Introduction

Being affected by displays of distress in conspecifics is highly adaptive for social animals because it has an important role in individual and inclusive fitness (Preston and de Waal 2002). For instance, parental responses to offspring distress enhance the young’s survival (Grandinson et al. 2003; Baxter et al. 2011; Melišová et al. 2014) and consolation of distressed group mates strengthens valuable bonds in animal societies (Romero et al. 2010; Plotnik and de Waal 2014). Individuals may also learn about their environment (e.g. presence of a predator) using indicators of distress (e.g. alarm call, chemical alarm cues or alarm substance) in their conspecific (Mateo 1996; Griffin 2004; Stensmyr and Maderspacher 2012).

The detection of distress in others may lead to a variety of behavioural and physiological responses such as an increase in pain sensitivity (Langford et al. 2006; Jeon et al. 2010; Martin et al. 2015), anti-threat behaviour (Kavaliers et al. 2001, 2003), greater maternal response (Walker et al. 2003; Hild et al. 2011; Edgar et al. 2012) or social transfer of fear (Kim et al. 2010; Knapska et al. 2010), indicating that animals are affected by perceiving another individual’s emotional state. Moreover, animals are not only sensitive to conspecific distress, but they sometimes act to alleviate this distress (rat: Bartal et al. 2011; Sato et al. 2015; rhesus monkey: Mirsky et al. 1958; pigeons: Watanabe and Ono 1986) and even give emotional support to the distressed animal (Fraser et al. 2008; Plotnik and de Waal 2014), although it is not clear whether the main motivation is reduction in personal distress or genuine psychological altruism (Sober and Wilson 1998; de Waal 2008).

The mechanism underlying responses to conspecific distress has yet not been fully revealed. Empathy, referring to the ability to recognize another individual’s mental states and to generate an appropriate emotional response to the states (Sanders et al. 2013), has been suggested to explain it. Empathy encompasses cognitive and emotional processes (de Waal 2008). Cognitive empathy refers to the capacity of understanding another individual’s emotional state, even if this differs from one’s own. It therefore requires self–other distinction, perspective-taking and mental state attribution (de Waal 2008). Emotional or affective empathy refers to the ability to be affected by, and to share, another individual’s emotional state (Edgar et al. 2011). Emotional contagion, identified as the most basic form of affective empathy, refers to matched emotional responses as a direct result of perceiving the state in another, without requiring an ability to discern whether the source of an affective experience comes from one’s self or from another individual (Singer and Lamm 2009).

Empathic responses to conspecific distress are relevant to the welfare of group living animals as an individual may be affected by the emotional state of others. This is particularly the case in farm animals which, under commercial conditions, are exposed to negative (aversive) situations like routine handling (e.g. vaccination, restraint, tail docking, castration, teeth clipping), transport or slaughter. Investigations of the effect of conspecific distress on farm animals have been limited so far. In pigs, the extent to which individuals are affected by direct or indirect observation of conspecifics in a negative emotional state has only been investigated in four studies. Reimert et al. (2013, 2015) found evidence of emotional contagion, albeit rather subtle, during anticipation and during positive and negative treatments. In contrast to Reimert et al.’s findings, Anil et al. (1997) concluded that witnessing killing did not appear to distress slaughter pigs. In a playback experiment, Düpjan et al. (2011) found that young pigs exposed to isolation were attentive to conspecific distress vocalizations, but they did not share the distress of the caller. However, the absence of empathic response may have been due to their experimental designs. Anil et al. (1997) carried out their observations directly in a slaughterhouse, which is a very challenging/stressful environment for pigs that may have hidden any potential response to another individual’s killing. Düpjan et al. (2011) used only acoustic stimulation through playbacks of calls of an unfamiliar conspecific. Moreover, the pigs were tested while being temporarily isolated and therefore stressed which may have hidden any potential response to another individual’s vocalizations.

