Non-Invited Review. Review of environmental enrichment for broiler chickens

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1 Non-Invited Review Review of environmental enrichment for broiler chickens A. B. Riber, 1, H. A. van de Weerd, I. C. de Jong, and S. Steenfeldt Department of Animal Science, Aarhus University, Blichers Allé 20, P.O. Box 50, DK-8830 Tjele, Denmark; Cerebrus Associates Ltd, The White House, 2 Meadrow, Godalming, Surrey, GU7 3HN, UK; and Wageningen Livestock Research, PO Box 338, 6700 AH Wageningen, The Netherlands ABSTRACT Welfare problems are commonly found in both conventional and organic production of broiler chickens. In order to reduce the extent of welfare problems, it has been suggested to provide stimulating, enriched environments. The aim of the present paper is to provide a review of the effect on behavior and welfare of the different kinds of environmental enrichments in the production of broilers that have been described in the scientific literature. Environmental enrichment is defined as an improvement of the environment of captive animals, which increases the behavioral opportunities of the animal and leads to improvements of the biological function. This definition has been broadened to include practical and economic aspects, as any enrichment strategy that adversely affects the health of animals or that has too many economic or practical constraints will never be implemented on commercial farms and thus never benefit animals. Environmental enrichment for broilers often has the purpose of satisfying behavioral needs and/or stimulating the broilers to an increased level of activity, which among others will reduce the occurrence of leg problems. Potentially successful environmental enrichments for broiler chickens are elevated resting-places, panels, barriers, and bales of straw ( point-source enrichment ), as well as covered verandas and outdoor ranges ( complex enriched environments ). Many of the ideas for environmental enrichment for broilers need to be further developed and studied, preferably in commercial trials, with respect to the use, the effect on behavior and on other welfare aspects such as leg health, and the interaction with genotype, production system, stocking density, light, and flock size. In addition, information on the practical application and the economics of the production system is often lacking, although it is important for application in practice. Key words: behavior, broiler, environmental enrichment, production system, welfare 2018 Poultry Science 97: INTRODUCTION Broiler chickens are commonly produced in barren environments at high stocking densities, causing a wide range of welfare problems (Bessei, 2006). One of the welfare problems associated with conventional broiler production is lameness of various degrees of severities (Bradshaw et al., 2002; EFSA, 2010). This is often related to high growth rates, high body weights, and low levels of activity (Sørensen et al., 1999; Kestin et al., 2001; Knowles et al., 2008; Reiter and Bessei, 2009). Another common welfare problem is contact dermatitis, i.e., hock burns, breast burns, and foot pad dermatitis (Bessei, 2006; EFSA, 2010), caused by continuing contact and pressure of the skin of the breast, hocks, and feet against humid and soiled bedding (Ekstrand et al., 1997, 1998). Due to their substantial feed intake and the resulting high metabolism, broilers produce a high level of surplus heat (Syafwan et al., 2011) that may C 2017 Poultry Science Association Inc. Received July 11, Accepted October 16, Corresponding author: anja.riber@anis.au.dk 378 cause heat stress (Reiter and Bessei, 2000). These welfare problems, in combination with increasing stocking densities that occur up to slaughter weight, lead to a limitation of behavioral expression (EFSA, 2010). This is further exacerbated by barren environments. Furthermore, fear, which may affect welfare, may result in adverse reactions such as panicked fleeing and piling up, leading to injuries, pain, and in some situations, suffocation (Jones, 1989; Mills and Faure, 1990). Organic broiler production systems use genotypes with a lower growth potential compared to conventional production. Although the environment of organic broiler production systems is often richer in stimuli, a number of welfare problems can still arise (van de Weerd et al., 2009). Just like conventional broilers, organic broilers may suffer from lameness, contact dermatitis, breast blisters, and cold stress (see review by van de Weerd et al., 2009). In addition to organic systems, there are systems with animal welfare standards positioned between conventional and organic systems, the so-called middle segment or conventionalplus systems (de Jonge and Van Trijp, 2013; Gocsik et al., 2016), including higher welfare indoor systems

2 ENRICHMENT FOR BROILERS A REVIEW 379 (e.g., RSPCA Assured, formerly Freedom Food 1 ). These systems often use broiler genotypes with a lower growth potential as compared to conventional production systems or they use fast-growing genotypes but have a lower maximum stocking density. Usually, the environment in these broiler systems is richer in stimuli as compared to conventional systems, e.g., they provide perches, straw bales, pecking objects, and natural light (windows). They may also have a covered veranda, which provides a halfway house between the indoor and outdoor environment and provides scratching opportunities. Prevalence of welfare problems such as contact dermatitis, lameness, and heat stress is considered to be lower in these systems as compared to conventional broiler production (EFSA, 2010). It has been suggested that by providing a more stimulating enriched environment, welfare problems can be reduced in all types of broiler production systems (Kells et al., 2001; Bessei, 2006; Bailie et al., 2013). Enriched environments can enhance the well-being of animals by allowing them to perform more of their species-specific behavioral repertoire and accommodate a larger range of behavioral choices (Van de Weerd and Day, 2009). Newberry (1995) defined environmental enrichment as a modification of the environment of captive animals, thereby increasing the animal s behavioral possibilities and leading