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Effect of social group size on aggressive behaviour between unacquainted domestic pigs
Applied Animal Behaviour Science 74 (2001) 203±215
Effect of social group size on aggressive behaviour between unacquainted domestic pigs Simon P. Turnera,*, Graham W. Horganb, Sandra A. Edwardsa,1 a
Scottish Agricultural College, Ferguson Building, Craibstone Estate, Bucksburn, Aberdeen AB21 9YA, UK b Biomathematics and Statistics Scotland, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK Accepted 19 June 2001
Abstract Domestic pigs (Sus scrofa) in small groups establish a dominance hierarchy using overt aggression and individual recognition. The impact of a large group size on group social organisation and aggression is poorly understood. The severity of aggression on mixing unacquainted pigs derived from large groups in which individual recognition may be impaired was studied and the implications for recognition of group members considered. Eight replicates of two group size treatments (20 versus 80) were used. After 6 weeks on treatment, a pair of pigs was introduced to a younger pair from an opponent pen in a barren arena. A total of 10 test pairs from each group were introduced to 10 opponent pairs from a group of 20 and 10 opponent pairs from a group of 80, giving 320 arena tests in total. Test duration was 5 min, but pigs which initiated a ®ght (rapid, persistent biting) were removed immediately. Pigs from groups of 80 displayed a lower frequency of aggressive acts (0.51 versus 0.90 S.E.D. 0.090 acts/pig/min) and initiated fewer ®ghts (19.7 versus 34.6 S.E.D. 3.62% of pigs, P < 0:01) in comparison with pigs from groups of 20. Aggression between pen mates accounted for a small amount of aggressive acts, and was unaffected by group size. Whilst retaining the ability to discriminate between pen mates and foreign pigs, pigs from large groups, therefore, displayed a marked reduction in aggressive tendency towards foreign individuals. # 2001 Published by Elsevier Science B.V. Keywords: Pig; Group size; Recognition; Aggression
* Corresponding author. Present address: Scottish Agricultural College, Sir Stephen Watson Building, Bush Estate, Penicuik, Midlothian EH26 0PH, UK. Tel.: 44-131-5353208; fax: 44-131-5353121. E-mail address: [email protected] (S.P. Turner). 1 Present address: Department of Agriculture, University of Newcastle, King George VI Building, Newcastle upon Tyne NE1 7RU, UK.
0168-1591/01/$ ± see front matter # 2001 Published by Elsevier Science B.V. PII: S 0 1 6 8 - 1 5 9 1 ( 0 1 ) 0 0 1 6 8 - X
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1. Introduction The social structure of wild Sus scrofa is centred on a small number of sows with their litters comprising of ®ve to six piglets each (von Gundlach, 1968). A clear and stable hierarchy exists between group members, where dominance rank is determined by a combination of sex, age, weight and strength (Mauget, 1981) and maintained through low intensity aggression and threats (McGlone, 1986). Under intensive commercial conditions, groups, typically of around 20 pigs, of very similar age and weight are penned at a high stocking density without the presence of more dominant adult animals. The mixing of unacquainted pigs, which is common in commercial practice, causes intense aggression which extends throughout the ®rst 24 h and results in a dominance hierarchy (Jensen and Wood-Gush, 1983; Fraser and Rushen, 1987). Aggression in commercial pig husbandry consequently presents a signi®cant cost to animal welfare and economic ef®ciency (e.g. Tan et al., 1991; Ayo et al., 1998). The number of commercial pigs housed in large groups of >50 members has increased signi®cantly in recent years (Penny, 1999). It has been suggested that the severity of aggression at introduction may increase in proportion to group size as a result of the escalating number of dyadic dominance relationships which must be established (Arey and Edwards, 1998). Casual observations would suggest, however, that very large groups of pigs, once established, can be maintained with minimal aggression (Bokma and Kersjes, 1988). However, the strategy of social organisation adopted in large groups is unknown (Wiepkema and Schouten, 1990; Arey and Edwards, 1998), and, without this knowledge, it is dif®cult to extrapolate the responses of pigs housed in small groups following the introduction of novel individuals to the large group context where the structure of social organisation may be markedly different. The ®rst purpose of this experiment was, therefore, to describe in detail the aggressive behaviour of pigs to novel conspeci®cs when derived from a small or large group. An assumption is made that the mixing of two unfamiliar animals, managed commercially, derived from small groups, and who are capable of recognising the other pig as from outwith their own group, would be expected to result in aggression in a high proportion of cases, as described by Erhard and Mendl (1997) and Erhard et al. (1997). Furthermore, the incorporation of a signi®cant liveweight difference between the two animals would encourage the display of aggression primarily by the larger pig (Erhard and Mendl, 1997). Recognition, at the level of group member/foreign pig discrimination and on an individual group member basis are pre-requisites for the functioning of a dominance hierarchy and without these abilities the establishment and maintenance of a dominance hierarchy would be untenable (Ewbank et al., 1974). The recognition capacity of the pig has not been adequately quanti®ed (Ewbank, 1976), but it is expected that at very large group sizes recognition will be impaired. The present experimental design does not allow a distinction to be made between the ability of pigs to perform group member/foreign pig discrimination and the individual recognition of all group members. The presence of either level of recognition would be accompanied by minimal aggression between pen mates, but the frequent expression of aggression towards foreign pigs (see D'Eath, 1996). However, in the absence of overt aggression when pigs are mixed, a failure to differentiate between pen mates and non-pen mates may be hypothesised (D'Eath and Keeling, 1998), even if no
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conclusion may be drawn regarding the recognition of pigs on an individual basis. The second purpose of the experiment was to interpret the aggressive responses of pigs in large groups as an indicator of the presence or absence of group member/foreign pig discrimination as a measure of a basic level of conspeci®c recognition. 2. Methods 2.1. Experimental design Domestic Large White Landrace growing pigs (start weight 29.3 S.E.M. 0.19 kg) were housed in groups of 20 or 80. The design of two treatments was replicated eight times using a total of 800 pigs. Animals were weaned at 4 weeks, fed a dry pelleted diet ad libitum (20% crude protein, 5% crude ®bre, 1.2% lysine, 14.2 MJ DE/kg), had ad libitum access to water and were housed on deep straw bedding. Fresh straw was provided daily and soiled litter was removed at 4-week intervals. A ¯oor space allowance of 0.88 m2 was provided per pig and ambient temperature was recorded at 1.5 m above ¯oor height. The mean minimum (12.4 S.E.M. 0.458C) and maximum (16.6 S.E.M. 0.398C) daily ambient temperature were similar in the two group sizes (P > 0:05). Ventilation was via an automatically controlled natural ventilation system and arti®cial light was provided constantly in addition to natural daylight. The management procedures and housing conditions experienced before introduction to the experiment were similar for all pigs. 2.2. Arena test procedure On day 41 post-mixing (during the 6th week) pen mates were introduced, in randomly chosen pairs, into an arena (test pigs). Simultaneously a younger pair of pen mates from a different pen, unacquainted with the test pigs and also randomly paired, were introduced at the diagonally opposite corner of the enclosure (opponent pigs). All instances of aggressive behaviour were recorded in the manner described below. Animals were introduced in group-mate pairs to avoid the repeated escape attempts demonstrated by pigs introduced alone, as observed in an earlier pilot study. Due to practical constraints, the duration between group formation at the start of the experimental period (day 0) and the time when animals were used as opponent pigs varied from 3 to 5 weeks. Opponent pigs were not weighed immediately before testing. However, it is possible to estimate their approximate weight from that measured at 3 (41.0 S.E.M. 0.41 kg) and 6 (55.9 S.E.M. 0.69 kg) weeks as growth rate varies little between these two points (Whittemore, 1993). On this basis, opponent pigs were used within a liveweight range of 41.0±50.9 kg. The opponent pig liveweight was, therefore, between 73.3 and 91.1% of that of the test pigs. Test pigs were subjected to two, randomly ordered, sessions of arena tests. In one session, 10 arena tests were performed using a total of 20 test pigs (from either group size) and 20 opponent animals from a group of 20. In the other session, the same 20 test pigs were tested against 20 opponent pigs from a group of 80. Opponent pigs were,
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consequently, used in one test only. Due to practical limitations, it was necessary for test pigs to be ®rst used as opponent pigs. Therefore, all pigs which were exposed to the arena tests were used once as opponent pigs during the period of weeks 3±5 and later as test pigs during each of sessions one and two in week 6. The number of times a pig was used as an opponent or a test animal was the same for both group sizes. 2.3. Arena layout The arena comprised a barren indoor enclosure with a solid concrete, unbedded ¯oor and without additional objects. Outwith test days, no pig entered the arena, was able to see it or was penned immediately adjacent to it. The enclosure measured 7 m 5 m and two solid gates were positioned at diagonally opposite corners (Fig. 1). Handling areas of 2:0 m 1:5 m dimensions secured a pair of animals near to each of the two arena entrances thereby allowing all four animals to be introduced simultaneously (Fig. 1). Pigs were housed as a group of 20 pen mates, for a maximum duration of 1 h in holding pens prior to testing. 2.4. Aggressive behaviour parameters On the simultaneous entry of test and opponent pigs into the arena, a stop watch was started. The frequency of occurrence of aggressive behaviours was recorded real time by a
Fig. 1. Plan of arena layout showing holding pens, observer location and arena access points; all walls were of solid blockwork; darkest shading represents gates or barriers.