Expression of emotional empathy may be modulated by factors involving cognitive processes. Response to distress has been found to increase with the intensity of the aversive experience (Morrison et al. 2007; Preis and Kroener-Herwig 2012) and familiarity with the distressed animal (Langford et al. 2006; Bartal et al. 2014; Gonzalez-Liencres et al. 2014). In addition, multiple sensory cues available to the observer animals facilitate communication between individuals (Partan and Marler 1999) and therefore possibly emotional transfer. Sharing similar aversive experiences has also been shown to facilitate behavioural and physiological responses of individuals witnessing conspecific distress (Preston and de Waal 2002). A prior shock experience (mice: Sanders et al. 2013; rats: Atsak et al. 2011; pigeons: Watanabe and Ono 1986) potentiates fear responses to witnessing the shock of another animal, and the observer’s experience promotes empathic helping behaviour (Sato et al. 2015). Vice versa, Langford et al. (2006) showed that pain levels in mice are influenced by the level of pain witnessed in a cage mate. In humans, sharing similar aversive experiences has been shown to facilitate the ability to recognize and share similar distressing emotions with other human beings (Eklund et al. 2009; Preis and Kroener-Herwig 2012). Investigating the extent to which pigs’ response to distress may be affected by previous similar aversive experience is very relevant under commercial situation. Pigs may witness littermates being caught, restrained, castrated or tail-docked after having being exposed to similar procedures themselves. So far, however, no such studies have been reported.

This study aimed at characterizing the response of young pigs to direct observation of a penmate in distress (exposed to restraint) and at investigating whether there was an effect of previous experience on the response to subsequent restraint or exposure to conspecific distress. We hypothesized that conspecific distress would elicit behavioural (locomotion, vocalizations, body/head/ear and tail postures) and physiological (heart rate and heart rate variability) responses, indicating empathic responses in observer piglets, and that this reaction would be more pronounced after being previously restrained.

Materials and methods

Animals and treatment

This study was undertaken at the Institute of Animal Science in Prague (Czech Republic). A total of 100 Landrace × Large White piglets (49.7 ± 0.7 days), coming from 14 different litters, were used. Before weaning, the animals were individually marked using ear tags. At weaning, pairs of litters were mixed together, resulting in piglets being housed in mixed-sex groups of approximately 20 animals in slatted concrete fattening pens (2.6 × 3.0 m) with straw bedding. Piglets had ad libitum access to water and to standard commercial feed formula for growing pigs. The animals were tested in pairs, which consisted of same-sex pigs randomly selected from the same litter. Pairs of pigs were used over three consecutive experimental days and randomly allocated to either a Stress treatment or a Control treatment. There were 32 male pairs and 18 female pairs uniformly distributed among the treatments.

Habituation

On the first experimental day, each piglet of the pair was randomly moved (over approx. 10 m) to one of the two adjacent pens of a test area, which were separated by a wire mesh partition (Fig. 1). The animals were therefore able to smell, hear and see each other. Touching was still possible but limited due to the physical separation. The pens were 1.30 m high to prevent the pigs from seeing the experimenter during testing. Each pen was divided into eight equal areas (0.50 × 0.40 m squares drawn with chalk) in order to assess locomotion. The animals were left in their individual pens for 20 min to get familiar with the testing environment and then returned to their home pen. On the second experimental day, prior to being moved to the test room, animals were fitted with heart rate monitors (Polar Team 2®, Polar Electro Oy, Kempele, Finland). Then, they were moved to the test pen to which they were assigned the previous day. Piglets were left in their test pen for 20–45 min, in order to assess the cardiac baseline defined as a 5-min period during which both piglets were lying down.

