1. Introduction
Worldwide, the seven billion laying hens raised every year are mainly housed in cages [
1]. In Europe, driven by strong societal sensitivity for animal welfare, the proportion of cage housing systems (furnished ones since 2012) has gradually decreased in recent years. However, 50.4% of laying hens in the European Union (EU) were still housed in furnished cages in 2018 [
2]. Furnished cages were initially designed to house relatively small groups of hens (e.g., 20). There is now a trend towards larger group sizes, increasing locomotion possibilities for animals but having implications for some behaviors, for instance the development of injurious pecking (IP). The notion of IP covers a range of behaviors such as aggressive pecking, feather pecking, cannibalism including vent pecking and toe pecking [
3]. In this paper, aggressive pecking will be excluded because it has a different cause than the other injurious pecking activities. Injurious pecking is currently the most problematic behavioral issue the poultry industry is facing, with impacts on welfare including health and productivity [
4,
5]. This problem may occur in all types of housing systems, during rearing of pullets, as well as during the laying period [
6,
7,
8,
9], and it is difficult to stop this behavior once it has begun [
7]. Injurious pecking is not a new problem: a large amount of research has been carried out to determine the factors influencing IP. However, it is still difficult to systematically prevent and treat because it is a multifactorial problem with a wide range of possible risk factors including genetics, stocking density, group size, floor type, feed, light (intensity, wave length) and others environmental factors [
4,
10,
11,
12,
13,
14,
15,
16].
Currently, the most effective and reliable method of reducing the damage caused by IP is beak trimming, consisting in most cases of infra-red radiation applied in day-old chicks at commercial hatcheries. The use of this method has become widespread, in a prophylactic manner on all flocks. The procedure appears to be efficient, because IP problems are more common and feather condition is worse in birds with intact beaks, in comparison to beak-trimmed birds [
17]. However, IP is also found in beak-trimmed flocks and as a result, beak trimming fails to completely prevent IP-related problems. Even though it is commonly used in egg production, beak trimming is heavily debated for animal welfare reasons, because of the pain or discomfort caused to chicks during and after the trimming procedure [
18], despite its improvements in the technique over the years. Therefore, understanding how to manage non-beak-trimmed pullets and hens is important to good ensure animal welfare.
In egg production, day-old chicks are transferred from the hatchery to a rearing farm, and then transferred around 18 weeks of age (WOA) to a variety of layer housing systems. It is recommended that laying hens be reared according to their later housing conditions for optimal welfare and productivity of layers [
19]. Generally, producers try to match the type of rearing facility with the type of layer facility, especially for aviary systems, but this is not always possible. In France, one of the leading egg producer in the EU with 1 million tons eggs in 2019 [
2], laying hens housed in cages are in 60% of cases housed in barn systems during the rearing period, without any enrichment except litter (personal data—survey used in [
14]). Rearing in a relatively spacious environment with access to substrate and other enrichments, followed by transfer to a restrictive environment without any substrate, or with a relatively poor substrate, may cause frustration inducing high reactivity and IP [
20].
Several reviews [
4,
12,
21] have been published and management guidelines [
10,
22,
23] developed to help farmers with IP control in free-range, barn and organic systems. Factors that could mitigate this multifactorial problem are multiple. For instance, providing birds with the opportunity to explore and forage reduces the risk of IP [
24]. Enriching the environments with suitable litter, various types of plastic toys or string enrichments can reduce IP, thereby improving feather cover [
25], with importance of renewing of enrichments [
26] to avoid animal boredom and lack of interest, and to train animals to accept novelty. Decreasing animal emotional reactivity and fear is also important [
15]. This can be done by giving animals time to adjust or prepare for change, or by providing hens the possibility to escape from feathers peckers thanks to perches or panels [
26], or by improving the human-animal relationship [
27]. Another aspect influencing IP mentioned in numerous experiments is nutrition (reviewed by [
28]). Presenting food in ways that stimulate foraging behavior may increase the time spent eating and decrease the time spent on IP [
29]. Finally, the conditions during the rearing period play an important role in the prevention of IP [
7,
25,
30]: with provision of an enriched environment to stimulate foraging behavior [
6], or the possibility to perch early to lower the risk of vent pecking during the laying period [
31].