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Table 1 Ethogram of categories of aggressive acts and responses used in arena testsa Behaviour
Description
Push
Aggressor presses shoulders against body of recipient for a minimum duration of 1 s; pushing is terminated when physical contact is lost; lunges made during bouts of pushing are recorded as single or multiple lunges as defined below; recipient may or may not respond Aggressor lunges head and shoulders towards recipient with mouth open or closed; physical contact may or may not be made; the aggressor does not initiate another attack within 2 s As above, aggressor repeats action one or more times with a delay of <2 s between each Aggressor pursues retreating recipient for a minimum of 2 m; mouth may be open or closed and physical contact may or may not be made; the chase is terminated when pursuit is suspended for 2 s or more Rapid and persistent biting in which bites are repeated with a delay of <1 s between each and the aggressive bout lasts not <2 s. Physical injury is typically inflicted on the recipient. The recipient may or may not respond Following aggression the recipient fails to retaliate or retreat; recipient continues with previous behaviour Recipient acts within 2 s to move away from the vicinity of the aggressor; a distance of 2 m or more must be traversed and the aggressor may or may not pursue
Single lunge Multiple lunge Chase Fight Ignore Retreat
a With the exception of the chase, ignore or retreat categories, the recipient may or may not respond to the aggression.
single observer throughout, but whom was not blind to the treatments. Duration of aggressive behaviour were not recorded. Aggressive behaviour was categorised as `push', `single lunge', `multiple lunge', `chase' or `®ght' (Table 1). The recipient's response was recorded as `retreat', `no response', `push', `single lunge', `multiple lunge', `chase' or `®ght'. The aggression categories selected were those used by Turner et al. (1999). Push coincided closely with the de®nitions of parallel and inverse parallel pressing detailed in Jensen (1983) and the de®nition of pushing given by McGlone (1985). Similarly, a single lunge may be viewed as synonymous with a head-to-body or head-to-head knock as de®ned by Jensen (1983). The aggressor was de®ned as the pig which initiated aggression in a single initiator/ responder sequence (i.e. one aggressive act followed by one recipient response). Where several aggressive acts/recipient response interactions occurred sequentially, the aggressor was the pig which initiated a new initiator/recipient sequence. For example, the sequence of behaviours; A single lunges, B pushes; B ®ghts, A retreats would be recorded as A (aggressor) single lunges; B (recipient) pushes; B (aggressor) ®ghts; A (recipient) retreats. Where behavioural transitions occurred (e.g. B (recipient) pushes; B (aggressor) ®ghts) no time delay was necessary between the response and the initiation of a new aggressive act. Where no activity transition took place (e.g. A (aggressor) single lunges, B (recipient) pushes; A (aggressor) single lunges, B (recipient) pushes) the de®nitions of bouts provided in Table 1 describe when one bout ended and a new one began. Where aggression developed into a ®ght, the stop watch was paused, the initiator of the aggressive bout was removed immediately by a separate observer and the stop watch
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allowed to continue. The initiator pig was removed irrespective of whether it attacked the recipient with a ®ght (A ®ghts B, B responds) or, more rarely, the recipient retaliated to a lower level of aggression using a ®ght (e.g. A multiple lunges, B ®ghts). The test was terminated when either both test or both opponent pigs had been removed following the initiation of ®ghts, excessive harassment or mounting occurred or 5 min duration had elapsed. Excessive harassment was de®ned as the continued following of a pig by another individual lasting for 2 min and resulting in the continued withdrawal of the recipient pig. In practice, the recipient pig frequently vocalised and showed persistent escape attempts (jumping of the forelegs against a pen division). Excessive mounting was de®ned as 10 mounting attempts when the actors forelegs were raised over the recipient pigs back. On termination of a test, opponent pigs were returned to their home pen and test pigs were returned to their holding pen for use in session two. 2.5. Measurements The effects of test pig group size, opponent pig group size and their interactions on test pig frequency and intensity of aggression were assessed using the following criteria. `Initiation' refers to the act of being an aggressor in an encounter. 2.5.1. Duration until aggression Duration until the ®rst aggressive act (i) and ®rst ®ght (ii) initiated by either pen mate. 2.5.2. Incidence of fights 1. Percentage of pigs removed for initiating a ®ght. 2. Percentage of tests where the first fight was initiated by a test pig. 2.5.3. Frequency of aggression 1. Number of aggressive acts per pig per minute. Where animals were removed due to ®ghting, the rate of aggression was corrected for the time they were present in the arena. 2. Percentage of tests where no aggression was shown by either pen mate. 3. Percentage of tests in which aggression occurred between two pen mates. 2.5.4. Severity of aggression 1. Frequency of pushes, single lunges, multiple lunges, chases or ®ghts as a percentage of all aggressive bouts. 2. Percentage of all responses to aggression which were categorised as ignore, retreat, push, single lunge, multiple lunge, chase or fight. 2.6. Statistical analysis As the pen was used as the statistical unit (n 16), a pen mean value for the above variables was calculated for each observation session. All variables were analysed using split plot analyses of variance with group size in the main plot stratum (pen of origin of test
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pigs) and opponent group size in the subplot stratum (session). The distribution of the datasets in each case was examined for normality and square root transformations were performed where necessary. Since the time following mixing at which the opponent pigs were used varied between treatments (between 3 and 5 weeks), opponent pig week following mixing was included as a covariate in those analyses in which it had a signi®cant in¯uence. 3. Results It was necessary to end a test or remove a pig due to excessive harassment in four tests and for persistent mounting in 10 tests. 3.1. Duration until aggression 1. The duration until the first instance of aggression shown by a test pig tended to be lower when the test pigs were from a group of 20 than 80 (Table 2). In addition the duration was lower when the opponent pigs were from a group of 20 (Table 2). 2. In those arena tests in which fights occurred, the duration until the first fight initiated by a test pig was significantly lower when the test pigs were from a group of 20 (Table 2). The duration until the first fight initiated by a test pig tended to be reduced when the opponent pigs were also from a group of 20 (Table 2). Test and opponent pig group sizes did not significantly interact to affect the duration until the first fight initiated by a test pig. 3.2. Incidence of fights 1. A significantly greater percentage of test pigs from groups of 20 were removed from the arena after initiating a fight than were test pigs from groups of 80 (Table 2). Similarly, when the opponent pigs were derived from a group of 20 the percentage of test pigs removed was significantly higher than when the opponent pigs were from a group of 80 (Table 2). Test pig group size and opponent pig group size did not significantly interact to affect the percentage of test pigs removed. 2. Test pigs derived from groups of 20 tended to be responsible for initiating a greater percentage of the first fights which developed following introduction than did test pigs from groups of 80 (Table 2). 3.3. Frequency of aggression 1. Test pigs from groups of 20 initiated a greater number of aggressive behaviours per minute than test pigs from groups of 80 (Table 3). 2. Pairs of test pigs housed in groups of 80 failed to display any aggression during a greater percentage of arena tests than did test pigs from groups of 20 (Table 3). 3. No significant differences occurred between treatments in the percentage of arena tests in which aggression between the two test pigs was observed (Table 3). The number of
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Main effects T pig group size
Time until first aggression (s) Time until first fight (s) Pigs removed for initiating fights (%) Tests where T pigs showed first fight (%) a
S.E.D. O pig group size 20
S.E.D.