Fig. 1
figure 1

Experimental apparatus and procedure during the first phase of stress (pen 1). Con Control treatment (sham-restraint). Restraint periods: the movable wall is not moved. Non-restraint periods: movable wall is moved backward (0.35 m) and then forward (0.35 m) to the initial position. St Stress treatment (restraint). Restraint periods: pig is restrained within the squeezing area using the movable wall. Non-restraint periods: the movable wall is in motion: a wall first moved forward 0.70 m, b after each restraint period, the wall is moved backward 0.35 m and then forward, back to the squeezing position and c after the last restraint, the wall is moved backward, back to its initial position

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Test

On the test day, pairs of pigs were used in a random order. They were fitted with heart rate monitors, and then, they were walked from their home pen to the test room. Each pig was moved in the test pen to which it had been assigned during habituation. In the test room (ambient temperature: 22.5 ± 0.3 °C), the animals were left in their pen for 4 min before Stress Phase 1 started. In Stress Phase 1, pigs in the Stress treatment housed in pen 1 (restrained pig) were exposed to a stressor, while pigs in pen 2 (observer) were not stressed. The stressor consisted of restraining the animal by moving the back wall of the pen towards the animal at a standardized speed (7 cm/s) until it did not have sufficient space to move freely and it was gently squeezed against the wire mesh partition. Throughout the 3 min of stress exposure, there were six 20 s periods of restraint (restraint periods) applied at 10 s intervals (non-restraint periods, Fig. 1). Pigs in the Control treatment housed in pen 1 were subjected to a sham-restraint while pigs in pen 2 (observer) were not. The sham-stress also consisted in moving the back wall (same speed and same duration as real stress) but without decreasing the initial space available to the animal as the wall was moved back and forth and not always towards the animal.

After Stress Phase 1, the animals were left in their pen for 4 min and then Stress Phase 2 commenced. During Stress Phase 2, roles were reversed: the observer pigs of both treatments were exposed to restraint in the way described above, while nothing happened to restrained and sham-restrained pigs, which became observers. At the end of the test, the animals were brought back to their home pen and the heart rate monitors removed. In order to avoid any transfer of information between the subsequent pairs, the pens were quickly cleaned between trials.

Data collection

Behaviour data

The trials were recorded using digital video cameras (Panasonic SDR-H85, 8 MP) to monitor behaviour (Table 1) of each pig during the different phases of this experiment. Vocalizations (grunts and squeals) were scored as a total of occurrences emitted by each pair. Video recordings were analysed using 5 s scan samplings for all behavioural parameters except vocalizations, escape attempts, freezing, defecation, urinating and locomotion which were scored using continuous (all occurrence) sampling. A 15 % sample of all recordings was recoded by an independent observer, and Table 2 records the agreement between the two coders.

Table 1 Definitions of observed behaviours
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Table 2 Reliability analysis of the video recordings (15 % sample): intraclass correlation coefficients (ICC: >0.7 acceptable; >0.8 good; >0.9 excellent) and upper and lower bounds of their 95 % confidence intervals (CI)
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Heart rate

Heart rate (beat-to-beat intervals) was recorded throughout the experiment, using Polar heart rate monitors attached to an elastic belt that was fitted around the pig’s chest. During habituation and test day, pigs were fitted with the elastic belt approximately 10 min before being moved to the experimental room. Data were corrected for artefacts (1 min sections; software: Polar Precision Performance SW, version 4.03.040; settings: very low sensitivity, peak detection on, minimal protection zone of 20). Data sections with more than 10 % artefacts were excluded. Mean heart rate and heart rate variability were calculated in 10-s intervals for each period. Heart rate variability was measured as the standard deviation of interbeat intervals (SDNN, an indicator of both sympathetic and parasympathetic activation) and the root mean of the squared distances of subsequent interbeat intervals (RMSSD, an indicator of parasympathetic activation). During the periods of physical restraint, the heart rate recording was often disrupted, and therefore, the heart rate data were only evaluated in the observer pigs.

