Review of rearing-related factors affecting the welfare of laying hens

Andrew M. Janczak,1 and Anja B. Riber

Animal Welfare Research Group, Department of Production Animal Clinical Sciences, Faculty of Veterinary
Medicine and Biosciences, Norwegian University of Life Sciences (NMBU), Oslo, Norway; and Department of
Animal Science, Aarhus University, Tjele, Denmark

Key words: laying hen, rearing conditions, animal welfare, behavior

2015 Poultry Science 00:116
http://dx.doi.org/10.3382/ps/pev123
also becoming increasingly clear that research exploring
and quantifying animals health and needs (Dawkins,
2008), combined with the ethical justification for various practices (Duncan and Fraser, 1997), can provide
an educated basis for decisions regarding how we treat
the animals in our care.
A large proportion of welfare problems in laying
hens are influenced by the method by which pullets
are reared from hatch until they are 15 to 18 weeks
of age, after which they are moved from the rearing
system to the laying system. Some problems may increase over time, mainly affecting welfare during the
laying period, although a few problems are unique to
the rearing period. It is well documented that early
experience has long-term effects on the development
of behavior, including unwanted abnormal behavior.
Layer chicks start pecking and learning about appropriate food and pecking substrates during the first 24
h of life, as well as imprinting on conspecifics and developing fear-related avoidance of people and unfamiliar objects (Hess, 1959, 1964; Phillips and Siegel, 1966;

INTRODUCTION
Consumers increasingly demand poultry products
that are produced using high welfare standards. The
2012 ban on the use of conventional cages to house laying hens in the European Union, and the 2015 ban in
California on selling eggs produced by hens in conventional cages, illustrate this trend. Ethical arguments
based on a synthesis of utilitarianism, animal rights,
and agent-centered views are increasingly accepted and
support the view that animals should be protected from
unnecessary suffering (Sande and Crisp, 1997). It is

C The Author 2015. Published by Oxford University Press on

behalf of Poultry Science Association. This is an Open Access article distributed under the terms of the Creative Commons Attribution
License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium,
provided the original work is properly cited. For commercial re-use,
please contact [email protected].
Received January 16, 2015.
Accepted March 28, 2015.
1
Corresponding author: [email protected]

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of gasses, age at transfer from rearing to production

facilities, similarity between rearing and production facilities, competence of staff, and interactions between
bird strain and environment. The present review aims
to summarize rearing-related risk factors of poor welfare in adult laying hens housed according to European
Union legislation. It aims to identify gaps in current
knowledge, and suggests strategies for improving bird
welfare by improving rearing conditions. Two main conclusions of this work are that attempts should be made
to use appropriate genetic material and that beak trimming should be limited where possible. In addition to
this, the rearing system should provide constant access
to appropriate substrates, perches, and mashed feed,
and should be as similar as possible to the housing system used for the adult birds. Finally, young birds (pullets) should be moved to the production facilities before
16 weeks of age. The measures outlined in this review
may be useful for improving the welfare of pullets and
adult laying hens.

ABSTRACT Laying hens may face a number of welfare problems including: acute and chronic pain caused
by beak trimming; exaggerated fearfulness that may
cause stress and suffocation; difficulties in locating resources, resulting potentially in emaciation and dehydration; frustration and boredom, caused by an environment that is barren; feather pecking; cannibalism;
foot lesions; and bone fractures. In Europe, a greater
proportion of laying hens are housed in non-cage systems compared to the rest of the world. The extent
of the different welfare problems may therefore vary
between countries as the type of housing system influences the risk of suffering. More generally, many of these
welfare problems are influenced by the rearing environment of the pullets. This article therefore focuses on
welfare problems in laying hens that can be traced back
to rearing. Factors that have been studied in relation
to their effects on bird welfare include beak trimming,
housing type, furnishing, enrichment, feeding, stocking
density, flock size, sound and light levels, concentration

JANCZAK AND RIBER

the interactions between breed and environment. We

aim to make recommendations for better rearing of pullets, but also to identify those topics that are not well
understood, including a number of factors involved in
rearing pullets for non-cage production systems.

