Factors Underlying The Performance of Redirected Oral Behaviors in Gestating Sows

Commercial ‘dry’ sows in today’s intensified production system are fed quantitatively restricted diet during most of their pregnancy. Such restriction is made not only with the aim to reduce the feed costs, but also to avoid excess body weight gain and fat deposition which may compromise animals’ welfare and consequently lower their reproductive performance. The behaviour of these breeding sows is often characterised by increased activity around feeding times and performance of redirected oral behaviours, such as excessive drinking and chewing, mainly after the feed. The latter has been widely accepted as stereotypic behaviours.

Research going back more than 30 years, when the gestating sows were tethered and kept in individual stalls, suggests that food restriction - particularly persistence of feeding motivation, and confined environment are primary reasons for the performance of these behaviours. Rushen, 1984 in his detailed observational study of 55 sows concluded that bar chewing and general excitement before feeding were related to anticipation, while the adjunctive drinking after food consumption resulted from the persistence of the feeding motivation which had not been satisfied by the ration. Similar findings were reported by Appleby and A. Lawrence, 1987 in their study where gilts were provided with twice the amount of their restricted ration and showed a low incidence of repetitive behaviour. The authors concluded that housing system which combines close confinement and food restriction is not suitable for pregnant pigs.

Motivation and Redirected Oral Behaviours

One approach for a better understanding of the oral repetitive behaviours in sows is to look at the mechanisms underlying their performance by using motivational concepts. For instance, Hughes and Duncan, 1988 by reviewing a number of behavioural models, proposed that the increased motivation which results from the additive effect of environmental and dietary factors triggers appetitive behaviour which itself has positive feedback on motivation. In the case with food restriction and confinement, the environment does not allow a sufficient expression of consummatory behaviour (negative feedback) for defusing this motivation, and the animal gets into a closed loop of performing repetitive elements of appetitive behaviours.

In support of the view that motivation persist after feeding, research measuring the operant response rates of boars maintained on similar levels of food restriction as sows showed sustained levels of feeding motivation even immediately after the end of the meal. Later, Terlouw et al., 1991a investigated the separate and interactive effects of restraint and food restriction and concluded that major factor affecting the performance of repetitive behaviours is food deprivation and to a much lesser extent confinement. Their research also indicated that appetitive behaviours such as nosing and rooting after feeding did not decrease with the increase of the performance of stereotypies such as drinking and chewing – activities which appear more related to consummatory behaviour. It should be noted that part of the animals in the latter study was not observed in the period before feeding which might have concealed the impact of the pre-feeding appetitive behaviour. Furthermore, the research was conducted on gilts, therefore, the stereotypic behaviours might not have been fully developed.

As A. Lawrence and Terlouw, 1993 discussed in their review, nonspecific factors such as behavioural arousal and learning might have a more significant impact on the long-term persistence of the repetitive behaviours than previously had been suggested, although the empirical evidence of this role might be quite controversial. For instance, Terlouw et al., 1993 tested whether the arousal of a novel sound or an unexpected meal at the afternoon would provoke the performance of stereotypic behaviour among sows. The ingestion of the meal was followed by increased levels of activity, chain manipulation and drinking, while the loud novel sound was not. However, when Haskell et al., 2000 manipulated sows’ pre-prandial arousal by delaying the delivery of food, the performance of repetitive behaviours after feeding increased. This suggests that although food delivery might have the most direct impact on the expression of post-prandial repetitive behaviours, the arousal which results from appetitive anticipatory behaviour before feeding also facilitates the performance of stereotypies. Moreover, the highly predictable feeding schedule on which sows are imposed possibly contributes further to the pre-feeding arousal and the persistence of the oral behaviours. Some research suggests that the performance of post-feeding stereotypic behaviours might be a coping strategy of reducing the stress from the invoked arousal. Terlouw et al., 1991b investigated the latter by comparing the levels of plasma cortisol (a hormone which increases with stress) between sow classified as either high or low stereotypers. Chain manipulation was not correlated with cortisol levels, but there was a tendency for lower levels of the hormone with increased drinking. However, the authors concluded that this might have been a physiological consequence of the consumption of a large amount of water.