to improvements of the biological function. This means that environmental enrichment is provided with the purpose of: 1) increasing the occurrence and range of the animal s normal or species-specific behavior, 2) preventing the development of abnormal behavior or reducing its extent and complexity, 3) increasing the positive exploitation of the environment (e.g., the use of an outdoor area), and 4) increasing the animal s ability to handle behavioral and physiological challenges. It is emphasized that environmental enrichment must be biologically relevant to be effective. Van de Weerd and Day (2009) broadened Newberry s definition on enrichment by proposing a framework that includes health, practical, and economic aspects. They defined successful enrichment as having to meet 4 criteria of success: 1) it should increase species-specific behavior, 2) it should maintain or improve levels of health, 3) it should improve the economics of the production system, and 4) it should be practical to employ (Van de Weerd and Day, 2009). This takes into consideration that any enrichment strategy that adversely affects the health of animals, or that has too many economic or practical constraints will never be implemented on commercial farms and thus never benefit animals (Van de Weerd and Day, 2009). For example, conventional broiler production works with very high animal densities, which may be prohibitive to enrichment structures 1 For an example of such a system, see: Compassion in World Farming, Broiler chicken case study. UK1: RSPCA Freedom Food indoor farm. Available online: /GAP-Broiler-Chicken-Case-Study-UK1-Higher-Welfare- Indoor-RSPCA-Freedom-Food.pdf (accessed on 17 February 2017) that take up too much space or may become a risk for leg injuries. Enrichment strategies can benefit various welfare aspects in a synergistic way. For example, enrichment that increases activity of broilers and the occurrence of species-specific behavior is also likely to improve other welfare aspects, such as health. Several studies have found that the development of bones and muscles in broilers can be strengthened by increasing activity, especially early in the growth period (Reiter and Bessei, 1998, 2009; Bizeray et al., 2002a). When bones and muscles are strengthened, it may have a reducing effect on lameness, although the results found in the study of Bizeray et al. (2002a) did not confirm this hypothesis. Also, a reduction in time spent lying down will decrease the duration that the hocks and breast are in contact with the bedding thus reducing the risk of dermatitis. Increased scratching of the litter improves drying and promotes the litter to stay loose, thereby decreasing the risk of dermatitis on feet and hocks (De Jong et al., 2013). Furthermore, dermatitis and lameness have been found to be correlated in broilers (Sørensen et al. 2000; Kristensen et al., 2006; Haslam et al. 2007). Therefore, both contact dermatitis and lameness can be reduced if broilers have less contact with bedding that contains high levels of humidity and ammonia. Enrichment should increase the animal s ability to handle behavioral and physiological challenges (Newberry, 1995). This means that the effects of enrichment should not only focus on biological functioning (such as lameness, hock burn, or activity), but should also benefit the animals experiences, i.e., their affective states (Mellor and Webster, 2014). For example, enrichment is generally considered to reduce fear in domesticated poultry (Jones, 1996), especially if the enrichment provides the birds with the possibility of temporarily escaping the floor surface (Brake et al., 1994) or if it provides shelter (e.g., cover panels; Cornetto and Estevez, 2001a,b). The aim of this review is to give an overview of the different kinds of environmental enrichment in all types of production systems for broilers, as described in the scientific literature. Furthermore, the purpose is to assess the effect of the described environmental enrichments on behavior and welfare according to Newberry s (1995) definition as well as Van de Weerd and Day s (2009) framework. MATERIALS AND METHODS The review is based on relevant scientific literature from the database Web of Science retrieved using the key words broiler environmental enrichment. In addition, the review includes references identified on reference lists of papers reviewed. With the exception of a few textbook sources and scientific reports, only peer-reviewed references have been included, written in English or German.

3 380 RIBER ET AL. The time frame for inclusion into the review was that sources were published in or after the year There is older literature available, but as intensive breeding of broiler chickens has changed the growth, body conformation, and the characteristics of leg problems (e.g., reduction of tibial dyschondroplasia; EFSA, 2010; Zuidhof et al., 2014), the interactions between enrichment, behavior, and welfare may not be of relevance for modern-day broilers. In cases where it was likely that the broilers growth rate (genetic background) may have influenced the results of a study, it will be commented on in the text. For example, when growth rate could have relevance, the genotype studied is indicated as either fast- or slowgrowing (the latter typically only grow a maximum of 35 g per d, as a lifetime average). However, there is high variation within the slow-growing category, as some genotypes have a considerable lower growth rate than others. Enrichment Categories The enrichment strategies described in the literature have been grouped into 2 main categories. The first category (A) are conventional environments enriched with point-source objects (Van de Weerd and Day, 2009). These are enrichment objects/devices that are generally limited in size, and their use is often restricted to a single or a few locations in an animal enclosure (e.g., perches, pecking objects). The second category (B) are more complex enriched environments that differ more radically from conventional production systems and have been designed to meet the key behavioral needs of the animals within them (Van de Weerd and Day, 2009). This category has 2 sub-categories: (B1) more complex enriched environments with