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Feather pecking behaviour and associated welfare issues in laying hens

Article in Avian biology research · September 2008 DOI: 10.3184/175815508X363251

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The user has requested enhancement of the downloaded file. AVIAN BIOLOGY RESEARCH 1 (2), 2008 73–87 Feather pecking behaviour and associated welfare issues in laying hens

Laura Marie Dixona,b aDepartment of Animal and Poultry Science, University of Guelph, Ontario, Canada N1G 2W1 bPresent address: Department of Biological Sciences, University of Lincoln, Riseholme Park, Lincoln, LN2 2LG, UK E-mail address: [email protected]

ABSTRACT

Feather pecking, the pecking at or removal of feathers from one bird by another, is a problem in the poultry industry. Elimination of damaging feather pecking from flocks is made especially difficult by the numerous factors that appear to influence its prevalence. This review outlines the various contributors to feather pecking organised around Tinbergen’s four questions on causation, ontogeny, phylogeny and function. There is growing evidence that feather pecking (especially severe feather pecking) is related to foraging motivation and gut function. However, other factors, such as improper early experiences, strain and individual differences and perseveration of the behaviour help explain its continued occurrence, even if the birds are kept in enriched environments. To date, methods of dealing with feather pecking are inadequate and involve welfare concerns of their own and alternate solutions, such as provision of forages, are not usually successful in abolishing feather pecking behaviour. The problems of excessive pelage/plummage removal or redirected oral/foraging related behaviour are not unique to poultry and seem to occur in other species in which foraging and forage intake is important. Between species comparisons of related behaviour patterns may improve our understanding of feather pecking and help to design effective solutions. In order to solve the problem of feather pecking, the factors discussed in this review need to be accounted for or we risk applying ‘band-aid’ solutions, which may appear outwardly to be solving the problem. However, the underlying cause(s) may still be present and the animal’s welfare may still be compromised.

Keywords: feather pecking, causation, ontogeny, function, phylogeny, stereotypic behaviour, poultry welfare

1. INTRODUCTION also prevent the birds from performing behaviour patterns, such as foraging and dustbathing (Dawkins, Modern day chickens (Gallus domesticus) were origin- 1977; Baxter, 1994). If captive animals are motivated to ally domesticated from the Red Jungle fowl (Gallus perform natural behaviours patterns that are not gallus) over eight thousand years ago. Initially, they possible (see for example Hughes and Duncan, 1988; were used for religious sacrifice or cockfighting until Mason et al., 2001), this may both cause stress and lead around Roman times when they began to be developed to stereotypic behaviour, defined as ‘‘repetitive beha- for food production (Wood-Gush, 1971). The modern viour induced by frustration, repeated attempts to cope poultry industry began in the early nineteenth century, andyor C.N.S. (brain) dysfunction’’, regardless of the with most producers having small flocks of dual degree of variation or repetition (cf. Mason, 2006). purpose (egg and meat) birds raised extensively with Since approximately five billion laying hens are used access to outdoors and with hens brooding their young. for production worldwide each year (estimated from As technology advanced, this changed; leading to more FAOSTAT, 2008), the welfare of a large number of intensive systems with all birds being raised indoors individuals may be compromised. Many countries are and brooded artificially, the use of dual purpose birds starting to ban the use of conventional wire or ‘battery’ decreased and selection for two different types of birds cages. For example, Switzerland has banned egg (high egg or meat production) increased (Appleby et al., production in cages for many years, whilst the EU 1992). will require all wire cages to provide perches, nest In contrast to their free ranging ancestors, modern boxes and foraging material from 2012. However, the egg layers tend to be housed in small wire cages enriching or banning of cages does not eliminate all (battery cages) which increase ease of egg collection, welfare problems and hens in alternative husbandry decrease the incidence of certain diseases and allow for systems also experience several of these (Appleby and large numbers of birds to be fed economically and Hughes, 1991; Baxter, 1994; Duncan 2001; Appleby housed (CARC, 2003). However, these cage systems et al., 2004).

doi: 10.3184/175815508X363251 74 Laura Marie Dixon

A welfare problem that often occurs more frequently 2. WHAT AFFECTS THE FEATHER PECKING BEHAVIOUR in alternative husbandry systems is the stereotypic OF DOMESTIC FOWL? behaviour of feather pecking (Blokhuis, 1986, 1989), the pecking at and possible removal of feathers from Over 40 years ago, Tinbergen wrote an influential one bird by another (Hoffmeyer, 1969). Feather paper describing methods that could be used to inves- pecking can be divided into two distinct types, gentle tigate behaviour patterns by dividing the study of feather pecking and severe feather pecking. Gentle behaviour into four questions relating to causation, feather pecking involves the feathers being gently ontogeny, phylogeny and function (Tinbergen, 1963). pecked at or nibbled and can be sub-divided into These levels of explanation are still thought to be useful pecks to various feather targets that are thought to be today (e.g. Olsson and Keeling, 2005) and thus will be driven by exploration and repeated pecks to a single used to organise this review of factors affecting feather location on a feather (Newberry et al., 2007). By pecking behaviour. contrast, severe feather pecking involves the vigorous pecking at and possible removal of feathers (McAdie 2.1 Causation and Keeling, 2002). It is unclear if gentle and severe feather pecking stem from different motivational Causation refers to what produces the behaviour systems (Kjaer and Vestergaard, 1999). However, it is pattern, taking into account both internal and external severe feather pecking that constitutes the greater stimuli and the mechanisms by which these produce welfare concern (e.g. Blokhuis and Wiepkema, 1998), the behaviour (Tinbergen, 1963). The two main moti- and thus will be the main focus of this review. vational hypotheses behind feather pecking involve Since feather pecking has been associated with redirected dustbathing motivation or redirected fora- barren and stressful environments, its occurrence ging motivation due to lack of appropriate litter may be an indicator of reduced welfare (Green substrates. The term ‘motivational’ refers to what et al., 2000; Huber-Eicher and Sebo, 2001). causes an animal to perform a particular behaviour However, the primary welfare concern is that it can pattern and the amount of effort put into performing lead to cannibalism, which can be divided into two that behaviour (Toates, 1986; Mason et al., 2001). types: (1) cloacal cannibalism in which the vent area Dustbathing and foraging behaviour patterns would of the bird is