression is a fairly uncommon behaviour in confined sows and that aggression in acquainted pigs is not elicited by frustration (Arnone & Dantzer 1980). Of course, the discovery that some behaviours are associated with the feed period does not necessarily imply that they are schedule induced (Roper 1978). This can only be demonstrated by adequate experimental manipulation of the feeding schedule. However, the fact that adjunctive drinking in rats has been shown unequivocally to be schedule induced (Roper 1978), and the evidence of some polydipsia (excessive drinking) in these sows, does support this interpretation. The most plausible account of the terminal responses of rats and pigeons is that they are classically conditioned responses (Schwartz & Gamzu 1977; Staddon 1977). In this piggery, the movement of the food trolley causes considerable excitement in the animals, and it is during this period that bar-biting, nose rubbing, and head-waving occur most rapidly. Although the feeding schedule is not strictly a fixedinterval one, the range of feeding times is sufficiently narrow for the pigs to show considerable expectation as feeding time approaches. Any movement or sudden disturbance can provoke outbursts of these behaviours. This conditioning interpretation is supported by the finding that older pigs, which had the most experience with the feeding schedules, showed the greatest amount of the terminal responses. Schwartz & Gamzu (1977) argue that the particular types of behaviour shown as terminal responses on feeding and drinking schedules are components of the behaviour used in feeding and drinking respectively. The bar-biting and nosing seen in the pigs may be components of rooting that have become classically conditioned by the movement of the trolley. However, head-waving also occurs yet this is not a component of feeding in pigs. In addition, the actual topography of the behaviours is different from that of rooting and feeding movements. During bar-biting, the bar is taken deep into the sow's mouth, and the head is often moved rapidly to one side. Chewing movements, although they do occur, are by no means invariably present. The rubbing movements are rapid, and
RUSFIEN: STEREOTYPEDBEHAVIOUROF PIGS do not resemble the strong, slow nosing used in rooting. Finally, the behaviours are not directed to the actual 'conditioned stimulus', i.e. the trolley, as is the case in the studies reviewed by Schwartz & Gamzu (1977), but rather to the bars of the cage. As the food trolley moves around the piggery, the behaviour of the sows suggests that they are attempting to approach it. The sows often tread in the food trough and thrust the head through the bars of the cage. The terminal responses may be frustration responses resulting from the restraint of the sows by the tethering crate. This may explain why the occurrence of these behaviours increases with the degree of restraint of the animals (Jensen 1980; Vestergaard 1981). Barbiting also occurs just before defaecation or urination (Fraser 1975), which Vestergaard (1981) takes as further evidence of frustration. A more appropriate view of terminal responses is that it is general food motivation that becomes classically conditioned rather than specific terminal behaviours (Bindra 1974), which then result from the restraint imposed. The variety of explanations of the interim behaviours are far less satisfactory, none being able to account for all the properties of these behaviours (Staddon 1977; Roper 1980, 1981). Our understanding of interim behaviours comes mainly from studies of adjunctive drinking in rats or pigeons. The explanations often invoke specific thirst motivation (Roper t981). However, since such drinking takes time to learn (Staddon 1977) and is relatively insensitive to conditioned taste aversions (Hyson et al. 1981) it is unlikely to be post-prandial. The fact that other behaviours besides drinking can occur as interim activities also argues against this interpretation. Indeed the causal factors associated with feeding behaviour would seem to be of more relevance. Since adjunctive drinking does not occur when food is delivered on a truly random interval (Millenson et al. 1977), and since it can also be elicited by stimuli that signal the absence of food (Minor & Coulter 1982), it appears to result from the fact that when food is delivered on a schedule the consumption of the food signals a period of definite food absence. A common explanation is that the interim period, marked by the absence of the causal factors responsible for feeding, is a period during which alternative behaviours such as drinking, that are normally inhibited by feeding, can be
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safely performed (Staddon & Simmelhag 1971; Falk 1977; Staddon 1977; Rachlin 1982). However, this disinhibition theory does not account for the exaggerated nature of the drinking (Roper 1980). Furthermore, the long duration interim drinking for these pigs was accompanied by continued rooting behaviour, suggesting that interim drinking occurs in the presence rather than the absence of continued feeding motivation. Stereotyped chain pulling by pigs (Dantzer & Mormede 1981, 1983), and adjunctive drinking and wood chewing by rats (Roper & Crossland 1982) are facilitated by periods of prior food deprivation. In general, adjunctive drinking is typically seen in laboratory animals that have been deprived of food. Two mechanisms could explain this persistence of feeding behaviour. Firstly, feeding may involve positive feedback resulting in the persistence of food motivation, and feed-related behaviours (Toates 1980). In natural conditions the pig spends some 6-7 h in feeding and foraging (Signoret et al. 1975), while in intensive conditions the highly concentrated food is consumed in less than 10 min. Secondly, although the nutrient value of