Introduction
There is widespread interest in the treatment of animals (Fraser, Reference FRASER2008). From the perspective of the public, captive environments that inhibit or prevent behaviours that are considered to be part of the normal behavioural repertoire are generally contentious. Confinement housing of farm animals, such as those used in modern poultry and pig farming systems, appear to be at the forefront of these concerns. Many factors may affect the welfare of commercial laying hens housed in cage and non-cage systems. The key welfare issues relate to space allowance and group size, and behaviour patterns constrained by conventional cages (nesting, dust bathing and foraging; covered in the companion paper, and perching; Hester, Reference HESTER2014). In addition to issues that relate to behaviour, there are welfare issues that relate to health, such as osteoporosis and broken bones, feather pecking and cannibalism, and health and hygiene (e.g. air quality, infectious disease, parasitic infections and foot health), which may be more prominent in non-cage systems (Rodenburg et al., Reference RODENBURG, VAN KRIMPEN, DE JONG, DE HAAS, KOPS, RIEDSTRA, NORDQUIST, WAGENAAR, BESTMAN and NICOL2013).
Although there is wide acceptance of scientific problem solving, its ability to contribute to the welfare debate has been limited by a lack of consensus on the approach to studying animal welfare and in particular methods used to assess the effects of behavioural constraints. For many scientists, animal welfare is defined and measured on the basis of how well the animal is performing from a biological functioning perspective (Broom, Reference BROOM1986). For others, welfare is determined by affective state, such as suffering, pain, and other feelings or emotions. Thus animal welfare can be studied by measuring animal preferences and strength of preferences on the basis that these are influenced by emotions, which have evolved to motivate behaviour to avoid harm and facilitate survival, growth, and reproduction (Duncan, Reference DUNCAN2005). Another concept is that welfare of animals is improved in environments or situations in which the animals display normal or ‘natural’ behaviour (Spinka, Reference SPINKA2006). These different concepts have led to different methodologies to assess welfare (Fraser, Reference FRASER2008).
Comparisons of the effects of different housing systems on welfare are difficult due to of the wide variation across systems, and because specific design features within systems often have greater effects on welfare than differences between systems. In addition, it is important to recognise that scientists may differ in the degree of importance they place on measures of biological functioning, affective state and natural behaviour as well as how they interpret research findings from varying methodologies. Although the biological functioning, affective state and natural living frameworks were initially seen as competing, Fraser et al. (Reference FRASER, WEARY, PAJOR and MILLIGAN1997) suggested that ethical concerns for quality of life for animals were more fully addressed when all three viewpoints were considered. Hemsworth et al. (Reference HEMSWORTH, MELLOR, CRONIN and TILBROOK2015) recently suggested a more unified orientation where biological functioning is taken to include affective experiences. Therefore, a comprehensive assessment of welfare should include available evidence from each of the different viewpoints and identify areas where different types of scientific evidence concur, where they conflict and where evidence is lacking.
These different viewpoints have been articulated in some working definitions of animal welfare used in policy, e.g. the Five Freedoms developed by the Farm Animal Welfare Council in 1979 in response to concepts originally proposed by the Brambell Report have shaped animal welfare policy in the UK for decades (FAWC, 2009). More recently the World Organization for Animal Health stated in its Terrestrial Animal Health Code (OIE, 2010) that ‘an animal is in a good state of welfare if (as indicated by scientific evidence) it is healthy, comfortable, well nourished, safe, able to express innate behaviour, and not suffering from unpleasant states such as pain, fear and distress’. In Canada, the Scientific Committees for the National Farm Animal Care Council were specifically tasked with reviewing scientific literature that encompassed all three aspects of welfare when producing reports used to inform the development of codes of practice for the care of farm animals (Widowski et al., Reference WIDOWSKI, CLASSEN, NEWBERRY, PETRIK, SCHWEAN-LARDNER, COTTEE and COX2013).
In the following and its companion paper the scientific literature specific to behavioural constraints imposed by different housing systems for laying hens from each of the different approaches to studying animal welfare is reviewed. The current paper focuses on space allowance, group size and the interactions between these two factors, i.e. stocking density. In order to avoid misunderstanding, the same terminology is used as defined by Keeling (Reference KEELING1995), i.e. space allowance is the amount of space per individual hen, group size is the number of hens in the group, and stocking density is the number of hens in a given area or in other words the combination of space allowance and group size.