pecked and which may lead to the normally (i.e. in free living birds) be directed to pecking out of abdominal organs; and (2) tissue substrates but instead may get redirected or transferred pecking in denuded areas where the exposed skin to an alternative stimulus (feathers of other birds) when is pecked, leading to haemorrhage (Savory, 1995). the animal’s response is inhibited or frustrated With both kinds of cannibalism, the damage can be (Dawkins, 1990). In this paper frustrated will refer to severe enough that the bird has to be euthanised. instances where the behaviour pattern is not possible or Hughes and Duncan (1972) did not find a correlation is being thwarted in some way (i.e. the bird is housed between cloacal cannibalism and feather pecking but with no substrate or can see but not access a substrate). severe feather pecking leading to blood on the Redirected will refer to instances where the behaviour feathers stimulates increased pecking of that area pattern is being directed to an inappropriate stimulus, and potentially leads to other types of cannibalism such as dustbathing or foraging behaviour being trans- (Allen and Perry, 1975; Cloutier et al., 2000). ferred to the feathers of other birds. This transference Feathers that have been damaged, but that are not can continue even if the original motivated behaviour bloody, also attract increased pecking (McAdie and is no longer frustrated (for example, the bird has access Keeling, 2000). to a substrate) due to habit formation or perseveration This review will describe the known factors that of the behaviour (see below). contribute to feather pecking behaviour organised Vestergaard (1994) proposed that feather pecking is around Tinbergen’s four questions on causation, onto- redirected dustbathing due to lack of appropriate geny, phylogeny and function (Tinbergen, 1963). There dustbathing substrates and lack of appropriate experi- are a variety of factors affecting feather pecking at each ence with these substrates early in life. In other words, of these levels: Some may be very specific to feather dustbathing behaviour that would normally be directed pecking; some probably have very general effects; to a substrate is transferred to the feathers of other birds some may affect the feather peckers; and some may (alternative stimulus) when there is no appropriate affect the recipients of the pecks. Here I will not attempt dustbathing substrate present and if chicks do not to disentangle these, but will simply present all the receive early exposure to dustbathing substrates (by factors that can influence this phenomenon. Next, the about day 10 of life), this may encourage the long- current methods of controlling severe feather pecking term mis-identification of feathers as appropriate will be reviewed, ending with a discussion of how the dustbathing substrates through habit formation or ‘four whys’ fit together to explain feather pecking perseveration (Vestergaard et al., 1990). Hens dust- behaviour. bathe for about ½ hour every other day (Vestergaard, Feather pecking behaviour and associated welfare issues in laying hens 75

1982). Dustbathing starts with the bird pecking, scratching priate foraging substrate is not present. Foraging is and bill-raking at the substrate. Next, the bird squats in the appetitive feeding behaviour, involving ground substrate and performs head rubbing, bill-raking, vertical pecking and scratching. Foraging generally leads to wing shaking and leg scratching interspersed by periods of feeding, which is the consummatory behaviour and side-lying or side-rubbing. A dustbathing bout generally involves ingestion of feed particles (Duncan, 1980). ends when the bird rises and vigorously shakes (Larsen Birds feed frequently throughout the day, at least once et al., 2000). Birds without access to litter will occa- per hour (Duncan et al., 1970) and given the space and sionally still go through the movements of dustbathing, opportunity will also spend a lot of time foraging. For suggesting that there may be a build up of internal example, when housed outdoors, junglefowl have been motivation (Vestergaard, 1982; Olsson and Keeling, observed to spend about 60% of their time ground 2005). pecking and 34% of their time ground scratching The provision of a dustbathing substrate does during the active part of the day (Dawkins, 1989). In decrease rates of feather pecking compared to that of early life, a number of different objects, both nutritious birds housed on wire flooring (Vestergaard et al., 1993; and non-nutritious are pecked and the chick quickly Johnsen and Vestergaard, 1996; Norgaard-Nielsen, learns to classify objects correctly (Hogan-Warburg and 1997). For example, birds housed on peat moss, a Hogan, 1981; Hogan, 1994). However, under commer- preferred dustbathing substrate (Petherick and cial conditions for laying hens, the consumption of Duncan, 1989) from weeks 1 to 4 of life, feather food is easily achieved without the need to forage, pecked less than those kept only on wire (Dixon and and there are generally no foraging substrates present. Duncan, in press). Early experience with a substrate Nevertheless, foraging behaviour may have its own may also be protective against feather pecking later in internal motivational factors which drive the bird to life, even if the substrate is no longer available (Johnsen perform the behaviour even when this is not necessary et al., 1998). Birds reared on sand and peat moss for food consumption (Hughes and Duncan, 1988). feather pecked less than birds reared on straw, and Feathers may thus be perceived as forages when no this continued even after all birds were switched to other substrates are present (Blokhuis, 1986; Huber- straw alone (Norgaard-Nielsen et al., 1993). Similarly, Eicher and Wechsler, 1997, 1998). Further support for provision of sand and straw during the first month of this hypothesis includes evidence of an inverse rela- life, compared to housing on wire, resulted in birds tionship between ground pecking and feather pecking, with improved plumage later in life when all birds had with birds housed on litter ground pecking more and been moved to straw only (Johnsen et al., 1998). Even feather pecking less than those housed on wire short term exposure to a substrate has been shown to (Blokhuis and Arkes, 1984; Huber-Eicher and have lasting effects against later feather pecking. For Wechsler, 1997). The quality of a forage, as measured example, exposure to wood shavings for a few hours a by the amount of pecking and scratching directed to it, day for 10 days was found to be protective against later also affects feather pecking since birds with higher feather pecking compared to birds never exposed to quality substrates (e.g. long cut straw) perform less wood shavings (Nicol et al., 2001). Further support for feather pecking than birds with lower quality substrates, this hypothesis includes the evidence that dustbathing e.g. shredded straw (Huber-Eicher and Wechlser, birds are often the targets of feather peckers 1998). Thus this hypothesis, too, has some empirical (Vestergaard et al., 1990) and even hens housed on support. litter have been pecked at while dustbathing; although Which hypothesis is correct? In addition, how can these pecks are thought to be mainly directed to both be supported by empirical evidence? The key particles on the plumage (Wennrich, 1974). Finally, problem