- Email: [email protected]
Does frustration induce aggression in pigs?
Applied Animal Ethology, 6 (1980) 351-362 0 Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
351
DOES FRUSTRATION INDUCE AGGRESSION IN PIGS?
MICHBLE
ARNONE and ROBERT
INRA, Station (France)
de Pharmacologic,
(Accepted for publication
DANTZER 180 chemin de Tournefeuille,
F-31300
Toulouse
24 October 1979)
ABSTRACT Arnone, M. and Dantzer, R., 1980. Does frustration induce aggression in pigs? Appl. Anim. Ethol., 6: 351-362. Behavioural and pituitary--adrenal responses of pairs of pigs to various competitive situations were investigated. Paired social encounters induced aggressive behaviour and increases in plasma corticosteroid levels in unacquainted pigs. Adreno-cortical activation was more marked in experienced than in inexperienced subordinate animals. Repeated food competition tests in an operant conditioning cage resulted in the development of stable dominance-subordinance relationships in pairs of pigs. Plasma corticosteroid levels were not influenced by the food competition test nor by social ranks. When no more food was delivered following operant responding (extinction), aggression developed between unacquainted pigs submitted by pairs to this aversive situation, but not in acquainted pigs. Adreno-cortical activation was observed only in pairs of unacquainted animals but, contrary to the paired social encounters, its occurrence did not depend on the presence of fighting. These experiments suggests that frustration induces aggression only when this behaviour has a minimal likelihood of occurrence under the experimental conditions studied. Moreover, the presence of a congener with which social bonds have been established plays a protective role against behavioural and physiological consequences of frustration.
INTRODUCTION
Frustration occurs when animals engaged in a sequence of behaviours are unable to complete it because there are physical and psychological obstacles in the environment (Hinde, 1970). Frustration is likely to be encountered in conditions of intensive husbandry because of restricted environment, pressures of social hierarchy and food availability. This psychological state is therefore believed to play a key role in the development of abnormal physiological and behavioural reactions observed in farm animals (WoodGush et al., 1975). However, little is known about the sensitivity of domestic species other than fowl (Duncan and Wood-Gush, 1972a,b) to frustration. There are several ways of inducing frustration. A common technique is to
352
subject animals previously trained to obtain food by operating a manipulandum in a Skinner box, to an extinction session in which no food reward is presented. They respond to this situation with behavioural and physiological changes typical of conflict situations (e.g. displacement activities, aggressive behaviour and activation of the pituitary-adrenal axis). Previous experiments demonstrate that pigs trained to get food by pushing a panel with their snout in a modified Skinner box are sensitive to physiological and functional consequences of extinction (Dantzer et al., 1980). Pigs exposed alone to the extinction situation display displacement activities such as rubbing the floor and the walls of the cage with their snout and scratching the floor with their feet. These activities were accompanied by escape attempts from the cage and pituitary-adrenal activation. When pigs were exposed by pairs to the extinction situation, they developed aggressive behaviour and fighting which were more severe when a partition prevented the animals from reaching the response panel and feeding area than when access was free. However, this last study used unacquainted pigs which already had a high probability of fighting when they were brought together (Fraser, 1974). In order to determine whether frustration induced by extinction of a food-reinforced response alone was able to induce aggression in pigs, behavioural and pituitary-adrenal responses of pairs of pigs to various competitive situations were investigated. The results suggest that frustration induces aggression only when this behaviour has a minimal likelihood of occurrence under the experimental conditions studied. GENERAL
METHODS
Three groups of four cross-bred pigs, castrated male and females, with liveweight ranging from 25 to 30 kg, were studied at about 3 months of age. They were housed in groups of four in an experimental piggery. Light was supplied from 7 a.m. to 8 p.m. Water was available ad libitum while food was rationed to about 4% of their body weight. The apparatus and experimental conditions have been described elsewhere (Dantzer et al., 1980). After a lo-day period of adaptation to the laboratory conditions, the subjects were individually trained to press a panel with their snout in order to get 5 g of a commercial granular feed as a reinforcement according to a continuous reinforcement schedule, i.e. one reinforcement for every panel press. Training all animals required two daily sessions. On the third day, they received the first of daily 20-min sessions on a continuous reinforcement schedule. The experiments began after stabilization of the performance, i.e. in the 4th week, and included two successive periods: food competition (Week 4 to Week 7) and extinction (Week 8 to Week 10). In the food competition sessions, two animals from the same pen were introduced together into the experimental cage during a 20-min continuous reinforcement session. From Week 8 to Week 10, all animals were submitted
353
by pairs of various compositions to extinction tests, i.e. with no food delivered. All conditioning sessions were run in the morning, at the same time of day, 5 days a week. Two paired encounter tests took place in mid-experimental periods, in the afternoon. To assess the pigs’ aversion to the experimental circumstances to which they were submitted, plasma corticosteroid levels were determined by a competitive protein binding method (Mormede and Dantzer, 1978). Before and 30 min after the completion of the experiment, 10 ml of blood was drawn from the vena cava. Plasma samples were obtained by centrifugation and frozen for biochemical assay. Blood collection was rapid enough to prevent a rise in the plasma corticiosteroid levels as a consequence of the sampling procedure. EXPERIMENT
I. SOCIAL
ENCOUNTERS