the concentrated food is not in doubt, there remains the question of whether it provides sufficient stomach bulk since stomach distension does play some role in switching off feeding (Bolles 1975; Toates 1980). Adding nonnutritive chopped straw to food does increase the amount of time the pigs spend lying down (Fraser 1975), the duration of which was actually reduced after feeding. This persistence of feeding motivation in the absence of any food, and the strong probability that food will not be forthcoming, may provide the crucial factors for the occurrence of long duration interim drinking, particularly where, due to the method of housing, the animals are forced into continued proximity to the area now devoid of food. However, for a number of pigs the post-food periods were not marked by persistent rooting. These pigs showed rapid drinking or rapid rubbing combined in stereotyped sequences, rather than prolonged drinking. That alternative interim behaviours can be exhibited is an interesting problem. The reduction in the occurrence of stereotypies that results from placing extra material such as straw into the environment has often been interpreted as indicating that stereotypies are a reaction to boredom. However, it is possible that the activities generated are simply alternative interim behaviours.
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ANIMAL
BEHAVIOUR,
A number of factors may affect the particular type of behaviour shown. The types of interim behaviour shown by rats is affected by the duration of the intervals between food deliveries (Roper 1978). However, the structure of the environment may also be an important factor. By placing young pigs on a fixed-interval food-delivery schedule, Dantzer & Mormede (1981, 1983) were able to induce interim chain pulling, but not drinking, arguing that for pigs, drinking was low on the 'hierarchy of needs'. However, the present study found far more interim drinking, while chain pulling did not appear to be related to food delivery. A more satisfactory explanation would involve the relative spatial position of the objects. In the Dantzer & Mormede study, the chain was hanging directly above the food trough, while in the pens in this study the tether chain was attached below the food trough, and to play with it the sow had to remove her head from the trough. However, the drinking nozzle was placed directly above the trough, and the sows could operate the drinker with the base of their snouts while keeping the mouth in the trough. The type of interim behaviour chosen by pigs also depends on the degree of arousal experienced while awaiting the delivery of food. In this piggery, a key factor appears to be the delay between the beginning of the movement of the food trolley, and when each pig actually receives food. It is during this period that intense excitement is evident, and the pigs that show the greatest amount of activity prior to the food delivery were most likely also to exhibit stereotyped behaviour after the food had finished. The reasons for the stereotypy are not clear. The delivery of reinforcement often leads to the d~velopment of stereotyped sequences of behav1our before the actual behaviour that is being reinforced (Schwartz 1980). However, if this were the factor responsible for these stereotypies then these behaviours should have been most apparent in the period before the delivery of food, which was not the case. These behaviours should have been most apparent in the pre-feed period, which was not the case. Stereotyped sequences tended to occur where behaviours were being performed rapidly, and this may be the crucial variable (Fentress 1976). As the nose and the mouth were the main body parts involved, this would result in considerable tactiIe sensory input. For pain sensations, a high degree of sensory activation actually results in a decrease in the number of signals reaching
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the brain (Melzack & Wall 1983). Possibly a similar 'gating' mechanism may exist whereby general arousal produced by the expectation of food delivery is reduced by high sensory input. There is a variety of evidence that the performmance of stereotypies can serve to regulate the level of arousal (Berkson 1967; Broom 1981). There is also evidence that the time periods associated with interim behaviours are aversive (Staddon 1977), so the causal factors present may not so much result in the production of specific behaviours but simply result in stress. The interim behaviours themselves may be learned means of coping with this stress, representing one of the animal's hierarchy of stress responses (McBride 1980). Both adjunctive drinking by rats (Brett & Levine 1979), and stereotyped chain pulling by pigs (Dantzer & Mormede 1981, 1983) appear to result in a reduction in plasma corticosteroid levels. Although the observed reduction in physiological stress measures as a result of behaviour may serve to define that behaviour as a 'coping strategy' (Levine et al. 1978) the question remains as to just how complete this coping is. In addition, it is not clear whether the animals that do not show stereotypies are not coping or are simply not stressed. Individual differences in the occurrence of these stereotypies need to be related to individual differences in the stress measures. Acknowledgments This research was partly funded by an Australian Pig Industries Research Commission grant to Professor G. McBride. I am very grateful to Mr B. Wilson and Mr J. McVeigh for providing facilities at the University of Queensland farm, Judith Blackshaw and John McVeigh for kindly providing me with a copy of their unpublished manuscript, Carol Petherick for helpful discussions, Peter Pamment and Fred Foenander for computing and technical assistance, and especially to Glen McBride for help at all stages of the research.
