T. Bas Rodenburg

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.

Welfare, Health, and Hygiene of Laying Hens Housed in Furnished Cages and in Alternative Housing Systems

The aim of this review was to compare welfare, health, and hygienic status of laying hens housed in furnished cages and in alternative systems. In alternative systems (floor housing and aviaries), birds have more freedom of movement and a more complex environment than in furnished cages. However, housing birds in much larger flocks in alternative systems leads to an increased risk of feather-pecking. Furthermore, air quality can be poorer in alternative systems than in furnished cages. This can affect health and hygienic status. There are only limited data on a direct comparison between furnished cages and alternative systems. Therefore, there is a need for an on-farm comparison of welfare, health, and hygienic status in these systems.

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.

Omnivores Going Astray: A Review and New Synthesis of Abnormal Behavior in Pigs and Laying Hens

Pigs and poultry are by far the most omnivorous of the domesticated farm animals and it is in their nature to be highly explorative. In the barren production environments, this motivation to explore can be expressed as abnormal oral manipulation directed toward pen mates. Tail biting (TB) in pigs and feather pecking (FP) in laying hens are examples of unwanted behaviors that are detrimental to the welfare of the animals. The aim of this review is to draw these two seemingly similar abnormalities together in a common framework, in order to seek underlying mechanisms and principles. Both TB and FP are affected by the physical and social environment, but not all individuals in a group express these behaviors and individual genetic and neurobiological characteristics play an important role. By synthesizing what is known about environmental and individual influences, we suggest a novel possible mechanism, common for pigs and poultry, involving the brain–gut–microbiota axis.

The relation between fearfulness in young and stress-response in adult laying hens, on individual and group level

Fearfulness of an individual can affect its sensitivity to stress, while at the same time the social situation in which an animal lives can affect its fear level. It is however unknown what the long-term effects of high fearfulness on sensitivity to stress are, on individual or group level in laying hens. We hypothesize that increased fearfulness at a young age results in increased sensitivity to stress at an adult age, and that this relation can differ between groups, due to differences in group composition. Therefore, we studied the relation between fearfulness in an Open Field (OF) test at six weeks of age and plasma-corticosterone (CORT) levels after a 5-min Manual Restraint test (MR) at 33 weeks of age, and assessed behavior in the home pen. We used birds from a low mortality line, selected for four generations on low mortality due to feather pecking and cannibalism and a control line (n=153 in total, eight pens/line). These lines are known to differ in fearfulness and stress physiology. Chicks from the low mortality line were more active in the OF compared to chicks from the control line. Chicks that showed a fearful response (no walking, no vocalizing) in the OF test had higher CORT at 33 weeks of age than chicks that walked and/or vocalized in the OF test and had higher activity in the home pen as adults. On group level, a passive response in the OF was related to high CORT levels after MR. Presence of at least one fearful bird in a group led to higher CORT in the other group mates compared to birds from groups with no fearful birds present. Birds from groups in which more than 50% of birds had severe comb lesions had higher CORT levels compared to birds from groups with less than 50% of birds affected. High fearfulness of laying hen chicks can on individual level have a long-term effect on stress sensitivity. The presence of fearful birds in a group as well as signs of social instability in a group, indicated by comb lesions, can affect sensitivity to stress of birds from the same group. The mechanism by which this occurs can lie in social transmission of (fear related) behavior, but this suggestion needs further investigation.

Effects of feather pecking phenotype (severe feather peckers, victims and non-peckers) on serotonergic and dopaminergic activity in four brain areas of laying hens (Gallus gallus domesticus)

Severe feather pecking (SFP) in laying hens is a detrimental behavior causing loss of feathers, skin damage and cannibalism. Previously, we have associated changes in frontal brain serotonin (5-HT) turnover and dopamine (DA) turnover with alterations in feather pecking behavior in young pullets (28-60 days). Here, brain monoamine levels were measured in adult laying hens; focusing on four brain areas that are involved in emotional behavior or are part of the basal ganglia-thalamopallial circuit, which is involved in obsessive compulsive disorders. Three behavioral phenotypes were studied: Severe Feather Peckers (SFPs), Victims of SFP, and Non-Peckers (NPs). Hens (33 weeks old) were sacrificed after a 5-min manual restraint test. SFPs had higher 5-HIAA levels and a higher serotonin turnover (5-HIAA/5-HT) in the dorsal thalamus than NPs, with intermediate levels in victims. NPs had higher 5-HT levels in the medial striatum than victims, with levels of SFPs in between. 5-HT turnover levels did not differ between phenotypes in medial striatum, arcopallium and hippocampus. DA turnover levels were not affected by feather pecking phenotype. These findings indicate that serotonergic neurotransmission in the dorsal thalamus and striatum of adult laying hens depends on differences in behavioral feather pecking phenotype, with, compared to non-pecking hens, changes in both SFP and their victims. Further identification of different SFP phenotypes is needed to elucidate the role of brain monoamines in SFP.