Space allowance
The minimum spatial need of an animal allows sufficient room to accommodate physical size and basic movement and to enable the animal to effectively change posture (e.g. lie down) or turn around without injuring itself (Fraser and Broom, Reference FRASER and BROOM1997). Dawkins and Hardie (Reference DAWKINS and HARDIE1989) showed that the minimum space used by brown laying hens to accommodate their size and basic movements is greater than provided in conventional cages. For example, using one to four birds per cage to modify floor space over the range of 450-6724 cm2/hen, video records showed that birds used 540-1006 cm2 when turning, 653-1118 cm2/hen when stretching wings and 540-1005 cm2/bird when ground scratching. Using three-dimensional kinematics, Mench and Blatchford (Reference MENCH and BLATCHFORD2014) showed that individually-housed light hybrids used, on average, 563 cm2 for standing, 1315 cm2 for turning and 1378 cm2 for wing flapping.
In addition to physical space, there may be a need for personal space, i.e. to maintain separation between individuals and their conspecifics (Fraser and Broom, Reference FRASER and BROOM1997). The latter space is particularly important for group housing, but its relative importance in small and large groups is not known. Mench and Keeling (Reference MENCH and KEELING2001) suggested that there is little evidence that birds have a personal space, although hens in groups do increasingly maximise distance to their nearest neighbour as floor space allowance increases (Keeling, Reference KEELING1994). Savory et al. (Reference SAVORY, JACK and SANDILANDS2006) found that average nearest neighbour distances in groups of six hens were around 20, 37, 44, 49, 51 and 53 cm at space allowances of 600, 2400, 4800, 7200, 9600 and 12,000 cm2/hen, respectively, with the rate of change levelling off at around 5000 cm2/hen. This suggested that hens have a requirement for physical space to stretch and exercise muscles and may prefer to distance themselves from other birds. Domestication does not appear to have influenced inter-individual distances in the fowl, although it may have reduced behavioural synchronisation (Eklund and Jensen, Reference EKLUND and JENSEN2011). Furthermore, many species are motivated to separate several important functions, for example nesting away from the feeding area.
Space may be needed for body care or grooming and assisting in thermoregulation i.e. when hot (Guo et al., Reference GUO, SONG, JIAO and LIN2012). Hence, when considering spatial requirements for individual animals, it should also be recognised that the animal may have further spatial requirements other than those necessary for physical size and basic movement - they also have requirements for space to perform a range of behaviours that are likely to affect their welfare.
Space allowance and behaviour
While behaviour changes as a consequence of different housing systems, and presumably space and group size are integral to this, comfort behaviours, such as preening, body shaking, scratching, stretching and beak cleaning were found to be similar in conventional cages (stocked at 720 cm2/hen) and aviary systems (stocked at 2953 cm2/hen) (Hansen, Reference HANSEN1994). However, wing stretching, leg stretching and tail wagging all increased in frequency when birds housed with less space were released into larger cages or enclosures (Baxter, Reference BAXTER1994; Nicol, Reference NICOL1987) and in furnished cages as stocking density was decreased (i.e. two and eight hens in the same-sized cage that changed space allowance from 750 to 3000 cm2/ hen; Albentosa and Cooper, Reference ALBENTOSA and COOPER2004). Keeling (Reference KEELING1994) found that walking and ground pecking decreased, but preening was unaffected as space allowance was varied from 5630 to 600 cm2/hen in groups of three White Leghorns. Engel (Reference ENGEL2015) found a 64% reduction in locomotion, a 36% reduction in floor and object pecking and a 17% reduction in preening when brown hens were stocked at 542 versus 1648 cm2/hen in 6-bird cages. Similarly, Guo et al. (Reference GUO, SONG, JIAO and LIN2012) observed birds in furnished cages in groups of 21 at 586 cm2 and 48 at 583 cm2 to sit less and walk more than hens in conventional cages comprised of four hens at 398 cm2/hen. The amount of vertical space provided may be important, although few differences in behaviour were found between cage heights of 38 and 45 cm (Cooper and Albentosa, Reference COOPER and ALBENTOSA2004; Albentosa et al., Reference ALBENTOSA, COOPER, LUDDEM, REDGATE, ELSON and WALKER2007).
Interestingly, Al-Rawi and Craig (Reference AL-RAWI and CRAIG1975) showed a curvilinear relationship between space allowance from 412-2884 cm2/hen in four-hen cages and agonistic interactions, with fewer interactions at the lowest and highest space allowances and more interactions at intermediate space allowances of 824 and 1442 cm2/hen. These results do provide evidence for a need for minimal personal space, but that at the lowest space allowance the birds did not have enough physical space to engage in normal agonistic behaviour.