BEAK TRIMMING
Legislation and Challenges connected with
Beak Trimming
According to European legislation, beak trimming
is permitted prior to 10 days of age (CEC, 1999:
1999/74/EC). In certain European countries, such as
Norway and Sweden, beak trimming is prohibited by
national legislation, and in Denmark the egg industry has decided to cease beak trimming. Beak trimming is performed primarily to reduce the incidence of
feather pecking and associated cannibalism. Comparison of beak-trimmed and non-beak-trimmed birds in
conventional cages and furnished cages suggests that
beak trimming reduces mortality from 40 to 51% to 4
to 8% (Guesdon et al., 2006). It has also been suggested
that beak trimming improves feather condition (Lee
and Craig, 1991; Staack et al., 2007; Lambton et al.,
2013), although one study found minimal feather pecking in both beak-trimmed and non-beak-trimmed birds
(Sandilands and Savory, 2002a). Furthermore, a recent
on-farm study found intact beaks to be a risk factor for
severe feather-pecking during the rearing period, but
not during the laying period (Gilani et al., 2013).
As a result of continual genetic selection, the genotypes used in todays egg production are likely to differ significantly from those used previously. Modern
layer strains are potentially less susceptible to feather
pecking and cannibalism, emphasizing the need for new
studies investigating the efficacy of, and necessity for,
beak trimming. Indeed, there are examples such as
Norway, a country in which beak trimming is prohibited, which has a laying hen mortality as low as
2.26% in furnished cages and 3.69% in aviary systems
(Hestetun, 2014). Stakeholders in other countries claim
that feather damage in intact hens is still at unacceptable levels, but recent data to support this claim are
lacking. Flock sizes in Norway are normally limited to
7,500 birds, whereas in countries such as The Netherlands a single producer may have three flocks of 30,000
birds each. Future studies are therefore called for in order to tease apart the effects of flock size, hybrid, management, housing, and rearing, on feather pecking in
laying hens that are non-beak-trimmed. Without these
studies, claims regarding the necessity of beak trimming
seem poorly substantiated.
The beak contains thermoreceptors, nociceptors, and
mechanoreceptors (Gentle, 1989). Partial amputation
of the beak therefore results in pain, sensory loss, and
a reduction in the birds ability to manipulate objects
(Gentle, 1986a). The beak is an important tool used
by the bird in many activities including grasping food

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Dawkins, 1968). Perch use starts during the first few

days of life (Workman and Andrew, 1989; Riber et al.,
2007a). This underpins the importance of the early
rearing environment for the birds adaptation to the
production environment which can affect appropriate
foraging and pecking behavior, sensitivity to potential
stressors, and ability the to navigate in a given production environment.
Development of welfare problems during rearing may
be predictive of welfare problems during lay. For example, the plumage condition during lay is better when
feather pecking had not started during rearing (Gilani
et al., 2013; de Haas et al., 2014a). This is further supported by the observation that increased feather damage at 17 to 20 weeks of age is later associated with
earlier onset of severe feather damage during lay (Drake
et al., 2010). Seventy-one percent of rearing flocks with
no feather damage continued without feather pecking
problems during the laying period; whereas the risk of
continued problems with feather pecking during lay is
90% for flocks in which feather pecking was recorded
during rearing (Bestman et al., 2009).
Certain welfare problems such as beak trimming of
one-day-old chicks, which causes acute pain (Gentle,
1986a), are unique to pullets, but most welfare challenges are interlinked and may impact birds both during
the rearing and production phases. The rearing system
may directly affect the welfare of the adult birds if the
transition from the rearing system to the layer system
induces fear, stress, emaciation, and dehydration. This
is more likely to occur if the production system is very
different from the rearing system. The consequences of
some of the welfare problems, such as feather pecking,
cannibalism, foot lesions, and bone fractures, may increase with age and be most apparent for adult layers.
This is certainly the case for difficulties in navigating
in a complex aviary system, which may result in the
production of a high percentage of floor eggs, the manual collection of which incurs large costs. A systematic
review of mortality in laying hens in aviaries indicated
that genotype and access to litter during rearing accounted for the majority of mortality during production (Aerni et al., 2005). Similar findings have been
reported for organic systems, where 79% of the variation in plumage condition between 23 organic farms
was found to be due to rearing-related factors (Knierim
et al., 2008). Appropriate rearing, as summarized here,
is thus essential for ensuring the welfare and productivity of laying hens.
This review summarizes existing knowledge about
rearing-related risk factors that influence the welfare
of pullets and laying hens. Experimental, on-farm, and
epidemiological studies are included. Factors during
rearing that have been studied in relation to their effects on both the rearing and the adult phase include:
effects of beak trimming, housing type, furnishing, enrichment, feeding, stocking density, flock size, sound
and light levels, concentration of gasses, transition from
rearing to production facilities, competence of staff, and