Bringing together pigs from different origins is known to induce aggressive behaviour. In a study of several pairs of pigs, Fraser (1974) recognized two distinct patterns of aggressive behaviour, one involving biting, and the other, less intense, involving butting and pushing. Biting predominated during the first encounters but was replaced by butting in acquainted animals. The first experiment was designed to delineate the variety of activities and physiological changes occurring in pigs submitted to paired social encounters. Methods
Pigs were moved, by pairs of animals from two different social groups, from the building in which they were housed to the experimental room, just before observations began. Observations were made in the afternoon on two occasions, every two weeks. Two of the pigs were put in a small pen (0.93 X 0.87 m), and an observer sat on a 2-m high platform from where he observed the behaviour of the two pigs for 20 min. Following this, pigs were returned to the piggery, the pen was cleaned and the next pair of pigs was brought in and observed. This procedure was repeated until all six pairs of pigs had been studied. On the second observation day, different pairs were formed with the same pigs. In each case, attempts were made to bring together pigs having no more than 2 -4 kg liveweight difference. No attention was paid to the sex of the experimental animals, since this factor had proven to be without effect (Fraser, 1974). During the observation periods, the experimenter made notes of all interactive behaviours by means of a keyboard connected to an event pen recorder. Smelling was scored when both pigs smelt one another. Pushing was scored when one pig pushed the other and when both pigs pushed each other for brief episodes. Biting was scored when one pig attempted to bite the
354
opponent, usually about the head and ears. Fighting was scored when two pigs vigorously engaged in mutual pushing and biting episodes. Running away and obstruction were scored when one pig deliberately avoided its partner, either by running away from it or by presenting it with its hindquarters. The dominant and the subordinate animals were noted in each pair. Results and discussion When the first two pigs were introduced into the pen there was smelling between animals. This was quickly followed by pushing and biting episodes. Fighting occurred in most cases. On occasions, one pig attempted to flee or to protect itself from the repeated attacks of the opponent by presenting it with its hind-quarters. The aggression observed in the second session tended to be more intense: fighting was more frequent (85% versus 50%) and lasted longer, but the difference did not reach significance (Table I). Plasma corticosteroid levels were significantly increased after the paired encounter test (Fig. 1). This effect was more marked in the second than in the first session. In the first session, final plasma corticosteroid levels were higher in pairs where fighting took place (2.53 + 0.35 pg/lOO ml versus 1.65 rt 0.16; F = 4.96; d.f. = 1,lO; P = 0.05). The same phenomenon occurred in the second session (3.19 + 0.31 pg/lOO ml versus 1.73 f 0.81; F = 3.61; d.f. = 1,lO; P < 0.10). Increases of plasma corticosteroid levels in subordinate animals in the second session could have been related to previous experiences, since five
;i $ =
0
Before
a
30 min after
t paired encounter test
e
0
n-12
(.....................
llZ6 Dominant
n-6 Subordinate
I
1st Session. . . . . . ..“..“..“..*~~....................
nr12
n-6 Dominant
n-6 Subordinate
2nd Session. . . . . . . . . . . . . . . . . . . . ..F
Fig. 1. Mean plasma corticosteroid levels of pigs submitted to paired encounter tests. Plasma corticosteroids were measured in blood samples taken before (blank columns) and 30 min after the completion of the experiment (dotted columns). Subordinate and dominant animals were identified according to their behaviour during the experimental session.
355
356
out of the six subjects were dominated in both period-paired encounter tests and dominance was achieved by more severe aggression on the second social encounter, After fighting episodes, victorious rats and mice have been shown to be more aggressive while defeated subjects become less aggressive (Ginsburg and Allee, 1942). These effects were even more marked when victories and defeats were incomplete (Leshner and Neck, 1976), which was to be expected in the present situation due to the space restriction which prevented the sub-dominant animal from fleeing and avoiding the dominant animal successfully. Similarly, increases in plasma corticosteroid levels are known to occur more easily in experienced than in inexperienced defeated mice (Bronson and Desjardins, 1971). EXPERIMENT
II. PAIRED
FOOD COMPETITIONS
Limited access to food in hungry animals usually results in aggressive interactions. Although their value is still debated (e.g. Richards, 1974; Syme, 1974; Drews and Wulczin, 1975), paired food competition tests are routinely used in the laboratory to assess dominance in experimental animals. The present experiment was initiated in order to investigate behavioural and physiological changes occurring in pairs of pigs submitted to food competition in an operant conditioning cage. Methods Pairs of pigs originating from the same social groups were introduced in the operant conditioning cage during daily 20-min sessions on a continuous reinforcement schedule. Fifteen sessions were allowed for stabilization of the dominance-subordinance relationship. The behaviour of each animal was noted by an observer by means of the same apparatus as in Experiment I. Two categories of behaviour were recognized: time spent controlling the feeding area and the number of times each pig pressed the response panel on the one hand, and aggressive interactions between the two members of each pair on the other hand. Blood samples were drawn from experienced pigs in the 16th session. Results and discussion The first sessions of food competition were characterized by high levels of aggression. A few sessions later, the pigs developed stable dominance-bordinance relationships. Aggressive behaviour at this stage consisted main!p of pushing and butting episodes. Little biting and no fighting were observed. Access to the feeding area could be obtained either by threats, i.e. aggressive interactions not involving physical contact, or by attacks accompanied in most cases by retaliations (Arnone, 1979). Plasma corticosteroid levels of experienced animals were not influenced by the food-competition
?
