Inonge Reimert

Indicators of positive and negative emotions and emotional contagion in pigs

For the welfare of group-housed animals, such as pigs, the emotional state of an individual pig is relevant, but also the extent to which pen mates are affected by the distress or pleasure of other individuals, i.e. emotional contagion, a simple form of empathy. Therefore, indicators of positive and negative emotions were investigated in pigs during anticipation and experience of a rewarding (access in pairs to a compartment with straw, peat and chocolate raisins) or aversive (social isolation combined with negative, unpredictable interventions) event. Thereafter the same indicators were investigated in naive pigs during anticipation and experience of a rewarding or aversive event by their trained pen mates. Positive emotions could be indicated by play, barks and tail movements, while negative emotions could be indicated by freezing, defecating, urinating, escape attempts, high-pitched vocalizations (screams, squeals or grunt-squeals), tail low, ears back and ear movements. Salivary cortisol measurements supported these behavioral observations. During anticipation of the aversive event, naive pigs tended to show more tail low. During the aversive event, naive pigs tended to defecate more, while they played more during the rewarding event. These results suggest that pigs might be sensitive to emotional contagion, which could have implications for the welfare of group-housed pigs. Pig emotions and the process of emotional contagion merit, therefore, further research.

The prospects of selection for social genetic effects to improve welfare and productivity in livestock

Social interactions between individuals living in a group can have both positive and negative effects on welfare, productivity, and health of these individuals. Negative effects of social interactions in livestock are easier to observe than positive effects. For example, laying hens may develop feather pecking, which can cause mortality due to cannibalism, and pigs may develop tail biting or excessive aggression. Several studies have shown that social interactions affect the genetic variation in a trait. Genetic improvement of socially-affected traits, however, has proven to be difficult until relatively recently. The use of classical selection methods, like individual selection, may result in selection responses opposite to expected, because these methods neglect the effect of an individual on its group mates (social genetic effects). It has become clear that improvement of socially-affected traits requires selection methods that take into account not only the direct effect of an individual on its own phenotype but also the social genetic effects, also known as indirect genetic effects, of an individual on the phenotypes of its group mates. Here, we review the theoretical and empirical work on social genetic effects, with a focus on livestock. First, we present the theory of social genetic effects. Subsequently, we evaluate the evidence for social genetic effects in livestock and other species, by reviewing estimates of genetic parameters for direct and social genetic effects. Then we describe the results of different selection experiments. Finally, we discuss issues concerning the implementation of social genetic effects in livestock breeding programs. This review demonstrates that selection for socially-affected traits, using methods that target both the direct and social genetic effects, is a promising, but sometimes difficult to use in practice, tool to simultaneously improve production and welfare in livestock.

Social support in pigs with different coping styles.

The presence of a conspecific during a stressful situation, i.e. social support, can considerably lower the stress response of an individual compared to experiencing the stressful situation alone. Pigs also benefit from social support, but it is not known whether the extent to which they benefit is dependent on their personality or coping style. In this study, therefore, the effect of social support on behavioral and physiological (i.e. salivary cortisol, heart rate and the heart rate variability parameters standard deviation (SDNN) and root mean square of successive differences (RMSSD)) stress responses was studied in pigs with different coping styles. Based on the backtest, piglets were classified as high-resisting (HR) or low-resisting (LR). At 11weeks of age, 12 gilts of each coping style were subjected to a 15min restraint test in a weighing cage without a pen mate present (i.e. no support treatment) and 12 other gilts of each coping style were subjected to this test with a pen mate, a boar with the same coping style, present (i.e. support treatment). With the pen mate present, LR gilts showed less standing alert behavior and they had their ears back less often than without the pen mate present. On the other hand, HR gilts seemed to spend less time on escaping the cage and more HR gilts seemed to urinate in the situation when the pen mate was present than without the pen mate present, but this was not significant. Independently of the test situation, HR gilts grunted more than LR gilts and they were more likely to urinate than LR gilts. Salivary cortisol concentrations were not affected by treatment or coping style, but were increased at 30min after the start of the test after which concentrations decreased again to starting levels. The heart rate and heart rate variability parameters RMSSD and RMSSD/SDNN ratio were not affected by treatment or coping style, but the SDNN was lower in the LR pigs during the first and last 5min of the test when a pen mate was present than without the pen mate present. In addition, heart rate and heart rate variability were increased during the test compared to before and after the test. No differences in behavior and salivary cortisol concentrations were found between the HR and LR accompanying boars. Although effects of social support were not found on all variables measured, the results do indicate that pigs may benefit from social support during a stressful situation and that pigs with a low-resisting coping style will likely benefit more than pigs with a high-resisting coping style.