REARING EFFECTS ON LAYING HEN WELFARE

items, preening, removing ectoparasites, exploring the

environment, nest building, and during agonistic interactions with other birds. Indeed, beak-trimmed birds
have been found to have a higher infestation of ectoparasites due to a reduced ability to remove them
(Mullens et al., 2010; Chen et al., 2011). The benefits
of beak trimming should therefore be weighed against
the costs.

Acute Effects of Hot Blade and Infrared

Beak-Trimming

8 weeks of age in trimmed compared with untrimmed

chicks (Angevaare et al., 2012). These studies indicate
that beak trimming is likely to cause acute pain in the
immediate period following the procedure.

Chronic Effects of HB and IR Methods

Applied to Adults or Chicks
In the long term, beak trimming may also cause both
chronic pain and reduced functionality of the beak. Intact birds eat more efficiently between 89 and 106 days
of age, and pick up approximately 63% more food in
a single peck than HB-trimmed birds (Duncan et al.,
1989). Litter-directed behavior after HB beak trimming
at 8 days of age is also performed less during the first
19 weeks of age in trimmed birds compared with intact controls (Sandilands and Savory, 2002b). Adult
HB beak-trimmed hens display longer nesting durations, which may indicate pain and/or a reduced ability
to manipulate nesting material (Eskeland, 1981). Although it is currently forbidden in the European Union,
Norway, and Switzerland, beak-trimming after 4 weeks
of age is still practiced in several other parts of the world
and certainly causes long-term adverse effects on behavior, feeding activity, and weight gain (Duncan et al.,
1989). Neuromas in the beak stump of birds that were
beak trimmed as adults have been found 20 to 30 days
after HB trimming one-third of the beak; and spontaneous firing of neurons has also been detected (Breward
and Gentle, 1985). There is no evidence that HB beak
trimming at 1 or 10 days of age causes neuroma formation (Gentle et al., 1997).
To summarize, chronic effects on bird welfare have
mainly been found in birds that have been beak
trimmed at one-week-old or later. Chronic pain due to
IR trimming has to our knowledge not been reported,
but this may be related to the fact that IR trimming
is only performed at the hatchery on chicks less than
2-day-old. These studies indicate that beak trimming of
birds older than one week is likely to reduce their welfare by causing chronic pain and inhibiting the normal
expression of behavior.

