1. Health of Laying Hen Flocks
There are many ways to define the health of productive animals. Considering the World Health Organisation definitions of 1946 and 2006, health is “a state of complete physical, mental and social well-being and not just the absence of disease or infirmity”. Animal health can be defined as “a lack of disease or normal functioning of the animal body and normal behaviour”
[1]. In the production sector, Gunnarson
[2] defines health as “the state of the animal organism that allows highest productivity based on a balance between animals and their environment, as well as the animal’s physical well-being”. The vision of One Health is that human health can be better protected through policies that ensure the health of animals and of ecosystems since human, animal, and environmental health are all interconnected
[3]. Within the One Health framework, animal welfare offers opportunities to define the conditions for animals to grow healthily and to be able to cope with pathogens while reducing the need for the use of antibiotics. Such conditions are defined by the animals´ behavioural needs that have been shaped by their own evolutionary history and are deeply imbedded in their genetic makeup. Understanding the factors that affect the social behaviour of laying hens
[4][5][6], or their responses to the features of their surrounding environment
[7][8][9], provides the scientific information needed to manage flocks according to these biological needs, to avoid sources of potential stressors, and to reduce the risk of damaging behaviour. This type of holistic approach will help to preserve animal health and welfare while allowing optimal animal performance in modern animal production systems. From the definitions of health cited above, researchers can see that they include the mental state of an animal and that both physical and mental health can be captured in the term “welfare”.
2. Damaging Behaviours in Laying Hens
2.1. Pecking Behaviours in Chickens
Pecking is a natural behaviour in chickens during foraging and exploration of the environment. When a chicken pecks a conspecific, a distinction is made between pecking arising from aggressive or non-aggressive motivations, as the body parts targeted and risk factors for the behaviour differ. Non-aggressive injurious pecking is considered a redirected form of foraging behaviour, as both pecking during feeding and injurious pecking show similar fixed motor patterns
[10]. An association has been found between the high occurrence of litter-directed pecks by individuals when they are young and a high level of severe feather pecking and litter-directed pecks when they are adults
[10]. This suggests that severe feather pecking is not a direct substitute for foraging but that some individuals have high pecking motivation overall and are, thereby, more prone to develop injurious pecking in addition to foraging.
In cage-free systems, hens have greater behavioural opportunities and freedom of movement, but these systems may also be associated with a greater risk of damaging behaviours as compared to cages
[11][12]. Even though these behaviours can still happen in cages, they are limited to the cage where they develop.
2.2. From Pecking Behaviour to Damaging Behaviour
Damaging behaviours represent a collection of unwanted behaviours that develop under certain circumstances at high frequency and intensity in laying hens, other poultry species, and avian species
[13] and can cause harm to other group members. They include feather pecking
[14][15][16], aggressive pecking
[17] (outside of the frame of hierarchy establishment), different forms of cannibalism
[18][19][20], which include vent/cloacal pecking
[16][21], and toe pecking
[22][23].
Gentle feather pecking is a frequent behaviour in young birds and is also important in social recognition. In adult birds, stereotyped gentle feather pecking can be observed, where birds, for instance, spend a long time pecking at the tips of the tail feathers of another bird. Although this behaviour indicates a welfare problem for the pecker, it usually does not lead to much feather damage
[19][24]. The main problematic behaviour is severe feather pecking, directly affecting the health of the hens—several feathers are lost, or whole stripping of certain areas of the body is observed. This is associated with pain in the affected hen
[25] and can cause skin eruption or bleeding. Severe cases of feather pecking can escalate into cannibalism and death of the bird victim, cannibalistic tissue pecking, and vent/cloacal pecking, potentially leading to severely wounded or dead birds
[19][20][24].
Cannibalistic behaviour involves beak-inflicted damage followed by the consumption of blood and tissues of conspecifics while they are still alive or after death
[26]. Cannibalistic behaviour is learned by individual birds and can spread to others through social learning
[26], even through adjacent cages
[27]. Severe feather pecking can lead to increased risks of cannibalism
[28]. Cannibalism in the cloacal area, also known as “vent pecking”, is considered a distinct form of cannibalistic pecking
[16] and may negatively affect the welfare and health of the bird by causing considerable pain and even leading to mortality
[29]. Serious inflammatory and even infectious processes can follow skin breakage. Toe pecking is another behaviour that is harmful to victims and that negatively affects hen health. It occurs when a bird starts to peck the toes of another bird
[22][23]. In severe forms, toe swelling can be attributed to cannibalism, and complications may be lethal
[30].