Statistical analysis

Only data from the restraint periods of Stress Phase 1 and Stress Phase 2 are reported in this paper. Behavioural variables scored using a continuous sampling were expressed as occurrences per minute, while the other variables were expressed as percentages of occurrences during restraint periods for both stress phases. Defecating, urinating, tail low and wagging tail were extremely rare (1, 0, 1 and 0 times, respectively) and, therefore, were excluded from further analyses. Similarly, no escape attempt was observed for observer animals. Normality was tested (Shapiro–Wilk test) before the analysis. A linear mixed-effects model (PROC MIXED procedure in SAS, SAS Inst. Inc., Cary, NC), with treatment (control sham-restraint vs restraint) and gender as fixed effects and litter as a random effect, was performed to analyse behavioural and cardiac data. A first analysis showed that there was no significant interaction between treatment and gender for any behavioural or cardiac variables during any periods; therefore, it was no longer considered in the analysis. When residual normality was not met, logarithmic transformation was used. Some behavioural variables contained many zeros, and therefore, they were transformed into binary data (0: behaviour never performed vs 1: performed at least once) and analysed with a generalized linear mixed model (PROC GLIMMIX in SAS). Holm–Bonferroni adjustments were used on the behavioural (except vocalizations) and cardiac data to compensate for the inflation of statistical significance that can result from making comparisons on many different dependent variables. Phase 1 and Phase 2 were analysed separately. Untransformed least squares means, standard errors of the mean (SEM) and adjusted P values are reported.

Results

First phase of stress: emotional contagion

Treated pigs

Behaviour

Pigs subjected to restraint spent more time with their ears back (F 1,33: 57.28; P = 0.0002) and looking at their penmate (F 1,33: 9.18; P = 0.0047), moved less (F 1,34: 46.20; P = 0.0005), made more escape attempts (F 1,33: 18.9; P = 0.0004), fewer snout contacts (F 1,33: 28.96; P = 0.0006) than the animals in the Control treatment (Fig. 2). They also spent less time lying down (38.0 vs 0.0 %; SEM: 5.1; F 1,34: 35.43; P = 0.0003).

Fig. 2
figure 2

Behaviour of treated pigs in Control and Stress treatments (N = 25) during the first phase of stress a locomotion, b ears in back position, c escape behaviour, d snout contacts and e head orientated towards penmate. *P < 0.05; **P < 0.01; ***P < 0.001. 1log transformation; 2binary analysis

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Observer pig

Behaviour

Observer pigs in the Stress treatment spent more time close to their penmate (F 1,33: 19.19; P = 0.0007), looking at it (F 1,33: 52.33; P = 0.0008), making more snout contacts (F 1,33: 42.78; P = 0.0009) and displayed more freezing behaviour (F 1,33: 23.93; P = 0.001) than the piglets in the Control treatment (Fig. 3b–e). They also moved less (F 1,34: 12.88; P = 0.005; Fig. 3a) and spent less time lying down (30.9 vs 6.4 %; SEM: 6.6; F 1,34: 13.13; P = 0.0054). No significant differences were found between pigs in Control and Stress treatments for the ears back (39.2 vs 33.7 % of animals that had ears back at least once; F 1,46: 0.15; P = 1.0).

Fig. 3
figure 3

Behaviour of observer pigs in Control and Stress treatments (N = 25) during the first phase of stress a locomotion, b freezing behaviour, c snout contacts, d head orientated towards penmate and e proximity to penmate. *P < 0.05; **P < 0.01; ***P < 0.001

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Heart rate data

Mean heart rate, RMSSD and SDNN did not differ between pigs in Control and Stress treatments (P > 0.05; Table 3).

Table 3 Cardiac data of observer pigs in Control and Stress treatments during the second day of habituation (baseline) and the restraint periods of the first (1) and second (2) phases of stress
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Vocalizations for the pair

The pairs of pigs in the Stress treatment produced fewer grunts (14.3 vs 21.1 grunts/min; SEM: 1.8; F 1,34: 11.09; P = 0.0021) and more squeals (17.8 vs 12.0 squeals/min; SEM: 2.1; F 1,34: 4.30; P = 0.0457) compared to the pigs in the Control treatment.