8 c F
0
Before
a
30min
after
’food ’
competition
n-6 Dominant
n-6 Subordinate
Fig. 2. Mean plasma corticosteroid levels of pigs submitted by pairs to a food competition session. Dominant animals had priority of access to the feeding area over subordinate animals.
test (F =
0.75; d.f. = 1,ll) (Fig. 2). Social rank did not influence initial and final plasma corticosteroid levels. This would indicate that subordinates had physiologically adapted to the situation and to their loss of status (Ely et al., 1974). EXPERIMENT
III. FRUSTRATION
Aggressive interactions observed in Experiment II might be related either to the restricted access to the feeding area imposed by the experimental conditions, or to frustration elicited by thwarted feeding behaviour because of the presence of the dominant pig. Frustration has been shown to enhance aggression in domestic fowl (Duncan and Wood-Gush, 1971), pigeons (Azrin et al., 1966), rats (Davis and Donenfeld, 1967; Thompson and Bloom, 1966) and squirrel monkeys (Hutchinson et al., 1968). This experiment investigated whether frustration elicited by non-reinforcement would induce aggression in pairs of pigs. Methods
Pairs of pigs were submitted to non-reinforcement, i.e. with no more food following operant responding. The first session of extinction took place after the last session of food competition and pairs of pigs which had developed a dominance-subordinance relationship in the food competition tests were used (Pairs A 1). The second session of extinction took place after exposure of individual pigs to continuous reinforcement schedules during 5 successive daily sessions. Pairs of pigs were formed with unacquainted animals from different social groups (Pairs B). Five days later, after four more food-reinforced sessions, extinction was induced in pairs of pigs from the same social
353
group but which had not been submitted together to the food competition tests (Pairs A 2). Blood samples were taken from pigs in Pairs A 1 and B only. Results and discussion With respect to the last session of food competition, all pairs submitted to extinction conditions displayed decreases in the time spent controlling the feeding area and the number of pushing episodes (Table II). However the number of biting episodes increased significantly in Pairs B and tended to decrease in Pairs A 1 and A 2. Fighting episodes occurred in three of the six Pairs B studied and were not observed in other experimental groups (Fisher’s exact test: P = 0.02). Plasma corticosteroid levels were measured in Pairs A 1 and B. In Pairs A 1, plasma corticosteroid levels were not modified by the extinction procedure (F = 1.93; d.f. = 1,ll) (Fig. 3). In pairs of unacquainted pigs, extinction induced large increases in plasma corticosteroid levels (F = 15.84; d.f. = 1,ll; P < 0.01). This increase was more marked in subordinate pigs than in dominant pigs (F = 7.25; d,f. = 1,lO; P < 0.05). Final plasma corticosteroid levels did not differ according to the presence or absence of fighting (3.57 + 0.44 pg/lOO ml versus 2.56 + 0.42 pg/lOO ml, respectively; F = 2.73; d.f. = 1,lO). Pigs have been shown to be sensitive to the effects of frustration elicited by the non-obtention of an expected food reward (Dantzer et al., 1980). When submitted individually to extinction conditions, they displayed dis0
&fore
m
36min after
Iextinction session
1
n-6 Dominant Pairs of acquainted animals
nr6 Subordinate
Pairs of unacquaintad animals
Fig. 3. Mean plasma corticosteroid levels of pigs submitted by pairs to extinction of an operant response for food. Acquainted pigs were from the same social group and bad previously developed a stable dominance-relationship in food competition tests. Unacquainted pigs were from different social groups. Subordinate and dominant animals were subsequently confirmed in a food-competition test.
Biting episodes
Pushing episodes
Control of feeding area (s)
(Z2)
(7?65;
1046 (945-1167)
Food comnetition test .
(0:36)
(3:16)
413 (244-565)
Pairs Al
Extinction
(0%)
(OJll)
310 (173-452)
Pairs A2
176 (O-366)
(OZ4)
161 (30-270)
Pairs B
H =
H =
8.05 (P < 0.05)
7.73 (P < 0.05)
H = 17.68 (P < 0.001)
Statistical comnarison (Kruskai-Wallis analysis of variance)
Effects of extinction on time spent controlling feeding area and aggressive interactions in pairs of acquainted (Al and A2) and unacquainted (B) pigs. Pairs Al were the same as those which had been submitted to food competition tests. Pairs A2 consisted of pigs from the same social group and Pairs B of pigs from different social groups. Extinction was induced by not rewarding panel presses with food. The mean value and the range of variation (in brackets) is given for each variable
TABLE II
360
placement activities and rises in plasma corticosteroid levels. The present experiment would indicate that the mere physical presence of a congener with which social bonds have been established plays a protective role against behavioural and physiological consequences of frustration. Little or no aggression was observed in pairs of acquainted pigs, and plasma corticosteroid levels remained low. Pairs of unacquainted pigs exposed to the extinction conditions developed aggressive behaviour and increases in plasma corticosteroid levels, which was in accordance with results of previous experiments (Dantzer et al., 1980). GENERAL
DISCUSSION