2.3. Main Causes of Damaging Behaviour and Control Strategies
Regarding the causal factors leading to feather pecking, a classical hypothesis suggests that it is a redirected form of foraging that develops in the absence of foraging material
[31][32][33][34]. The hypothesis is that under commercial conditions where chicks are reared in the absence of their mother’s guidance, the direction of foraging pecks toward flock mates could result from a chick’s failure to learn to direct these pecks toward appropriate substrates and food items. In addition, the absence of suitable manipulable foraging material can lead to injurious pecking in chicks
[10]. In a review, De Haas et al.
[10] explored how behavioural programming via prenatal conditions (role of maternal stress, egg conditions, incubation settings) and early postnatal conditions (chick brooding conditions) could influence the development of injurious pecking in laying hens. This review argues that it may be possible to prevent injurious pecking in commercial laying hen flocks by adapting the environmental conditions of previous generations, optimising incubation conditions, reducing stress around hatching, and guiding the early learning of chicks.
Damaging behaviour can emerge at different ages in most breeds, although with varying intensity depending on the genetic line
[8], and can affect a large number of birds in the flock. Reported percentages of affected flocks at the end of lay can reach values as high as 60% of the flocks, with more than 10% of hens having moderate or severe feather damage in one body region
[35], or 86% of the flocks in which severe feather pecking was observed
[36].
Although no strategy can guarantee the complete absence of pecking behaviours, optimised management practices, especially concerning feeding, lighting, and climatic conditions
[9] and environmental enrichment in pullets and adult birds
[37][38][39], can help to reduce the risk. Access to outdoor free-range areas is associated with plumage preservation
[7][40][41] and a reduced risk of injurious pecking
[42]. Genetic selection at the commercial scale will help in the control of feather pecking
[15][18][43]. For instance, Rodenburg et al.
[44] offer various genetic means to limit feather pecking, cannibalism, and vent/cloacal pecking based on the systematic selection of birds with less-pronounced damaging behaviours than other birds.
Another hypothesis suggests that mild feather pecking could be a redirected form of social grooming and may have a social recognition function
[45]. Kjaer et al.
[46][47] suggest that severe feather pecking is related to neurological changes that cause hyperactivity, although Krause et al. showed that selection for high locomotor activity did not result in an increase in feather pecking
[48]. Recent studies found that genes involved in cholinergic signalling, channel activity, synaptic transmission, and immune response are involved in feather-pecking mechanisms
[43].
Although Borda-Molina et al. did not find any relations between microbiota and feather pecking
[49], there is growing evidence that gut microbiota influence hens behaviour and physiology
[50][51]. However, whether microbiota can influence the development of feather pecking is not fully demonstrated
[51][52]. This shows the complexity of the situation, involving the modulation by the gut microbes of the immune system, or maybe brain function not modulated through the immune system.
The way neurophysiology, gut physiology, and health in a broader sense impact the development of damaging behaviours in layers is described in the chapter below, immediately followed by the description of how, in return, the consequences of damaging behaviours will impact the health and welfare of animals.
3. Inter-Relationships between Damaging Behaviours and Health Problems in Current Housing Systems for Layers
3.1. Recent Knowledge about the Impact of the Health Condition, Including Immune Status of Animals, on the Occurrence of Damaging Behaviours
3.1.1. Immune System
The immune system plays a critical role in brain development. In particular, microglia (macrophage-like immune cells in the brain) have been shown to be involved in many aspects of brain development, such as synapse formation and neuronal survival
[53]. Cytokines, chemokines, major histocompatibility complex (MHC) molecules, and toll-like receptors (TLRs) have been shown to play a critical role in neural development
[53][54][55]. Cytokines can target neurocircuits that are involved in regulating mood, motor activity, motivation, and anxiety
[56]. As a result, the immune system could influence behaviours through its role in brain development.
The immune system is also more directly involved in regulating behaviour. Cytokines and chemokines can alter behaviour, for example, in sickness behaviour, where sick animals show reduced feed and water intake, lower activity levels, decreased exploration and social interactions, and increased sleep
[57][58]. Cytokines could influence behaviour via their effects on the synthesis, re-uptake, and release of neurotransmitters, such as serotonin, dopamine, and glutamate
[56][59][60]. As an example, cytokines can influence the functioning of the hypothalamic-pituitary-adrenal axis (HPA axis). They can activate corticotropin-releasing hormone (CRH) and thereby stimulate the release of adrenocorticotropic hormone (ACTH) or can stimulate ACTH release, directly resulting in glucocorticoid release
[56][61]. Cytokines can, in fact, influence behaviour via multiple routes.
In humans, there are similarities between sickness behaviour and behaviour expressed by individuals with certain neuropsychiatric disorders, such as depression
[62]. Furthermore, many psychiatric disorders have been linked to immune dysregulation, including schizophrenia, anxiety and stress disorders, autism, and major depressive disorder
[54].