Second phase of stress: effect of previous experience

Treated pig

Behaviour

No significant differences were found between pigs in Control and Stress treatments for locomotion (53.3 vs 40.2 % of animals that moved at least once; F 1,45: 0.78; P = 1.0) ears back (24.7 vs 38.7 %; SEM: 5.3; F 1,32: 4.84; P = 0.2106), snout contacts (16.6 vs 24.1 % of animals that made contact at least once; F 1,45: 0.46; P = 1.0), escape attempts (4.0 vs 3.7 occurrences/min, SEM: 0.6; F 1,32: 0.03; P = 0.863) and body (lying down 13.4 vs 17.8 % of animals that lie down at least once; F 1,45: 0.18; P = 1.0) or head (15.2 vs 13.8 %, SEM: 3.0; F 1,32: 0.22; P = 1.0) postures.

Observer pig

Behaviour

Pigs previously subjected to restraint spent more time close to their penmate (F 1,32: 26.06; P = 0.001), looking at it (F 1,32: 9.68; P = 0.0273) displayed more freezing behaviour (F 1,32: 12.78; P = 0.0099) and also moved less (F 1,32: 11.65; P = 0.0144) than the pigs that had not previously been restrained (Fig. 4). No significant differences were found between pigs in Control and Stress treatments for the number of snout contacts (7.6 vs 8.7, SEM 0.9; F 1,33: 0.89; P = 1.0), the body (40.6 vs 53.1 % of animals that moved at least once; F 1,45: 0.75; P = 1.0) or ear (ears back: 30.5 vs 34.8 % of animals that had their ears back at least once; F 1,45: 0.10; P = 0.756) postures.

Fig. 4
figure 4

Behaviour of observer pigs in Control and Stress treatments (N = 24) during the second phase of stress a locomotion, b freezing behaviour, c head orientated towards penmate and d proximity to penmate. *P < 0.05; **P < 0.01; ***P < 0.001

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Heart rate data

There were no differences (P > 0.05) in cardiac indicators during restraint periods (Table 3).

Vocalizations for the pair

No significant differences (P > 0.05) were found between pigs in Control and Stress treatments for the number of either grunts (16.8 vs 16.0, SEM: 2.3; F 1,32: 0.09; P = 0.768) or squeals (22.6 vs 20.8, SEM: 2.6; F 1,32: 0.60; P = 0.444).

Gender effect

No significant effect (P > 0.05) of gender was found for any of the behavioural and cardiac variables in the test or observer pigs in Phase 1 and Phase 2.

Discussion

The aims of this study were to characterize the response of young pigs to conspecific distress and to assess whether previous experience influences this response. The results showed that (1) young pigs increased attention towards a stressed conspecific compared to a non-stressed conspecific and showed indications of fear when witnessing a conspecific in distress; (2) this response was strengthened by previous exposure of the observer pig to the same stressor, i.e. a series of brief restraints; and (3) previous perception of a conspecific in distress did not enhance the pigs’ reaction to its restraint. We will discuss these three effects separately.

Reaction of observer pigs to a conspecific in distress

The restrained pigs were obviously distressed, as indicated by their escape attempts, ears laid back and more frequent high-pitched vocalizations. Unlike in previous studies (Düpjan et al. 2011; Reimert et al. 2013), all sensory cues (visual, acoustic, olfactory and—to a limited extent—tactile) were available to the observer animals. Multimodal stimulation is known to facilitate communication between individuals (Partan and Marler 1999; McLeman et al. 2008; Brosch et al. 2009) including emotional transfer (Atsak et al. 2011). The stressor (restraint) was biologically relevant because the pigs may have experienced squeezing or witnessed another littermate being squeezed by the sow during the farrowing/lactation period. The test pairs of piglets were from the same litter as it has been shown that familiarity and/or relatedness is important when it comes to sharing of emotions (Palagi et al. 2009; Špinka 2012; Campbell and de Waal 2014; Gonzalez-Liencres et al. 2014; Jones et al. 2014). Thus, conditions were made conducive for emotional transfer to occur.

