Housing systems and chicken behaviour

Chicken housing systems have been the focus of scientific research aiming to improve the well-being of animals to obtain higher quality products (Figure 1). Chicken behaviour is largely dependent on the housing system and welfare refers to quality of life (El-Sabrout, Reference EL-SABROUT2018). Free-range (outdoor) conditions can benefit the welfare of chickens because the birds have access to more natural environments and have more opportunities to exhibit natural behaviours compared with indoor systems. The concept of good welfare is achieved when the individual is able to adapt to or cope with the constraints of the housing and management conditions to which it is exposed (Duncan, Reference DUNCAN2002). The concept of safe production that takes animal welfare and environmental conditions into account is gaining importance throughout the world. Poor welfare is usually associated with a reduction in productivity, and is therefore undesirable (Jones et al., Reference JONES, FEBER, HEMERY, COOK, JAMES, LAMBERTH and DAWKINS2007). Behavioural measures are often used as the starting point for assessing an animal's response to its environment (Dawkins, Reference DAWKINS2003).

Figure 1

Chicken housing systems.

Chicken behaviour is a reaction to environmental changes and depends on both genetic and non-genetic factors (Manteuffel, Reference MANTEUFFEL2002). In fact, chicken behaviour is clearly associated with the effects of all aspects of genotype and environmental conditions (Duncan, Reference DUNCAN2002). Therefore, understanding how the environment affects animals allows the identification and to quantification of welfare. Environmental enrichment can foster and encourage natural behaviours and create a greater number of behavioural opportunities (Mellen and MacPhee, Reference MELLEN and MACPHEE2001). All animals have a range of behavioural expectations regarding their surroundings. Environmental and housing conditions have been found to be an extremely important factor of chicken production as it directly affects chicken behaviour. According to Ferrante et al. (Reference FERRANTE, VERGA, MANGIAGALLI and CARENZI2001), animal behaviour depends on the housing environment, although further study of chicken behaviour is necessary to obtain a better understanding of the important requirements of intensive rearing housing conditions.

Access to free-range conditions can improve animal welfare and allows animals to exhibit behaviour such as dust and sunbathing (Gonçalves et al., Reference GONÇALVES, FERREIRA, PEREIRA, OLIVEIRA, AMARAL, GARBOSSA and FONSECA2017). Ruis and Coenen (Reference RUIS and COENEN2004) concluded that access to an outdoor run potentially improves welfare. Thus, an outdoor system can decrease stress conditions. Rummaged feeding is a commonly proposed approach for promoting the natural behaviour and improving activities of chickens (Zelnter and Maurer, Reference ZELNTER and MAURER2009) and can enhance the taste of the resulting poultry products (Fanatico et al., Reference FANATICO, PILLAI, CAVITT, EMMERT, MEULLENET and OWENS2006). However, chickens that are provided outdoor access often do not fully use the range area. Natural cover, such as trees, can provide shelter and increase range use but might not be practical for use in all free-range operations.

Free-range management is undoubtedly a key issue of health and welfare standards in outdoor poultry housing systems. The employment of inappropriate genetic strains or pasture management systems is expected to result in serious welfare problems, such as higher mortality and greater rates of dermatitis and skeletal damage in organic and free-range systems. Although, in an outdoor system, laying hens might show beneficial behavioural activities that cannot be achieved in an indoor system (Zelnter and Maurer, Reference ZELNTER and MAURER2009). Furthermore, Bogosavljević-Bošković et al. (Reference BOGOSAVLJEVIĆ-BOŠKOVIĆ, RAKONJAC, DOSKOVIĆ and PETROVIĆ2012) reported that the reduced feed intake observed in outdoor housing systems plays an effective role in lowering weight gains. Outdoor activity increases the energy requirements of chickens and provide more space for animal movement and these combined with decreased feed intake can result in lower growth.

The housing system of chickens is related to behavioural, hygienic, environmental and welfare aspects. Verga et al. (Reference VERGA, ZINGARELLI, HEINZL, FERRANTE, MARTINO and LUZI2004) reported that housing system can affect animal behaviour. Several studies have revealed the effect of group size and density on the behaviour and productive performance of chickens, although results often may be confounded by other variable factors. Chickens raised in larger groups exhibit less rest and increased activity; in fact, these chickens spend more time moving around and exhibiting aggressive behaviours. Aggressive behaviour is one of the main problems associated with housing chickens in large, dense groups. Upon reaching sexual maturity, chickens experienced increased numbers of aggressive conflicts, which results in injuries with different levels of severity to different parts of the body.