with these two hypotheses is that the results chicks can be trained to dustbath on a skin with found for one could easily be substituted to fit the other. feathers and when offered a choice between sand Dustbathing and foraging both include pecking and and feathers as a dustbath, these chicks still chose the scratching at the ground, so observations of ‘‘ground feathers in over fifty percent of trials, demonstrating that pecking behaviour’’ could actually be the start of either long-lasting associations can be made between feathers activity (Savory, 1995). There is also an overlap and dustbathing behaviour (Vestergaard and Lisborg, between substrate classification as dustbaths or 1993). Thus there is some evidence consistent with the forages. For example, in one study designed to inves- dustbathing hypothesis. tigate feather pecking as redirected dustbathing, straw An alternate hypothesis states that feather pecking is and sand were used as the dustbathing substrates foraging behaviour directed at feathers when appro- (Johnsen et al., 1998). However, another study priate substrates are absent (Hoffmeyer, 1969; Hughes intending to look at feather pecking, also used straw, and Duncan, 1972; Blokhuis, 1986, 1989). In other but this time as a foraging substrate (Aerni et al., 2000). words, foraging behaviour that would normally be In cases like this it would be hard to tell if the pecking directed to substrates, gets transferred to the feathers directed at the straw was motivated by foraging or of other birds (alternative stimulus) when an appro- dustbathing. To solve this problem, the Fixed Action 76 Laura Marie Dixon

Patterns (FAPs) involved in foraging and dustbathing 2001; Dixon and Duncan, in press). Providing enrich- pecks, as well as drinking and novel object pecks can ment for the birds, such as string or novel objects, be compared to feather pecking pecks. FAPs are decreases feather pecking compared to controls but this unlearned (innate), repetitive movements in response may be due to providing the birds with more to occupy to external stimuli that are relatively unaffected by their time (Jones et al., 2002; McAdie et al., 2005; feedback, influenced by underlying motivation, and Dixon et al., in prep). Enrichment does not solve all are species-specific (Lorenz and Tinbergen, 1938). feather pecking problems because some levels of Previous work on pigeons has shown that the detailed feather pecking are still found when birds are housed morphology of pecks involved in drinking and feeding, with a substrate or moved to enriched environments or in working for food or water, involves motivationally (Nicol et al., 2001; van Hierden et al., 2002; Dixon, distinct FAPs (Jenkins and Moore, 1973). These techni- 2008). This may be due to perseveration of the beha- ques have been applied to the study of feather pecking viour (see below for discussion). and it was found that the motor patterns involved in There are a number of other internal and external severe feather pecks were similar to foraging pecks, but factors known to influence feather pecking behaviour, different from all other pecks including dustbathing. In such as the nutritional content of the feed and the feed addition, the action patterns involved in foraging and form (mash, crumble or pellet). There is more pecking dustbathing pecks were different, suggesting different damage to feathers when chickens are provided with underlying motivation for these behaviour patterns. pelleted feed compared to mash and even dilution of Overall, the results of this study indicate that severe the pelleted food with water does not affect feather feather pecking is more likely to be derived from pecking (Savory et al., 1999; El-Lethey et al., 2000). redirected foraging motivations, not dustbathing (cf. However, these higher levels of feather pecking appear Dixon et al., 2008). to be due to the shorter time required to eat pelleted As mentioned earlier, the main cause of feather food, even if the pellets have expanded in size from pecking is thought to stem from redirected motivation being soaked in water (Savory et al., 1999). Thus, the to either dustbath or forage due to lack of an appro- time available appears to influence the amount of priate substrate (Blokhuis, 1989; Vestergaard and feather pecking performed. Lisborg, 1993) and the inability to properly fulfil the Proper feather development requires certain nutri- motivation (either to forage or dustbathe) may lead to ents, such as the amino acids methionine and cysteine frustration. In birds whose feeding behaviour was (van Krimpen et al., 2005), without which the number frustrated by covering feed rewards the pecking of the of improperly developed or irregular looking feathers environment increased (Duncan and Wood-Gush, may increase, and these irregular or damaged feathers 1972). It has been proposed that frustration increased receive higher levels of feather pecking than normal arousal, aggression and fear and in these circumstances feathers (McAdie and Keeling, 2000; van Krimpen et al., occasional pecks to other birds’ feathers may develop 2005). Supplementing diets with protein, such as into damaging feather pecking (Lindberg and Nicol, casein, gelatin or soybean oil meal, or the amino 1994). However, when Rodenburg et al. (2005) acid, L-trypotophan decreases feather pecking levels induced frustration in High Feather Pecking and Low compared to when birds are fed a standard diet Feather Pecking birds (see more on HFPs and LFPs (Schaibnle et al., 1947; Savory et al., 1999). Since below) by training them to peck a key for a food reward feathers are made up of 89–97% protein it is possible (each test bird was housed and tested with a compa- that the levels of protein in a standard poultry diet may nion bird) then preventing physical but not visual not be sufficient to ensure that all feathers develop contact with the food by covering the food dish with properly and these irregular feathers may receive more clear Perspex, levels of feather pecking did not increase feather pecks. as a result. Although, this was short term frustration L-tryptophan has also been shown to reduce aggres- (three fifteen-minute test sessions for three days) and, as sion in males by causing sedative-like effects (Shea the birds were food deprived, may have been more et al., 1990) and this general reduction of activity related to hunger and motivation to feed, than to may be the cause of the decreased feather pecking frustration-related redirection of foraging, even though found. However, low levels of serotonin (which is foraging is an appetitive part of feeding, it has its own synthesised from tryptophan) have also been impli- motivational factors and satiated birds can still be cated in other behavioural disorders in humans and motivated to forage (Hughes and Duncan, 1988), or animals, such as depression and obsessive compulsive frustration-related redirection of dustbathing motiva- disorder, and supplementation with tryptophan, which tion. However, the type of flooring available, such as leads to increased levels of serotonin, has been shown wire or slatted floors compared to floors with a to improve these conditions (Sandyk, 1992; Weld et al., substrate, does affect feather pecking behaviour, with 1998). Chickens selected for high levels of feather birds housed on shavings consistently performing less pecking also have lower