20
80
47.2 96.2 34.6 81.4
69.1 10.76 50.2 66.1 7.35 173.8 18.05 118.2 151.8 16.60 19.7 3.62 34.4 19.9 3.45 62.6 8.37 69.2 74.7 9.79
Interactions
Significance
T 20, T 20, T 80, T 80, S.E. O 20 O 80 O 20 O 80
T
O
80
T: test pigs, O: opponent pigs, T O: test opponent pig group size interaction.
43.0 93.6 41.7 78.5
51.4 98.7 27.5 84.2
57.4 80.9 7.35 P 0.072 142.8 204.8 16.60 P < 0.01 27.1 12.3 3.45 P < 0.01 60.0 65.1 9.79 P 0.051
P 0.051 P 0.066 P 0.001
TO
S.P. Turner et al. / Applied Animal Behaviour Science 74 (2001) 203±215
Table 2 Duration until aggression and incidence of fights for test and opponent pigs under the four combinations of test and opponent pig group sizes and group size main effectsa
Main effects T pig group size 20 Frequency of aggressive acts (acts/pig/min) Tests where no aggression was shown by either pig (%) Tests where aggression occurred between pen mates (%) a b
0.90
Interactions S.E.D.
80 0.51
O pig group size 20
Significance
S.E.D.
T 20, O 20
T 20, O 80
T 80, O 20
T 80, O 80
S.E.
T
O
TO
80
0.090
0.74
0.68
0.083
0.92
0.89
0.56
0.47
0.083
P < 0.01
3.1 a
2.6 a
10.1 ab
12.9 b
2.00
P < 0.01
27.7
28.6
6.30
2.9
11.5
3.22
6.6
7.7
2.00
25.3
30.5
7.62
24.3
31.5
6.30
T: test pigs, O: opponent pigs, T O: test opponent pig group size interaction. Different letters indicate a significant difference between means.
23.9
26.8
P < 0.05
S.P. Turner et al. / Applied Animal Behaviour Science 74 (2001) 203±215
Table 3 Frequency of aggressive acts for test and opponent pigs under the four combinations of test and opponent pig group sizes and group size main effectsa,b
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aggressive acts directed at a pen mate expressed as a percentage of all aggressive acts was similar for the two test pig group sizes (10.1 versus 14.6 S.E.D. 1.93% for groups of 20 and 80 respectively, P > 0:05). 3.4. Severity of aggression 1. With the exception of fights, the percentage of all aggressive bouts initiated by a test pig which was of each severity category showed no significant effects of treatment. Chases were excluded from the analysis because their incidence was too low to allow a meaningful comparison. Fights contributed to a greater percentage of the total aggression shown by test pigs when the opponent pigs were derived from a group of 20 than 80 (17.6 versus 7.6 S.E.D. 3.75% of total aggressive occurrences, P < 0:05). 2. Test pigs responded by using a fight to aggressive acts initiated by an opponent pig more often when the opponent pig group size was 20 than 80 (9.2 versus 4.4 S.E.D. 1.98% of all responses, respectively, P < 0:05). Again chases were excluded from the analysis. 4. Discussion On the introduction of two pairs of pigs from different pens, pigs derived from groups of 20 showed aggressive behaviour signi®cantly more rapidly, demonstrated aggression in more tests, gave aggression at a faster rate and initiated ®ghts more rapidly and on signi®cantly more occasions than did pigs from groups of 80. All pigs used in the arena tests, irrespective of group size, were ®rst used as opponent animals between weeks 3 and 5 post-mixing and subsequently as test pigs during each of two sessions during week 6. Animals tested during week 6 had experience of the testing location, and the amount of experience was the same for pigs derived from groups of 20 and 80. Previous experience of the testing location may have encouraged a degree of territorial aggression from the test pigs (see van Putten and van de Burgwal, 1990), but this would have been equivalent for pigs from both group size treatments. The greater liveweight of the test pigs compared to the opponent pigs is likely to have conferred an advantage on the test animals and made them more con®dent in instigating aggression (Jensen et al., 1996; Erhard and Mendl, 1997). Again, however, this in¯uence was similar for the two group sizes. A clear reduction in the expression of aggressive behaviour by pigs derived from large groups was apparent. However, this did not re¯ect impaired discrimination between pen mates and foreign pigs, as evidenced by the fact that the majority of aggression was directed towards the latter. The targeting of aggression primarily at the foreign pigs indicates that pen mates were familiar with each other to a greater or lesser extent. Differentiating empirically between the existence of individual recognition and the ability only to discriminate between pen mate and foreign pigs is dif®cult (D'Eath, 1996) and was not possible using the present experiment design. Thus, the existence of pen mate/foreign pig discrimination in this experiment can not be automatically extended to indicate individual recognition of all group members.