Preference for space
A few studies have investigated hens’ preferences and motivation for environmental space (Cooper and Albentosa, Reference COOPER and ALBENTOSA2003). When given free choice among different sized cages, individual hens reared in floor pens spent more time in larger enclosures than in smaller ones, although the hens regularly visited and spent short periods of time in the small cages (Nicol, Reference NICOL1986). Using an operant method, Lagadic and Faure (Reference LAGADIC and FAURE1987) showed that groups of four hens would work to increase space above 400 cm2 /hen, but only for 25% of the time, suggesting that there may be an intermittent preference for a larger cage that is context dependent (Cooper and Albentosa, Reference COOPER and ALBENTOSA2003).
Faure (Reference FAURE1991) found that when hens were trained to peck at a key in order to increase their cage size, rearing conditions had a significant effect. Hens reared in cages worked less to enlarge their cages than those from floor pens. However, Engel (Reference ENGEL2015) found no effect of either rearing space allowance (315 versus 945 cm2/hen) or adult space allowance of 542 versus 1648 cm2/hen on hens’ choice of an enlarged cage over feed offered in a small cage in a Y-maze; only 7% of hens housed with reduced space chose the side offering additional space.
Space and biological function
Published data on the effects of space allowance in conventional layer cages shows that in general as floor space decreases, within a range of 300 to 650 cm2/hen, biological function generally decreases, based on either higher mortality, lower egg production and body weight or poorer feed conversion (Hill, Reference HILL1977; Hughes, Reference HUGHES1983; Adams and Craig, Reference ADAMS and CRAIG1985; Sohail et al., Reference SOHAIL, BRYANT and ROLAND2004). An explanation, as suggested by Hughes (Reference HUGHES1983), is the reduced feeding space and in turn its effects on feed intake associated with a floor area reduction in cages of generally constant depth. Another explanation is that crowding may lead to elevated corticosterone concentrations, which in turn may adversely affect both production efficiency and health. Mench et al. (Reference MENCH, TIENHOVEN, VAN MARSH, MCCORMICK, CUNNINGHAM and BAKER1986) reported that reducing space allowance in 2-bird cages from 1394 to 697 cm2/bird increased plasma corticosterone concentrations. Koelkebeck et al. (Reference KOELKEBECK, AMOSS and CAIN1987) reported an 11% increase in plasma corticosterone concentrations in caged hens when space allowance was decreased from 460 to 350 cm2/bird, although the increase was not statistically significant. However, Engel (Reference ENGEL2015) found no effect of space allowances on body weight, measures of egg production, blood or egg corticosteroids or heterophil:lymphocyte ratio when hens were stocked at 542 versus 1648 cm2/hen in 8-bird cages, although feather condition was significantly better at the higher space allowance. Elson (Reference ELSON2004) found better plumage condition as space allowance increased in furnished cages from 600 to 870 cm2/hen.
Group size
For caged hens, while there are studies that show detrimental effects of increasing group size in conventional cages from four to 28 hens per cage on agonistic pecking (Al-Rawi and Craig, Reference AL-RAWI and CRAIG1975); from four to 14 hens (space allowance in both studies of 412 cm2/hen) on agonistic pecking and mortality (Al-Rawi et al., Reference AL-RAWI, CRAIG and ADAMS1976) and in furnished cages from four or five to eight hens per cage on feather pecking and mortality (Appleby et al., Reference APPLEBY, WALKER, NICOL, LINDBERG, FREIRE, HUGHES and ELSON2002). However, similar effects were not apparent in another study on groups of five to eight hens in furnished cages (Abrahamsson and Tauson, Reference ABRAHAMSSON and TAUSON1997). Nevertheless, a review by Mench and Keeling (Reference MENCH and KEELING2001) reported that increasing group size was associated with increased mortality, feather and skin damage and decreased egg production. Appleby (Reference APPLEBY2004) recommended that groups of 10 to 12 birds were best for hen welfare in furnished cages as there was a larger total cage size, yet a lower risk of aggression among birds. Wall et al. (Reference WALL, TAUSON and ELWINGER2004) acknowledged that the risk of aggression increased with group size and undertook a study to determine the effects of an ‘escape area’. They compared hens in standard 16-bird furnished-cages with the same cage divided into two compartments by a partition with pop-holes. They found no benefits based on heterophil:lymphocyte ratios as a measure of stress or feather condition as a measure of aggression. Barnett et al. (Reference BARNETT, TAUSON, DOWNING, JANARDHANA, LOWENTHAL, BUTLER and CRONIN2009) found evidence of increased stress in hens in furnished cages kept in groups of 16 compared to groups of eight hens, based on egg albumen corticosterone concentrations, a lower ACTH-induced corticosterone response at mid-lay, and immunosuppression based on proliferation test to determine the lymphocyte response, controlling for space allowance.