serotonin turnover than feather pecking than those housed on wire (Nicol et al., those selected for low levels of feather pecking (as Feather pecking behaviour and associated welfare issues in laying hens 77 discussed below). Thus, tryptophan and associated rates are higher in floor pens than cages (Tauson, serotonin turnover appear to be in some way associated 2005). This is thought to be due to the stable social with feather pecking behaviour. groups in cages and the larger group sizes housed in Fibre levels also affect feather pecking. When floor pens, as these larger groups increase the number chickens were fed high fibre diets (which had low of birds primary feather peckers have access to and the energy) they feather pecked less than controls but primary feather peckers can encourage more secondary they also spent more time at the feeder and consumed feather pecking, i.e. a small number of primary birds more feed. This suggested that the difference found first draw attention to the feathers of the victim bird and may have been due to a difference in activity distribu- this encourages other birds start pecking at the feathers tion, i.e. they spent more time eating so had less time as well (Hughes and Duncan, 1972; Savory et al., available to feather peck (Bearse et al., 1940; van 1999). Some studies have found a relationship Krimpen et al., 2005). The addition of roughages, between a bird’s ranking in the dominance order and such as clover or maize-silage, also decreased feather its tendency to feather peck others, with birds higher in pecking (and also mortality rates) but did not affect feed the dominance order more likely to feather peck birds efficiency (Steenfeldt et al., 2001). lower in the dominance order (Hughes and Duncan, Neuropeptides (short links of amino acids), like 1972; Vestergaard, et al., 1993). However, these dopamine and endogenous opioids, are thought to authors suggest that this is not a direct effect but play a role in self mutilating and stereotypic behaviour simply due to the fact that a more dominant bird is in birds (Goodman et al., 1983; Kjaer et al., 2004). One more likely to approach a subordinate bird than the possible explanation is that these neuropeptides are converse, and so is more likely to be in a position to associated with pleasure systems in the brain and feather peck. reinforce motivation for certain activities that stimulate Higher levels of feather pecking are also shown with these systems (Arias-Carrion and Poppel, 2007). For higher light intensities and decreased light has been example, chickens given a low dose of haloperidol (a recommended to control feather pecking outbreaks dopamine antagonist) decreased their feather pecking (Hughes and Duncan, 1972; Kjaer and Vestergaard, behaviour compared to that of birds injected with 1999). This increase in feather pecking is most likely saline (Kjaer et al., 2004), thus implicating involvement due to the increased visibility of particles on the of the dopaminergic system. plumage of other birds, thus increasing motivation to Hormones also influence feather pecking levels. peck, as dark feathered birds also receive more pecks There is an increase in feather pecking behaviour at compared to light feathered birds, most likely due to the start of lay and this is endocrine mediated: this the darker feathers having a greater colour contrast with increase can be stimulated by implanting gonadal the particles than light coloured feathers, increasing hormones in 12-week-old pullets (Hughes, 1973). particle visibility on the feathers (Savory and Mann, This research revealed that progesterone alone causes 1999). Or there may be non-motivational explanations, an increase in pecking, a combination of progesterone such as a general increase in activity. and oestrogen causes a greater increase, while Feather pecking also appears to have a diurnal oestrogen implantation alone has no effect. However, rhythm, at least in older birds: laying hens at 38 and the increase of damaging feather pecking can be 50 weeks of age showed increased levels of feather blocked with testosterone. Chickens kept in barren pecking in the later part of the daylight hours, that is 10 conditions (no substrate) feather pecked more and hours or more after lights on (Preston, 1987; Kjaer, also had an increase in their heterophilylymphocyte 2000). However, Bright (2007) found higher levels of ratio, an indicator of avian stress (for review of this severe feather pecking in the early part of the day in measure see Maxwell, 1993), than birds housed with a similarly aged birds. This difference may be due to the substrate (El-Lethey et al., 2000). Corticosterone division of feather pecks into gentle and severe pecks in supplementation in the feed also increases feather Bright’s study while Preston (1987) and Kjaer (2000) pecking levels of birds housed on litter compared to lumped both types of feather pecking together. Thus, it similarly housed control birds (El-Lethey et al., 2001). It is possible that the increase in feather pecking found in is not clear if there is a causal relationship between later parts of the day may be due to higher levels of stress and feather pecking or if they both occur in the gentle feather pecks. barren commercial environments chickens are housed A final causal explanation of feather pecking may be in. due to perseveration of the behaviour. Perseveration Social factors also affect feather pecking behaviour. refers to the continuation, or re-occurrence, of an Feather pecking is present in both floor pens and activity without the appropriate stimulus present to battery cages, and whilst some early studies, such as release the behaviour (Sandson and Albert, 1984). that of Hughes and Duncan (1972), found the Perseveration can be induced by stress, such as frequency of feather pecking to be higher in cages barren and predictable captive environments (Francis compared to pens, more commonly feather pecking et al., 1995; Lewis et al., 2006), andyor by lasting CNS 78 Laura Marie Dixon changes caused by for example rearing without moti- (1972) suggested that there was social transmission of vationally significant stimuli, such as seen with rearing severe feather pecking among groups of birds, as this infant primates without their mothers (Novak and type of feather pecking appeared to begin with a few Harlow, 1975). In cases like this, frustration may there- birds being primary feather peckers and eventually the fore lead to the stereotypic behaviour indirectly, by behaviour spread to other birds (secondary feather mediating changes in the brain that alter how beha- peckers). Zeltner et al. (2000) who introduced chicks viour is controlled, thence causing animals to be more showing either high levels or low levels of feather generally prone to abnormal repetition. An animal pecking to groups of chicks that were performing only whose stereotypic behaviour is perseverative may be low levels of feather pecking behaviour. Groups in abnormally persistent in other aspects of its behaviour which the high feather pecking chicks were added as well (Sandson and Albert, 1984; Garner, 2006; increased their levels of feather pecking while groups Mason, 2006). Thus, stereotypic behaviour patterns of chicks that had birds showing low levels of feather like feather pecking may not stem from normal beha- pecking did not. However, when a later study differ- viour but instead from changes that make the animal entiated between severe and gentle feather pecks, only abnormally persistent in all types of behaviour (cf. gentle feather pecking, which does not cause feather Garner, 2006). damage, seemed to be socially transmitted (McAdie and Keeling, 2002). 