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It is apparent, therefore, that although pen mate recognition was not impaired by a large group size, yet a change in group size was still associated with a change in aggressive propensity towards a novel individual. This change in aggressive behaviour may have been an overt consequence of an alteration in the strategy of group social organisation, which in turn may have been brought about by a de®cit in individual recognition ability required for the maintenance of a dominance hierarchy structure of organisation akin to that in the groups of 20. Alternatively, individual recognition may have been adequate to allow the formation of a dominance hierarchy, but the energetic costs and physical injury associated with establishing and frequently reinforcing the large number of dyadic relationships possible in large groups, may have encouraged the adoption of an alternative strategy (Pagel and Dawkins, 1997) which may have placed less emphasis on ®ghting at introduction. Other authors have reported a similarly reduced aggressive response by animals from large groups during introduction to foreign individuals. Hughes et al. (1997) reported that the frequency of aggressive behaviours of laying hens in stable ¯ocks of 700 was considerably less than that reported for smaller group sizes. Furthermore, the integration of two adjacent ¯ocks, each of 300 birds, resulted in no signi®cant increase in aggression and when groups of six birds were mixed, in a neutral arena, with six unfamiliar birds from a foreign pen, the frequency of agonistic behaviour equated closely to that between groups of six ¯ock mates selected from opposite ends of the home pen. Similarly, D'Eath and Keeling (1998) observed a signi®cant reduction in the tendency to display aggression towards an unfamiliar bird when hens were housed in groups of 120 in comparison with groups of 10. Erhard et al. (1997) examined the existence of individual differences in aggressive propensity by isolating a pig in part of its home pen and introducing an unfamiliar, smaller intruder pig. Animals which showed a long latency to bite the intruder were observed to be less aggressive when later mixed into a new group. It is uncertain whether the prolonged latency until the ®rst aggressive act and ®rst ®ght initiated by the pigs from groups of 80 in the present experiment indicates that post-mixing aggression could be reduced in severity by mixing pigs from large groups, or whether it only represents a transient delay before the escalation of more intense aggression. Mixing pigs with no prior experience of large-group housing, into groups of either 20 or 60 (Turner et al., 1999) or groups of 20 or 80 (Turner et al., 2000) has been shown to have no effect on the frequency of post-mixing aggressive behaviour or the number of skin lesions. Given that the number of group members with which a pig must establish a social relationship increases dramatically with group size, it would be predicted that the amount of aggression following mixing in a large group would be greater than that in a small group (Arey and Edwards, 1998). However, the similarity in observed post-mixing aggression between contrasting group sizes would indicate that either the proportion of dyadic relationships established using overt aggression must be reduced in large groups, or the severity, duration or frequency of aggression adopted must be reduced. The ®nding of Spoolder et al. (1999) that skin lesion score increased signi®cantly with group size apparently contradicts this theory. Pigs in groups of 20, 40 and 80 were recorded to have 7.8, 9.1 and 10.2 lesions respectively. However, given that the groups of 80 contained four times as many group members as the smallest group, the actual difference in lesion score of 2.4 lesions per pig is considerably lower than that which
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would be predicted from the number of dyadic relationships which could potentially have been established. The aggressive behaviour of pigs from a large group when subsequently mixed into a second large group and observed for a more prolonged period is yet to be empirically studied. Until then, it is not possible to conclude whether the behaviour observed by Spoolder et al. (1999) and Turner et al. (1999, 2000) in naive pigs is representative of that in animals with previous experience of large group housing. In conclusion, a dramatic reduction in the frequency and severity of aggression by pigs previously housed in large groups was demonstrated following introduction to a foreign pig, although these pigs were still capable of discriminating between group members and foreign animals. This paradox may be explained by a modi®cation of the social structure prevailing in small groups which in turn may have been precipitated by an inadequate capacity for individual recognition or a move towards a more energetically ef®cient strategy. This ®nding has potentially important consequences for pig welfare and economic productivity under commercial conditions. Acknowledgements We thank the staff of Tillycorthie Farm and D.S. Arey for their assistance. This work was supported by a Cruden Foundation scholarship for SPT and SAC receives ®nancial support from SERAD. References Arey, D.S., Edwards, S.A., 1998. Factors influencing aggression between sows after mixing and the consequences for welfare and production. Livest. Prod. Sci. 56, 61±70. Ayo, J.O., Oladele, S.B., Fayomi, A., 1998. Stress and its adverse effects on modern swine production. Pig News Info. 19, 51N±56N. Bokma, S., Kersjes, G.J.K., 1988. The introduction of pregnant sows in an established group. In: Unshelm, J., van Putten, G., Zeeb, K., Ekesbo, I. (Eds.), Proceedings of the International Congress on Applied Ethology in Farm Animals. Skara, Sweden, pp. 166±169. D'Eath, R.B., 1996. Social recognition of flockmates in laying hens. Ph.D. thesis. Magdalen College, University of Oxford, Oxford, pp. 1±7. D'Eath, R.B., Keeling, L.J., 1998. Social discrimination by hens in large flocks: implications for social organisation. In: Veissier, I., Boissy, A. (Eds.), Proceedings of the 32nd International Congress Society on Applied Ethology. Clermont-Ferrand, France, p. 68. Erhard, H.W., Mendl, M., 1997. Measuring aggressiveness in growing pigs in a resident-intruder situation. Appl. Anim. Behav. Sci. 54, 123±136. Erhard, H.W., Mendl, M., Ashley, D.D., 1997. Individual aggressiveness of pigs can be measured and used to reduce aggression after mixing. Appl. Anim. Behav. Sci. 54, 137±151. Ewbank, R., 1976. Social hierarchy in suckling and fattening pigs: a review. Livest. Prod. Sci. 3, 363±372. Ewbank, R., Meese, G.B., Cox, J.E., 1974. Individual recognition and the dominance hierarchy in the domesticated pig. The role of sight. Anim. Behav. 22, 473±480. Fraser, D., Rushen, J., 1987. Aggressive behaviour. Vet. Clin. North Am: Food Anim. Pract. 3, 285±305. Hughes, B.O., Carmichael, N.L., Walker, A.W., Grigor, P.N., 1997. Low incidence of aggression in large flocks of laying hens. Appl. Anim. Behav. Sci. 54, 215±234.