outdoor access and (B2) more complex enriched environments of the higher welfare indoor systems (e.g., conventional-plus, RSPCA Assured). Each point-source enrichment object or complex enriched environment, within a category, has subsequently been described in terms of the resource it provides (the inputs) and in terms of its effects on the animals (outcomes). This reflects the shift from the traditional way of measuring welfare by assessing a housing system and the resources that have been provided to the animals (input- or resource-based measures) towards focusing on the effects on the animals themselves (outcome- or animal-based measures) (Webster et al., 2004). An animal s current welfare state also integrates long-term consequences of past husbandry (Ibid.). Assessing Effectiveness (Outcomes) for Broiler Chickens A range of indicators can be applied when assessing the welfare outcomes for poultry some indicators are specifically for broilers, while others can be applied to poultry in general (Bessei, 2006; Welfare Quality, 2009). In this review we have focused on assessing the effects of environmental enrichment on the level of activity, lameness, and contact dermatitis of broilers. Furthermore, we assessed variables such as time spent perching, foraging, social disturbances, injuries, heat-stress, bone strength, cleanliness of the plumage, fear, breast blisters, keel bone deviations, growth, body weight, and mortality. In addition, the distribution of broilers in the house was used as a welfare indicator, as a heterogeneous (or patchy) distribution of broilers results in high local stocking densities which can affect many of the welfare indicators mentioned above (Hall, 2001; Dawkins et al., 2004; Abudabos et al., 2013). When indicated in the literature, any effects on feed conversion reported, have been reviewed in order to give an insight into potential production-related consequences of environmental enrichment. TYPES OF ENVIRONMENTAL ENRICHMENT FOR BROILER CHICKENS (A) Point-Source Objects in Standard Environments The following types of Point-Source Objects in Standard Environments are reviewed in this section: perches and platforms; barriers, panels, and bales of substrates (e.g., straw and wood shavings); materials and methods stimulating foraging and dustbathing behavior; and novel objects. Perches and Platforms Resting on elevated structures, such as on trees or perches, is a natural behavior for both jungle fowl and their domesticated relatives (Collias and Collias, 1967; Sandilands et al., 2009). Therefore, an obvious method to enrich the environment of broiler chickens is to offer structures for perching. Table 1 lists the main features of the perches and platforms (resource inputs) used in the studies reviewed in this section. Different designs of perches and platforms have been studied which mostly consist of wood or plastics and sometimes metal. Traditional designs tested are suspended bars and A-frame structures, similar to those offered to laying hens. Other designs are platforms with or without ramps. Experimental studies of fast-growing broilers use of perches, have shown to vary from a minimum use (<2% of the flock registered on perches during observations) to an average use of 25% of the daytime (LeVan et al., 2000; Su et al., 2000; Pettit-Riley and Estevez, 2001; Ventura et al., 2012; Groves and Muir, 2013). The reason for the low use of perches compared to laying hens appears to be poor design of perches that does not consider the high body weight, weak bones, and the broilers body conformation with a heavy breast muscles. Groves and Muir (2013) found that the use of perches in 2 fast-growing genotypes depended on

4 ENRICHMENT FOR BROILERS A REVIEW 381 Table 1. Perch and platform design for broilers used in different studies (N/A = information not available). Reference Material Design Genotype Stocking density Height above ground Dimensions (length width depth OR length, Ø) Shape and access ramp Slow growing Fast-growing Aksit et al.,2017 Bailie and O Connell, 2015 Bailie and O Connell, 2016 Galvanized steel pipes Supported wooden beam 15 cm 200 cm, Ø2 cm - Ross /m 2 15 cm cm Rounded upper edge N/A N/A N/A A-frame with platform - Ross (but not exceeding 30 kg/m 2 ) - Ross 308 Cycle 1 = 12,Cycle2 = 17 Suspended platform Flat topped ramp Curved ramp Wooden beams Fixed bar Suspended bar Bizeray et al., 2002b Wooden beams 15 cm 100/ Ross cm Bokkers and Koene, Wooden slat 10 cm cm Rounded upper JA 657 HI-Y (Hubbard) edge Groves and Muir, 2013 Wooden beams 15 and 30 cm cm - - N/A, BW at d 28: 3.8 breed A 1,590 g, breed B 1,502 g Estevez et al., 2002 Iron pipes, cooled 15 cm 456 cm, Ø3.8 cm Round - Peterson Cobb with 10 C water Iron pipes, cooled 7.5 cm with 10 C water Iron pipes 15 cm Kaukonen et al., 2016 Elevated plastic 30 cm cm Ramps with 15 - Ross platforms angles Wooden beams 10 cm cmor cm Rounded upper edge 30 cm LeVan et al., 2000 PVC pipes 8.5 cm 91 cm (main bar), Without ramp, - Avian Avian cm (crossbar), Ø2.6 cm round 17 cm Ramps with 10 angle, round 35.5 cm Ramps with 20 angles, round Martrenchar et al., 2000 Wooden beams 20 and 33 cm 200/ cm Nielsen, 2004 Wooden beams 40, 65, 90, 115, and 140 cm Norring et al., 2016 Pedersen et al., 2017 Pettit-Riley and Estevez, 2001 Rounded upper edge Elevated plastic platforms 30 cm cm Ramps with 15 angles Wooden perches 10 cm cmor Rounded upper cm edge 30 cm Elevated plastic 30 cm cm Ramps with 15 platforms angles PVC pipes 8.5 cm 91 cm (main bar), Without ramp, 0 28 cm (crossbar), angle, round Ø2.6 cm 17 cm (max) Ramps with 10 angle, round 35.5 cm (max) Ramps with 20 angle, round Pettit-Riley et al., 2002 PVC pipes 8.5 cm 91 cm (main bar), 28 cm (crossbar), Ø2.6 cm - Ross 1 Exp. 1: 11 or 22 Exp. 2 & 3: cm - i657-6 Without ramp, 0 angle, round 17 cm (max) Ramps with 10 angle, round 35.5 cm (max) Mixed: 0,10,and 20 angle, round Sandilands et al., 2016 Wooden beams N/A 150 cm?? A-frame with 42 angles A-frame with 12 angles, wire ramps Labresse - Ross Ross Avian Avian 10, 15, and 20 Avian Avian 10, 15 and 20 - Ross 308 N/A