2.2 Ontogeny As with most populations of captive animals, there are animals that perform stereotypic behaviour patterns Ontogeny refers to the development of a behaviour and there are those that do not, even when reared and pattern in an individual through integration of learned housed in the same conditions (Mason, 2006). While and innate aspects of the behaviour (Tinbergen, 1963). work has been done to identify factors that predispose a ‘Feather’ pecking (i.e. down pecking) can be found in bird to become a feather pecking victim, such as chicks from day one of life (e.g. Savory and Mann, plumage colour (Keeling et al., 2004), it has not been 1999; Chow and Hogan, 2005; Dixon and Duncan, in determined if these are the birds who do not perform press), with most pecks initially being gentle rather than feather pecking. Not all birds develop damaging feather severe; however, the incidence of severe feather pecks pecking behaviour. In a survey of 64 flocks, 40% of increases as the birds age (Newberry et al., 2007). As those raised in aviaries and 35.9% of those raised in mentioned previously, there is a marked peak in feather deep litter systems developed severe feather pecking pecking at the onset of lay, around 18 to 24 weeks of (Huber-Eicher and Audige, 1999). Thus, research life that appears to be due to increased hormone levels examining differences between flocks that do, and do and perhaps in nest-building motivation; in natural not, develop severe feather pecking, as well as indi- situations, forages would be used as nesting material viduals who do, and do not, develop this behaviour as well (Hughes, 1973). could lend insight into other factors that influence the The development of feather pecking may also be development of feather pecking. influenced by early experience with or without a substrate for foraging or dustbathing as discussed 2.3 Function above. The perception of a substrate as appropriate for feeding or dustbathing occurs during trial-and-error Function refers to the survival value of a behaviour pecking of nutritious and non-nutritious objects during pattern or the way it enhances fitness, either in a the first few days of life (Hogan-Warburg and Hogan, proximate (short-term) or ultimate (long-term) manner 1981). Jensen et al. (2006) found that providing dark (Tinbergen, 1963). The true function of feather pecking brooding areas where chicks can rest, results in long- is still unknown; and if the behaviour is in fact term reductions of feather pecking behaviour pathological, it may have no true function. compared to when the chicks were given traditional Alternatively, it has been suggested that feather heat lamps. The likely mechanism for this reduction in pecking may be a type of coping mechanism that feather pecking is simply by decreasing the availability allows chickens to manage with a less than ideal of inactive chicks which are preferred to active chicks environment, that is a response to help reduce aversion as targets for pecking. Chicks reared by a broody hen or stress in undesirable conditions (Cooper and Nicol, show more ground pecking and less feather pecking 1993; Korte et al., 1997; Rodenburg et al. 2004). It is than non-brooded chicks. It is thought that the hen thought that the benefits associated with performing encourages the chicks to explore the environment and coping behaviour may reinforce the behaviour pattern, direct more pecks at the ground (Riber et al., 2007). potentially leading to the performance of stereotypic Laying hens can modify their own behaviour when behaviour patterns (Wu¨rbel et al., 2006). watching the behaviour of others (Nicol, 1995) and this There are two general types of coping or responding could cause an increase in the levels of feather pecking strategies: (1) Proactive responding involves the animal development. For example, Hughes and Duncan actively trying to deal with the situation, for example, Feather pecking behaviour and associated welfare issues in laying hens 79 trying to escape; and (2) Reactive responding involves decreases levels of feather pecking or if the flooring suppression of environmentally directed activities, for substrate most successful at decreasing feather pecking example, the animal may remain immobile for long is also consumed the most, although these are both periods (Bolles, 1970; Koolhaas et al., 1999). It is logical predictions. It is known that birds given free- thought that birds performing high levels of feather choice with a variety of feedyforage types adjust pecking (both gentle and severe pecking) have a consumption levels to obtain sufficient dietary compo- proactive responding strategy while those performing nents, such as insoluble fibres; however, this is not low levels of feather pecking have a reactive commonly practised in production systems (e.g. responding strategy (Korte et al., 1997). Proactive Emmans, 1979; Hetland et al., 2003). responders may also be more intrinsically driven Thus, it is possible that the function of severe feather (need less input from the environmental stimuli) and pecking, where feathers are removed and consumed, is with repeated experience they tend to develop routines to improve gut function by increasing dietary insoluble and rigid behaviour patterns, as opposed to reactive fibres, while the function of gentle feather pecking, responders, who react more strongly to environmental where feathers are nibbled, may be related to other stimuli and are more flexible in their behaviour patterns behaviour patterns, such as preening (van Hierden (Rodenburg et al., 2004). There is some evidence that et al., 2002) or social exploration (Riedstra and proactive responders may be more vulnerable to devel- Groothuis, 2002). However, provision of fibrous oping stereotypic behaviour patterns than reactive substrates does not eliminate feather pecking entirely. responders (Koolhaus et al., 1999). For example, the Thus, it is also possible that feather pecking has greater levels of gentle and severe feather pecking become emancipated from its original function – the found in High Feather Pecking lines (proactive respon- factors that influenced the behaviour during develop- ders) compared to Low Feather Pecking lines (reactive ment are different than the factors that affect the fully responders) that forage and dustbath more (Johnsen and established behaviour (Odberg, 1978; Dantzer, 1986). Vestergaard, 1996; van Hierden et al., 2002). In addi- Thus, feather pecking may have become perseverative tion, high feather pecking chicks had stronger immune in birds that continue with this behaviour even if their responses when challenged (Buitenhuis et al., 2006), conditions improve. lower plasma corticosterone levels, and lower dopa- mine and serotonin turnover levels in the forebrain than 2.4 Phylogeny low feather pecking chicks (van Hierden et al., 2002), and these characteristics have been shown to be Phylogeny refers to the evolutionary development of a associated with proactive responding strategies in behaviour pattern and thus focuses mainly on genetics rodents and pigs (e.g. deBoer et al., 1990). However, and species comparisons (Tinbergen, 1963). Feather the above results only indicate a possible correlation, pecking has a heritable component with heritability not a causal relationship between copingyresponding estimates (h2) ranging from 0.14 to 0.56 (Cuthbertson, style and feather pecking. 