Lebas (Reference LEBAS2001) found that housing in floor pens or colony cages reduced stress and aggressive behaviour of birds, but increased mortality rates and decreased growth rates, feed intake, feed efficiency, and, sometimes, meat quality (McNitt et al., Reference MCNITT, WAY, WAY and FORRESTER-ANDERSON2003). Previous studies on extensive housing systems have often been inconclusive due to the numerous variables involved, such as group size and stocking density. Outdoor housing systems have a potentially favourable effect on chicken welfare because it allows the animal to exhibit natural behaviour, such as moving and feeding (Tuyttens et al., Reference TUYTTENS, HEYNDRICKX, DE BOECK, MOREELS, VAN NUFFEL, VAN POUCKE, VAN COILLIE, VAN DONGEN and LENS2005). In agreement, Freire et al. (Reference FREIRE, WILKINS, SHORT and NICOL2003) found that outdoor access might exert a positive effect on hen welfare by reducing aggressive behaviours. On the other hand, Hegelund et al. (Reference HEGELUND, SØRENSEN, KJÆR and KRISTENSEN2005) reported that outdoor production systems might cause some health issues (poor management conditions or bad weather).

The interest in obtaining chicken meat from extensive housing systems has increased in the last decade. Housing systems can affect reproductive behaviour, body weight and meat quality of animal (Pla, Reference PLA2008). According to Ferrante et al. (Reference FERRANTE, VERGA, MANGIAGALLI and CARENZI2001), the behaviour of an animal depends on its housing environment, whereas Jones et al. (Reference JONES, FEBER, HEMERY, COOK, JAMES, LAMBERTH and DAWKINS2007) reported that improve ambient conditions might yield benefits. Conventional, intensive production systems have the potential to influence poultry welfare in both positive and negative ways. The concern with conventional cages is mainly due to its inherent restriction of behavioural. The traditional rearing cage can produce stress in animals (Drescher, Reference DRESCHER1992), which is reflected in aspects of adaptive behaviour (Wiepkema and Koolhaas, Reference WIEPKEMA and KOOLHAAS1993). Keeping chickens in cages is not compatible with their housing demands with respect to animal welfare and the narrowness of the cage and the wire floor might explain why caged chickens show nervous behaviour, altered forms of movement and deceased levels of relaxed resting behaviour. Conventional confined systems can lead to domestic bird stress (Jones and Mills, Reference JONES and MILLS1999), resulting in physiological and behavioural responses (Marin et al., Reference MARIN, FREYTES, GUZMAN and BRYAN JONES2001) and poor performance (Mendl, Reference MENDL1999).

Non-cage systems enable the expression of a more diverse array of ancestral behaviour patterns, and greatest behavioural diversity has been observed in free-range systems. Unfortunately, this type of system restricts the ability of the chickens to protect themselves from an unfavourable environment.

The housing system affects chicken meat quality

Among the numerous non-genetic factors that can affect meat quality traits of chickens, housing systems have been recognised to have a large impact on meat quality. The notable discrepancies in the literature with respect to the effects of alternative production systems on poultry meat quality likely result from the different ages and genetic origins of the birds studied. Pla (Reference PLA2008) reported that housing systems can affect the meat quality of animals. Fattened chickens can be characterised by various features, such as dressing percentage, desired conformation, highest possible amount of meat on the carcass, optimal distribution of fat, appropriate skin colour and amount of damage due to rearing management, catching, loading and unloading. Thus, the chicken housing system is one of many non-genetic factors that can considerably affect meat quality (Bogosavljević-Bošković et al., Reference BOGOSAVLJEVIĆ-BOŠKOVIĆ, KURĆUBIĆ, PETROVIĆ and RADOVIĆ2006). Meat products obtained through ecological rearing are characterised by higher nutritive quality and better taste (Horsted et al., Reference HORSTED, ALLESEN-HOLM and HERMANSEN2010). Additionally, these animals have more space and exhibit increased environmental enrichment, which could lead to better leg health and decreased fearfulness. In practice, however, free-range systems are not widely used, and lack of shelter and weather conditions likely play an important role in the low implementation of free-range systems.

Zhao et al. (Reference ZHAO, LI, LI and BAO2014) revealed that birds housed in an outdoor system exhibit increased their activities, ate a slightly higher amount of feed and had a significantly lower abdominal fat content compared with birds that are housed indoors. Bogosavljević-Bošković et al. (Reference BOGOSAVLJEVIĆ-BOŠKOVIĆ, RAKONJAC, DOSKOVIĆ and PETROVIĆ2012) reported that indoor-housed chickens had higher body weights than outdoor-housed chickens, which might be due to decreases in the feed intake. Fast-growing hybrids attain a higher body weight under free-range housing conditions than slow- and moderately fast-growing hybrids (Fanatico et al., Reference FANATICO, PILLAI, CAVIT, OWENS and EMERT2005).