Aggressive interactions were observed mainly in three instances: paired encounter tests, food competition experiments, and extinction in pairs of unacquainted pigs. Little or no aggression developed in pairs of acquainted pigs submitted to the extinction conditions. Aggression may be defined as a response that delivers noxious stimuli to another organism (Buss, 1961). The use of this term has therefore mainly a descriptive value and does not imply any assumption of possible common origin and causes of aggressive acts. Aggression observed between two pigs brought together in a neutral environment had nothing in common with aggression occurring between pigs which had limited access to food. In the former case, familiarity with the partner was the main factor determining the result of social encounters (Fraser, 1974). In the latter case, familiarity between the two animals was already achieved and limited access to the feeding area, food motivation and individual social ranks were the predominant factors of variation (Arnone, 1979). Behavioural analysis did not allow differentiation between frustration-induced aggression and aggression observed in paired encounter tests. The lack of familiarity with the partner was, in both cases, the determining factor for aggression to occur. Differences between acquainted and unacquainted pigs submitted to extinction would indicate that as a rule aggression does not occur in frustrating situations. Frustration might be seen as a central motivational state which instigates a number of responses, one of which is aggression only when this behaviour has a minimal likelihood of occurrence under the experimental conditions, e.g. when two unacquainted pigs are brought together. Plasma corticosteroid levels increased only in paired encounter tests and in pairs of unacquainted pigs submitted to extinction, in spite of the fact that extinction per se activated the pituitary--adrenal axis in individual pigs (Dantzer et al., 1980). There are numerous studies suggesting that the stress of fighting stimulates the release of adreno-cortical steroids in a variety of rodent species (Brain, 1977). This effect is more pronounced in defeated animals, especially when they are subjected to repeated exposures to trained fighters. In the present experiments, adreno-cortical activation was more pronounced in fighting pairs than in non-fighting pairs of pigs submitted to
361
social encounters, but this was not the case for pairs of unacquainted pigs subjected to extinction. This would suggest that aggression observed in the latter situation did not share the same functional properties as aggression observed in paired encounter tests, and would point out a role of its own for frustration in the development of aggressive behaviour. Another point worth emphasizing is the homeostatic properties of established social hierarchies, demonstrated by the lack of adreno-cortical activation in pairs of acquainted pigs submitted to the extinction procedure. This is in contrast with the sharp adreno-cortical activation observed in pigs submitted either alone or in pairs of unacquainted animals to this aversive situation. The existence of social bonds is known to formalize the interactions between members of the same group and permit them to cope more easily with physical factors, e.g. cold (Mount, 1968). The results of the present experiments suggest that social organizations also enable members of a group to sustain emotional stimulation more efficiently. This would stress the necessity of husbandry techniques which allow for the development and keeping of stable and functional social orders. ACKNOWLEDGEMENTS
This work has received financial support from INRA, Recherches Veterinaires, and from DGRST (Grant No. 78-7-0681). The authors gratefully acknowledge the technical assistance provided by Mrs. N. Brunel and Ms. R.M. Bluthe.
REFERENCES Arnone, M., 1979. Etude Comportementale et Pharmacologique des Conduites Aggressives Chez le Port. These Doctorat 36 cycle, Universite Paul Sabatier, Toulouse. Azrin, N.H., Hutchinson, R.R. and Hake, D.F., 1966. Extinction induced aggression. J. Exp. Anal. Behav., 9: 191-204. Brain, P.F., 1977. Hormones and aggression. Annu. Res. Rev., 1: l-126. Bronson, F.H. and Desjardins, C., 1971. Steroid hormones and aggressive behavior in mammals. In: B. Eleftheriou and J. Scott (Editors), The Physiology of Aggression and Defeat. Plenum, London, pp. 43-64. Buss, A.H., 1961. The Psychology of Aggression. Wiley, New York. Dantzer, R., Arnone, M. and Mormsde, P., 1980. Effects of frustration on behaviour and plasma corticosteroid levels in pigs. Physiol. Behav., in press. Davis, H. and Donenfeld, I., 1967. Extinction induced social interaction in rats. Psychonom. Sci., 7: 65--86. Drews, D.R. and Wulczin, F.H., 1975. Measuring dominance in rats. Psychol. Rec., 25: 573-581. Duncan, I.J.H. and Wood-Gush, D.G.M., 1971. Frustration and aggression in the domestic fowl. Anim. Behav., 19: 500-504. Duncan, I.J.H. and Wood-Gush, D.G.M., 1972a. Thwarting of feeding behaviour in the domestic fowl. Anim. Behav., 20: 444-451. Duncan, I.J.H. and Wood-Gush, D.G.M., 1972b. An analysis of displacement preening in the domestic fowl. Anim. Behav., 20: 68-71.
362 Ely, D.L., Henry, J.P. and Ciaranello, R.D., 1974. Long-term behavioral and biochemical differentiation of dominant and subordinant mice in population cages. Psychosom. Med., 36: 463. Fraser, D., 1974. The behaviour of growing pigs during experimental social encounters. J. Agric. Sci., Cambridge, 82: 147-163. Ginsburg, B. and Allee, W.C., 1942. Some effects of conditioning on social dominance and subordination in inbred strains of mice. Physiol. Zool., 15: 485-506. Hutchinson, R.R., Azrin, N.H. and Hunt, G.M., 1968. Attack produced by intermittent reinforcement of a concurrent operant response. J. Exp. Anal. Behav., 11: 83-88. Hinde, R.A., 1970. Animal Behaviour. McGraw-Hill, New York. Leshner, A.I. and Neck, B.L., 1976. The effects of brief experience on agonistic responding. An expectancy theory interpretation. Behav. Biol., 17: 561-566. Mourn&de, P. and Dantzer, R., 1978. Pituitary-adrenal influences on avoidance behavior of pigs. Horm. Behav., 10: 285-297. Mount, L.E., 1968. The Climatic Physiology of the Pig. Edward Arnold, London. Richards, S.M., 1974. The concept of dominance and methods of assessment. Anim. Behav., 22: 914-930. Syme, G.J., 1974. Competitive orders as measures of social dominance. Anim. Behav., 22: 931-940. Thompson, T. and Bloom, W., 1966. Aggressive behavior and extinction-induced response rate increase. Psychonom. Sci., 5: 335-336. Wood-Gush, D.G.M., Duncan, I.J.H. and Fraser, D., 1975. Social stress and welfare problems in agricultural animals. In: E.S.E. Hafez (Editor), The Behaviour of Domestic Animals, Bailhere Tindall, London, pp. 182-200.