1980; Kjaer and Sorensen, 1997; Rodenburg et al., Feather pecking involves ingestion and so another 2003). In addition, different strains of birds have possible function of feather pecking involves improving different levels of feather pecking (Hughes and gut function and digestion. Insoluble fibres stimulate Duncan, 1972) and within one strain of birds, High the gizzard and are beneficial to nutrient digestion and Low Feather Pecking lines (HFP and LFP) have (Hetland et al., 2003). Commercial chicken feed gener- been selected for and developed, i.e. there are indi- ally does not contain much insoluble fibre, even vidual differences in feather pecking levels (Kjaer et al., though insoluble fibre may be necessary to maintain 2001), and these strain and individual differences may normal gizzard function (Hetland et al., 2005). Chicken contribute to the high variability found in the herit- feathers are considered non-nutritive (McCasland and ability estimates. In lines selected for different levels of Richardson, 1966) but are often consumed by feather feather pecking, the amount of both gentle and severe peckers after being pecked from the victim bird feather pecking was higher in the high feather pecking (McKeegan and Savory, 1999) or if provided in a line (van Hierden et al., 2002) while Low Feather bowl to feather pecking birds (Harlander-Matauschek Pecking lines performed more dustbathing (Johnsen et al., 2007). Feather consumption has been shown to and Vestergaard, 1996), foraging and feeding (van increase the speed of feed passage in a manner similar Hierden et al., 2002), indicating a potential inverse to insoluble fibres (Harlander-Matauschek et al., relationship between feather pecking and ground 2006b). Feather pecking chickens will also work to pecking activities. HFP and LFP also react differently obtain feathers they can consume by pecking a key an to frustration. As mentioned above, birds have been increasing number of times, demonstrating that they are operantly trained to peck a key for a food reward but motivated to access and eat the feathers (Harlander- access to the reward can be frustrated by covering of Matauschek et al., 2006a). It is not yet known if the food dish. During this frustration, LFPs pecked more providing birds with feathers for consumption at the environment (especially at the covered food 80 Laura Marie Dixon dish), which was thought to indicate higher frustration can be reduced in captivity by the provision of more (Rodenburg et al., 2002) while HFPs performed more naturalistic food with a higher fibre content and gentle feather pecking and aggressive pecking to their increased volume (Bergeron et al., 2006). In addition, housing companion and more ground scratching the performance of these behaviours are thought to (Rodenburg et al., 2005). Research in molecular either improve gut function by, for example, increasing genetics has also identified possible Quantitative Trait nutrient digestion or saliva production (McGreevy and Loci (QTLs), allele variations associated with pheno- Nicol, 1998) andyor attempting to satisfy natural fora- typic variations, involved in gentle feather pecking on ging (Bashaw et al., 2001). There are also genetic DNA micro-satellite markers GGA1 and GGA2 and a components involved in these redirected behaviours. QTL for severe feather pecking on GGA2 (Buitenhuis For example, female chinchillas are prone to higher et al., 2003). Birds whose plumage colour is due to levels of fur-chewing than males (Ponzio et al., 2007) melanisation controlled by the wild recessive allele and Garner et al. (2006) found that different families of PMEL17 may be genetically predisposed to become parrots performed different levels of feather picking, victims of feather pecking (Keeling et al., 2004). suggesting there might be a genetic component to this Feather pecking is also found in other types of avian particular behaviour. Stress has been implicated in the species, such as broiler chickens (e.g. Kristensen et al., performance of other stereotypic behaviours, with 2007), turkeys (e.g. Sherwin et al., 1999), ducks (e.g. animals that are more stressed (e.g. close to a noisy, Gustafson et al., 2007), pheasants (e.g. Hoffmeyer, high traffic area versus a more quiet, less travelled area) 1969), ostriches (Deeming and Bubier, 1999), and performing higher levels of stereotypic behaviour parrots (e.g. Meehan et al., 2003). The factors contri- (Garner et al., 2006) with anti-depressants and sero- buting to feather pecking have been most extensively tonin reuptake inhibitors recommended for treatment studied in laying hens (approximately 235 hits in a Web (Seibert, 2007). of Science search for feather pecking and laying hen Thus, motivation to forage andyor to ingest high versus less than 100 hits for feather pecking in all other levels of fibre are a potential cause of stereotypic types of birds). Feather removal in these other types of behaviour found in other taxa – making the hypothesis birds appears analogous to feather pecking in laying that chickens feather peck as re-directed foraging to hens due to behavioural similarities between these increase fibre intake and improve gut function species (e.g. they all forage, preen, etc.) and the (Harlander-Matuaschek et al., 2006a, 2007) particu- performance of feather pecking occurring primarily in larly plausible. Further studies into this type of stereo- barren captive conditions with the provision of forages typic behaviour could also increase our understanding or other types of enrichment reducing this pecking of feather pecking and review of multi-species literature (Martrenchar et al., 2001; Meehan et al., 2003; when examining behavioural problems should be Gustafson et al., 2007). In addition, similar stereotypic encouraged. pelage removal has also been reported in non-avian species, such as chimpanzees (Smith et al., 2004), mice 3. CURRENT SOLUTIONS TO FEATHER PECKING (Garner et al., 2004), rabbits (Jackson, 1991), sheep (Marsden and Wood-Gush, 1986), cats and dogs Current commercial solutions to feather pecking are to (Sawyer et al., 1999) and even humans (Schlosser beak trim the birds andyor to keep them in small, et al., 1994). Research into these different types of confined groups, for example in conventional battery integument removal may lend further insight into the cages. These practices, however, do not actually causation, development, function and phylogeny of succeed in stopping feather pecking per se, but do stereotypic feather pecking behaviour in poultry. decrease the measurable damage and involve welfare Oral, foraging-related stereotypic behaviour patterns problems of their own. Instead we should advocate are also found in captive herbivores – even though they ethologically-based methods that solve the problems do not all involve pelageyplummage ingestion. Similar underlying feather pecking and thus improve bird to chickens, these species also normally have high fibre welfare. diets that may not be satisfied by concentrate feeding in Beak trimming or debeaking is the removal of captivity and this could