J. Elizabeth Bolhuis

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.

Prenatal flavor exposure affects growth, health and behavior of newly weaned piglets

Young animals can learn about flavors from the maternal diet that appear in the amniotic fluid and mothers milk, which may reduce neophobia for similarly flavored food types at weaning. Flavor learning may be beneficial for piglets, which after the rather abrupt weaning in pig husbandry frequently show a period of anorexia, reduced health, and stress-induced behaviors. We investigated the effects of pre- and postnatal flavor exposure through the maternal diet on acceptance of a similarly flavored food and subsequent growth, health and behavior of newly weaned piglets. Sows were offered anise-flavored (F) or control (C) food during late gestation. Piglets were cross-fostered after birth, with each sow fostering 5 piglets from an F sow and 5 from a C sow. During lactation, sows were offered F or C food, resulting in FF, CF, FC and CC piglets. Piglets were weaned on day 25 and were given both control and flavored food for two weeks using a double food choice approach. The flavored food was not preferred. Yet, prenatally exposed animals showed a higher food intake and a higher body weight in the first days after weaning, and a lower occurrence of diarrhoea than non-exposed piglets. Prenatal exposure also increased the latency to fight, and reduced oral manipulation of pen mates and mounting during the first two weeks after weaning. Prenatal exposure, but not postnatal exposure alone, to anisic flavor through the maternal diet reduced weaning-associated problems in piglets and enhanced their health and welfare in the period after weaning.

The Observer XT: A tool for the integration and synchronization of multimodal signals

The Observer was originally developed as a manual event recorder for the collection, management, analysis, and presentation of observational data in animals. Because of the flexibility of later versions, it became clear that The Observer was suitable for almost any study involving collection of observational data in both animals and humans. Furthermore, the most recent version of The Observer (The Observer XT) allows the integration and synchronization of multimodal signals from various sources, such as observational, video, tracking, and physiological data. This article describes how The Observer XT was used to integrate and synchronize video, observational, tracking, and physiological data from an experiment carried out in 2001 at the Wageningen Institute of Animal Sciences of Wageningen University and Research Centre. The integration and synchronization of these multimodal signals in The Observer XT allows the user to draw a more complete picture of the phenomena under study.

Prenatal Flavor Exposure Affects Flavor Recognition and Stress-Related Behavior of Piglets

Exposure to flavors in the amniotic fluid and mothers milk derived from the maternal diet has been shown to modulate food preferences and neophobia of young animals of several species. Aim of the experiment was to study the effects of pre- and postnatal flavor exposure on behavior of piglets during (re)exposure to this flavor. Furthermore, we investigated whether varying stress levels, caused by different test settings, affected behavior of animals during (re)exposure. Piglets were exposed to anisic flavor through the maternal diet during late gestation and/or during lactation or never. Piglets that were prenatally exposed to the flavor through the maternal diet behaved differently compared with unexposed pigs during reexposure to the flavor in several tests, suggesting recognition of the flavor. The differences between groups were more pronounced in tests with relatively high stress levels. This suggests that stress levels, caused by the design of the test, can affect the behavior shown in the presence of the flavor. We conclude that prenatal flavor exposure affects behaviors of piglets that are indicative of recognition and that these behaviors are influenced by stress levels during (re)exposure.

Effects of dietary fibers with different physicochemical properties on feeding motivation in adult female pigs.

The satiating effects of dietary fiber may depend more on physicochemical properties of the fiber than on total fiber intake. These properties are expected to affect satiety feelings and feeding motivation due to different effects in the gastrointestinal tract. The aim of the current study was to assess the effects of fibers with varying physicochemical properties (bulkiness, viscosity and fermentability) on feeding motivation in adult female pigs. Sixteen pair-housed pigs received four diets: lignocellulose (LC), pectin (PEC), resistant starch (RS), and control (C) without fiber, in four periods in a Latin square design. Each fiber was fed at a low (L) followed by a high (H) inclusion level (7 days each). At 1h, 3h, and 7h after the morning meal, feeding motivation was assessed in an operant test, where turning a wheel yielded multiple food rewards, and in a runway test, where walking a fixed U-shaped track yielded one food reward. Pigs were observed in their home pen for 6h, using 90-s instantaneous scan sampling. In the operant test, throughout the day feeding motivation was higher for pigs on PEC compared with pigs on LC. In the runway, feeding motivation increased particularly at 1h after the meal for pigs on PEC compared with pigs on RS. Also at 7h, feeding motivation tended to decrease for pigs on RS compared with pigs fed other diets. In their home pen, pigs on PEC showed more feeder-directed behavior compared with pigs on RS. In conclusion, PEC was the least satiating fiber. LC and RS, despite a lower supply of available energy, were the most satiating fibers, possibly due to their bulky and fermentation properties, respectively.