Although the group sizes in furnished cages is restricted to less than 20 birds in some countries (Elson and Tauson, Reference ELSON and TAUSON2012), many newer models of furnished cages house around 60 hens. Reports on different models of large furnished cages stocked at the EU standard of 750 cm2/hen indicated no effects of group size ranging from ten to 60 hens on mortality (Weitzenbürger et al., Reference WEITZENBÜRGER, VITS, HAMANN and DISTL2005), eight to 40 hens (Wall, Reference WALL2011) or 20 to 60 hens (Huneau-Salaun et al., Reference HUNEAU-SALAUN, GUINBRETIERE, TAKTAK, HUONNIC and MICHEL2011) on either production parameters or mortality.
In non-cage systems, aggression appears to be reduced in both small (0 to 20) and large (>100) bird groups (Rodenburg et al., Reference RODENBURG, TUYTTENS, SONCK, REU, HERMAN and ZOONS2005). A comparison of housing birds on the floor in groups of 15, 30 and 60 hens, found production problems with the intermediate group size of 30 hens (Keeling et al., Reference KEELING, ESTEVES, NEWBERRY and CORREIA2003) . Results of several studies on laying hens suggest that as group sizes increase and hens are no longer able to discriminate between all individuals in the group, they switch from a social strategy of maintaining pecking order to a strategy of social tolerance (D'Eath and Keeling, Reference D'EATH and KEELING2003) where group distribution immediately around resources, such as feeders, has a greater effect on aggression than the overall group size (Estevez et al., Reference ESTEVEZ, NEWBERRY and KEELING2002).
In a review of group life in animals, Lindberg (Reference LINDBERG2001) makes some salient points on optimum group size. Groups of optimal size may vary in the wild because if there were such a group size, it would pay for other individuals to join the group and increase it (Sibly, Reference SIBLY1983). This may result in unstable groups. Hence in nature, while groups may be stable, they may be larger than optimum (Pulliam and Caraco, Reference PULLIAM and CARACO1984). Dawkins (Reference DAWKINS1982) refers to the elusive concept of preferred group size as a range of factors that will affect what is optimum for different individuals in a flock. Thus, the stability of groups, stocking density and features of the physical environment may be more important than group size per se.
Stocking density
At any given space allowance, increasing group size alters the dynamics of space use resulting in changes in the amount of space provided to individual hens. While the total amount of space available for locomotion and other behavioural patterns increases, birds tend to cluster around resources resulting in high density in some areas and leaving other areas largely unoccupied (Channing et al., Reference CHANNING, HUGHES and WALKER2001; Collins et al., Reference COLLINS, ASHER, PFEIFFER, BROWNE and NICOL2011).