lead to redirection of foraging approximately the last third of the upper and lower and feeding behaviour. Thus, feather pecking may be beak. This can be done using a heated blade that cuts similar to many other types of redirected oral behaviour through and cauterises the beak or with electronic beak found in ungulates with similar foraging requirements, trimmer which uses a high voltage electrical current to some of which involve ingestion such as wood- burn a small hole in the upper beak (Gentle et al., chewing in horses and slat-chewing in sheep, and 1990). The cells in the beak tip die and slough off after some which do not, such as tongue rolling in cattle three to seven days (Cunningham et al., 1992). A more and crib biting in horses. Like feather pecking, the main recently developed method is the use of an infrared hypotheses for the motivation behind these behaviour beam directed at the tip of the beak, which damages patterns are that they derive from natural foraging and the underlying tissue, causing the tip to fall off in about Feather pecking behaviour and associated welfare issues in laying hens 81 two weeks (Gentle and McKeegan, 2007). Beak trim- conditions with little effect of additional enrichment ming does not stop the action of feather pecking but (e.g. Garner, 2006). since the hooked end of the beak is removed, the Battery cages in general are coming under criticism amount of feather damage from pecking is reduced and there is an increased demand for eggs that are not (Blokhuis and van der Haar, 1989). Since studies produced in them (Huber-Eicher and Sebo, 2001). involving feather pecking tend to use non-beak Other welfare problems associated with battery cages trimmed birds, it is difficult to say if the levels of include lack of space (Nicol, 1987), dustbaths, and feather pecking are even decreased. However, perches (Duncan, 2001). Also, the reduced space does chickens that were beak trimmed pecked less at a not allow for much movement, which can contribute to bunch of feathers than non-beak trimmed chickens, bone weakness (Leeson and Morrison, 1978). Thus, it indicating that rates of feather pecking may decrease seems clear that alternative husbandry systems or the after beak trimming (Martinec et al., 2002). In addition, addition of enrichment to conventional cages are beak trimming has many negative side effects. needed to improve the problem of feather pecking. Extensive neuromas, swelling of the nerve, may form on the stump of the beak (Breward and Gentle, 1985) 4. ‘FOUR WHYS’: HOW DO THEY FIT TOGETHER? and acute and chronic pain have been associated with beak trimming (Duncan et al., 1989; Gentle et al., Based on the above review, it is clear that feather 1990). Feed intakes falls temporarily after hot blade pecking is a complex problem, whose underlying beak trimming (Gentle et al., 1982), and there is a motivation is still uncertain. However, there is evidence reduction in use of the beak for manipulatory beha- that feather pecking (especially severe feather pecking) viour, such as preening and exploration (Duncan et al., may be related to foraging behaviour and gut func- 1989). Also, after trimming, the beak continues to grow tioning, while the motivation behind gentle feather and may get to a length where another trim is required, pecking is less clear and may relate to other behaviour when the bird is older and the beak is larger (Gentle patterns not often focused on in feather pecking studies, and McKeegan, 2007). such as motivation to preen or allo-groom. In addition Battery cages, cages made primarily of wire-mesh to the causal basis of feather pecking, other factors also and including a feeder and drinker, and originally influence its prevalence. Improper early experiences, designed for single hens were implemented to sepa- such as having no substrate to peck at, and no hen to rate hens from their faeces. Today anywhere from 5 encourage ground pecking, may exacerbate the (CEMA, 2008) to as many as 60 (BEIS, 2008) birds per problem and in some instances perseveration of the cage are more common. They also have the advan- behaviour may occur. If this happens, the behaviour tage of allowing larger numbers of birds to be kept in may persist, even if the bird is moved to enriched, more a building (CARC, 2003) and decreasing the incidence natural conditions. Feather pecking also has a genetic of cannibalism (Huber-Eicher and Sebo, 2001). Access component and it is possible that there has been some to a limited number of other hens and the restricted indirect selection for it, either because it is linked to a movement available in cages may decrease the production trait or because birds with very good feather amount of damaging feather pecking behaviour (espe- cover (and therefore with a higher risk of performing cially since these birds also tend to be beak trimmed) the pecking rather than being the pecked birds) have when compared to floor or pen housed birds which been selected for breeding. If feather pecking is a are kept in larger numbers with more space available coping mechanisms to help deal with continually for movement and targeting of birds with damaged stressful environments, then birds performing this beha- feathers (Hughes and Gentle, 1995). Keeping birds in viour (proactive copersyresponders – actively deal with smaller groups also reduces the risk of social transmis- problems) may have better welfare than those that do sion from primary peckers to secondary peckers not (reactive copersyresponders – are in ‘depression’- (Hughes and Duncan, 1972). However, birds are still like state). Thus, proactive individuals may be trying to able to feather peck in battery cages, and in some satisfy foraging motivation or gut abnormalities through cases at higher rates than in other systems such as feather pecking while reactive individuals are doing enriched cages (Appleby et al., 2002), which may be nothing to alleviate the problems and, thus, may related to the lack of substrate. Hens in alternative potentially also be a welfare concern. However, experi- systems can also perform a larger number of beha- mental evidence is still needed to prove or disprove viour patterns than those in cages, including foraging these claims. and nesting, which in addition to potentially satisfying To date, our methods of dealing with feather pecking motivations, may give the birds more to do, leaving are inadequate – feather pecking is still found in battery less time available for feather pecking (Appleby et al., cages and beak trimming does not seem to prevent 1992). However, there is also the possibility that feather pecking, although it does decrease damage feather pecking may become perseverative, thus high from feather removal. It is possible that beak trimmed rates of feather pecking may still be found in extensive birds continue to feather peck with little or no feedback 82 Laura Marie Dixon from feather ingestion because of habit-formation or kept in free range situations, rarely experience natural perseveration of this behaviour (appropriate stimuli are early social conditions, that is, being brooded by a hen, no longer necessary). It is also possible that the act of and together with their siblings, learning about the feather pecking itself is reinforcing – foraging behaviour environment from her, this may help explain reports is thought to have its own internal motivational