5 382 RIBER ET AL. Table 1. Continued. Reference Material Design Genotype Stocking density Height above ground Dimensions (length width depth OR length, Ø) Shape and access ramp Slow growing Fast-growing Su et al., 2000 Wooden beams Weeks 0 2: 10 cm, wk 2 6: 25 cm?, Ø1.5 cm Ventura et al., 2010 Wooden beams 10 cm cm Simple barrier: I-shape? cm - - Ross cm and cm Complex barrier: E-shape Ventura et al., 2012 Wooden beams 10 cm cm Simple barrier: I-shape cm Complex barrier: and 20 4 E-shape 15 cm - Ross 308 8, 13, and 18 - Ross 308 8, 13, and 18 Yngvesson et al., 2016 N/A N/A N/A - Rowan Ranger Ross 308 N/A Hubbard CYJA57 Zhao et al., 2013 Iron pipes, cooled with 10 C water N/A N/A - - Arbor Acres 12, 16, and 20 1 Genotype not specified further. Slow-growing broilers are genotypes that typically grow a maximum of 35 g per d, as a lifetime average. Growth period 10 wk. genotype but was independent of body weight, indicating that differences in conformation may have played a role. Slow-growing genotypes use the perches more than fast-growing genotypes. For instance, Bokkers and Koene (2003) found that a slow-growing genotype (JA 657) spent 34.3% of the daytime on perches when 1 to 6 wk old compared to 10.1% for the fast-growing genotype (HI-Y from the breeding company Hubbard). Yngvesson et al. (2016) found that slow-growing birds (Rowan Ranger, Hubbard CYJA57) perched more than twice as much as Ross 308 birds under organic conditions. Pullets of fast-growing genotypes use perches more often than cockerels (Martrenchar et al., 2000; Estevez et al., 2002), which is likely related to the lower body weight of females. Age influences the use of perches and producers have reported a decline in use with increasing age (Sandilands et al., 2016). Normally, the use of perches starts around 1 wk of age (depending on the level of the lowest perch) after which fast-growing genotypes (Ross 308 and Avian Avian) increase their use of perches until 3 to 4 wk of age, followed by a decrease during the last part of the broilers life (LeVan et al., 2000; Pettit- Riley and Estevez, 2001; Ventura et al., 2012; Bailie and O Connell, 2015). In slow-growing genotypes, the decrease is often not seen until much later probably dependent on how slow the growth is. In slow-growing JA 657 s the decrease was only seen around 10 wk of age (Bokkers and Koene, 2003). However, Martrenchar et al. (2000) found a continued increase in perch use in Ross 308 birds until slaughter in wk 6. Likewise, Sandilands et al. (2016) observed an increase in perch use with increasing age (in wk 5, >40% of birds were on perches at lights off) in an experimental study of Ross 308. Ross 308 birds in organic production have been observed perching up until slaughter at 82 d of age (Yngvesson et al., 2016). The way in which access to perches is provided appears to be an important factor influencing usage. Perches that the broilers had to hop onto were preferred over perches that could be reached via a ramp from the floor (LeVan et al., 2000). The broilers preferred to use perches without a ramp and that were 8.5 cm high. The use of perches that were accessible via a ramp was lower, if the ramp was steeper. Sandilands et al. (2016) observed that perch use increased if the perches were easier to negotiate, e.g., by using shallower angles and wire to move from rail to rail, and that such designs increased night-time use with bird age. Both of these studies were done with fast-growing genotypes. The influence of stocking density on the use of perches is still unclear as studies show conflicting results. Martrenchar et al. (2000) found an increased use of perches at an increased stocking density (11 vs. 22 Ross broilers per m 2 ). Pettit-Riley and Estevez (2001) also found an increased use of perches in increasing stocking densities (10, 15, and 20 Avian Avian broilers per m 2 ). Zhao et al. (2013) found the same pattern at 4 wk of age (12, 16, and 20 fast-growing broilers per m 2 ) but not at 5 to 6 wk of age. Like Ventura et al. (2012), Zhao et al. (2013) found an early peak (at 3 wk of age) at a high stocking density (18 Ross 308 broilers per m 2 ) after which the increase in use at the high stocking density ceased while it continued to increase at 4 to 5 wk of age in broilers at the low stocking density (8 broilers per m 2 ). Access to perches is believed to improve the broilers opportunities for thermoregulation as they can get away from the heat-emitting litter, and will get air under their bodies. This has been studied by using perches

6 ENRICHMENT FOR BROILERS A REVIEW 383 consisting of metal water pipes in which water of 10 C is circulated (Estevez et al., 2002).When tested at high temperatures (30 to 34 C), Peterson Cobb broilers preferred cooling perches over non-cooled metal pipe perches, and they preferred the most cooling part of the cooling perches compared to the less cooling part (Estevez et al., 2002). The use of perches is reduced at very high air temperatures (from around 28 C; LeVan et al., 2000) unless cooled perches are used. Providing perches did not affect lameness scores (Su et al., 2000; Bailie and O Connell, 2015) nor prevalence of tibia dyschondroplasia or tibia curvature (Su et al., 2000) in fast-growing broilers. Despite a low occurrence of use of perches, Groves and Muir (2013) found that broilers (2 genotypes, not further specified) with access to perches had a higher endurance in a test where the latency for the birds to lie down was measured. This can be used to assess if perching results in stronger legs or reduced lameness. In fast-growing broilers, Zhao et al. (2013) found a reduction in the number of hock burns and foot pad dermatitis associated with access to perches, while Ventura et al. (2010) only found a tendency for foot pad dermatitis to be reduced. The plumage is kept cleaner when perches are provided (Zhao et al., 2013). Perches may reduce the level of aggression in the flock (Ventura et al., 2012). The effect is, however, dependent on the design of the perch; the choice between several kinds of perches reduced the level of aggression more than by providing only one kind of perch (Pettit-Riley et al., 2002). Access to perches reduced the number of disturbances, i.e., pushing and trampling (Ventura et al., 2012). Disturbances are of great importance to welfare as they disrupt sleep and behaviors such as preening, sitting, and lying (Buijs et al., 2010). If