Few studies have focused on the effects of stocking density in large furnished cages, where the larger group sizes afford more total and free space per individual bird. Based on their determination of the space envelope required for wing-flapping, Mench and Blatchford (Reference MENCH and BLATCHFORD2014) calculated that the individual space allowance per hen required to perform wing-flapping decreased as group size increased. They estimated that the floor space required per hen to perform this behaviour essentially levelled off at around 599 cm2/hen at group sizes of 60 or more. Recently, Widowski et al. (Reference WIDOWSKI, CASTON, HUNNIFORD, LEESON, COOLEY, GUERIN and TORREY2014) and Karcher et al. (Reference KARCHER, MAKAGON, ROBISON and TEMPELMAN2014) examined the effects of stocking density on productivity and welfare measures in large furnished (enriched colony) cages. When comparing performance of light hybrid hens housed in two sizes of furnished cage stocked at either 520 cm2 or 748 cm2 total floor space (group sizes of 40 or 28 hens in the smaller and 80 or 55 in the larger cages), Widowski et al. (Reference WIDOWSKI, CASTON, HUNNIFORD, LEESON, COOLEY, GUERIN and TORREY2014) found no effects on egg production, egg quality, body weight or mortality. However, stocking birds at higher densities resulted in poorer feather condition, cleanliness and foot health in both cage sizes. Karcher et al. (Reference KARCHER, MAKAGON, ROBISON and TEMPELMAN2014) found similar results when comparing light hybrid hens stocked at 464, 581, 652, 748, 800 and 929 cm2/hen. There were no effects of stocking density on hen day egg production, but keel deformities were greater and feather condition poorer in the more crowded cages. The authors suggested that space allowance at or above 581 cm2/hen was appropriate for maintaining the production and welfare of hens in enriched colony cages. The effects of stocking density in non-cage systems are poorly understood. Surprisingly, in studies that had a relatively large space allowance, there was a consistent trend for egg production to increase as space decreased from 2980 to 1580 cm2/hen and from 1050 to 940 cm2/hen (Appleby et al., Reference APPLEBY, HOGARTH, ANDERSON, HUGHES and WHITTEMORE1988). Nicol et al. (Reference NICOL, BROWN, GLEN, POPE, SHORT, WARRISS, ZIMMERMAN and WILKINS2006) reported that mortality was lower but feather loss was worse in small commercial flocks (2450-3150 birds/flock) stocked at 12 birds/m2 (833 cm2/bird) compared to those stocked at either 7 birds/m2 (1428 cm2/bird) or 9 birds/m2 (1111 cm2/bird) in single-tiered aviaries. Egg production, faecal corticosterone and heterophil:lymphocyte ratios were not affected by stocking rate, but stress measures at the end of lay were substantially elevated compared to the end of the rearing period, and the authors considered them to be at levels indicative of poor welfare at all of the stocking densities. Behavioural observations reported for those same flocks showed a density by age interaction with feather pecking and aggression being the highest in the low stocking density initially (at 30 weeks) but it increased with age so that there were no differences by 60 weeks of age (Zimmerman et al., Reference ZIMMERMAN, LINDBERG, POPE, GLEN, BOLHUIS and NICOL2006). When Nicol et al. (Reference NICOL, GREGORY, KNOWLES, PARKMAN and WILKINS1999) compared flocks varying from 72 to 368 birds, at stocking densities of 6, 14, 22 or 30 birds/m2 (1666 to 333 cm2/bird), from 14 to 30 weeks of age, six birds /m2 had higher egg production at 23 weeks and better plumage at 30 weeks compared to birds at all other densities. Channing et al. (Reference CHANNING, HUGHES and WALKER2001) found that the spatial distribution of birds in group sizes ranging from 323 to 912 birds at a constant density of 18.5 birds/m2, varied considerably over time, with specific areas of densities ranging from 9 to 41 birds/m2 and the flux of birds from one part of the pen to another being greater in larger group sizes. Therefore system design, as it affects distribution of birds, may have a greater effect on bird welfare than group size and space.
Conclusions
Within cage systems, there appear to be different thresholds for the effects of space allowance on different measures of hen welfare. In conventional cages or small group furnished cages (two to 30 birds), there is evidence of higher mortality, lower egg production and body weight or poorer feed conversion below 542-650 cm2/hen. However, there are conflicting reports regarding stress (corticosterone concentrations) in hens kept in increasing larger spaces above 542-697 cm2/hen, and evidence of behavioural restriction in terms of wing stretching, leg stretching, tail wagging, locomotion, floor and object pecking and preening at 542-750 cm2/hen. These results suggest biological disruption, in terms of behaviour, stress physiology, mortality and productivity, at the lower end of the space range of 300 to 650 cm2/caged laying hens in conventional or small group furnished cages. The more recent literature on furnished cages suggests that these effects do not necessarily hold true with larger group sizes due to economy of scale and social dynamics.
Hens may prefer to distance themselves from other birds, but their strength of motivation to do so has not been thoroughly investigated and appears to depend on the activities that hens are engaged in. Furthermore, there is still limited knowledge on the effects of group size, in cages or non-cage systems. The effect of stocking density, and particularly through the effects of larger group size on individual space allowance, social dynamics of space use and behaviour, are poorly understood in large cages systems and non-cage systems.
Future work is needed to determine the space requirements of hens for particular resources (e.g. feeders, litter or scratch areas, nests) rather than space allowance per se, in these more complex housing systems. Additionally, differences in social distancing, behavioural synchrony and the time-of-day around specific resources need to be identified in order to design systems that minimise crowding or competition.