351
DOES FRUSTRATION INDUCE AGGRESSION IN PIGS?
MICHBLE
ARNONE and ROBERT
INRA, Station (France)
de Pharmacologic,
(Accepted for publication
DANTZER 180 chemin de Tournefeuille,
F-31300
Toulouse
24 October 1979)
ABSTRACT Arnone, M. and Dantzer, R., 1980. Does frustration induce aggression in pigs? Appl. Anim. Ethol., 6: 351-362. Behavioural and pituitary--adrenal responses of pairs of pigs to various competitive situations were investigated. Paired social encounters induced aggressive behaviour and increases in plasma corticosteroid levels in unacquainted pigs. Adreno-cortical activation was more marked in experienced than in inexperienced subordinate animals. Repeated food competition tests in an operant conditioning cage resulted in the development of stable dominance-subordinance relationships in pairs of pigs. Plasma corticosteroid levels were not influenced by the food competition test nor by social ranks. When no more food was delivered following operant responding (extinction), aggression developed between unacquainted pigs submitted by pairs to this aversive situation, but not in acquainted pigs. Adreno-cortical activation was observed only in pairs of unacquainted animals but, contrary to the paired social encounters, its occurrence did not depend on the presence of fighting. These experiments suggests that frustration induces aggression only when this behaviour has a minimal likelihood of occurrence under the experimental conditions studied. Moreover, the presence of a congener with which social bonds have been established plays a protective role against behavioural and physiological consequences of frustration.
INTRODUCTION
Frustration occurs when animals engaged in a sequence of behaviours are unable to complete it because there are physical and psychological obstacles in the environment (Hinde, 1970). Frustration is likely to be encountered in conditions of intensive husbandry because of restricted environment, pressures of social hierarchy and food availability. This psychological state is therefore believed to play a key role in the development of abnormal physiological and behavioural reactions observed in farm animals (WoodGush et al., 1975). However, little is known about the sensitivity of domestic species other than fowl (Duncan and Wood-Gush, 1972a,b) to frustration. There are several ways of inducing frustration. A common technique is to
352
subject animals previously trained to obtain food by operating a manipulandum in a Skinner box, to an extinction session in which no food reward is presented. They respond to this situation with behavioural and physiological changes typical of conflict situations (e.g. displacement activities, aggressive behaviour and activation of the pituitary-adrenal axis). Previous experiments demonstrate that pigs trained to get food by pushing a panel with their snout in a modified Skinner box are sensitive to physiological and functional consequences of extinction (Dantzer et al., 1980). Pigs exposed alone to the extinction situation display displacement activities such as rubbing the floor and the walls of the cage with their snout and scratching the floor with their feet. These activities were accompanied by escape attempts from the cage and pituitary-adrenal activation. When pigs were exposed by pairs to the extinction situation, they developed aggressive behaviour and fighting which were more severe when a partition prevented the animals from reaching the response panel and feeding area than when access was free. However, this last study used unacquainted pigs which already had a high probability of fighting when they were brought together (Fraser, 1974). In order to determine whether frustration induced by extinction of a food-reinforced response alone was able to induce aggression in pigs, behavioural and pituitary-adrenal responses of pairs of pigs to various competitive situations were investigated. The results suggest that frustration induces aggression only when this behaviour has a minimal likelihood of occurrence under the experimental conditions studied. GENERAL
METHODS
Three groups of four cross-bred pigs, castrated male and females, with liveweight ranging from 25 to 30 kg, were studied at about 3 months of age. They were housed in groups of four in an experimental piggery. Light was supplied from 7 a.m. to 8 p.m. Water was available ad libitum while food was rationed to about 4% of their body weight. The apparatus and experimental conditions have been described elsewhere (Dantzer et al., 1980). After a lo-day period of adaptation to the laboratory conditions, the subjects were individually trained to press a panel with their snout in order to get 5 g of a commercial granular feed as a reinforcement according to a continuous reinforcement schedule, i.e. one reinforcement for every panel press. Training all animals required two daily sessions. On the third day, they received the first of daily 20-min sessions on a continuous reinforcement schedule. The experiments began after stabilization of the performance, i.e. in the 4th week, and included two successive periods: food competition (Week 4 to Week 7) and extinction (Week 8 to Week 10). In the food competition sessions, two animals from the same pen were introduced together into the experimental cage during a 20-min continuous reinforcement session. From Week 8 to Week 10, all animals were submitted
353
by pairs of various compositions to extinction tests, i.e. with no food delivered. All conditioning sessions were run in the morning, at the same time of day, 5 days a week. Two paired encounter tests took place in mid-experimental periods, in the afternoon. To assess the pigs’ aversion to the experimental circumstances to which they were submitted, plasma corticosteroid levels were determined by a competitive protein binding method (Mormede and Dantzer, 1978). Before and 30 min after the completion of the experiment, 10 ml of blood was drawn from the vena cava. Plasma samples were obtained by centrifugation and frozen for biochemical assay. Blood collection was rapid enough to prevent a rise in the plasma corticiosteroid levels as a consequence of the sampling procedure. EXPERIMENT
I. SOCIAL
ENCOUNTERS