Several studies have found relationships between the immune system and feather pecking. Most show genetic associations between feather damage (as an indicator of feather pecking) and the immune system. As mentioned previously, cytokines can influence the serotonergic and dopaminergic systems, and, in turn, these systems seem to be involved in the development of damaging behaviours such as feather pecking (for a review, see de Haas and van der Eijk
[63]). In addition, through their effects on HPA axis functioning, cytokines could further influence how animals respond to or cope with stress. Feather pecking has been linked to coping styles and increased stress sensitivity
[24][64]. Furthermore, feather pecking has been linked to motor activity
[47], motivation, and fearfulness
[65], and cytokines target brain areas that are involved in the regulation of these behaviours. The serotonergic and dopaminergic systems also appear to be dysregulated in many of these brain areas when feather pecking occurs
[63]. The immune system may, therefore, play a role in the development of feather pecking.
Genetic associations have been found between immune-related genes, such as interleukin (IL4, IL9), nuclear factor NF-kappa-B (NFKB), chemokine (CCL4) genes, and feather damage score, providing evidence of a relationship between feather pecking and immunity at the genetic level
[66]. Genetic mutations in the
IL4 and
IL9 genes were also associated with levels of natural antibodies (NAb) IgM and IgG
[67]. NAb are antibodies that can bind antigens without prior exposure to the antigen
[68]. These associations were mostly associative genetic effects on feather damage scores and not direct genetic effects, suggesting that NAb levels may be related to the propensity to perform feather pecking. This is further supported by the finding that when cage mates had higher NAb IgG levels, the individual had more feather damage
[67]. Genetic associations were further found between severe feather pecking and specific antibody responses
[69], indicating that there are genes simultaneously involved in both feather pecking and specific antibody response. Interestingly, several genes involved in immune responses, for example, TNF ligand and mitogen-activated protein kinase, were either upregulated or downregulated in the hypothalamus of feather-pecking birds compared to neutrals and victim birds
[14]. Furthermore, a chicken line performing more feather damage showed upregulation of genes related to immune system processes in the brain compared to a chicken line showing less feather damage
[70][71]. These findings provide additional arguments supporting a relationship between the immune system and feather pecking (see also Brunberg et al.
[72]).
Further evidence for a relationship between the immune system and feather pecking comes from lines that were divergently selected on feather pecking and that differ in several immune parameters. High-feather-pecking (HFP) birds showed a higher antibody response to infectious bursal disease virus vaccination, while low-feather-pecking (LFP) birds had a higher number of white blood cells and higher expression of MHC class I molecules on T (CD4, CD8) and B cells
[73]. Recently, the FP selection lines were shown to differ in both innate and adaptive immune characteristics, with HFP birds having lower IgM NAb but higher IgG NAb levels, specific antibody levels, and nitric oxide production by monocytes compared to LFP birds
[74]. These findings suggest that HFP and LFP birds differ in immune responsiveness and provide further support to a relationship between the immune system and feather pecking. Yet, these relationships could be the result of genes that are simultaneously involved in the immune system and in feather pecking, as also indicated by previous studies
[66][75].
It remains to be elucidated whether these relationships between the immune system and feather pecking are causal. Preliminary findings show that the immune system may play a role in feather pecking. Birds that received an immune challenge at a young age showed more feather damage at an adult age
[76], suggesting that activation of the specific immune response at a young age may stimulate birds to feather peck. Following this rationale, it can be considered that a health issue in a flock, such as infection implying immune system activation, may increase the risk of feather pecking in the future. More research is needed on this topic.
3.1.2. Other Impacts of Health on Damaging Behaviour
The health and integument status of laying hens are closely related. Plumage presence, persistence, and distribution on the body can be indicative of the nutritional status, health, and behaviour of the birds
[77][78]. Close inspection of growing feathers can also provide information about physiological and systemic infectious issues while the feathers are formed.
Other dimensions of health, such as parasitic infestation, may affect the development of damaging behaviour in laying hens. Parasitic infestation, for example, with
Ascaridia galli, can decrease health, performance production, and plumage coverage in layer flocks
[79]. Parasitic infestation was significantly associated with plumage damage, while treated animals showed better plumage conditions. The authors claim that lower worm burdens were associated with improved plumage condition, possibly through reduced parasite-induced stress, without providing a precise explanation of the mechanism. These results are consistent with the previous hypothesis of this , where immune stimulation might trigger feather pecking.
Concerning external parasites, red mite (
Dermanyssus gallinae) infestation can cause anaemia, while the presence of red mites can also lead to itching, disturbing the flock, and possibly acting as a trigger for injurious pecking
[78]. The poultry red mite is the most common ectoparasite on laying hen farms worldwide, causing considerable economic losses and reduced hen health and welfare. Even in moderate numbers, they can cause considerable stress, agitation, and severe feather pecking in hens. As an example, it was shown in a study undertaken in 47 Belgian aviaries that the plumage condition of the flock is better on farms with no red mite infestations
[77]. Temple et al.