Exposure to Increased Environmental Complexity during Rearing Reduces Fearfulness and Increases Use of Three-Dimensional Space in Laying Hens (Gallus gallus domesticus)

The complexity of the rearing environment is important for behavioral development and fearfulness. The aim of this study was to test the hypothesis that laying hens reared in a complex aviary system with exposure to mild intermittent stressors would be less fearful, less sensitive to stress, and would use elevated areas of the pen more often as adults than hens reared in a barren cage environment. Laying hens (N = 160) were housed in the same rearing house; half of the birds (n = 80) in an aviary and the other half (n = 80) in cages. At 16 weeks of age, the birds were transported to the experimental facilities. Their behavior was recorded at 19 and 23 weeks of age and analyzed by analysis of variance on individual scores for a fearfulness-related principal component generated using principal component analysis. The results indicate that aviary-reared birds have lower levels of fearfulness compared with cage-reared birds both at 19 weeks and at 23 weeks of age. When comparing the response induced by initial exposure to a novel object at 19 and 23 weeks of age, more aviary-reared birds tended to fly up at 19 weeks compared to the cage-reared birds, indicating a tendency toward a more active behavioral response in the aviary-reared birds than in cage-reared birds. There was no difference between treatments in the flight response at 23 weeks. The groups did not differ in defecation frequency or the concentration of fecal corticosterone metabolites at either age. At 19 weeks, observation of the spatial distribution in the home pens indicated that more aviary-reared birds spent time on the low perch, the elevated platform, and the upper perch, compared to the cage-reared birds. However, at 23 weeks of age, these differences were no longer detected. The results of this study support the hypothesis that increased environmental complexity during rearing reduces fearfulness of adult laying hens.

Specific characteristics of the aviary housing system affect plumage condition, mortality and production in laying hens.

Feather pecking and high mortality levels are significant welfare problems in non-cage housing systems for laying hens. The aim of this study was to identify husbandry-related risk factors for feather damage, mortality, and egg laying performance in laying hens housed in the multi-tier non-cage housing systems known as aviaries. Factors tested included type of system flooring, degree of red mite infestation, and access to free-range areas. Information on housing characteristics, management, and performance in Belgian aviaries (N=47 flocks) were obtained from a questionnaire, farm records, and farm visits. Plumage condition and pecking wounds were scored in 50 randomly selected 60-week-old hens per flock. Associations between plumage condition, wounds, performance, mortality, and possible risk factors were investigated using a linear model with a stepwise model selection procedure. Many flocks exhibited a poor plumage condition and a high prevalence of wounds, with considerable variation between flocks. Better plumage condition was found in wire mesh aviaries (P<0.001), in aviaries with no red mite infestation (P=0.004), and in free-range systems (P=0.011) compared to plastic slatted aviaries, in houses with red mite infestations, and those without a free-range area. Furthermore, hens in aviaries with wire mesh flooring had fewer wounds on the back (P=0.006) and vent (P=0.009), reduced mortality (P=0.003), and a better laying performance (P=0.013) as compared to hens in aviaries with plastic slatted flooring. Flocks with better feather cover had lower levels of mortality (P<0.001). Red mite infestations were more common in plastic slatted aviaries (P=0.043). Other risk factors associated with plumage condition were genotype, number of diet changes, and the presence of nest perches. Wire mesh flooring in particular seems to have several health, welfare, and performance benefits in comparison to plastic slats, possibly related to decreased feather pecking, better hygiene, and fewer red mite infestations. This suggests that adjustments to the aviary housing design may further improve laying hen welfare and performance.

Selection for low mortality in laying hens affects catecholamine levels in the arcopallium, a brain area involved in fear and motor regulation

Feather pecking (FP) in laying hens may cause mortality due to cannibalism. Novel breeding methods using survival days of group-housed siblings allow for the genetic selection of laying hens with low mortality (LML: low mortality line) due to cannibalism. Previous studies have demonstrated less fear-related behavior and also less FP in LML hens compared to CL. Selection also caused changes in locomotor behavior in an open field. It is unknown, however, whether selection for low mortality affects central neurotransmitter levels. In this study, brain monoamine levels were measured in the dorsal thalamus, medial striatum, hippocampus and arcopallium of adult laying hens of both LML and CL using HPLC. Brain samples were collected after 5-min of manual restraint. The most prominent line differences were found in the arcopallium. Compared to CL, LML had lower levels of noradrenaline (NA) and 3,4-dihydroxyphenylacetic acid (DOPAC) and tended to have lower levels of dopamine (DA), homovanillic acid (HVA), and 5-hydroxyindoleacetic acid (5-HIAA). Levels of serotonin (5-HT), 5-HT- and DA-turnover in this brain area were not affected by line. LML showed less fear-related behavior during the restraint than CL. These findings show that selection for low mortality in hens leads to changes of predominantly the dopaminergic system in the chickens arcopallium, a forebrain somatomotor area also related to fear. This suggests a relationship between catecholamine functioning in this brain area and FP and cannibalistic behavior in chickens and underpins previously found relationships between FP, fear and high activity.