a significant number of broilers rests on perches, active individuals remaining on the floor will encounter and possibly step on fewer other broilers when moving through the flock. Consequently, fewer disturbances will result in fewer scratches (Estevez, 2007). Provision of perches did not result in a reduction of the level of fear in Ross 308 broilers (Bizeray et al., 2002b; Aksit et al., 2017). There is concern that the use of perches is associated with the occurrence of breast blisters (Nielsen, 2004). Breast blisters are swellings of the sternal bursa (a fluidfilled sac). The primary cause of breast blisters is believed to be long-term or repeated pressure against the keel bone, such as during use of perches. However, it appears that genotype and sex have considerable higher impact on the risk of developing breast blisters than the use of perches in itself (Nielsen, 2004). It is possible that a broiler s anatomy also plays a role (possibly linked to growth rate), as some genotypes are more susceptible to developing breast blisters, due to the angularity of the keel bone. However, this also depends on actual usage by the birds, as in Nielsen s 2004 study, slow-growing i657 birds used perches more (9.5 vs 0.1 birds perching at midnight) than slow-growing Labresse birds, and were therefore less likely to develop breast blisters. These birds were also much heavier than Labresse birds (2246 g vs 2011 g). There is a risk that breast blisters make perching painful (Nielsen, 2004). Damage to the keel bone is another risk of perching that has been observed in broilers. The risk of keel bone deviations may be higher for slow-growing genotypes who use perches considerably more and live longer than fastgrowing genotypes. In one study, keel bone deviations were found in 19.1% of birds of a slow-growing genotype and in only 2.4% of birds of a fast-growing genotype (Bokkers and Koene, 2003). No effects of perches have been found on body weight, feed consumption, and feed conversion at slaughter age in Ross 308 (Aksit et al., 2017). Another method of providing elevated options for perching is to offer raised platforms, which are usually (plastic) slatted areas accessible by a ramp. They are already in use on commercial farms, e.g., in Switzerland where they are used for broiler breeders (Gebhardt- Henrich and Oester, 2014) and for fast-growing broiler genotypes. In a Finnish study, fast-growing broilers (Ross 508) on commercial farms were offered plastic platforms (20 platforms per 797 m 2 ) with ramp access. On average good usage of the platforms was observed (48 birds were observed on each platform during the observations; flock size 12,945), but the presence of platforms had no effect on any other measures of activity compared with the control birds housed without platforms (Norring et al., 2016). Leg health was better in birds with access to the platforms, as this resulted in significantly lower mean gait scores (i.e., better gait) and lower percentage of tibial dyschondroplasia (Kaukonen et al., 2016). Furthermore, the presence of platforms had no effect on foot pad condition and 72% (±3.7%) of the assessed birds had healthy foot pads (Ibid). Bailie and O Connell (2016) showed that fast-growing Ross 308 broilers showed a preference for occupying suspended, raised platforms, compared to traditional perches (bars) or ramps. This preference might have been related to the higher rate of successful attempts at perching on these platforms, as the birds had more problems with perching on suspended bars (measured as failed attempts to perch). Platforms offer additional possibilities for locomotion. It is possible that broilers make better use of these types of elevated resting places as compared to perches, as raised platforms will be easier to access and heavy birds may have fewer problems with finding their balance when resting. However, there is very limited scientific knowledge about the effects of such resting places on behavior and other welfare aspects, but on-going studies are in progress, showing, among other results, promising reducing effects on the fear level of fast-growing broilers (Pedersen et al., 2017). In summary, the opportunity to perch is utilized by broilers and will be suitable enrichment for both slowand fast-growing broilers. As such, it is an effective form of enrichment. Designing perches low and wide

7 384 RIBER ET AL. for better support of the broilers increases usage, and perching of up to 25% of daytime has been recorded. Usage of elevated resting places is also influenced by genotype, age, environmental temperature, flock size, and stocking density. Outcomes for animals have been described as effects on leg/foot health, behavior disturbances, and aggression. The knowledge on the risk for breast blisters and keel bone damage is low or unknown. Panels, Barriers, and Bales of Substrate Broilers do not disperse evenly in the house; they prefer the area along the walls over the middle of the house (Newberry and Hall, 1990; Arnould et al., 2001; Arnould and Faure, 2004; Buijs et al., 2010). An uneven distribution of broilers in the house results in high, local stocking densities and this may contribute to welfare problems related to high stocking densities, such as in contact dermatitis due to deterioration of the litter (Hall, 2001; Bassler et al., 2013; Knierim, 2013) and more disturbances of resting birds (Hall, 2001; Dawkins et al., 2004). It has been proposed that broilers prefer the area along the walls because they are less disturbed there (Arnould et al., 2001; Buijs et al., 2010), although Cornetto et al. (2002) found that there were more disturbances along the walls than in the middle of broiler houses. Another theory is that a lack of cover in the environment may be the reason that broilers have a tendency to seek protection along the walls (Newberry and Shackleton, 1997). The placement of panels and barriers in the central part of a broiler houses has been suggested as a possible solution to increasing the complexity of the environment and thereby achieving a more homogeneous distribution of broilers in the house. A similar effect has been described in rats who showed reduced thigmotaxis (wall-hugging behavior) in enriched environments (Harris et al, 2009). Barriers can be designed so that the birds may also use them as perches. Substrate bales (e.g., straw or wood shavings) in the central part of the house can have the same function and may, in addition, stimulate explorative behavior. Table 2 lists the main features (resource inputs) of the panels, barriers, and bales of substrate used in the studies reviewed in this section. Cornetto and Estevez (2001a,b) found a more even distribution of fast-growing broilers when panels were provided in the central part of the house. More broilers were found in the middle of the house and fewer aggregated along the walls. Even panels that only Table 2. Panel, barrier, and substrate bale design for broilers used in different studies (N/A = information not available). Reference Material Design Genotype PANELS Cornetto and Estevez 2001a,b; Cornetto et al., 2002 Rodriguez- Aurrekoetxea et al., 2014 BARRIERS Bizeray et al., 2002a Ventura et al., 2010, 2012 SUBSTRATE BALES Bailie et al., 2013 Bailie and O Connell, 2014 Frame: white PVC, Mesh: black plastic Frame: white PVC Frame: white PVC, Mesh: green plastic Height Dimensions (length width) Style 61 cm 61 2cm Framewith mesh Frame without mesh 50 cm cm Frame with mesh Wooden beams 9 cm 100 4cm and cm Wooden beams 10 cm 100 4cm and cm 100 4cm and 20 4cm Location/ Quantity provided Slow-growing Fast-growing Stocking density Centre of house Center of house and outdoor area - Between feed and water Simple barrier: I-shape Complex barrier: E-shape Wheat straw 40 cm cm Bale edges wrapped in plastic Wheat straw 40 cm cm Bale edges wrapped in plastic Between feed and water Dispersed evenly, 1 bale per 44 m 2 Dispersed evenly, 1 - Avian Avian, BW at d 44: 2.10 kg 9 and 12.3 Sasso T44 - Indoor: 12, Outdoor: 2 - Ross Ross 308 8, 13 and 18 - Ross 17 (but not exceeding 30 kg/m 2 ) - Ross and Cobb 1 bale/44 m 2 Dispersed evenly, 1 bale/29 m 2 Kells et al., 2001 Straw 30 cm cm - 1 bale/17 m 2 - Ross and Cobb Numbers indicated are the effectively heights derived from 15 cm high barriers placed in 5 6 cm wood shavings. 1 Genotypes not specified further. 17 (but not exceeding 30 kg/m 2 ) N/A

8 ENRICHMENT FOR BROILERS A REVIEW 385 consisted of a frame without any solid in-fills had an attractive effect on the broilers (Cornetto and Estevez, 2001b). Likewise, Rodriguez-Aurrekoetxea et al. (2014) found that provision of panels, increased the use of the central part of the house by slow-growing broilers. The presence of panels reduced the number of incidents in which broilers were disturbed making them stand up while resting (Cornetto et al., 2002). Broilers from houses with panels rested more and foraged less than broilers from houses without panels, regardless whether the panel was only a frame without in-fill or a frame with netting (Cornetto and Estevez, 2001a). The higher level of resting may be due to more highly valued resting places against a partition and because the broilers were less disturbed while sleeping. The higher occurrence of resting and lower occurrence of foraging could possibly increase the risk of contact dermatitis and locomotion problems. The presence of panels has been found to have no influence on body weight at 44 d of age (Cornetto and Estevez, 2001b) or daily growth (Rodriguez- Aurrekoetxea et al., 2014). As far as we know, there are no studies on the effect of panels on leg problems in broilers. Barriers differ from panels, in that they are generally lower, but wider than panels, thus allowing perching (see Table 2). Barriers provide elevated resting places for broilers, but may also increase activity, as birds have to walk around them (Bizeray et al., 2002a). In a study where barriers were placed between feed and water lines, it was found that the number of times the barriers were passed did not change significantly with age (varying between 2.2 to 5.8 times per individual per hour). The use of barriers for perching, however, increased from the age of 1 to 4 wk, after which it remained at the same level (each broiler spent an average of 15 to 17% of the light period time perching on the barriers; Bizeray et al. 2002a). Broilers with access to barriers made fewer visits to feed and water and were less frequently observed feeding and drinking than control broilers, indicating that the barriers were actually perceived as barriers. Barriers stimulated perching but did not stimulate other activities, as was expected (Bizeray et al. 2002a; Ventura et al., 2012). Broilers were able to compensate for fewer visits to the feeders, by increasing feed intake during a visit. No effects on feed conversion, growth, final body weight, or mortality were found, indicating no negative effects of barriers on broiler performance (Bizeray et al., 2002a; Ventura et al., 2010). Ventura et al. (2012) found that barriers reduced the number of occurrences of aggression and disturbances. In addition, Ventura et al. (2010) found that simple barriers tended to reduce the occurrence of foot pad dermatitis, while more complex barriers increased the symmetry and the length of tibias. Furthermore, broilers exposed to simple barriers demonstrated an increased susceptibility to the induction of tonic immobility than broilers exposed to complex barriers or broilers housed without barriers. The duration of tonic immobility (a more accepted measure of fear) did not differ between treatments. Kells et al. (2001) studied the effect of bales of straw on fast-growing broilers behavior and level of activity in a farm study. They allocated one small bale per 17 m 2 and found that the broilers used the bales of straw to sit on or sit against, but that overall, they rested and sat less and stood and walked more than birds without bales. The mean number of birds standing on a bale at any time was 1.59 birds per bale. Bailie et al. (2013) examined the effect of bales of straw (1 bale per 44 m 2 ) and natural light on behavior and leg problems in Ross broilers on a commercial farm. There was no effect of bales of straw on activity levels or the time spent sitting, but the latency to lie, a test that assesses potential leg problems, was longer for broilers housed with bales of straw as compared to those housed without bales. In addition, the lameness