Indirect Genetic Effects and Housing Conditions in Relation to Aggressive Behaviour in Pigs

Indirect Genetic Effects (IGEs), also known as associative effects, are the heritable effects that an individual has on the phenotype of its social partners. Selection for IGEs has been proposed as a method to reduce harmful behaviours, in particular aggression, in livestock and aquaculture. The mechanisms behind IGEs, however, have rarely been studied. The objective was therefore to assess aggression in pigs which were divergently selected for IGEs on growth (IGEg). In a one generation selection experiment, we studied 480 offspring of pigs (Sus scrofa) that were selected for relatively high or low IGEg and housed in homogeneous IGEg groups in either barren or enriched environments. Skin lesion scores, a proxy measure of aggression, and aggressive behaviours were recorded. The two distinct IGEg groups did not differ in number of skin lesions, or in amount of reciprocal fighting, both under stable social conditions and in confrontation with unfamiliar pigs in a 24 h regrouping test. Pigs selected for a positive effect on the growth of their group members, however, performed less non-reciprocal biting and showed considerably less aggression at reunion with familiar group members after they had been separated during a 24 h regrouping test. The enriched environment was associated with more skin lesions but less non-reciprocal biting under stable social conditions. Changes in aggression between pigs selected for IGEg were not influenced by G×E interactions with regard to the level of environmental enrichment. It is likely that selection on IGEg targets a behavioural strategy, rather than a single behavioural trait such as aggressiveness.

Parents and early life environment affect behavioral development of laying hen chickens

Severe feather pecking (SFP) in commercial laying hens is a maladaptive behavior which is associated with anxiety traits. Many experimental studies have shown that stress in the parents can affect anxiety in the offspring, but until now these effects have been neglected in addressing the problem of SFP in commercially kept laying hens. We therefore studied whether parental stock (PS) affected the development of SFP and anxiety in their offspring. We used flocks from a brown and white genetic hybrid because genetic background can affect SFP and anxiety. As SFP can also be influenced by housing conditions on the rearing farm, we included effects of housing system and litter availability in the analysis. Forty-seven rearing flocks, originating from ten PS flocks were followed. Behavioral and physiological parameters related to anxiety and SFP were studied in the PS at 40 weeks of age and in the rearing flocks at one, five, ten and fifteen weeks of age. We found that PS had an effect on SFP at one week of age and on anxiety at one and five weeks of age. In the white hybrid, but not in the brown hybrid, high levels of maternal corticosterone, maternal feather damage and maternal whole-blood serotonin levels showed positive relations with offsprings’ SFP at one week and offsprings’ anxiety at one and five weeks of age. Disruption and limitation of litter supply at an early age on the rearing farms increased SFP, feather damage and fearfulness. These effects were most prominent in the brown hybrid. It appeared that hens from a brown hybrid are more affected by environmental conditions, while hens from a white hybrid were more strongly affected by parental effects. These results are important for designing measures to prevent the development of SFP, which may require a different approach in brown and white flocks.

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.

Perinatal Flavour Learning and Adaptation to Being Weaned: All the Pig Needs Is Smell

Perinatal flavour learning through the maternal diet is known to enhance flavour preference and acceptance of flavoured food in many species, yet still little is known about the mechanism underlying perinatal flavour learning. Previously we found positive effects of perinatal flavour learning on food intake, growth and behaviour of piglets postweaning, but no increased preference for the flavour. This suggests that flavour learning in pigs works through a reduction of weaning stress by the presence of the familiar flavour instead. The aim of this study was to investigate whether perinatal flavour learning reduces stress at weaning, and whether the effect is stronger when the familiar flavour is present in the food. Sows were offered an anethol-flavoured diet (Flavour treatment) or control diet (Control treatment) during late gestation and lactation. Flavour and Control piglets were provided with anethol either in their food (Food treatment) or in the air (Air treatment) after weaning. Preweaning and postweaning treatments did not affect food intake, preference or growth in the first two weeks postweaning but flavour treatment reduced the latency to eat (24 versus 35 hours, P = 0.02) and within-pen variation in growth (SD within-pen: 0.7 versus 1.2 kg, P<0.001). Salivary cortisol levels tended to be lower four and seven hours postweaning for Flavour piglets compared to Control piglets (4 hours: 2.5 versus 3.0 ng/ml, P = 0.05, 7 hours: 3.1 versus 3.4 ng/ml, P = 0.08). Flavour piglets played more and showed less damaging behaviours than Control piglets, indicating that the familiar flavour reduced stress around weaning. Few interaction effects were found between preweaning and postweaning treatment, and no effects of postweaning treatment. We conclude that in the newly weaned pig, perinatal flavour learning results in a reduction of stress when the familiar flavour is present, regardless of providing the flavour in the food or in the air.

Maternal presence and environmental enrichment affect food neophobia of piglets

Young omnivores show food neophobia in order to avoid the potential harmful effects of ingesting unfamiliar food items. We investigated whether the presence of the mother and an enriched rearing environment would reduce food neophobia in piglets. A mother may provide information on suitable food types to include in the diet, whereas an enriched environment may stimulate behavioural development and reduce reactivity towards novel stimuli (including food). Five barren-reared or enriched-reared piglets per litter were exposed to two novel food items in the presence, and the other five per litter in the absence, of the mother in a 7 min test. Maternal presence reduced food neophobia profoundly as reflected in a reduced latency to touching the food, a higher proportion of piglets sampling the two different food items and a higher intake. Latency to touch the food, however, was affected by maternal presence more strongly for barren-reared piglets than for enriched-reared piglets, and in the absence of the sow, consumption of one novel food type and time spent in the feeding area were higher for enriched-reared piglets. Environmental enrichment does have the potential to reduce food neophobia, but the presence of the mother during the encounter with novel food seems more efficient in decreasing food neophobia of piglets.