Severity of Beak Trimming

The severity of beak trimming, reflected in the
amount of beak removed and the duration of the cauterization procedure, influences the likelihood of neuroma development as well as the development of chronic
pain. If birds are HB trimmed with varying severity at
hatch using different durations of cauterization, neuromas are found in the beaks of all trimmed birds at
10 weeks of age. The neuromas found in the mildest
treatments regress, whereas those found in the severely
trimmed beaks persist to 70 weeks of age (Lunam et al.,
1996). More deformities are also observed on the beaks
of the severely trimmed birds (Lunam et al., 1996). In
addition to this, inappropriate temperatures may cause
damage to the beak past the point of the cut (Gentle,

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When discussing the welfare implications of beak

trimming, consideration should be made of the specific
technique used, the age of the birds, and the severity of
the treatment relative to acute and chronic effects. Two
different beak-trimming methods are routinely used in
Europe. Hot blade (HB) is the traditional method and
can be performed at any age whereas infrared (IR)
trimming is a more recently developed and more precise method that can only be performed at the hatchery.
Unless stated otherwise, only results for birds trimmed
at 10-day-old or younger are reported here.
The effects of HB trimming have been studied comprehensively. There appears to be a short pain-free period immediately after HB trimming which may last
up to 26 h (Gentle et al., 1991; Glatz et al., 1992).
After this period, trimmed birds not given analgesics
show a significant reduction in feed intake compared
with those given analgesics (Glatz et al., 1992). Both
HB-trimmed and more severely IR-treated birds spend
less time walking at 5 weeks of age than less severely
IR-treated birds (Dennis and Cheng, 2012).
Both IR and HB trimming reduce feed intake relative to controls until 4 weeks of age (Marchant-Forde
et al., 2008). Furthermore, both HB- and IR-trimmed
birds were less active than controls up to one-week-old,
with IR-trimmed birds having the largest proportion
of the beak removed, being the least active (less time
eating and drinking) and the controls being the most
active (Marchant-Forde et al., 2008). Birds that are HB
trimmed at 7 to 10 days change their meal patterns
(Persyn et al., 2004). Beak-trimmed hens eat smaller
meals and have shorter intervals between feeding than
hens with intact beaks at 77 to 80 weeks of age. Another study indicates that HB beak trimming at one
or 10 days of age reduces the activity of birds during the week following treatment, but not thereafter
(Gentle et al., 1997). HB trimming at 2 days of age reduced the time spent pecking and the force of pecking
relative to untrimmed birds at 3 weeks of age, but not
at 4 or 5 weeks (Dennis and Cheng, 2010). Chicks that
are beak-trimmed on the day of hatching do not appear
to show a reduction in feeding or total pecking behavior at 10 weeks of age compared with controls, but the
peak force used during exploratory pecks is significant
less at 12 weeks of age (Jongman et al., 2008).
IR beak trimming causes a reduction in body weight
from first weighing at 5 days of age that lasted until

JANCZAK AND RIBER

1986b). If practiced, beak trimming should therefore

involve removal of the smallest possible portion of the
upper beak.

Comparison of HB and IR Beak-Trimming

REARING CONDITIONS AFFECTING THE

WELFARE OF LAYING HENS
Transfer from Rearing to Laying
Environment
A study of 28 rearing flocks producing 51 flocks of
laying hens indicates that earlier transfer of birds from

Transfer from Cages to Loose Housing

Systems
There is general consensus that hens should be reared
in an environment similar to that in which they will
live as adults. Matching the rearing environment to the
adult environment is thought to ease the transition to
the layer house and reduce problems such as feather
pecking and cannibalism, especially in non-cage systems (van de Weerd and Elson, 2006). The number of
scientific studies in this area is however rather limited.
A range of welfare problems have been related to the
combination of rearing in cages, followed by housing
in aviaries during the laying period. The major concern
about transferring pullets from cages to aviaries is their
lack of experience with navigation in a 3-dimensional
space. At 16 weeks of age, birds reared with access to
perches from the time of hatching are more skilled at
reaching the higher tiers by jumping from one tier to
the next in comparison to birds who first gained access
to perches at 8 weeks of age (Gunnarsson et al., 2000).
Lack of ability to navigate in 3-dimensional space increases the risk of emaciation, dehydration, and floor
eggs when food, water, perches, and nest boxes are located on the different levels found in aviary systems
(Tauson, 2005). Flight accidents may be prevalent in
birds reared without perches, resulting especially in keel
bone fractures. Birds reared without access to perches
lay more floor eggs and exhibit a higher incidence of
cloacal cannibalism (Gunnarsson et al., 1999). Birds
perching on the floor may be more susceptible to cannibalism because of a reduced ability of subordinate individuals to avoid aggressive pen mates (Cordiner and
Savory, 2001; Yngvesson et al., 2002). Because of the
significant problems associated with cage rearing followed by production in loose housing systems, to the
authors knowledge, this is not commonly practiced.
Practical experience suggests that certain hybrids may