The observer pigs responded to conspecific distress with enhanced behaviours specifically directed to their restrained penmates (snout contact, proximity, head orientation). All these behavioural patterns have been observed during empathic responses to conspecific distress (Rice and Gainer 1962; Chen et al. 2009; Hild et al. 2011; Reimert et al. 2013). However, it has also been argued that similar responses are due to increased attention rather than to empathy (Düpjan et al. 2011). When presented with (social or physical) novel or unexpected stimuli, animals respond with behaviours motivated by both curiosity (to gather information and reduce uncertainty) and fear (to avoid potential threats) (Pisula et al. 2012). In the present study, some behaviours displayed by the observer pig in response to the conspecific distress did suggest that the animal’s curiosity was raised. The greater occurrence of snout contacts and head orientation to the penmate may reflect a phase of investigation/approach (Camerlink and Turner 2013; Reimert et al. 2013) during which the animal gathers information on the current situation, including its penmate’s emotional state. On the other hand, the more frequent head orientation towards a penmate, together with reduced locomotion and lying down behaviour, may also indicate increased vigilance as a sign of fear (Welp et al. 2004). The more frequent freezing behaviour in the observer pigs witnessing a conspecific being restrained is a clear sign of fear (Jeon et al. 2010; Sanders et al. 2013; Campbell and de Waal 2014; Jones et al. 2014). Thus, the results indicate that emotional contagion, specifically in the form of transfer of fear from the restrained to the observer pig, occurred in the current study. However, fear in the observer pig was obviously not very strong, as indicated by the absence of escape and also by the fact that other behaviours associated with fear (urination/defecation: Pairis et al. 2009; tail low: Noonan et al. 1994; ears back: Reimert et al. 2013) were either not present (urinate/defecate and tail low) during the stress period or showed no differences (ears back) between the Stress and Control treatments.

No difference in cardiac data was found between observer pigs in the sham-restraint and restraint treatments. Although it has been shown in some studies that observer animals exhibit heart rate correlates of empathy while they experience conspecific distress (Chen et al. 2009; Miller et al. 1966), the cardiac results are not always clear. Other studies found no change in heart rate in animals observing adult conspecifics in distress (Anil et al. 1997; Edgar et al. 2012). Edgar et al. (2011) found that hens’ heart rate increased when their chicks were subjected to stress (a puff of air); however, no effect on heart rate variability indicators was found. Variations between the different studies, including the present study, may indicate that heart rate and heart rate variability may not be the most reliable indicator to assess empathy.

As pointed out by Edgar et al. (2012), evidence for emotional contagion requires a valenced response in the observer pigs, i.e. signs of negative emotional state, as a result of watching a conspecific’s distress, rather than just heightened physical arousal. In the present study, greater response was triggered in the observer pigs by a restrained than by a sham-restrained conspecific. Although some of the indicators (e.g. orientation towards and contacts with the conspecific) could not be assigned a valence with certainty, at least two indicate a negatively valenced response, namely the increased freezing and reduced locomotion.

Further evidence for empathy could be investigated by giving more control to the animal. Rats (Bartal et al. 2011; Sato et al. 2015), dogs (Custance and Mayer 2012), elephants (Plotnik and de Waal 2014), monkeys (Mirsky et al. 1958; Palagi et al. 2014) and apes (Romero et al. 2010) have been observed to actively work to alleviate the distress of another conspecific or even a heterospecific individual (Custance and Mayer 2012). This helping behaviour has been interpreted as a higher more complex level of empathy (de Waal 2008) than the simple emotional contagion and is different from the social buffering (i.e. social support acquired through the mere presence of a conspecific) that has been extensively described in many species (Rault 2012; Gonzalez-Liencres et al. 2014; Mogil 2015). It could be hypothesized that closer proximity and more frequent snout contact found in observer pigs in the Stress treatment may suggest an attempt to influence the situation of their penmate. Therefore, further research could investigate whether, given the opportunity, young pigs would try to reduce distress in a conspecific, e.g. through releasing it from a restraint.