Although the literature on the causes of IP and potential solutions is abundant, it is sometimes difficult to apply the findings to the current French situation. Most research on non-beak-trimmed hens focusses on free-range or other cage free birds. In cage housing systems, introducing enrichment and renew it is challenging because of financial costs and time demands, even though it may be more important given the relatively barren environment of a cage [
32]. Therefore, simple, robust and inexpensive solutions are required for cages in commercial poultry production. Moreover, research had a strong focus on the laying phase, with less interest on the rearing phase. Finally, experimental studies have often shown the value of the tested strategies in an individual manner. However, the various influencing factors may interact, and the successful transfer of the results of these studies into farming practice is difficult.
The goal of this study was to measure the effect of a combination of several management strategies from rearing to laying stages that have proven to be individually efficient to control IP. The different management strategies were chosen taking into account the potential benefit for the animals, feasibility and cost for farm implementation. The objective was first to decrease reactivity (giving pullets the possibility to escape from feather peckers, providing gradual changes in light to create dusk and dawn phases, providing music), and to decrease animal fear of humans (allowing the animals to anticipate the person’s arrival, improving the human-animal relationship). A second objective was to promote more natural behaviors with an extra environmental enrichment. Concurrently, the enrichment should be feasible, robust and inexpensive for commercial application. Thus, during rearing period, objects were renewed in contrast to the laying period, where objects were deliberately left until the end of the experiment, without being renewed to mimic commercial conditions. A last objective was to increase the time spent eating, by fiber supplementation in the diet during laying period. The hypothesis was that the combination of the different management strategies altogether leads to a decrease of IP and resulting problems related to body status, fear and laying performance. As IP is found in non-beak-trimmed but also in beak-trimmed flocks, comparisons of effectiveness of such management strategies on these two situations were carried out.
4. Discussion
Supplementing feed with fiber did not result in the expected decrease of IP consequences, even when added to other management strategies. In [
36,
37], increase in the crude fiber content did not reduce animal losses and plumage damage neither. This is not consistent with the findings of other studies where higher crude fiber content led to better plumage condition in laying hens by reducing feather pecking and pecking damage to skin. This was explained by a prolonged feeding period, with prolonged intestinal passage, and thus a longer lasting feeling of satiety [
28,
38,
39]. Several explanations can be made for these inconsistent results. First, fiber supplementation was kept low in our study in order to maintain high zootechnical performances for farm implementation, but possibly too low to see an effect on IP consequences. Second, interactions with other feed characteristics (energy, protein and amino acids levels) seem to be important [
40]. Fibers can also be more effective if ingested through routes other than via feed, for example through foraging in the environment (hay or dehydrated alfalfa bales, [
41]). Finally, if supplementation in feed with fiber had been provided as early as the pullet rearing period in our study, this could have led to reduced IP consequences. This needs further investigation.
With or without fiber supplementation in feed, the management strategies provided in our study both at the rearing and laying stages showed many positive effects on several aspects. Positive effects of management strategies were even more visible on NT animals where E treatments lead to lower pullet and laying hen mortalities, and better feather cover during the laying period. This confirms previous results observed on laying hens in floor housing systems, reviewed by [
26].
In particular, birds housed in E environment were less fearful (or more attracted) towards a novel object during the laying period and to a lesser extent tended to be less fearful towards an unfamiliar human (or more attracted) during the rearing period. This suggests that E birds would have a lower risk to experience stress than NE animals, and shows the effectiveness of using multiple sources of management strategies, from the very beginning of the rearing period, from physical objects, sounds, lights and human sources. This is consistent with [
42], who found, under commercial free-range conditions, significant relationships between stockperson attitudes, the number of hens that could be approached and touched, and the feather damage and mortality rates of these hens.
An interesting result was that mortality in NT pullets was rare, but even lower in E pens. The difference in mortality appeared after the first two weeks, and was not directly linked to IP related problems. This may be associated with an overall decrease in stress, and/or increase in positive emotions with secondary effects on health. In fact, enriched housing environments can have positive impacts on immunocompetence (reviewed by [
26]).