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Jensen, P., 1983. Effects of confinement on social interaction patterns in dry sows. In: Confinement and Continuous Noise as Environmental Factors Affecting Communication in the Domestic Pig, Report 8. Swedish University of Agricultural Sciences, Skara, Sweden, pp. 35±46. Jensen, P., Wood-Gush, D.G.M., 1983. Social interactions in a group of free ranging sows. In: Confinement and Continuous Noise as Environmental Factors Affecting Communication in the Domestic Pig, Report 8. Swedish University of Agricultural Sciences, Skara, Sweden, pp. 47±62. Jensen, P., Forkman, B., Yngvesson, J., Furuhaug, I.L., 1996. Assessment in pig conflicts. In: Duncan, I.J.H., Widowski, T.M., Haley, D.B. (Eds.), Proceedings of the 30th International Congress Society on Applied Ethology. The Colonel K.L. Campbell Centre for the Study of Animal Welfare, Ont., Canada, p. 46, abstract. Mauget, R., 1981. Behavioural and reproductive strategies in wild forms of Sus scrofa (European Wild Boar and feral pigs). In: Sybesma, W. (Ed.), The Welfare of Pigs. A Seminar in the EEC Program of Co-ordination of Research on Animal Welfare, Brussels. Martinus Nijhoff, London. pp. 3±13. McGlone, J.J., 1985. A quantitative ethogram of aggressive and submissive behaviours in recently regrouped pigs. J. Anim. Sci. 61, 559±565. McGlone, J.J., 1986. Influence of resources on pig aggression and dominance. Behav. Process. 12, 135±144. Pagel, M., Dawkins, M.S., 1997. Peck orders and group size in laying hens: `futures contracts' for nonaggression. Behav. Processes 40, 13±25. Penny, P., 1999. The performance and behaviour of large group nurseries. In: Proceedings of the Pig Veterinary Conference. Fairmont, Minnesota, 7 pp. Spoolder, H.A.M., Edwards, S.A., Corning, S., 1999. Effects of group size and feeder space allowance on welfare in finishing pigs. Anim. Sci. 69, 481±489. Tan, S.S.L., Shackleton, D.M., Beames, R.M., 1991. The effect of mixing unfamiliar individuals on the growth and production of finishing pigs. Anim. Prod. 52, 201±206. Turner, S.P., Edwards, S.A., Bland, V.C., 1999. The influence of drinker allocation and group size on the drinking behaviour, welfare and production of growing pigs. Anim. Sci. 68, 617±624. Turner, S.P., Ewen, M., Rooke, J.A., Edwards, S.A., 2000. The effect of space allowance on performance, aggression and immune competence of growing pigs housed on straw deep-litter at different group sizes. Livest. Prod. Sci. 66, 47±55. van Putten, G., van de Burgwal, J.A., 1990. Vulva biting in group-housed sows: preliminary report. Appl. Anim. Behav. Sci. 26, 181±186. von Gundlach, H., 1968. (Maternal care (pre- and post-natal), behavioural ontogeny and circadian activity in the European Wild Boar (Sus scrofa l.)). Zeitschrift fur Tierpsychologie 25, 955±995. Whittemore, C., 1993. The Science and Practice of Pig Production. Longman, Harlow, UK, pp. 54±56. Wiepkema, P.R., Schouten, W.G.P., 1990. Mechanisms of coping in social situations. In: Zayan, R., Dantzer, R. (Eds.), Social Stress in Domestic Animals. A Seminar in the Community Program for the Co-ordination of Agricultural Research, Brussels. Kluwer Academic Publishers, Dordrecht, The Netherlands. pp. 8±23.
Effect of social group size on aggressive behaviour between unacquainted domestic pigs Simon P. Turnera,*, Graham W. Horganb, Sandra A. Edwardsa,1 a
Scottish Agricultural College, Ferguson Building, Craibstone Estate, Bucksburn, Aberdeen AB21 9YA, UK b Biomathematics and Statistics Scotland, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK Accepted 19 June 2001
Abstract Domestic pigs (Sus scrofa) in small groups establish a dominance hierarchy using overt aggression and individual recognition. The impact of a large group size on group social organisation and aggression is poorly understood. The severity of aggression on mixing unacquainted pigs derived from large groups in which individual recognition may be impaired was studied and the implications for recognition of group members considered. Eight replicates of two group size treatments (20 versus 80) were used. After 6 weeks on treatment, a pair of pigs was introduced to a younger pair from an opponent pen in a barren arena. A total of 10 test pairs from each group were introduced to 10 opponent pairs from a group of 20 and 10 opponent pairs from a group of 80, giving 320 arena tests in total. Test duration was 5 min, but pigs which initiated a ®ght (rapid, persistent biting) were removed immediately. Pigs from groups of 80 displayed a lower frequency of aggressive acts (0.51 versus 0.90 S.E.D. 0.090 acts/pig/min) and initiated fewer ®ghts (19.7 versus 34.6 S.E.D. 3.62% of pigs, P < 0:01) in comparison with pigs from groups of 20. Aggression between pen mates accounted for a small amount of aggressive acts, and was unaffected by group size. Whilst retaining the ability to discriminate between pen mates and foreign pigs, pigs from large groups, therefore, displayed a marked reduction in aggressive tendency towards foreign individuals. # 2001 Published by Elsevier Science B.V. Keywords: Pig; Group size; Recognition; Aggression
* Corresponding author. Present address: Scottish Agricultural College, Sir Stephen Watson Building, Bush Estate, Penicuik, Midlothian EH26 0PH, UK. Tel.: 44-131-5353208; fax: 44-131-5353121. E-mail address: [email protected] (S.P. Turner). 1 Present address: Department of Agriculture, University of Newcastle, King George VI Building, Newcastle upon Tyne NE1 7RU, UK.
0168-1591/01/$ ± see front matter # 2001 Published by Elsevier Science B.V. PII: S 0 1 6 8 - 1 5 9 1 ( 0 1 ) 0 0 1 6 8 - X
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1. Introduction The social structure of wild Sus scrofa is centred on a small number of sows with their litters comprising of ®ve to six piglets each (von Gundlach, 1968). A clear and stable hierarchy exists between group members, where dominance rank is determined by a combination of sex, age, weight and strength (Mauget, 1981) and maintained through low intensity aggression and threats (McGlone, 1986). Under intensive commercial conditions, groups, typically of around 20 pigs, of very similar age and weight are penned at a high stocking density without the presence of more dominant adult animals. The mixing of unacquainted pigs, which is common in commercial practice, causes intense aggression which extends throughout the ®rst 24 h and results in a dominance hierarchy (Jensen and Wood-Gush, 1983; Fraser and Rushen, 1987). Aggression in commercial pig husbandry consequently presents a signi®cant cost to animal welfare and economic ef®ciency (e.g. Tan et al., 1991; Ayo et al., 1998). The number of commercial pigs housed in large groups of >50 members has increased signi®cantly in recent years (Penny, 1999). It has been suggested that the severity of aggression at introduction may increase in proportion to group size as a result of the escalating number of dyadic dominance relationships which must be established (Arey and Edwards, 1998). Casual observations would suggest, however, that very large groups of pigs, once established, can be maintained with minimal aggression (Bokma and Kersjes, 1988). However, the strategy of social organisation adopted in large groups is unknown (Wiepkema and Schouten, 1990; Arey and Edwards, 1998), and, without this knowledge, it is dif®cult to extrapolate the responses of pigs housed in small groups following the introduction of novel individuals to the large group context where the structure of social organisation may be markedly different. The ®rst purpose of this experiment was, therefore, to describe in detail the aggressive behaviour of pigs to novel