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A number of studies have directly compared the effects of HB and IR trimming on the behavior and welfare of chicks. HB-trimmed birds, and the more severely
IR-treated birds, spent less time walking at 5 weeks
of age than less severely IR-treated birds (Dennis and
Cheng, 2012). HB-trimmed birds also spent less time
drinking than IR-treated birds up to 10 weeks of age,
which may be indicative of pain (Dennis and Cheng,
2012). IR-trimmed birds had better plumage than HBtrimmed birds (Dennis et al., 2009). Compared with
HB-treated beaks, IR-treated beaks were more consistent in length (Carruthers et al., 2012) and had fewer
abnormalities (cracks, asymmetrical regrowth, blisters,
etc.) (Carruthers et al., 2012; Marchant-Forde et al.,
2008). This study also indicated that both treatment
techniques resulted in a reduction in feed intake relative to controls, with the IR-trimmed birds consuming
the least food until 4 weeks of age. Furthermore, both
HB- and IR-trimmed birds were less active than controls up to one week of age, with IR-trimmed birds being the least active (less time eating and drinking) and
the controls being the most active. HB-trimmed birds,
which had less of the beak removed, were intermediate
in their activity levels. This comparison between the
two trimming methods may however be confounded by
the severity of the beak trimming, as the IR-treated
birds were more severely trimmed than the HB-treated
birds.
Another large study comparing IR- and HB-trimmed
birds with intact birds indicated that the IR treatment
reduced pullet body weight and feed consumption relative to the other treatments (Honaker and Ruszler,
2004). In addition, IR-trimmed pullets suffered higher
mortality than HB-trimmed pullets. Thus existing results are to some degree contradictory, although the
majority of studies find IR trimming to be a gentler
method of beak trimming. Because beak trimming is
likely to cause acute and chronic pain, and to detrimentally influence behavior, it should ideally be replaced by
breeding, housing, and husbandry methods that make
beak trimming unnecessary. The remainder of this review will focus on these latter possibilities for influencing laying hen welfare.

the rearer to the producer decreases the severity of

feather damage in adult birds, and leads to greater use
of outdoor areas in organic production (Bestman and
Wagenaar, 2003). Earlier transfer (16 weeks or less) of
floor-reared birds to conventional laying cages that are
modified by the incorporation of 2 nests also reduces
the risk of laying outside of the nest area (Sherwin and
Nicol, 1993). Similarly, birds remaining on the same
farm during rearing and laying have a delayed onset of
severe feather damage (Drake et al., 2010). In this case,
an increasing number of differences between the rearing and the laying environments within the farm (feeder
type, drinker type, light intensity etc.) were not shown
to be associated with earlier onset of serious feather
damage (Drake et al., 2010), possibly suggesting that
environmental changes have a cumulative effect. Further research needs to be performed on the role of the
transition from the rearing facility to the laying system as a risk factor for decreased welfare in the laying
period.

REARING EFFECTS ON LAYING HEN WELFARE

be more reluctant to go up into the aviary system than

other hybrids, causing more floor eggs and associated
problems. This illustrates the fact that some hybrids
may need more training, irrespective of the system in
which they are reared.