Bringing together pigs from different origins is known to induce aggressive behaviour. In a study of several pairs of pigs, Fraser (1974) recognized two distinct patterns of aggressive behaviour, one involving biting, and the other, less intense, involving butting and pushing. Biting predominated during the first encounters but was replaced by butting in acquainted animals. The first experiment was designed to delineate the variety of activities and physiological changes occurring in pigs submitted to paired social encounters. Methods
Pigs were moved, by pairs of animals from two different social groups, from the building in which they were housed to the experimental room, just before observations began. Observations were made in the afternoon on two occasions, every two weeks. Two of the pigs were put in a small pen (0.93 X 0.87 m), and an observer sat on a 2-m high platform from where he observed the behaviour of the two pigs for 20 min. Following this, pigs were returned to the piggery, the pen was cleaned and the next pair of pigs was brought in and observed. This procedure was repeated until all six pairs of pigs had been studied. On the second observation day, different pairs were formed with the same pigs. In each case, attempts were made to bring together pigs having no more than 2 -4 kg liveweight difference. No attention was paid to the sex of the experimental animals, since this factor had proven to be without effect (Fraser, 1974). During the observation periods, the experimenter made notes of all interactive behaviours by means of a keyboard connected to an event pen recorder. Smelling was scored when both pigs smelt one another. Pushing was scored when one pig pushed the other and when both pigs pushed each other for brief episodes. Biting was scored when one pig attempted to bite the
354
opponent, usually about the head and ears. Fighting was scored when two pigs vigorously engaged in mutual pushing and biting episodes. Running away and obstruction were scored when one pig deliberately avoided its partner, either by running away from it or by presenting it with its hindquarters. The dominant and the subordinate animals were noted in each pair. Results and discussion When the first two pigs were introduced into the pen there was smelling between animals. This was quickly followed by pushing and biting episodes. Fighting occurred in most cases. On occasions, one pig attempted to flee or to protect itself from the repeated attacks of the opponent by presenting it with its hind-quarters. The aggression observed in the second session tended to be more intense: fighting was more frequent (85% versus 50%) and lasted longer, but the difference did not reach significance (Table I). Plasma corticosteroid levels were significantly increased after the paired encounter test (Fig. 1). This effect was more marked in the second than in the first session. In the first session, final plasma corticosteroid levels were higher in pairs where fighting took place (2.53 + 0.35 pg/lOO ml versus 1.65 rt 0.16; F = 4.96; d.f. = 1,lO; P = 0.05). The same phenomenon occurred in the second session (3.19 + 0.31 pg/lOO ml versus 1.73 f 0.81; F = 3.61; d.f. = 1,lO; P < 0.10). Increases of plasma corticosteroid levels in subordinate animals in the second session could have been related to previous experiences, since five
;i $ =
0
Before
a
30 min after
t paired encounter test
e
0
n-12
(.....................
llZ6 Dominant
n-6 Subordinate
I
1st Session. . . . . . ..“..“..“..*~~....................
nr12
n-6 Dominant
n-6 Subordinate
2nd Session. . . . . . . . . . . . . . . . . . . . ..F
Fig. 1. Mean plasma corticosteroid levels of pigs submitted to paired encounter tests. Plasma corticosteroids were measured in blood samples taken before (blank columns) and 30 min after the completion of the experiment (dotted columns). Subordinate and dominant animals were identified according to their behaviour during the experimental session.
355
356
out of the six subjects were dominated in both period-paired encounter tests and dominance was achieved by more severe aggression on the second social encounter, After fighting episodes, victorious rats and mice have been shown to be more aggressive while defeated subjects become less aggressive (Ginsburg and Allee, 1942). These effects were even more marked when victories and defeats were incomplete (Leshner and Neck, 1976), which was to be expected in the present situation due to the space restriction which prevented the sub-dominant animal from fleeing and avoiding the dominant animal successfully. Similarly, increases in plasma corticosteroid levels are known to occur more easily in experienced than in inexperienced defeated mice (Bronson and Desjardins, 1971). EXPERIMENT
II. PAIRED
FOOD COMPETITIONS
Limited access to food in hungry animals usually results in aggressive interactions. Although their value is still debated (e.g. Richards, 1974; Syme, 1974; Drews and Wulczin, 1975), paired food competition tests are routinely used in the laboratory to assess dominance in experimental animals. The present experiment was initiated in order to investigate behavioural and physiological changes occurring in pairs of pigs submitted to food competition in an operant conditioning cage. Methods Pairs of pigs originating from the same social groups were introduced in the operant conditioning cage during daily 20-min sessions on a continuous reinforcement schedule. Fifteen sessions were allowed for stabilization of the dominance-subordinance relationship. The behaviour of each animal was noted by an observer by means of the same apparatus as in Experiment I. Two categories of behaviour were recognized: time spent controlling the feeding area and the number of times each pig pressed the response panel on the one hand, and aggressive interactions between the two members of each pair on the other hand. Blood samples were drawn from experienced pigs in the 16th session. Results and discussion The first sessions of food competition were characterized by high levels of aggression. A few sessions later, the pigs developed stable dominance-bordinance relationships. Aggressive behaviour at this stage consisted main!p of pushing and butting episodes. Little biting and no fighting were observed. Access to the feeding area could be obtained either by threats, i.e. aggressive interactions not involving physical contact, or by attacks accompanied in most cases by retaliations (Arnone, 1979). Plasma corticosteroid levels of experienced animals were not influenced by the food-competition
?