conspeci®cs when derived from a small or large group. An assumption is made that the mixing of two unfamiliar animals, managed commercially, derived from small groups, and who are capable of recognising the other pig as from outwith their own group, would be expected to result in aggression in a high proportion of cases, as described by Erhard and Mendl (1997) and Erhard et al. (1997). Furthermore, the incorporation of a signi®cant liveweight difference between the two animals would encourage the display of aggression primarily by the larger pig (Erhard and Mendl, 1997). Recognition, at the level of group member/foreign pig discrimination and on an individual group member basis are pre-requisites for the functioning of a dominance hierarchy and without these abilities the establishment and maintenance of a dominance hierarchy would be untenable (Ewbank et al., 1974). The recognition capacity of the pig has not been adequately quanti®ed (Ewbank, 1976), but it is expected that at very large group sizes recognition will be impaired. The present experimental design does not allow a distinction to be made between the ability of pigs to perform group member/foreign pig discrimination and the individual recognition of all group members. The presence of either level of recognition would be accompanied by minimal aggression between pen mates, but the frequent expression of aggression towards foreign pigs (see D'Eath, 1996). However, in the absence of overt aggression when pigs are mixed, a failure to differentiate between pen mates and non-pen mates may be hypothesised (D'Eath and Keeling, 1998), even if no
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conclusion may be drawn regarding the recognition of pigs on an individual basis. The second purpose of the experiment was to interpret the aggressive responses of pigs in large groups as an indicator of the presence or absence of group member/foreign pig discrimination as a measure of a basic level of conspeci®c recognition. 2. Methods 2.1. Experimental design Domestic Large White Landrace growing pigs (start weight 29.3 S.E.M. 0.19 kg) were housed in groups of 20 or 80. The design of two treatments was replicated eight times using a total of 800 pigs. Animals were weaned at 4 weeks, fed a dry pelleted diet ad libitum (20% crude protein, 5% crude ®bre, 1.2% lysine, 14.2 MJ DE/kg), had ad libitum access to water and were housed on deep straw bedding. Fresh straw was provided daily and soiled litter was removed at 4-week intervals. A ¯oor space allowance of 0.88 m2 was provided per pig and ambient temperature was recorded at 1.5 m above ¯oor height. The mean minimum (12.4 S.E.M. 0.458C) and maximum (16.6 S.E.M. 0.398C) daily ambient temperature were similar in the two group sizes (P > 0:05). Ventilation was via an automatically controlled natural ventilation system and arti®cial light was provided constantly in addition to natural daylight. The management procedures and housing conditions experienced before introduction to the experiment were similar for all pigs. 2.2. Arena test procedure On day 41 post-mixing (during the 6th week) pen mates were introduced, in randomly chosen pairs, into an arena (test pigs). Simultaneously a younger pair of pen mates from a different pen, unacquainted with the test pigs and also randomly paired, were introduced at the diagonally opposite corner of the enclosure (opponent pigs). All instances of aggressive behaviour were recorded in the manner described below. Animals were introduced in group-mate pairs to avoid the repeated escape attempts demonstrated by pigs introduced alone, as observed in an earlier pilot study. Due to practical constraints, the duration between group formation at the start of the experimental period (day 0) and the time when animals were used as opponent pigs varied from 3 to 5 weeks. Opponent pigs were not weighed immediately before testing. However, it is possible to estimate their approximate weight from that measured at 3 (41.0 S.E.M. 0.41 kg) and 6 (55.9 S.E.M. 0.69 kg) weeks as growth rate varies little between these two points (Whittemore, 1993). On this basis, opponent pigs were used within a liveweight range of 41.0±50.9 kg. The opponent pig liveweight was, therefore, between 73.3 and 91.1% of that of the test pigs. Test pigs were subjected to two, randomly ordered, sessions of arena tests. In one session, 10 arena tests were performed using a total of 20 test pigs (from either group size) and 20 opponent animals from a group of 20. In the other session, the same 20 test pigs were tested against 20 opponent pigs from a group of 80. Opponent pigs were,
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consequently, used in one test only. Due to practical limitations, it was necessary for test pigs to be ®rst used as opponent pigs. Therefore, all pigs which were exposed to the arena tests were used once as opponent pigs during the period of weeks 3±5 and later as test pigs during each of sessions one and two in week 6. The number of times a pig was used as an opponent or a test animal was the same for both group sizes. 2.3. Arena layout The arena comprised a barren indoor enclosure with a solid concrete, unbedded ¯oor and without additional objects. Outwith test days, no pig entered the arena, was able to see it or was penned immediately adjacent to it. The enclosure measured 7 m 5 m and two solid gates were positioned at diagonally opposite corners (Fig. 1). Handling areas of 2:0 m 1:5 m dimensions secured a pair of animals near to each of the two arena entrances thereby allowing all four animals to be introduced simultaneously (Fig. 1). Pigs were housed as a group of 20 pen mates, for a maximum duration of 1 h in holding pens prior to testing. 2.4. Aggressive behaviour parameters On the simultaneous entry of test and opponent pigs into the arena, a stop watch was started. The frequency of occurrence of aggressive behaviours was recorded real time by a
Fig. 1. Plan of arena layout showing holding pens, observer location and arena access points; all walls were of solid blockwork; darkest shading represents gates or barriers.
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Table 1 Ethogram of categories of aggressive acts and responses used in arena testsa Behaviour
Description
Push
Aggressor presses shoulders against body of recipient for a minimum duration of 1 s; pushing is terminated when physical contact is lost; lunges made during bouts of pushing are recorded as single or multiple lunges as defined below; recipient may or may not respond Aggressor lunges head and shoulders towards recipient with mouth open or closed; physical contact may or may not be made; the aggressor does not initiate another attack within 2 s As above, aggressor repeats action one or more times with a delay of <2 s between each Aggressor pursues retreating recipient for a minimum of 2 m; mouth may be open or closed and physical contact may or may not be made; the chase is terminated when pursuit is suspended for 2 s or more Rapid and persistent biting in which bites are repeated with a delay of <1 s between each and the aggressive bout lasts not <2 s. Physical injury is typically inflicted on the recipient. The recipient may or may not respond Following aggression the recipient fails to retaliate or retreat; recipient continues with previous behaviour Recipient acts within 2 s to move away from the vicinity of the aggressor; a distance of 2 m or more must be traversed and the aggressor may or may not pursue
Single lunge Multiple lunge Chase Fight Ignore Retreat
a With the exception of the chase, ignore or retreat categories, the recipient may or may not respond to the aggression.