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Millenson, J. R., Allen, R. B. & Pinker, S. 1977. Adjunctive drinking during variable and random-interval food reinforcement schedules. Anita. Learn. Behav., 5, 285-290. Minor, T. R. & Coulter, X. 1982. Associative and postprandial control of schedule induced drinking: implications for the study of interim behaviour. Anita. Learn. Behav., 10, 455-464. Palya, W. L. & Zacny, J. P. 1980. Stereotyped adjunctive pecking by caged pigeons. Anita. Learn. Behav., 8, 293-303. Pamment, P. & Stephens, J. B. 1981. A multicharmel, multiobserver portable event recorder. Behav. Res. 2r lnstrum., 13, 732-734. Rachlin, H. 1982. Absolute and relative consumption space. Nebraska Syrup. Motiv., 29, 129-167. Ridley, R. M. & Baker, H. F. 1982. Stereotypy in monkeys and humans. Psychol. Med., 12, 61-72. Roper, T. J. 1978. Diversity and substitutability of adjunctive activities under fixed-interval schedules of food reinforcement. J. exp. Anal. Behav., 30, 83-96. Roper, T. J. 1980. 'Induced' behaviour as evidence of nonspecifie motivational effects. In: Analysis of MotivationalProcesses (Ed. by F. N. Toates & T. R. Halliday), pp. 221-228. London: Academic Press. Roper, T. J. 1981. What is meant by the term 'scheduleinduced' and how general is schedule induction. Anim. Learn. Behav., 9, 433-440. Roper, T. J. & Crossland, G. 1982. Schedule-induced wood-chewing in rats and its dependence on body weight. Anita. Learn. Behav., 10, 65-71. Schwartz, B. 1980. Development of complex, stereotyped behaviour in pigeons. J. exp. Anal. Behav., 33, 153-166. Schwartz, B. & Gamzu, E. 1977. Pavlovian control of operant behaviour. In: Handbook of Operant Behaviour (Ed. by W. K. Honig & J. E. R. Staddon), pp. 53-97. Englewood Cliffs, N. J.: Prentice Hail. Signoret, J. P., Baldwin, B. A., Fraser, D. & Hafez, E. S. E. 1975. The behaviour of swine. In: The Behaviour of Domestic Animals (Ed. by E. S. E. Hafez), pp. 295-329. London: Balli~re Tindall. Staddon, J. E. R. 1977. Schedule induced behaviour. In: Handbook of Operant Behaviour (Ed. by W. K. Honig & J. E. R. Staddon), pp. 125-152. Englewood Cliffs, N. J. : Prentice Hall. Staddon, J. E. R. & Simmelhag, V. L. 1971. The 'superstition' experiment: a reexamination of its implications for the principles of adaptive behaviour. Psyehol. Rev., 78, 3-43. Toates, F. M. 1980. Animal Behaviour: A Systems Approach. New York: John Wiley. Vestergaard, K. 1981. Influence of fixation on the behaviour of sows. In: The Welfare of Pigs (Ed. by W. Sybesma), pp. 16-30. The Hague: Martinus Nijhoff. Winer, B. J. 1971. Statistical Principles in Experimental Design. Sydney: McGraw-Hill Kogakusha. Wood-Gush, D. G. M. & Beilharz, R. G. 1983. The enrichment of a bare environment for animals in confined conditions. AppL Anita. Ethol., 10, 209-218. Yanofsky, R. & Markowitz, H. 1978. Changes in general behaviour of two mandrills (Papio sphinx) concomitant with behavioural testing in the zoo. Psyehol. Rec., 28, 369-373.
(Received 12 September 1983; revised 23 November 1983; MS. number: 2439)