8 c F
0
Before
a
30min
after
’food ’
competition
n-6 Dominant
n-6 Subordinate
Fig. 2. Mean plasma corticosteroid levels of pigs submitted by pairs to a food competition session. Dominant animals had priority of access to the feeding area over subordinate animals.
test (F =
0.75; d.f. = 1,ll) (Fig. 2). Social rank did not influence initial and final plasma corticosteroid levels. This would indicate that subordinates had physiologically adapted to the situation and to their loss of status (Ely et al., 1974). EXPERIMENT
III. FRUSTRATION
Aggressive interactions observed in Experiment II might be related either to the restricted access to the feeding area imposed by the experimental conditions, or to frustration elicited by thwarted feeding behaviour because of the presence of the dominant pig. Frustration has been shown to enhance aggression in domestic fowl (Duncan and Wood-Gush, 1971), pigeons (Azrin et al., 1966), rats (Davis and Donenfeld, 1967; Thompson and Bloom, 1966) and squirrel monkeys (Hutchinson et al., 1968). This experiment investigated whether frustration elicited by non-reinforcement would induce aggression in pairs of pigs. Methods
Pairs of pigs were submitted to non-reinforcement, i.e. with no more food following operant responding. The first session of extinction took place after the last session of food competition and pairs of pigs which had developed a dominance-subordinance relationship in the food competition tests were used (Pairs A 1). The second session of extinction took place after exposure of individual pigs to continuous reinforcement schedules during 5 successive daily sessions. Pairs of pigs were formed with unacquainted animals from different social groups (Pairs B). Five days later, after four more food-reinforced sessions, extinction was induced in pairs of pigs from the same social
353
group but which had not been submitted together to the food competition tests (Pairs A 2). Blood samples were taken from pigs in Pairs A 1 and B only. Results and discussion With respect to the last session of food competition, all pairs submitted to extinction conditions displayed decreases in the time spent controlling the feeding area and the number of pushing episodes (Table II). However the number of biting episodes increased significantly in Pairs B and tended to decrease in Pairs A 1 and A 2. Fighting episodes occurred in three of the six Pairs B studied and were not observed in other experimental groups (Fisher’s exact test: P = 0.02). Plasma corticosteroid levels were measured in Pairs A 1 and B. In Pairs A 1, plasma corticosteroid levels were not modified by the extinction procedure (F = 1.93; d.f. = 1,ll) (Fig. 3). In pairs of unacquainted pigs, extinction induced large increases in plasma corticosteroid levels (F = 15.84; d.f. = 1,ll; P < 0.01). This increase was more marked in subordinate pigs than in dominant pigs (F = 7.25; d,f. = 1,lO; P < 0.05). Final plasma corticosteroid levels did not differ according to the presence or absence of fighting (3.57 + 0.44 pg/lOO ml versus 2.56 + 0.42 pg/lOO ml, respectively; F = 2.73; d.f. = 1,lO). Pigs have been shown to be sensitive to the effects of frustration elicited by the non-obtention of an expected food reward (Dantzer et al., 1980). When submitted individually to extinction conditions, they displayed dis0
&fore
m
36min after
Iextinction session
1
n-6 Dominant Pairs of acquainted animals
nr6 Subordinate
Pairs of unacquaintad animals
Fig. 3. Mean plasma corticosteroid levels of pigs submitted by pairs to extinction of an operant response for food. Acquainted pigs were from the same social group and bad previously developed a stable dominance-relationship in food competition tests. Unacquainted pigs were from different social groups. Subordinate and dominant animals were subsequently confirmed in a food-competition test.
Biting episodes
Pushing episodes
Control of feeding area (s)
(Z2)
(7?65;
1046 (945-1167)
Food comnetition test .
(0:36)
(3:16)
413 (244-565)
Pairs Al
Extinction
(0%)
(OJll)
310 (173-452)
Pairs A2
176 (O-366)
(OZ4)
161 (30-270)
Pairs B
H =
H =
8.05 (P < 0.05)
7.73 (P < 0.05)
H = 17.68 (P < 0.001)
Statistical comnarison (Kruskai-Wallis analysis of variance)
Effects of extinction on time spent controlling feeding area and aggressive interactions in pairs of acquainted (Al and A2) and unacquainted (B) pigs. Pairs Al were the same as those which had been submitted to food competition tests. Pairs A2 consisted of pigs from the same social group and Pairs B of pigs from different social groups. Extinction was induced by not rewarding panel presses with food. The mean value and the range of variation (in brackets) is given for each variable
TABLE II
360
placement activities and rises in plasma corticosteroid levels. The present experiment would indicate that the mere physical presence of a congener with which social bonds have been established plays a protective role against behavioural and physiological consequences of frustration. Little or no aggression was observed in pairs of acquainted pigs, and plasma corticosteroid levels remained low. Pairs of unacquainted pigs exposed to the extinction conditions developed aggressive behaviour and increases in plasma corticosteroid levels, which was in accordance with results of previous experiments (Dantzer et al., 1980). GENERAL
DISCUSSION