single observer throughout, but whom was not blind to the treatments. Duration of aggressive behaviour were not recorded. Aggressive behaviour was categorised as `push', `single lunge', `multiple lunge', `chase' or `®ght' (Table 1). The recipient's response was recorded as `retreat', `no response', `push', `single lunge', `multiple lunge', `chase' or `®ght'. The aggression categories selected were those used by Turner et al. (1999). Push coincided closely with the de®nitions of parallel and inverse parallel pressing detailed in Jensen (1983) and the de®nition of pushing given by McGlone (1985). Similarly, a single lunge may be viewed as synonymous with a head-to-body or head-to-head knock as de®ned by Jensen (1983). The aggressor was de®ned as the pig which initiated aggression in a single initiator/ responder sequence (i.e. one aggressive act followed by one recipient response). Where several aggressive acts/recipient response interactions occurred sequentially, the aggressor was the pig which initiated a new initiator/recipient sequence. For example, the sequence of behaviours; A single lunges, B pushes; B ®ghts, A retreats would be recorded as A (aggressor) single lunges; B (recipient) pushes; B (aggressor) ®ghts; A (recipient) retreats. Where behavioural transitions occurred (e.g. B (recipient) pushes; B (aggressor) ®ghts) no time delay was necessary between the response and the initiation of a new aggressive act. Where no activity transition took place (e.g. A (aggressor) single lunges, B (recipient) pushes; A (aggressor) single lunges, B (recipient) pushes) the de®nitions of bouts provided in Table 1 describe when one bout ended and a new one began. Where aggression developed into a ®ght, the stop watch was paused, the initiator of the aggressive bout was removed immediately by a separate observer and the stop watch
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allowed to continue. The initiator pig was removed irrespective of whether it attacked the recipient with a ®ght (A ®ghts B, B responds) or, more rarely, the recipient retaliated to a lower level of aggression using a ®ght (e.g. A multiple lunges, B ®ghts). The test was terminated when either both test or both opponent pigs had been removed following the initiation of ®ghts, excessive harassment or mounting occurred or 5 min duration had elapsed. Excessive harassment was de®ned as the continued following of a pig by another individual lasting for 2 min and resulting in the continued withdrawal of the recipient pig. In practice, the recipient pig frequently vocalised and showed persistent escape attempts (jumping of the forelegs against a pen division). Excessive mounting was de®ned as 10 mounting attempts when the actors forelegs were raised over the recipient pigs back. On termination of a test, opponent pigs were returned to their home pen and test pigs were returned to their holding pen for use in session two. 2.5. Measurements The effects of test pig group size, opponent pig group size and their interactions on test pig frequency and intensity of aggression were assessed using the following criteria. `Initiation' refers to the act of being an aggressor in an encounter. 2.5.1. Duration until aggression Duration until the ®rst aggressive act (i) and ®rst ®ght (ii) initiated by either pen mate. 2.5.2. Incidence of fights 1. Percentage of pigs removed for initiating a ®ght. 2. Percentage of tests where the first fight was initiated by a test pig. 2.5.3. Frequency of aggression 1. Number of aggressive acts per pig per minute. Where animals were removed due to ®ghting, the rate of aggression was corrected for the time they were present in the arena. 2. Percentage of tests where no aggression was shown by either pen mate. 3. Percentage of tests in which aggression occurred between two pen mates. 2.5.4. Severity of aggression 1. Frequency of pushes, single lunges, multiple lunges, chases or ®ghts as a percentage of all aggressive bouts. 2. Percentage of all responses to aggression which were categorised as ignore, retreat, push, single lunge, multiple lunge, chase or fight. 2.6. Statistical analysis As the pen was used as the statistical unit (n 16), a pen mean value for the above variables was calculated for each observation session. All variables were analysed using split plot analyses of variance with group size in the main plot stratum (pen of origin of test
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pigs) and opponent group size in the subplot stratum (session). The distribution of the datasets in each case was examined for normality and square root transformations were performed where necessary. Since the time following mixing at which the opponent pigs were used varied between treatments (between 3 and 5 weeks), opponent pig week following mixing was included as a covariate in those analyses in which it had a signi®cant in¯uence. 3. Results It was necessary to end a test or remove a pig due to excessive harassment in four tests and for persistent mounting in 10 tests. 3.1. Duration until aggression 1. The duration until the first instance of aggression shown by a test pig tended to be lower when the test pigs were from a group of 20 than 80 (Table 2). In addition the duration was lower when the opponent pigs were from a group of 20 (Table 2). 2. In those arena tests in which fights occurred, the duration until the first fight initiated by a test pig was significantly lower when the test pigs were from a group of 20 (Table 2). The duration until the first fight initiated by a test pig tended to be reduced when the opponent pigs were also from a group of 20 (Table 2). Test and opponent pig group sizes did not significantly interact to affect the duration until the first fight initiated by a test pig. 3.2. Incidence of fights 1. A significantly greater percentage of test pigs from groups of 20 were removed from the arena after initiating a fight than were test pigs from groups of 80 (Table 2). Similarly, when the opponent pigs were derived from a group of 20 the percentage of test pigs removed was significantly higher than when the opponent pigs were from a group of 80 (Table 2). Test pig group size and opponent pig group size did not significantly interact to affect the percentage of test pigs removed. 2. Test pigs derived from groups of 20 tended to be responsible for initiating a greater percentage of the first fights which developed following introduction than did test pigs from groups of 80 (Table 2). 3.3. Frequency of aggression 1. Test pigs from groups of 20 initiated a greater number of aggressive behaviours per minute than test pigs from groups of 80 (Table 3). 2. Pairs of test pigs housed in groups of 80 failed to display any aggression during a greater percentage of arena tests than did test pigs from groups of 20 (Table 3). 3. No significant differences occurred between treatments in the percentage of arena tests in which aggression between the two test pigs was observed (Table 3). The number of
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Main effects T pig group size
Time until first aggression (s) Time until first fight (s) Pigs removed for initiating fights (%) Tests where T pigs showed first fight (%) a
S.E.D. O pig group size 20
S.E.D.
20
80
47.2 96.2 34.6 81.4
69.1 10.76 50.2 66.1 7.35 173.8 18.05 118.2 151.8 16.60 19.7 3.62 34.4 19.9 3.45 62.6 8.37 69.2 74.7 9.79
Interactions
Significance
T 20, T 20, T 80, T 80, S.E. O 20 O 80 O 20 O 80
T
O
80
T: test pigs, O: opponent pigs, T O: test opponent pig group size interaction.
43.0 93.6 41.7 78.5
51.4 98.7 27.5 84.2
57.4 80.9 7.35 P 0.072 142.8 204.8 16.60 P < 0.01 27.1 12.3 3.45 P < 0.01 60.0 65.1 9.79 P 0.051
P 0.051 P 0.066 P 0.001
TO
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Table 2 Duration until aggression and incidence of fights for test and opponent pigs under the four combinations of test and opponent pig group sizes and group size main effectsa
Main effects T pig group size 20 Frequency of aggressive acts (acts/pig/min) Tests where no aggression was shown by either pig (%) Tests where aggression occurred between pen mates (%) a b
0.90
Interactions S.E.D.
80 0.51
O pig group size 20
Significance
S.E.D.
T 20, O 20
T 20, O 80
T 80, O 20
T 80, O 80
S.E.
T
O
TO
80
0.090
0.74
0.68
0.083
0.92
0.89
0.56
0.47
0.083
P < 0.01
3.1 a
2.6 a
10.1 ab
12.9 b
2.00
P < 0.01
27.7
28.6
6.30
2.9
11.5
3.22
6.6
7.7
2.00
25.3
30.5
7.62
24.3
31.5
6.30
T: test pigs, O: opponent pigs, T O: test opponent pig group size interaction. Different letters indicate a significant difference between means.
23.9
26.8
P < 0.05
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Table 3 Frequency of aggressive acts for test and opponent pigs under the four combinations of test and opponent pig group sizes and group size main effectsa,b
211
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aggressive acts directed at a pen mate expressed as a percentage of all aggressive acts was similar for the two test pig group sizes (10.1 versus 14.6 S.E.D. 1.93% for groups of 20 and 80 respectively, P > 0:05). 3.4. Severity of aggression 1. With the exception of fights, the percentage of all aggressive bouts initiated by a test pig which was of each severity category showed no significant effects of treatment. Chases were excluded from the analysis because their incidence was too low to allow a meaningful comparison. Fights contributed to a greater percentage of the total aggression shown by test pigs when the opponent pigs were derived from a group of 20 than 80 (17.6 versus 7.6 S.E.D. 3.75% of total aggressive occurrences, P < 0:05). 2. Test pigs responded by using a fight to aggressive acts initiated by an opponent pig more often when the opponent pig group size was 20 than 80 (9.2 versus 4.4 S.E.D. 1.98% of all responses, respectively, P < 0:05). Again chases were excluded from the analysis. 4. Discussion On the introduction of two pairs of pigs from different pens, pigs derived from groups of 20 showed aggressive behaviour signi®cantly more rapidly, demonstrated aggression in more tests, gave aggression at a faster rate and initiated ®ghts more rapidly and on signi®cantly more occasions than did pigs from groups of 80. All pigs used in the arena tests, irrespective of group size, were ®rst used as opponent animals between weeks 3 and 5 post-mixing and subsequently as test pigs during each of two sessions during week 6. Animals tested during week 6 had experience of the testing location, and the amount of experience was the same for pigs derived from groups of 20 and 80. Previous experience of the testing location may have encouraged a degree of territorial aggression from the test pigs (see van Putten and van de Burgwal, 1990), but this would have been equivalent for pigs from both group size treatments. The greater liveweight of the test pigs compared to the opponent pigs is likely to have conferred an advantage on the test animals and made them more con®dent in instigating aggression (Jensen et al., 1996; Erhard and Mendl, 1997). Again, however, this in¯uence was similar for the two group sizes. A clear reduction in the expression of aggressive behaviour by pigs derived from large groups was apparent. However, this did not re¯ect impaired discrimination between pen mates and foreign pigs, as evidenced by the fact that the majority of aggression was directed towards the latter. The targeting of aggression primarily at the foreign pigs indicates that pen mates were familiar with each other to a greater or lesser extent. Differentiating empirically between the existence of individual recognition and the ability only to discriminate between pen mate and foreign pigs is dif®cult (D'Eath, 1996) and was not possible using the present experiment design. Thus, the existence of pen mate/foreign pig discrimination in this experiment can not be automatically extended to indicate individual recognition of all group members.
