Elsevier

Physiology & Behavior

Volume 143, 1 May 2015, Pages 151-157
Physiology & Behavior

Evidence for a link between tail biting and central monoamine metabolism in pigs (Sus scrofa domestica)

https://doi.org/10.1016/j.physbeh.2015.02.049Get rights and content

Highlights

  • There appears to be a link between brain neurotransmission and tail biting in pigs.

  • Tail biters tended to have an increase in their prefrontal cortex 5-HT metabolism.

  • Tail biting victims had altered limbic and striatum dopamine and 5-HT metabolism.

  • The results support the theory that tail biting is a stress-related behaviour.

Abstract

Tail biting in pigs is a major welfare problem within the swine industry. Even though there is plenty of information on housing and management-related risk factors, the biological bases of this behavioral problem are poorly understood. The aim of this study was to investigate a possible link between tail biting, based on behavioral recordings of pigs during an ongoing outbreak, and certain neurotransmitters in different brain regions of these pigs. We used a total of 33 pigs at a farm with a long-standing problem of tail biting. Three equally big behavioral phenotypic groups, balanced for gender and age were selected, the data thus consisting of 11 trios of pigs. Two of the pigs in each trio originated from the same pen: one tail biter (TB) and one tail biting victim (V). A control (C) pig was selected from a pen without significant tail biting in the same farm room. We found an effect of tail biting behavioral phenotype on the metabolism of serotonin and dopamine, with a tendency for a higher 5-HIAA level in the prefrontal cortex (PFC) of TB compared to the other groups, while V pigs showed changes in both serotonin and dopamine metabolism in the striatum (ST) and limbic cortex (LC). Trp:BCAA and Trp:LNAA correlated positively with serotonin and 5-HIAA in the PFC, but only in TB pigs. Furthermore, in both ST and LC, several of the neurotransmitters and their metabolites correlated positively with the frequency of bites received by the pig. This is the first study indicating a link between brain neurotransmission and tail biting behavior in pigs with TB pigs showing a tendency for increased PFC serotonin metabolism and V pigs showing several changes in central dopamine and serotonin metabolism in their ST and LC, possibly due to the acute stress caused by being bitten.

Introduction

Tail biting is a common behavioral problem in pigs. Under suboptimal housing and management conditions, pigs are prone to start biting each other's tails, causing wounds, amputation of the tail, and infections [1], [2]. Tail biting is thus a serious animal welfare problem, indicating an underlying welfare problem, and causing additional stress to the victim [3] as well as production losses due to increased need for medication, reduced growth and increased prevalence of carcass condemnation of affected pigs [4], [2], [5].

The external risk factors for tail biting are reasonably well-known, including factors that cause stress, such as lack of manipulable materials to fulfill their need for exploration; crowding in the pen; competition by the feeder; poor environmental conditions, such as air quality; and feeding-related problems [6]. However, even in clearly suboptimal situations, such as barren housing conditions, not all pigs end up biting tails [7], [8], indicating that there are individual differences between pigs, making some more prone to bite than others. Based on behavioral patterns and suggested motivational background it has been suggested [9] that there might, in addition, be several different types of tail biting behavior. Some forms of tail biting, such as the sudden-forceful type, where tail biting occurs in situation of competition, such as at the feeder, have been proposed to be linked to aggressive behavior, while other, more common types do not show a link to aggression [9].

Being a tail biter does not appear to be a stable individual trait [8], but rather a temporary behavioral change, due to challenges in the environment. These changes might, in turn, be related to changes in neurotransmission, as have been indicated in relation to behavioral problems in other captive animals, eg. feather pecking in chicken [10], [11] and stereotypic behavior in bank voles and horses [12], [13].

The serotonergic system is involved in the regulation of mood, eating behavior, aggressive behavior and mental disorders in humans and other species (for a review, see [14]). In pigs, the serotonergic system has been linked to aggressive behavior [15], [16]. Furthermore, genetically stress-susceptible pigs have been shown to have lower levels of serotonin in several brain regions than stress-tolerant pigs [17], while increased feeding levels of tryptophan, which is the precursor of serotonin, inhibit physiological stress activity [18] and decreases aggression and stress reactions in pigs [15], [19], [20]. Increased level of orally administered tryptophan has also been shown to reduce tail and ear biting in pigs [21]. Ursinus et al. [8] were the first to show a link between tail biting behavior and the serotonergic system, by showing a decrease of blood serotonin in both tail biting and victim pigs. Stressful situations change serotonin activity in the brain [22], [23].

The dopaminergic system is of great importance for both the reward system and for handling environmental challenges and emotional responses, such as fear and anxiety (for reviews, see [24], [25]). In pigs, the dopaminergic system has been related to exploratory propensity [26] and the frustration level during a delay test [27]. Dopamine responds to stressful situations [22], [23], for example, it has been shown that stress caused by restraining pigs increases dopamine turnover in certain brain areas [23].

Also noradrenaline activity in the brain has been linked to aggressive behavior and dominance in pigs [15]. As for the other monoamines, stress causes changes also in central noradrenaline levels and noradrenaline metabolism [23], [28].

The aim of this study was to investigate a possible link between tail biting, based on behavioral recordings of pigs during an ongoing outbreak, and certain neurotransmitters in different brain regions of these pigs. The motivational background of tail biting appears to be complex [9], and we do not know, for example, if the behavior involves learning. Thus, the brain regions were selected to represent areas important for the organization of stress-related processes on different cognitive levels (for reviews, see [14], [29]). Chronic and/or acute stress is assumed to be the main underlying factor behind the development of tail biting. As tail biting is known to induce stress in the victims [3], [30], we hypothesized that both pigs performing tail biting and victims of tail biting should show changes in central monoamine levels and metabolism.

Section snippets

Material and methods

The study protocol was approved by the Ethical Committee at the University of Helsinki (ECUH).

Descriptive data

Overall levels of plasma amino acids are presented in Table 2. Levels of brain neurotransmitters and their metabolites, as well as the ratio between neurotransmitters and metabolites, are presented in Table 3. The number of performed and received tail bites in the different phenotypic groups is given in Table 4.

Correlations between performed and received bites and neurotransmitters

None of the neurotransmitters nor their metabolites measured in PFC or H correlated with the number of performed or received tail bites (p > 0.1 for all). In LC a positive correlation

Discussion

We were able to show evidence for the expected link between neurotransmission in the pig brain and tail biting. Changes in neurotransmission were seen both in pigs performing tail biting and pigs that had been victims of tail biting. As this study was conducted during an actual outbreak of tail biting, we cannot make conclusions about cause and effect of the observed differences. However, this is, to our knowledge, the first study showing that there exists a link between central monoamines and

Conclusions

This is the first study indicating a link between brain neurotransmission and tail biting behavior in pigs. We showed that during an ongoing tail biting outbreak, tail biters tended to have an increase in their prefrontal cortex serotonin metabolism as compared to victims of tail biting and control pigs from pens where tail biting hardly occurred. The mechanism behind this possible link can only be discussed and further studies are warranted on links between, among others, neurotransmission and

Acknowledgments

This study was a part of the NKJ (Nordic Joint Committee for Agricultural and Food Research)-funded project ‘Tail biting and tail docking in the pig: biological mechanisms, prevention, treatment and economic aspects’ (grant number NKJ 129) and national funding was provided by the Finnish Ministry of Agriculture and Forestry (grant number 45/502/2008). The authors wish to thank the farm for allowing the research team to use their facilities, and for all their help. A special acknowledgement goes

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