Backtest and novelty behavior of female and castrated male piglets, with diverging social breeding values for growth.

Pigs housed together in a group influence each others growth. Part of this effect is genetic and can be represented in a social breeding value. It is unknown, however, which traits are associated with social breeding values. The aim of this study was, therefore, to investigate whether personality and response to novelty could be associated with social breeding values for growth in piglets. Female and castrated male piglets from 80 litters, with either an estimated relative positive or negative social breeding value (+SBV or -SBV) for growth, were individually tested in a backtest and novel environment test, and group-wise in a novel object (i.e., a feeder with feed) test and human approach test. All tests were performed during the suckling period. No differences between +SBV and -SBV piglets were found for the frequency and latency of struggling and vocalizing in the backtest (at least, P > 0.30). In the novel object test, piglets with a +SBV for growth touched the feeder faster than piglets with -SBV for growth (P = 0.01) and were more frequently present near the person in the human approach test (P < 0.01). No behavioral differences between +SBV and -SBV piglets were found in the novel environment test (at least, P > 0.40), but piglets that struggled more in the backtest walked more in this test (P = 0.02). Behavior was affected by gender in each test. Female piglets were faster than castrated male piglets to start struggling in the backtest (P = 0.047). In the novel object test, females were faster than males to touch the feeder and sample the feed. In the human approach test, they were also faster than male piglets to touch a person (all, P < 0.001). Females were also more frequently present near the feeder (P < 0.001) and person (P = 0.03). In the novel environment test, female piglets explored the floor more (P = 0.046), produced less low- (P = 0.04) and high-pitched vocalizations (P = 0.02), and defecated (P = 0.08) and urinated less than male piglets (P < 0.01). It was concluded that +SBV and -SBV piglets do not differ in their response to the backtest, and only subtle differences were found in their response to novelty. More research is warranted to identify the traits underlying SBV for growth in pigs. Moreover, castrated male piglets seemed to react more fearfully to each test than female piglets.

Tail Biting in Pigs: Blood Serotonin and Fearfulness as Pieces of the Puzzle?

Tail biting in pigs is a widespread problem in intensive pig farming. The tendency to develop this damaging behaviour has been suggested to relate to serotonergic functioning and personality characteristics of pigs. We investigated whether tail biting in pigs can be associated with blood serotonin and with their behavioural and physiological responses to novelty. Pigs (n = 480) were born in conventional farrowing pens and after weaning at four weeks of age they were either housed barren (B) or in straw-enriched (E) pens. Individual pigs were exposed to a back test and novel environment test before weaning, and after weaning to a novel object (i.e. bucket) test in an unfamiliar arena. A Principal Component Analysis on behaviours during the tests and salivary cortisol (novel object test only) revealed five factors for both housing systems, labeled ‘Early life exploration’, ‘Near bucket’, ‘Cortisol’, ‘Vocalizations & standing alert’, and ‘Back test activity’. Blood samples were taken at 8, 9 and 22 weeks of age to determine blood platelet serotonin. In different phases of life, pigs were classified as tail biter/non-tail biter based on tail biting behaviour, and as victim/non-victim based on tail wounds. A combination of both classifications resulted in four pig types: biters, victims, biter/victims, and neutrals. Generally, only in phases of life during which pigs were classified as tail biters, they seemed to have lower blood platelet serotonin storage and higher blood platelet uptake velocities. Victims also seemed to have lower blood serotonin storage. Additionally, in B housing, tail biters seemed to consistently have lower scores of the factor ‘Near bucket’, possibly indicating a higher fearfulness in tail biters. Further research is needed to elucidate the nature of the relationship between peripheral 5-HT, fearfulness and tail biting, and to develop successful strategies and interventions to prevent and reduce tail biting.