Aggressive interactions were observed mainly in three instances: paired encounter tests, food competition experiments, and extinction in pairs of unacquainted pigs. Little or no aggression developed in pairs of acquainted pigs submitted to the extinction conditions. Aggression may be defined as a response that delivers noxious stimuli to another organism (Buss, 1961). The use of this term has therefore mainly a descriptive value and does not imply any assumption of possible common origin and causes of aggressive acts. Aggression observed between two pigs brought together in a neutral environment had nothing in common with aggression occurring between pigs which had limited access to food. In the former case, familiarity with the partner was the main factor determining the result of social encounters (Fraser, 1974). In the latter case, familiarity between the two animals was already achieved and limited access to the feeding area, food motivation and individual social ranks were the predominant factors of variation (Arnone, 1979). Behavioural analysis did not allow differentiation between frustration-induced aggression and aggression observed in paired encounter tests. The lack of familiarity with the partner was, in both cases, the determining factor for aggression to occur. Differences between acquainted and unacquainted pigs submitted to extinction would indicate that as a rule aggression does not occur in frustrating situations. Frustration might be seen as a central motivational state which instigates a number of responses, one of which is aggression only when this behaviour has a minimal likelihood of occurrence under the experimental conditions, e.g. when two unacquainted pigs are brought together. Plasma corticosteroid levels increased only in paired encounter tests and in pairs of unacquainted pigs submitted to extinction, in spite of the fact that extinction per se activated the pituitary--adrenal axis in individual pigs (Dantzer et al., 1980). There are numerous studies suggesting that the stress of fighting stimulates the release of adreno-cortical steroids in a variety of rodent species (Brain, 1977). This effect is more pronounced in defeated animals, especially when they are subjected to repeated exposures to trained fighters. In the present experiments, adreno-cortical activation was more pronounced in fighting pairs than in non-fighting pairs of pigs submitted to
361
social encounters, but this was not the case for pairs of unacquainted pigs subjected to extinction. This would suggest that aggression observed in the latter situation did not share the same functional properties as aggression observed in paired encounter tests, and would point out a role of its own for frustration in the development of aggressive behaviour. Another point worth emphasizing is the homeostatic properties of established social hierarchies, demonstrated by the lack of adreno-cortical activation in pairs of acquainted pigs submitted to the extinction procedure. This is in contrast with the sharp adreno-cortical activation observed in pigs submitted either alone or in pairs of unacquainted animals to this aversive situation. The existence of social bonds is known to formalize the interactions between members of the same group and permit them to cope more easily with physical factors, e.g. cold (Mount, 1968). The results of the present experiments suggest that social organizations also enable members of a group to sustain emotional stimulation more efficiently. This would stress the necessity of husbandry techniques which allow for the development and keeping of stable and functional social orders. ACKNOWLEDGEMENTS
This work has received financial support from INRA, Recherches Veterinaires, and from DGRST (Grant No. 78-7-0681). The authors gratefully acknowledge the technical assistance provided by Mrs. N. Brunel and Ms. R.M. Bluthe.
REFERENCES Arnone, M., 1979. Etude Comportementale et Pharmacologique des Conduites Aggressives Chez le Port. These Doctorat 36 cycle, Universite Paul Sabatier, Toulouse. Azrin, N.H., Hutchinson, R.R. and Hake, D.F., 1966. Extinction induced aggression. J. Exp. Anal. Behav., 9: 191-204. Brain, P.F., 1977. Hormones and aggression. Annu. Res. Rev., 1: l-126. Bronson, F.H. and Desjardins, C., 1971. Steroid hormones and aggressive behavior in mammals. In: B. Eleftheriou and J. Scott (Editors), The Physiology of Aggression and Defeat. Plenum, London, pp. 43-64. Buss, A.H., 1961. The Psychology of Aggression. Wiley, New York. Dantzer, R., Arnone, M. and Mormsde, P., 1980. Effects of frustration on behaviour and plasma corticosteroid levels in pigs. Physiol. Behav., in press. Davis, H. and Donenfeld, I., 1967. Extinction induced social interaction in rats. Psychonom. Sci., 7: 65--86. Drews, D.R. and Wulczin, F.H., 1975. Measuring dominance in rats. Psychol. Rec., 25: 573-581. Duncan, I.J.H. and Wood-Gush, D.G.M., 1971. Frustration and aggression in the domestic fowl. Anim. Behav., 19: 500-504. Duncan, I.J.H. and Wood-Gush, D.G.M., 1972a. Thwarting of feeding behaviour in the domestic fowl. Anim. Behav., 20: 444-451. Duncan, I.J.H. and Wood-Gush, D.G.M., 1972b. An analysis of displacement preening in the domestic fowl. Anim. Behav., 20: 68-71.
362 Ely, D.L., Henry, J.P. and Ciaranello, R.D., 1974. Long-term behavioral and biochemical differentiation of dominant and subordinant mice in population cages. Psychosom. Med., 36: 463. Fraser, D., 1974. The behaviour of growing pigs during experimental social encounters. J. Agric. Sci., Cambridge, 82: 147-163. Ginsburg, B. and Allee, W.C., 1942. Some effects of conditioning on social dominance and subordination in inbred strains of mice. Physiol. Zool., 15: 485-506. Hutchinson, R.R., Azrin, N.H. and Hunt, G.M., 1968. Attack produced by intermittent reinforcement of a concurrent operant response. J. Exp. Anal. Behav., 11: 83-88. Hinde, R.A., 1970. Animal Behaviour. McGraw-Hill, New York. Leshner, A.I. and Neck, B.L., 1976. The effects of brief experience on agonistic responding. An expectancy theory interpretation. Behav. Biol., 17: 561-566. Mourn&de, P. and Dantzer, R., 1978. Pituitary-adrenal influences on avoidance behavior of pigs. Horm. Behav., 10: 285-297. Mount, L.E., 1968. The Climatic Physiology of the Pig. Edward Arnold, London. Richards, S.M., 1974. The concept of dominance and methods of assessment. Anim. Behav., 22: 914-930. Syme, G.J., 1974. Competitive orders as measures of social dominance. Anim. Behav., 22: 931-940. Thompson, T. and Bloom, W., 1966. Aggressive behavior and extinction-induced response rate increase. Psychonom. Sci., 5: 335-336. Wood-Gush, D.G.M., Duncan, I.J.H. and Fraser, D., 1975. Social stress and welfare problems in agricultural animals. In: E.S.E. Hafez (Editor), The Behaviour of Domestic Animals, Bailhere Tindall, London, pp. 182-200.