Transfer from Loose Housing Systems to

Cages

deterioration of plumage. This problem may be exacerbated by the common practice of not providing enough
scratching material in furnished cages. In addition, the
pans or mats commonly used as scratching materials
are not designed to limit loss of substrate but to maximize ease of cleaning. Substrate is therefore likely to be
lost very quickly if it is used by hens.
Floor-reared birds transferred to furnished cages during the laying phase are more likely to lay eggs outside
of the nest area and to be less stable in their choice
of nest sites than cage-reared birds after transfer to
modified conventional laying cages containing two nests
(Sherwin and Nicol, 1993). Earlier transfer to laying
cages reduces this effect however, and the time of transfer to the laying environment (16 weeks or earlier) has
more influence on the numbers of floor eggs than the
rearing environment alone. The use of dust baths in furnished cages has been found to be higher in floor-reared,
as opposed to cage-reared, hens during the entire laying period (Roll et al., 2008). Indeed, cage-reared laying
hens may not use dust-bathing substrate at all, as indicated by the accumulation of undisturbed materials in
the litter pan in some furnished cages (A.M. Janczak,
unpublished data).
Litter-reared birds housed in cages during the laying period have paler adrenal glands than birds
reared in cages (Struwe et al., 1992). This suggests a
lower chronic activation of the hypothalamicpituitary
adrenal axis in birds reared on the floor. In contrast,
a similar study indicated no effect of the rearing system on adrenal responsiveness at 50 or 70 weeks of age
(Moe et al., 2010). The same study did, however, indicate that heterophil-to-lymphocyte ratios were significantly higher at 70 weeks of age in hens reared on deep
litter and later moved to furnished cages, compared to
those who were later moved to conventional cages (Moe
et al., 2010). Conversely, antibody production in response to an immune challenge was greater in the hens
that had been reared on litter (Moe et al., 2010). The
authors suggest that the effects on immune response
may have been associated with pathogenic load found in
the floor and furnished-cage environments, rather than
stress due to the rearing system or housing system.
Existing studies thus suggest that hens should be
reared in an environment similar to the one in which
they will live in as adults.

Transfer between Loose Housing Systems

There are several different designs of loose housing
system. In the European Union, there is a trend away
from floor systems in favor of multi-tier aviaries for both
rearing and production phases. This trend is partly a
result of the fact that these systems facilitate better
utilization of available space in the shed, and partly a
result of producers experience that aviaries work better
than older floor systems. Aviary-reared birds have been
found to use aviary platforms on which feed troughs,

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Loose housing systems provide birds with more opportunities to express natural behavior and may thus
better fulfill their behavioral needs. However, if the pullets are destined for cages in the laying period, the transition may be associated with welfare problems. One of
the concerns is that birds perceptions of space may be
affected by their early experience (Faure, 1991). The
general activity of floor-reared pullets following transfer to cages is reduced in the first days after transfer relative to cage-reared birds, likely reflecting the
greater change that the floor-reared birds were thus exposed to (Craig et al., 1988). Another commercial scale
study showed that aviary-reared birds exhibited more
alert behavior near to a novel object than did cagereared birds at 3, but not at 5, weeks after transfer
(Tahamtani et al., 2014). Alert behavior in response
to a novel object in the home environment is associated with a positive choice and therefore is an indicator of good welfare in laying hens (Nicol et al.,
2009; Nicol et al., 2011). This finding suggests that
the aviary-reared birds initially cope better with transfer from the rearing to production facilities than cagereared birds (Tahamtani et al., 2014). However, mortality recorded throughout the production period was
found to be higher in the aviary-reared than in the
cage-reared birds, indicating long-term negative effects
of aviary rearing for birds later producing in furnished
cages.
At the end of lay at 68 weeks of age, hens reared in
cages show more passive and less flighty responses to a
human outside their home cage than floor-reared birds
(Anderson and Adams, 1994a, using methods described
by Jin and Craig, 1988; Hansen, 1976). Another study
using the same recording method reported no effect on
response to a person standing outside of the cage in
60- and 75-week-old hens reared in cages or floor pens
and then housed in conventional cages during the laying period(Jin and Craig, 1988). The plumage condition was poorer at 60 but not at 75 weeks in the floorreared birds. A similar study of cage- or floor-reared
birds housed during the production period in furnished
cages found floor-reared birds to have a poorer plumage
at the end of lay (Roll et al., 2009).
These studies, with the exception of that of Jin and
Craig (1988), yield similar results in suggesting that
rearing in an unrestricted environment with access to a
rich substrate, followed by transfer to a restricted environment with a relatively poor substrate, may cause
frustration, resulting in damaging feather-pecking and