Enriched Housing Reduces Disease Susceptibility to Co-Infection with Porcine Reproductive and Respiratory Virus (PRRSV) and Actinobacillus pleuropneumoniae (A. pleuropneumoniae) in Young Pigs

Until today, anti-microbial drugs have been the therapy of choice to combat bacterial diseases. Resistance against antibiotics is of growing concern in man and animals. Stress, caused by demanding environmental conditions, can reduce immune protection in the host, influencing the onset and outcome of infectious diseases. Therefore psychoneuro-immunological intervention may prove to be a successful approach to diminish the impact of diseases and antibiotics use. This study was designed to investigate the effect of social and environmental enrichment on the impact of disease, referred to as “disease susceptibility”, in pigs using a co-infection model of PRRSV and A. pleuropneumoniae. Twenty-eight pigs were raised in four pens under barren conditions and twenty-eight other pigs were raised in four pens under enriched conditions. In the enriched pens a combination of established social and environmental enrichment factors were introduced. Two pens of the barren (BH) and two pens of the enriched housed (EH) pigs were infected with PRRSV followed by A. pleuropneumoniae, the other two pens in each housing treatment served as control groups. We tested if differences in disease susceptibility in terms of pathological and clinical outcome were related to the different housing regimes and if this was reflected in differences in behavioural and immunological states of the animals. Enriched housed pigs showed a faster clearance of viral PRRSV RNA in blood serum (p = 0.014) and histologically 2.8 fold less interstitial pneumonia signs in the lungs (p = 0.014). More barren housed than enriched housed pigs developed lesions in the lungs (OR = 19.2, p = 0.048) and the lesions in the barren housed pigs showed a higher total pathologic tissue damage score (p<0.001) than those in enriched housed pigs. EH pigs showed less stress-related behaviour and differed immunologically and clinically from BH pigs. We conclude that enriched housing management reduces disease susceptibility to co-infection of PRRSV and A. pleuropneumoniae in pigs. Enrichment positively influences behavioural state, immunological response and clinical outcome in pigs.

Heritability of the backtest response in piglets and its genetic correlations with production traits

The backtest response of a pig gives an indication of its coping style, that is, its preferred strategy to cope with stressful situations, which may in turn be related to production traits. The objective of this study was therefore to estimate the heritability of the backtest response and estimate genetic correlations with production traits (birth weight, growth, fat depth and loin depth). The backtest was performed by placing the piglet on its back for 60 s and the number of struggles (NrS) and vocalizations (NrV), and the latency to struggle and vocalize (LV) was recorded. In total, 992 piglets were subjected to the backtest. Heritability estimates for backtest traits were statistically moderate (although high for behavioral traits), with LV having the highest heritability estimate (0.56±0.10, P<0.001) and NrS having the lowest estimate (0.37±0.09, P<0.001). Backtest traits also had high genetic correlations with each other, with vocalization traits (NrV and LV) having the highest (-0.94±0.03, P<0.001), and NrS with NrV the lowest correlation (0.70±0.09, P<0.001). No significant correlations were found between backtest traits and production traits, but correlations between NrS and birth weight (-0.38±0.25), and NrV and loin depth (-0.28±0.19) approached significance (P=0.07). More research into genotype-by-environment interactions may be needed to assess possible connections between backtest traits and production traits, as this may depend on the circumstances (environment, experiences, etc.). In conclusion, heritability estimates of backtest traits are high and it would therefore be possible to select for them. The high genetic correlations between backtest traits indicate that it may be possible to only consider one or two traits for characterization and selection purposes. There were no significant genetic correlations found between backtest traits and production traits, although some of the correlations approached significance and hence warrant further research.

Effects of environmental enrichment and regrouping on natural autoantibodies-binding danger and neural antigens in healthy pigs with different individual characteristics

Pigs living in commercial husbandry systems may experience both acute stress due to standard management procedures and chronic stress through limitations in their barren housing environment. This might influence their immune status, including antibody responses to neural and danger autoantigens. Levels of natural autoantibody (NAAb)-binding phosphorylcholine-conjugated bovine serum albumin (PC-BSA) and myelin basic protein (MBP) were measured over time in pigs that were kept in environmental enriched v. barren housing, and that underwent a regrouping test. In total, 480 pigs were housed in 80 pens in either barren or straw-enriched pens from 4 through 23 weeks of age. Blood samples were taken from pigs before (week 8), and 3 days after a 24 h regrouping test (week 9), and at 22 weeks of age. Phosphorylcholine-conjugated bovine serum albumin (PC-BSA) and MBP antibody titres in serum were measured using ELISA. Enriched-housed pigs had higher levels of IgM-binding MBP, and tended to have higher levels of IgG-binding MBP and IgA-binding PC-BSA than barren-housed pigs. Each NAAb measured in this study was affected by gender and litter. These results suggest that enriched housing conditions, as well as acute regrouping stress, have an influence on levels of serum NAAb-binding danger and neural antigens in pigs.