scores for the broilers housed without straw bales and without natural light were worse compared to the birds in other treatments. Subsequently, Bailie and O Connell (2014) examined the effect of the density of bales of straw (1 bale per 44 m 2 vs. 1 bale per 29 m 2 ), but they found no effect of bale density on the level of activity, lameness score, or contact dermatitis. However, they did find higher latencies to lie down, suggesting better locomotion, at the lower density (1 bale per 44 m 2 ). No effect of straw bales has been found on slaughter weight and number of birds culled or found dead (Bailie et al., 2013, Bailie and O Connell, 2014). As far as we know, the effect of straw bales on broilers distribution in the house has not been studied. In addition to bales of straw, bales of other types of substrates (such as wood shavings, miscanthus, or silage) are used on commercial farms. However, there appear to be no scientific studies on the use and effects of these types of substrates on broiler welfare. In summary, panels, barriers, and bales of straw are all types of environmental enrichment that broilers use for perching or for a quiet resting area to lie against with reduced disturbance, and as such, it can be effective enrichment. Furthermore, panels and barriers can contribute to a more even distribution of birds in the house, which ameliorates potential localized problems associated with high stocking densities. Scientific knowledge is unclear about effects of these objects on leg/foot health and on activity. Materials and Distribution Methods Stimulating Foraging and Dustbathing Behavior Many materials have been tested for their suitability as bedding for broilers (see review in Su et al., 2000; Toghyani et al., 2010). In preference tests, broilers preferred sand over wood shavings, rice hulls, a recycled paper bedding product, and no litter (Arnould et al., 2004; Shields et al., 2004, 2005; Toghyani et al., 2010). Therefore, it has been suggested that the provision of sand can stimulate activity levels in broilers, possibly resulting in fewer leg problems (Shields et al., 2004). However,

9 386 RIBER ET AL. Shields et al. (2005) could not demonstrate a higher level of activity in broilers housed on sand, compared to broilers on wood shavings. In contrast, Arnould et al. (2004) did find a higher level of foraging in broilers with access to sand, in combination with bedding of wood shavings, compared to broilers with only bedding of wood shavings. Baxter and O Connell (2016) offered commercial broilers a choice of 5 different foraging and dustbathing substrates in steel rings (0.96 m 2 area, 10 cm high; 3 rings/substrate), placed evenly throughout a house enclosing 23,000 broiler. Substrates tested were moss-peat, oat husks, straw pellets, or clean wood shavings. Control rings were empty with only the standard sawdust bedding. All substrates were offered from d 10. The moss-peat and clean wood shavings attracted more birds than the other substrates. Moss-peat and oat husks had the highest levels of dustbathing and foraging, and the lowest levels of (inactive) sitting. This shows that birds have preference for certain types of substrate and that these substrates elicit active behavior, thus reducing overall levels of inactivity. Only a few studies have examined if bird activity is stimulated by offering increased possibilities for foraging or through changes in the method of how feed is presented. Jordan et al. (2011) examined the effect of scattering feed in the bedding on the level of activity and growth in fast-growing broilers (Ross 308). Groups of broilers received either a) no feed in the bedding, b) all feed scattered in the bedding, 5 times daily, from the age of 15 d, or c) whole wheat scattered in the bedding twice daily, in addition to feed from the feeders. Scattering of whole wheat in the bedding (treatment c) did not change the broilers time budget or growth compared to control broilers. In contrast, the time budget of broilers that had all their feed scattered in the bedding (treatment b) was markedly different: they spent less time lying down in wk 3 and 4, and more time on locomotor activity and foraging in wk 3, 4, and 5. However, growth was significantly reduced in broilers with all the feed scattered in the bedding, and the final live body weight was 13% lower. In a study with Ross 308, Bizeray et al. (2002a) scattered whole wheat in the bedding twice daily (from d 8 to 17), comparable to treatment c by Jordan et al. (2011), supplementary to the standard feed in the feeders. They also did not find any changes in the time budget. In a recent study, Pichova et al. (2016) came to the same conclusion that scattering of whole wheat or wood shavings did not increase locomotor or foraging activity of Ross 308 broilers. Whole wheat or wood shavings were scattered once daily (100 ml each) in floor pens (100 cm 100 cm) with 10 broiler chickens per pen. Interestingly they included a treatment with scattering of meal worms in the litter, considered as a highly valued food by broilers. The meal worms (100 ml) were spread on the litter once daily and increased activity levels, litter pecking, and scratching significantly compared to the other treatments. However, the effect was transient as the activity decreased after 10 min., when there were no more meal worms available in the litter. Pichova et al. (2016) concluded that in order to prolong the effect of food based enrichment, more frequent feeding with smaller amounts would be necessary, as well as development of specific feeding systems for distribution under practical conditions. Even though this study presents encouraging results on the effect of alternative feed items to stimulate activity, it should be kept in mind, that in the EU (Commission Implementing Regulation (EU) No 836/2014), it is not permitted to feed insect protein to food producing animals. The provision of roughage (forage, fodder) is mandatory in organic broiler production in the EU (Commission Regulation (EC) No 889/2008) and is considered as a valuable addition to foraging in outdoor areas, where the vegetation is often eroded and insufficient during the winter period. Since the dry matter content of roughage varies a lot (Steenfeldt and Hammershøj, 2015) there is an increased risk of humid bedding in the house thus increasing the risk of contact dermatitis. For this reason, provision of roughage in organic production often takes place in a specific area, for instance in a covered veranda built against the house. Alternatively, small amounts of roughage can be distributed automatically several times daily to reduce the risk of leftovers. When the birds are scratching and foraging in the distributed material, the risk of wet bedding is reduced. Provision of roughage in this way is common in Danish organic egg-production, although at present, only large organic broiler producers have implemented this automatic system (J.S. Petersen, SEGES advisory center, Aarhus, Denmark, personal communication). No studies exist on allocation of roughage for conventional broilers. Arnould et al. (2004) examined whether hanging strings (minimum distance between strings: 10 cm; hanging 1 cm above the head of a standing broiler; material and number of broilers per string: not mentioned) were suitable as environmental enrichment but found that broilers showed very little pecking activity at the strings. The lack of interest was suggested to be due to the strings hanging in an area with low light intensity that was mainly used for resting by the broilers. Bailie and O Connell (2015) placed 24 strings in a commercial flock of 23,000 broilers (958 broilers/string; material: white nylon rope; height: 3 cm and then gradually raised to 20 cm above the litter) close to the feed troughs and found the frequency of string use peaking when the broilers were 3 wk old. They also found that birds spent more time on locomotion at the age of 3 wk compared to locomotion at 4 and 5 wk of age. In wk 3 and 4, broilers with access to strings had a small improvement in gait score, but this was not supported by another test in which broilers latency to lie down was measured, assessing potential leg problems. In summary, the provision of a foraging substrate such as sand that is preferred by broilers will stimulate its usage and can lead to increased foraging, thereby reducing inactivity. Offering different substrates in

10 ENRICHMENT FOR BROILERS A REVIEW 387 smaller local quantities can stimulate dustbathing and foraging in preferred substrates (moss-peat and oat husks). Scattering all of the broilers feed in the bedding, rather than offering it in feeders stimulates activity of fast-growing broilers, but as a consequence reduces body weight. Scattering of additional food items, such as whole wheat, in the bedding, has not been found to be effective, as it did not influence time budgets, mortality, or other welfare parameters. The limited knowledge on providing strings as foraging or pecking objects, shows that their use varied and their effect (if any) was limited. Novel Objects Increasing the complexity of the environment by enriching it is generally considered to reduce fear in domesticated poultry (Jones, 1996). Altan et al. (2013) added a variety of novel objects, including colored plastic balls, plastic bottles, toys, and mirrors, from d 0 to d 21 to experimental pens (50 broilers/pen) housing commercial broilers (genotype and number of objects not specified). All the objects were placed on the floor, except the mirrors, which were hung from the ceiling at chicks eye level. Every third day the objects were replaced to avoid adaptation and maintain novelty. No objects were added to the control pens. On d 22, the broilers were exposed to 3 acute stress treatments; sound-, heat-, or crating-stress. The authors found that broilers reared in the enriched environment were less fearful after exposure to the acute stressors compared to control birds, as shown by shorter durations of tonic immobility and lower amounts of basophils in the blood. No differences were found between enriched and control birds in body weight, feed conversion ratio, mortality, other leucocyte components, and heterophil: lymphocyte ratio. This study suggest that increasing the complexity of the environment by frequently adding novel objects increases the resistance of broilers to acute stressors. Summing Up on Point-Source Enrichments Table 3 summarizes the broilers use of the different point-source enrichments reviewed and its effects on the prevalence of different welfare and production indicators measured. The practical implications of providing the enrichment items as reviewed in this section will be discussed in the discussion. (B1) More Complex Enriched Environments with Outdoor Access The Use of Outdoor (Free Range) Areas An outdoor area (or free range) can provide broilers with access to an enriched environment that offers space and freedom of movement and also exposure to varying weather conditions and sensory inputs such as sounds and smells. In commercial broiler production, outdoor access (free range) is hardly ever provided, other than in organic broiler production systems and will then mostly be combined with slower growing genotypes (see e.g., Table 3. A summary of broilers use of the different kinds of point-source environmental enrichment reviewed in the present review and its effect on the prevalence of different welfare and production indicators measured. Fast and slow refer to growth rate. Type Genotype Use by the birds Effect on Keel bone damages Breast blisters Disturbances Growth Distribution in house Leg/foot problems Heat stress Fear Activity level Perches Fast Little Reduced Reduced No effect Reduced No effect Increased Slow Moderate Increased Increased Platforms Fast Moderate No effect Reduced Reduced Panels Fast Well used Reduced Improved Reduced Slow Improved Barriers Fast Moderate No effect 1 Reduced Unclear 2 Reduced No effect Bales of straw Fast Moderate Unclear 3 Reduced Foraging substrates (supplement) Fast Well used Unclear 3 Whole wheat (supplement) Fast No effect No effect spread in bedding All feed spread in bedding Fast Increased Reduced Suspended strings Fast Little Increased Reduced - Novel objects Fast Reduced 1 Except stimulation of perching; 2 Simple barriers increased susceptibility to the induction of TI compared to complex barriers or no barriers; 3 Some studies show an increased activity level, others do not.