Previous individual restraint affects the reaction of observer pigs to conspecific distress

In the second part of this experiment, we tested the hypothesis that after experiencing a similar stressful situation, pigs would react more strongly to conspecific distress than animals not having experienced the negative situation themselves. The results support this hypothesis. During Stress Period 2, the observer pigs that had been previously restrained reacted more strongly to seeing the penmate in restraint than observer pigs that had not been restrained. This was demonstrated in a similar set of behavioural measures as the “empathic” reaction of the pigs in the first half of the experiment, i.e. in reduced locomotion, more freezing and more time spent close to and looking at the restrained penmate. Having previously experienced what the other animal was going through thus potentiated the pigs’ reaction to conspecific distress. These results are in line with previous works in humans (Eklund et al. 2009; Preis et al. 2013), rodents (Church 1959; Atsak et al. 2011; Sanders et al. 2013) and birds (Watanabe and Ono 1986) which demonstrated that prior experience with a stressor potentiates responses to witnessing another animal exposed to the same stressor. The observer pig in the Stress treatment, when seeing its penmate being restrained, might have feared that it could be subjected to the stressor once again (Sanders et al. 2013). The current finding has important animal welfare implications because most domestic pigs are housed in high concentrations and often witness their penmates being subjected to the same aversive procedures (such as castration, tail docking, teeth clipping, vaccination, restraint) with which they have their negative experience.

Previous witnessing of conspecific distress does not affect reaction to individual restraint

We did not find evidence that reaction of piglets to their restraint was enhanced when they had previously witnessed a penmate subjected to the same procedure. Findings in laboratory mice and rats demonstrated an effect of witnessing others’ distress on later personal distress (Jeon et al. 2010; Atsak et al. 2011). In our study, the absence of this effect might be explained by the fact that seeing a conspecific in restraint may induce only weak fear, and therefore, this previous experience was overshadowed by the stronger distress of undergoing the restraint “in person”. In contrast, the mice studies utilized an electric foot-shock paradigm which probably produced much more salient distress cue from the foot-shocked conspecific.

Gender effects

No gender effects and no interaction effects between gender and treatment were found. This leads us to conclude that the above effects of emotional contagion and previous experience apply similarly to both sexes. Many but not all previous studies have found that females are more prone to emotional contagion than males (review by Christov-Moore et al. 2014). However, as documented in meta-analyses (for human studies) by McClure (2000) and Thompson and Voyer (2014), the general size of the sex effect on empathic abilities is small to moderate in relation to the interindividual variability. Thus, a sex difference might not be apparent in a study with modest sample size. Also, it has been shown for humans that the sex difference in empathic perception and behaviour gets fully developed after puberty when the biological sex roles become more prominent determinants of adaptive behaviour (Christov-Moore et al. 2014). So it is possible that while sex differences in emotional contagion in post-weaning pigs are small or non-existent, they may become more pronounced later in ontogeny.

Implications and conclusion

The findings of the current study (contagion of fear from a distressed conspecific and potentiation of this response by previous stress) have implications for welfare of group housed pigs as each of them can cause extra negative affective experience above that caused by the physical stressor directly. Obviously, each of these two indirect effects impairs pig welfare less than the direct stress from the physical restraint. Nevertheless, in combination, their impact on welfare could be quite significant. When pigs are repeatedly submitted to certain types of stressor (e.g. catching and restraint, or intraspecific fighting), then they additionally suffer from contagious fear when they witness the stress of the others, plus they cross-inflate their fear reactions to the next event of their or another’s distress. The next question for research is to quantify how significant (biologically, not just statistically) the indirect, socially transmitted welfare impairments are, relative to the direct effects of various stressors. This question is important for housing, handling and management of many species including farm, laboratory and zoo animals, as well as species affected by wildlife management and tourism.

In conclusion, the study indicates that young pigs react to distress of their companions through a mixture of attention and fear contagion. Moreover, the experience of distress makes piglets more sensitive to the fear cues from a stressed conspecific. These findings enlarge the list of species in which emotional contagion was proven and have important practical and ethical implications for aversive procedures that are being routinely applied to group housed domestic pigs on farms across the world.