Enrichment in the cage, like the artificial turf mat in the pecking and scratching area of the cage, did not relocate egg laying to this area. On the contrary, the percentage of egg laying into the nest was higher in E cages, showing better distribution of resources and a better use of the cage areas by the hens. In the same way, T hens better used the nest for egg laying than NT hens. In NE and NT cages, hens may have used the nest as an escape from peckers, making it less available for egg laying. The better use of nest for laying can partly explain the better laying rates in E (tendency) and in T cages.
The management strategies provided in the rearing up to laying stages have therefore shown their value for the welfare of animals, without a negative impact on productivity. However, this approach still showed some limitations and can be improved.
The E treatments limited feather cover damage for NT hens during the laying period, but at 71 WOA it was no longer sufficient: all hens showed severe damage of the feather cover. This shows some difficulties for field application in comparison with the beak trimming procedure. Also, during the IP episode in the laying period, NE hens were far more affected than E hens, but mortality varied greatly between cages within the same group treatment, especially for NT hens. The causes of this IP episode were unknown and probably multifactorial (it took place in the middle of the laying peak, and just after a change in feed formula). This shows the complexity of the problem and how difficult it is to control on the farm.
Applying a similar environment between the rearing and laying periods would probably play a role in decreasing the risk of IP. Our experimental setup limited the implementation of certain management strategies: one single room housed E and NE cages with the same environmental conditions for all cages. However, on commercial farms, solutions can be added during the laying period as provided during the rearing period such as music playing, warning of human arrival and improving the human-animal relationship. Altogether, this would probably further increase the effectiveness of management strategies on IP consequences reduction.
Moreover in our study, the effects of management strategies during the laying phase could be long-term effects of the rearing treatment. Indeed, in [
13], where extra environmental enrichment was applied only during the laying period in furnished cages, no effect was observed on IP consequences. Whether the management strategies, applied only during the rearing period, would have had positive effects still needs to be investigated.
Our study proposed various management strategies, both at the rearing and laying stages, based on the existing literature but also on the practical and economic feasibility of installing such enrichments in commercial farms in barn system and in furnished cages. The objects provided were simple, easily obtained directly on farms or inexpensive if purchased. In barn systems, the farmer can easily renew them. However in furnished cages, we decided not to renew the objects in order to propose the simplest situation for farmers (but perhaps not as positive from the animal welfare point of view). It is thus possible that the management strategies provided in our study could be even more effective if objects were renewed during the laying period. The farmer could do this several times during the laying period, during hens’ presence as objects are placed on the façade of the cage.
Although precautions have been taken to avoid observer bias in body condition assesment, inter-observer reliability testing should be added for future studies in order to improve methodology.
Unsurprisingly, beak trimming considerably limited the consequences of IP during the laying period: lower mortality, better feather cover and lower skin damage. These results are similar to those reported in previous studies that have been conducted on commercial farms [
43,
44] in barn or cage housing systems. Probably as a result, T hens were heavier, likely linked to better feather cover and less energy loss for thermoregulation and recovery [
45,
46]. Trimmed hens also had higher laying rates than NT hens perhaps due to a lower stress level caused by IP in cages: stress can result in a decrease in egg laying rates [
46].
However, negative consequences of beak-trimming were highlighted in our study. More than a third of T pullets were affected by beak defects at the end of the rearing period (reaching half at the end of the laying period). This demonstrates poor treatment of the beak and regrowth problems. This is in line with field results [
6,
14,
47], also with infra-red beak trimming. It therefore seems that the technique still needs to be better controlled and adapted to the anatomy of the beak. Although the question of pain directly due to infra-red beak trimming or beak defects is under debate [
44,
48], beak defects may have led to discomfort in beak use affecting normal behavior, such as foraging, feeding, drinking, and preening [
49,
50]. In our study, the droppers used during rearing had an overpressure in water that could not technically be adjusted, probably making it difficult for the most sensitive individuals to drink. As a possible consequence, T birds in comparison to NT birds showed decreased body weights until 3 WOA, albeit without further decrease, as found in previous studies ([
51] up to 4 WOA and [
52] up to 8 WOA), and mortality was higher, especially at the beginning of rearing.