It should also be noted that pigs are very responsive to cues indicative of food and its absence, thus with the experience of being fed on a fixed schedule sows probably learn that food will not be present out of feeding times. According to A. Lawrence and Terlouw, 1993 stereotypies might be seen as an extreme form of learning - shaping. In physically and behaviourally restrictive environment on which the animals do not have control, the behavioural repertoire can be reduced to just a few behaviours which are focused towards the limited incentives allowing the performance of foraging behaviour (such as pen bars). The long repetition of these few behaviours gradually becomes something of a habit which is difficult to reverse. In support of this view, some studies report an increase in levels of standing and performance of repetitive behaviours among older sows in later parity. Rushen, 1985 also indicated that higher parity pigs performed appetitive and adjunctive behaviours in a more stereotyped manner compared to younger sows. On the other hand, Terlouw and Lawrence, 1993 reported relatively consistent levels of activity across parities and a reduced amount of trough and floor directed behaviours among low fed sows in later parities but an increase in drinking-related activities. Furthermore, when the low fed sows in the latter study were provided with increased food allowance in parity four, the performance of repetitive behaviours did not decrease even after two months.

Each of the studies mentioned above explains somehow partly the complex picture behind the motivational processes underlying the performance of oral repetitive behaviours in breeding pigs. In the last years, considerable research has been focused on a qualitative restriction of sows’ food or in other words, alternative fibre diets with a lower energy density which are provided in a greater quantity. Thus, most of the up to date studies investigate the effect of fibre diets on sows’ feeding motivation. Less work is focused on the primary motivational processes underlying the performance of the actual oral behaviours mainly because often such research requires considerable funds and is highly time-consuming. However, the demand for meat has led to significant changes in pigs’ industry mainly related to improved productivity – animals are bred for increased appetite and large litter size. The latter may have had an impact on animals’ behavioural needs especially in terms of satiety and hunger. Therefore, detailed up to date research looking at how the industry pressure might have altered sows’ behaviour itself is needed.

Health problems as underlying factors for the performance of repetitive oral behaviours

It would be difficult to get a better understanding of the development and the persistence of the repetitive oral behaviours in gestating sows only by looking at behavioural models. Some physiological (health) problems such as gut diseases and tooth decay might also affect the performance of these behaviours.

Gastrointestinal diseases

Studies done on horses and veal calves show that oral stereotypies such as tongue playing, crib-biting and wind sucking which are also commonly performed by sows might be associated with underlying gastrointestinal dysfunctions. For instance, (Wiepkema et al. (1987) indicated that abomasal ulcers were rare in calves who increasingly performed tongue playing, in contrast, animals who did not engage in this behaviour had developed the condition. In experimental research K. Johnson et al. (1998) manipulated the diet of horses by adding Founderguard (a supplement reducing the acidosis in the hindgut) to their concentrated feed. The treatment led to a decrease in the performance of abnormal oral behaviours, suggesting an association with gastrointestinal dysfunction affected by acidity such as ulcers. Nicol et al., 2002 investigated the latter by looking at whether providing horses with antacid diet would influence the development of ulcers and diminish crib-biting behaviour. The treatment significantly reduced the ulceration scores, and the authors reported a decrease in the performance of crib-biting. However, the results of the latter study were close to significant, probably because of the small sample size, and they should be interpreted with care. Although none of the aforementioned research identifies direct causality, some authors speculate that by performing these behaviours the animals secrete excess saliva which may counteract with the acidity in the stomach).

On the other hand, further research on horses suggests that other health problems related to the gastrointestinal tract might also be associated with the performance of oral stereotypies. For instance, an epidemiological study conducted in 21 clinics showed a high positive correlation between crib-biting/wind sucking and epiploic foramen entrapment colic. Malamed et al., 2010 reported similar findings from their research and concluded that these behaviours are not associated with a particular category or severity of colic.