Tail biting in pigs: (in)consistency, blood serotonin, and responses to novelty

Chronic stress is a long-lasting negative emotional state which induces negative consequences on animals’ behavior. This study aimed at assessing whether unpredictable and repeated negative stimuli (URNS) influence feeding behavior in quail, and whether this can be modulated by their emotionality. Two lines of quail divergently selected on their inherent emotionality (low emotionality, STI; high emotionality, LTI) were either daily exposed to URNS or undisturbed from 17 to 40 days of age (n=32 for each line, in each group). During this time, quail were submitted twice to a sequential feeding procedure: they were offered a hypocaloric diet (7% less caloric than the normocaloric diet) on odd days and a hypercaloric diet (7% more caloric) on even days, for 8 days; then, they received a normocaloric diet (metabolizable energy=12.56 MJ) for 3 days. This sequential feeding procedure was used to assess anhedonia and diet preferences thanks to choice tests (hypo vs. hypercaloric diets) performed at the end of each period. Short-term (30 min) and daily intake were also measured each day. Behavioral tests were performed to assess quail’s emotional reactivity. Results showed that URNS enhanced quails’ emotional reactivity, e.g. in the reactivity to human test, disturbed quail came later (P=0.011) and spent less time (P 0.1), but URNS reduced their daily intake during the 2nd period (P<0.05). Motivation for each diet (assessed by their short-term intake) was differently affected by URNS during the 2nd period: STI quail decreased their motivation to eat the hypercaloric diet (P<0.01) whereas LTI increased their motivation to eat the hypocaloric diet (P<0.01). In conclusion, both lines of quail experienced a chronic stress as URNS induced an increase of their emotional reactivity. Interestingly, URNS induced opposite changes in quail’s feeding behavior: LTI disturbed quail seemed to express a short-term compensatory behavior because of their high motivation to eat, whereas STI disturbed quail seemed to be in a devaluation process as shown by their anhedonia and their decrease of daily intake.Farm animals have to adapt to human presence from birth and being handled may lead to fear and stress reactions. It is known that the mother can be used as a postnatal model in the development of young-human relationship. Through her, some information like auditory ones may even be learnt prenatally. We tested this idea in pigs because they communicate a lot by acoustic signals. The hypotheses were that prenatal experience with human voice could modify behavioural reactions to the experienced voice and to an unfamiliar voice expressing different emotions. We worked with 30 pregnant sows from the last month of gestation. Ten sows (treatment A) were submitted to recordings of human voices during handling: vA during positive interactions and vB during negative interactions, twice a day, 5 days a week, for 10 minutes. Ten other sows (treatment B) received the contrary, i.e. vB during positive interactions and vA during negative interactions. Ten last sows (treatment C) received no vocal stimulations during handling sessions. Two days old piglets (36 A, 39 B, 35 C) were submitted to a 5 min choice test between voices vA and vB in a testing pen (2×1 m). Each voice was played back through loudspeakers positioned at each end of the pen. At 15-18 days of age, 20 other piglets from each treatment were tested in the same conditions except that we played back the voice of an unknown person, reading the same text with a joyful or angry intention. In both tests we recorded vocalisations and locomotion. Data were analysed using non parametric statistics (Statview). In both tests, A and B piglets started to move sooner (P 0.05) to be and the time spent (178 s (46s)) close to the loudspeakers did not depend on the treatment (P>0.05). We also found no difference between the time spent close to one loudspeaker or the other, neither for vA versus vB, nor for joyful versus angry intention (P>0.05). The results show that the prenatal experience of human voice reduces postnatal behavioural reactions of stress (vocalisations, latency to move) during the playback human voices. However, it does not seem to induce specific attraction toward human voice, or human emotional intention. Therefore prenatal experience with human voice may be a good way of reducing fear reactions to human voice after birth.