Mortality is an important parameter in chicken production and requires consideration of the overall environmental conditions. Mortality in indoor housing systems is increased by temperature, humidity, feed supply and stocking density (Sorensen et al., Reference SORENSEN, SU and KESTIN2000; Heier et al., Reference HEIER, HOGASEN and JARP2002). Poorly growing chickens with lower body weight show increased mortality under pen-housing conditions. Sossidou et al. (Reference SOSSIDOU, DAL BOSCO, ELSON and FONTES2011) reported that the main cause of death in these production systems is higher exposure to disease (e.g., avian influenza); Salmonellosis and parasites that could be directly transmitted from other domesticated or wild (migratory) birds are more prevalent in outdoor systems.

Consumers in the United States are increasingly interested in both free-range and organic chickens. However, when consumers evaluated breast fillets using a ranking test (1-least intense to 5-most intense), the results revealed that consumers found no difference in fillet juiciness, tenderness or flavour, but commercial breast fillets were preferred over free-range fillets (Alvarado et al., Reference ALVARADO, WENGER and O'KEEFE2005). Trained panellists evaluated drumsticks and found no difference in tenderness or flavour, although the meat from free-range birds was juicier and was more strongly attached to the bone. Commercial and free-range chickens have many similarities in terms of meat quality and sensory attributes, but the meat from free-range poultry has a shorter shelf-life than that from commercially raised chickens (Alvarado et al., Reference ALVARADO, WENGER and O'KEEFE2005).

Dal Bosco et al. (Reference DAL BOSCO, CASTELLINI and MUGNAI2002) stated that the housing system affects some meat parameters and, sometimes, the meat quality. However, with the increasing customer demand for high-quality animal products (Keskin et al., Reference KESKIN, KOR and KARACA2012), the production of homemade products and meat derived from alternative housing systems complying with improved welfare conditions has become increasingly needed. Animals that exhibit increased movement show a higher number of mitochondria in αW fibres which are responsible for the conversion of the predominant glycolytic energy metabolism of chickens into oxidative energy metabolism. Some of the αW fibres are then converted into αR fibres which are richer in myoglobin. In contrast, reduced movement increases the muscle storage of glycogen, which is used for anaerobic energy metabolism (Gregory, Reference GREGORY2003). A higher fat content might be related to the productive performance of outdoor chickens with significantly higher live weights (D'Agata et al., Reference D'AGATA, MAGAL, OLIVIER, RUAN and WEBB2007).

The chemical composition of chicken meat is different than that of other livestock, whereby protein and fat contents are strongly associated with the housing system (Castellini et al., Reference CASTELLINI, BERRI, LE BIHAN-DUVAL and MARTINO2008). Sirri et al. (Reference SIRRI, CASTELINI, RONCARATI, FRANCHINI and MELUZZI2010) found that genotype was the major factor affecting the chemical composition and quality of meat derived from non-intensive housing systems. In agreement, Meluzzi et al. (Reference MELUZZI, SIRRI, CASTELLINI, RONCARATI, MELOTTI and FRANCHINI2009) observed that the housing system affects carcass and meat quality.

For a comparison with other species, Dal Bosco et al. (Reference DAL BOSCO, CASTELLINI and BERNARDINI2000) found that caged rabbits have higher slaughter weights and carcass fat percentages than outdoor rabbits, whereas the dressing percentage is similar. Chicken meat derived from birds reared under outdoor systems showed an increased red colour, and a lower lightness colour, respectively, than those derived from indoor systems (Monin and Ouali, Reference MONIN and OUALI1991). The increase in meat redness can be explained by the fact that exercise increases the oxidative capacity of muscle and thus the proportion of oxidative myofibres and the myoglobin content. Increased activity could result in relatively stronger muscle fibres, which would affect meat tenderness (Fanatico et al., Reference FANATICO, PILLAI, CAVIT, OWENS and EMERT2005).

Smith and Teeter (Reference SMITH and TEETER1987) reported that an outside air temperature that exceeds the optimal range could affect meat traits and decrease the dressing percentage. This finding is important for animals raised in free-range conditions, where the temperature cannot be controlled. A clear variation in chicken meat quality has been observed between different housing systems (Castellini et al., Reference CASTELLINI, BERRI, LE BIHAN-DUVAL and MARTINO2008). During fattening, chickens are maintained under markedly different conditions, which may include different stocking densities and different group sizes. The profitability of chicken production is therefore largely determined by the proportion of prime meat parts and the fat content, i.e., improved profitability can be obtained by increasing the proportion of prime meat and reducing fat. However, quality standardisation in the chicken industry is lacking due to the lack of knowledge regarding proper housing conditions and management.

Acknowledgements

The authors are grateful to the Egyptian Knowledge Bank (https://www.ekb.eg/web/ guest/home) for its support.

Conflict of interest

The authors declare that there is no known conflict of interest associated with this publication.