factors of feather pecking in more enriched conditions (Mason, which drive the bird to perform the behaviour even 2006; Riber et al., 2007). when this is not necessary for food consumption Another reason for the inability to abolish feather (Hughes and Duncan, 1988), and feather pecking pecking which is commonly found in past research may behave similarly. In addition, there are chickens may be due to differences in genetics. Feather pecking given the opportunity to fulfil foraging motivation, by has a genetic component (Cuthbertson, 1980) and housing them on litter (usually wood shavings) or even different strains of chickens have been shown to with access to outdoor runs, that still feather peck. perform different levels of feather pecking (Hughes Furthermore, the average amount of feather pecking and Duncan, 1972). There have not been behavioural can be decreased by the provision of other enrichments profiles done comparing these strains in terms of (e.g. string to peck, novel objects), at least in some birds general activity levels. If some strains of birds tend (McAdie et al., 2005; Dixon et al., in prep), but again to forage more than others, they may have a higher feather pecking is not abolished. There are a few motivation to forage and when this gets frustrated, possible reasons for this. they may feather peck more than birds with lower It is possible that the enrichment provided doesn’t foraging motivation. Alternatively, if some birds spend completely satisfy the motivation (i.e. the enrichment is more time foraging than others, this may take up more an inadequate substitute), thus frustration continues as of their time, leaving less time available to feather does performance of the stereotypic behaviour peck. There may also be genetic or even individual (Swaisgood and Shepherd, 2006). Another possibility differences in what constitutes a ‘good quality’ forage, is that the feather pecking shown in these housing i.e. differences in individual perception. Thus, conditions may be gentle in nature and possibly part substrates that satisfy foraging motivation in some of a normal allo-preening behaviour. Not all trials have strains, or in some individuals, may not be as satis- distinguished between gentle and severe feather pecks fying for others. There is fairly clear evidence that the (Kjaer, 2000) and thus reports of feather pecking on provision of some type of foraging enrichment litter-housed or free rangeyfree run birds may be a decreases feather pecking behaviour (Huber-Eicher product of this. It has also been shown that the and Wechsler, 1997; Chow and Hogan, 2005; quality of a substrate, determined by the amount of Dixon et al., in prep), but the decrease may vary pecking and scratching directed to it, affects the between strains. These genetic differences may also amount of feather pecking shown. Higher quality help explain the conflicting results on the effects of substrates, substrates that have an increased amount early experience on later feather pecking. Some strains of time spent with them (more pecking and scratching) of birds may benefit from proper early substrate compared to a lower quality substrate, also have less experience andyor being brooded by the mother feather pecking associated with them (Huber-Eicher hens and this may have lasting effects in some and Wechsler, 1998). It is possible that the birds that strains, while in others it may not. Moreover, what have been observed feather pecking while housed on constitutes as ‘proper early experience’ may differ substrates were kept with a low quality variety, and between strains or even individuals. thus foraging motivation may not be satisfied. Based on the many known differences between Finally it is possible that as the birds age, feather different strains of birds, or even the differences pecking becomes perseverative, or habit-like, and between individuals in one strain, it is possible that continues even if the appropriate stimulus is provided some birds may feather peck primarily due to frustrated to release the behaviour (e.g. foraging motivation) or if foraging motivation while others may feather peck the birds are housed in near-to-nature conditions, such primarily due to chronic stress and potential changes as free range (e.g. Swaisgood and Shepherd, 2006). in CNS function. Birds showing high levels of feather Commercial poultry housing can be quite stressful for pecking have lower serotonin turnover than those the birds and aside from foraging, a number of ‘natural’ selected for low levels of feather pecking (van behaviour patterns, such as nesting, often cannot be Hierden et al., 2005). Low levels of serotonin turnover performed (Duncan, 2001). This chronic stress may have also been implicated in other behavioural disor- lead to a pathological condition or even a change in ders (in humans and animals), such as depression and the brain of the birds (Garner, 2005), whereby feather obsessive compulsive disorder, and supplementation pecking cannot be controlled through fulfilment of its with tryptophan (which leads to increased levels of original motivation. The degree of perseveration shown serotonin) has been shown to improve these conditions can be affected by a number of factors, such as stress (Sandyk, 1992). Thus, there appears to be changes in and early social environment. As chickens, even those brain function between these birds. Feather pecking behaviour and associated welfare issues in laying hens 83

Future applied work should aim to address the when implementing any enrichment program because questions raised above. Multi-factorial experiments while they appear outwardly to be solving the problem can be designed that use different strains of birds on (decreasing stereotypic behaviour), the underlying an individual basis to investigate: (i) the effects of early cause may still be present and thus, the animal’s experience with and without a certain substrate; (ii) the welfare may still be compromised. effects of being brooded and reared by the mother hen on later feather pecking levels; (iii) later housing condi- ACKNOWLEDGEMENTS tions with or without the substrate (does substrate influence feather pecking if given later in life); and Thanks to Georgia Mason, Ian Duncan, Suzanne (iv) the types of substrates that reduce feather pecking Millman, Ruth Newberry, Tina Widowski and an the most. Answering these questions will help deter- anonymous reviewer for their helpful comments on mine if designing an effective, practical forage will previous drafts of this manuscript. need to be done on a strain basis or if certain early experiences need to be ensured to decrease the risk of perseveration of the behaviour. These forages could be as simple as scattered feed on the ground in floor REFERENCES systems to increase opportunities to forage or in cage Aerni, V., El-Lethey, H. and Wechsler, B. (2000) Effect of foraging systems, ‘hay bags’, like those used for horses, can be material and food form on feather pecking in laying hens. Brit. hung along the sides of the cages and filled with high Poult. Sci., 41, 22–28. fibre forages, which again increase foraging opportu- Allen, J. and Perry, G.C. (1975) Feather pecking and cannibalism nities while also potentially improving gut function due in a caged layer flock. Brit. Poult. Sci., 16, 441–451. to increased fibre intake. 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