[80], in an experiment where infested layers were treated with fluralaner (Exzolt
®), showed improvements in behavioural variables (less preening, head scratching, head checking, severe feather pecking, and aggressive behaviour), physiological biomarkers, and health parameters following the elimination of red mites on a commercial farm. These results indicate that infestations can reduce hen welfare. The severity of feather pecking associated with red mite infestation may increase in non-beak-trimmed flocks.
Other mites, such as the northern fowl mite (
Ornithonyssus sylviarum), are also key pest species for caged laying hens. Jacobs et al.
[81] showed that mite-infested hens had increased nocturnal activity, including preening, as well as fragmentation of behavioural activities together with decreased dozing, indicating disturbed resting behaviour and suggesting a reduction in the welfare of hens infested by these mites.
Plumage and integument damage can also result from clinical diseases, such as diarrhoea or nutrient deficiency. Hens perform more feather pecking when diets contain mineral, protein, or amino acid (methionine, arginine) levels below recommended levels
[82]. Systemic bacterial infections such as
Erysipelas can be associated with poor feather coverage and skin damage
[78].
These findings indicate that health issues may stimulate damaging behaviour, but more research is needed to explain the mechanisms involved and to identify prevention strategies. The following chapter explores the consequences of damaging behaviour on laying hen health outcomes.
3.2. Impact of Damaging Behaviours on Health
When discussing the effects of damaging behaviour on the physical and mental health of laying hens, researchers are primarily referring to the “victim”, i.e., “the recipient”. First of all, the feather-pecking activity may degrade feather cover in recipients, which may interfere with the bird’s body heat regulation, and hens that have lost parts of their plumage are extremely susceptible to the cold
[83]. Chickens are sensitive to touch; their skin contains numerous receptors for temperature, pressure, and pain
[84]. In crowded systems, feather loss may give rise to skin damage caused by abrasion from the environment and flock mates
[32]. Additionally, skin damage can trigger cannibalism
[85], often resulting in the mortality of recipients. It has been shown that the victims of cannibalism have lower body weight than feather peckers
[86][87]. Furthermore, feather damage may impact the structural cohesiveness of the feathers and lower the aerodynamic capacity of the wings
[88][89], making them less efficient in helping to maintain balance
[90], which can be problematic when using perches and navigating through a complex 3D aviary environment.
Even feather removal is a strong stressor for a bird; during feather pecking, the bird being pecked often shows crouching immobility with no outward sign of pain. Gentle
[91] explained this immobility as learned helplessness, which develops when an animal experiences traumatic events that are aversive and that continue to happen independently of any attempts by the animal to reduce or eliminate them. Studies have shown that during initial feather removal, the birds become agitated, with wing flapping and/or vocalisation and increased heart rate, blood pressure, and EEG arousal as clear signs of pain. Over time, the continued removal of feathers does not produce an exaggerated escape response but an immobile “helplessness” state. During this period of immobility, the EEG of the victim shows activity similar to that seen in sleep or catatonic states, such as tonic immobility. Basically, this is an anti-predator strategy following capture to prevent further damage produced by struggling and to allow escape should the occasion arise. This strategy is, however, counterproductive in production systems where hens have no possibility to escape and are, in effect, making themselves available to be pecked
[91]. This type of learned helplessness or anticipation of the negative event may lead to the appearance of negative emotions in hens related to fear and anxiety
[84].
Tahamtani et al.
[87] suggest that feather peckers and victims experienced similar levels of negative experiences during rearing, causing stress and developmental instability, leading to either pecker or victim status. For example, it is considered that fearfulness, proactive coping, or hyperactivity may predispose chickens to develop severe feather pecking. In the study by Kops et al.
[92], the severe feather-pecking problem was discussed because of the lack of monoamines (serotonin and dopamine) in certain brain areas, which affects both emotional perception and behavioural output. Due to neurochemical deficits early in life, high-feather-pecking-line chickens are prone to increased general behavioural activity. In turn, this hyperactivity seems to be a clear risk factor for the development of feather pecking.
To conclude, damaging behaviour leads to denuded overall plumage, with an increased risk of poor thermoregulation, skin damage, and possibly wounds with an increased risk of infection (infection of the skin and tissues and peritonitis). These effects act negatively on hen health and welfare and possibly lead to increased mortality
[24][36][93][94].
Consequently, there is a clear need to monitor laying hen health and welfare in order to ensure early detection of damaging behaviour and/or health issues and to use corrective measures. Most modern poultry husbandry systems house thousands of animals in a single barn, leading to challenges in the assessment of individual animals. The next chapter will summarise current knowledge on monitoring systems allowing early detection of damaging behaviour and health issues in order to prevent their spread.