There is not much research done on investigating possible gastric or ulcer conditions which might be related to the development and persistence of oral stereotypies in pregnant pigs but there is some evidence that a relationship might be indeed present. In a study looking at the effect of antacid diet on ulcers and stereotypies of gestating sows, treatment did not affect ulceration or behaviour, but the authors indicated a relationship between an increased amount of bar biting among animals with high ulcer scores. More recently, Rutherford et al., 2018 reported that finishing pigs with gastric ulcers spent significantly more time standing compared to animals without ulcerations. Although the research was conducted among finishers, these results might explain the increased time standing and performance of oral behaviours among sows in later parity reported in some studies. There are also findings suggesting a prevalence of ulcers among gestating sows, which further support the view that part of the oral behaviours performed around feeding may be a result of deterioration of the gut health. Research investigating risk factors for gastric ulcers in pigs at slaughter by examining the stomachs of 15 741 animals reported the highest occurrence of ulceration in culled sows. Such findings can be expected as in today’s intensified production sows are often fed with pelleted food which consists of small particles. The latter combined with ration feeding have been identified as main reasons for the development of ulcerations in pigs and other animals (.

Further detailed research combining diet manipulation, detailed behavioural observation and a post-mortem examination is needed to get a better understanding of the possible relationship between oral behaviours and gastrointestinal health in breeding pigs.

Dental diseases

When addressing health problems, which might provoke the performance of abnormal oral behaviours, it would be worth discussing teeth decay. Possible dental disease probably is accompanied by pain and general discomfort for the animal which may lead to the performance of repetitive oral behaviour. Only a few papers have addressed dental health among sows focussing mainly on post-mortem examination. E. Johnson et al., 2003 examined heads of sows from two abattoirs and reported that around 85% of the animals had one or more significant tooth lesions. Other studies have indicated a lower incidence of teeth wearing and injuries, but the percentage was still noticeably high - between 30% and 42%. Some authors suggest that the significant molar or incisor lesions are a result of bar-biting, while others argue that these conditions are time-related. However, other factors may also contribute to the development of tooth decease in sows. Routine husbandry practices such as clipping and grinding piglets’ teeth have been reported to cause necrosis, gingivitis and severe pulp inflammation in the weeks after the performance of the procedures. It can be argued that these deciduous teeth will be replaced later in life, but from human dentistry is known that untreated infection of a primary tooth can lead to an alternation in the development of the permanent successor and bacterial invasion of the surrounding tissue (Cordeiro and Rocha, 2005). Thus, it is highly likely sows whose teeth have been clipped or grinded to suffer from tooth decay and severe gingivitis. Another point to consider is that breeding pigs are fed restricted diet. Research looking at the effect of calorie deficiency on dental development in pigs at the first 20 months of life has shown that undernourishment may lead to overcrowding and displacement of the teeth and malocclusion of the jaw. Pigs do not get their teeth fully developed till 18-24 months of age and gilts are about six-seven months at the time of their first service, after which they are fed restricted diet during most of their pregnancy. Therefore, it can be expected that certain dental abnormalities in adult animals might be related to a food restriction imposed on them in the early stages of life. The latter is partly supported by the findings of E. Johnson et al. (2003) that there was a retention of one or more deciduous incisors in 15 % of the mature sows in their research.

Pig dentistry is not a widely researched topic, and most of the work is focused on investigating the impact of clipping and grinding of piglets’ teeth as routine practices possibly causing discomfort. Thus, a study exploring the relationship between the performance of oral stereotypies in sows and teeth decay may contribute to a better understanding of the long-term impact of dental conditions on pigs’ well-being.

Conclusion

The additive effect of multiple physiological and motivational factors may underline the performance of oral redirected behaviours in pregnant sows. It has been recognised that these behaviours are related to undernutrition and hunger and are possible signs of compromised welfare. However, untreated physiological problems can also compromise animals’ long-term well-being. Further research should be focused on up to date systematic quantification of these abnormal behaviours and the possible reasons for their performance.