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It is apparent, therefore, that although pen mate recognition was not impaired by a large group size, yet a change in group size was still associated with a change in aggressive propensity towards a novel individual. This change in aggressive behaviour may have been an overt consequence of an alteration in the strategy of group social organisation, which in turn may have been brought about by a de®cit in individual recognition ability required for the maintenance of a dominance hierarchy structure of organisation akin to that in the groups of 20. Alternatively, individual recognition may have been adequate to allow the formation of a dominance hierarchy, but the energetic costs and physical injury associated with establishing and frequently reinforcing the large number of dyadic relationships possible in large groups, may have encouraged the adoption of an alternative strategy (Pagel and Dawkins, 1997) which may have placed less emphasis on ®ghting at introduction. Other authors have reported a similarly reduced aggressive response by animals from large groups during introduction to foreign individuals. Hughes et al. (1997) reported that the frequency of aggressive behaviours of laying hens in stable ¯ocks of 700 was considerably less than that reported for smaller group sizes. Furthermore, the integration of two adjacent ¯ocks, each of 300 birds, resulted in no signi®cant increase in aggression and when groups of six birds were mixed, in a neutral arena, with six unfamiliar birds from a foreign pen, the frequency of agonistic behaviour equated closely to that between groups of six ¯ock mates selected from opposite ends of the home pen. Similarly, D'Eath and Keeling (1998) observed a signi®cant reduction in the tendency to display aggression towards an unfamiliar bird when hens were housed in groups of 120 in comparison with groups of 10. Erhard et al. (1997) examined the existence of individual differences in aggressive propensity by isolating a pig in part of its home pen and introducing an unfamiliar, smaller intruder pig. Animals which showed a long latency to bite the intruder were observed to be less aggressive when later mixed into a new group. It is uncertain whether the prolonged latency until the ®rst aggressive act and ®rst ®ght initiated by the pigs from groups of 80 in the present experiment indicates that post-mixing aggression could be reduced in severity by mixing pigs from large groups, or whether it only represents a transient delay before the escalation of more intense aggression. Mixing pigs with no prior experience of large-group housing, into groups of either 20 or 60 (Turner et al., 1999) or groups of 20 or 80 (Turner et al., 2000) has been shown to have no effect on the frequency of post-mixing aggressive behaviour or the number of skin lesions. Given that the number of group members with which a pig must establish a social relationship increases dramatically with group size, it would be predicted that the amount of aggression following mixing in a large group would be greater than that in a small group (Arey and Edwards, 1998). However, the similarity in observed post-mixing aggression between contrasting group sizes would indicate that either the proportion of dyadic relationships established using overt aggression must be reduced in large groups, or the severity, duration or frequency of aggression adopted must be reduced. The ®nding of Spoolder et al. (1999) that skin lesion score increased signi®cantly with group size apparently contradicts this theory. Pigs in groups of 20, 40 and 80 were recorded to have 7.8, 9.1 and 10.2 lesions respectively. However, given that the groups of 80 contained four times as many group members as the smallest group, the actual difference in lesion score of 2.4 lesions per pig is considerably lower than that which
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would be predicted from the number of dyadic relationships which could potentially have been established. The aggressive behaviour of pigs from a large group when subsequently mixed into a second large group and observed for a more prolonged period is yet to be empirically studied. Until then, it is not possible to conclude whether the behaviour observed by Spoolder et al. (1999) and Turner et al. (1999, 2000) in naive pigs is representative of that in animals with previous experience of large group housing. In conclusion, a dramatic reduction in the frequency and severity of aggression by pigs previously housed in large groups was demonstrated following introduction to a foreign pig, although these pigs were still capable of discriminating between group members and foreign animals. This paradox may be explained by a modi®cation of the social structure prevailing in small groups which in turn may have been precipitated by an inadequate capacity for individual recognition or a move towards a more energetically ef®cient strategy. This ®nding has potentially important consequences for pig welfare and economic productivity under commercial conditions. Acknowledgements We thank the staff of Tillycorthie Farm and D.S. Arey for their assistance. This work was supported by a Cruden Foundation scholarship for SPT and SAC receives ®nancial support from SERAD. References Arey, D.S., Edwards, S.A., 1998. Factors influencing aggression between sows after mixing and the consequences for welfare and production. Livest. Prod. Sci. 56, 61±70. Ayo, J.O., Oladele, S.B., Fayomi, A., 1998. Stress and its adverse effects on modern swine production. Pig News Info. 19, 51N±56N. Bokma, S., Kersjes, G.J.K., 1988. The introduction of pregnant sows in an established group. In: Unshelm, J., van Putten, G., Zeeb, K., Ekesbo, I. (Eds.), Proceedings of the International Congress on Applied Ethology in Farm Animals. Skara, Sweden, pp. 166±169. D'Eath, R.B., 1996. Social recognition of flockmates in laying hens. Ph.D. thesis. Magdalen College, University of Oxford, Oxford, pp. 1±7. D'Eath, R.B., Keeling, L.J., 1998. Social discrimination by hens in large flocks: implications for social organisation. In: Veissier, I., Boissy, A. (Eds.), Proceedings of the 32nd International Congress Society on Applied Ethology. Clermont-Ferrand, France, p. 68. Erhard, H.W., Mendl, M., 1997. Measuring aggressiveness in growing pigs in a resident-intruder situation. Appl. Anim. Behav. Sci. 54, 123±136. Erhard, H.W., Mendl, M., Ashley, D.D., 1997. Individual aggressiveness of pigs can be measured and used to reduce aggression after mixing. Appl. Anim. Behav. Sci. 54, 137±151. Ewbank, R., 1976. Social hierarchy in suckling and fattening pigs: a review. Livest. Prod. Sci. 3, 363±372. Ewbank, R., Meese, G.B., Cox, J.E., 1974. Individual recognition and the dominance hierarchy in the domesticated pig. The role of sight. Anim. Behav. 22, 473±480. Fraser, D., Rushen, J., 1987. Aggressive behaviour. Vet. Clin. North Am: Food Anim. Pract. 3, 285±305. Hughes, B.O., Carmichael, N.L., Walker, A.W., Grigor, P.N., 1997. Low incidence of aggression in large flocks of laying hens. Appl. Anim. Behav. Sci. 54, 215±234.
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