JANCZAK AND RIBER

Effects of Furnishing and Enrichment

Birds may be especially sensitive to environmental effects during the early sensitive periods (Bateson, 1979).
Early experience with furnishings and enrichment materials may therefore have long-lasting consequences
(Johnsen et al., 1998), and exposure to appropriate enrichment experiences during the rearing period may reduce the risk of abnormal behavioral development. For
example, feather pecking is thought to develop because
of a lack of experience with foraging or dust-bathing
material, resulting in ground pecks being redirected to
the feathers of conspecifics (Hoffmeyer, 1969; Blokhuis
and Arkes, 1984; Vestergaard et al., 1993; Vestergaard
and Lisborg, 1993). The sensitive period for learning
about food and dust-bathing material is during the first
10 days of life (Brown, 1964; Hess, 1964; Sanotra et al.,
1995; Vestergaard and Baranyiova, 1996). In addition,
rearing in a complex environment increases the chances
that the birds will develop the necessary skills to navigate in a complex environment (Gunnarsson et al.,
2000); and early exposure to varied stimulation may reduce later fearfulness (Jones, 1982; Reed et al., 1993).
Documented positive correlations between fearfulness
and feather pecking (de Haas et al., 2014a; b) suggest
that early exposure to environmental variability may
also reduce the risk of developing feather pecking.

Depending on perch height, chicks begin perching between 7 and 10 days of age (Workman and Andrew,
1989; Riber et al., 2007a). The amount of time spent
perching increases steadily over time and there are positive correlations between early daytime perch use and
later night time perch use in connection with roosting (Heikkil
a et al., 2006). It is well documented that
adult perch use is influenced by access to perches during
rearing (Faure and Jones, 1982; Appleby et al., 1983),
suggesting that learning to use perches is slower after
the rearing period and may become permanently impaired (Gunnarsson et al., 2000). Whereas the physical
process of jumping up onto perches (that is, the motor
mechanism) is thought to be prefunctionally developed
in chicks, they have to learn to move in more than 2
dimensions (Appleby and Duncan, 1989). Thus the perceptual mechanism for recognizing the perches as possible resting or escape routes requires functional experience to develop (Appleby and Duncan, 1989). A positive association between first perch use and time spent
under perches during the first 2 weeks post-hatch supports this argument (Heikkil
a et al., 2006). The importance of early experience with perches has been highlighted in many studies. A more complex rearing environment produces birds that demonstrate greater use
of elevated aviary levels, higher accuracy of long flights
and jumps, lower pullet mortality, and a higher proportion of eggs laid in nest boxes during adulthood (Colson
et al., 2008).
A study of 59 Swedish flocks of different hybrid
showed that access to perches during rearing reduces
the prevalence of both floor eggs and cloacal cannibalism in loose-housed birds during the laying period
(Gunnarsson et al., 1999). Another study of 64 Swiss
flocks indicated that rearing with access to perches
also reduces the occurrence of feather pecking during
the rearing period (Huber-Eicher and Audige, 1999).
Impaired development of perching, associated with
increased fearfulness and resulting in poor usage of
perches, may increase the risk of smothering caused by
panic and the piling up of birds into heaps (Hansen,
1976; Brake et al., 1994; Keeling, 1997). Furthermore,
access to perches during rearing results in fewer broken back claws, improved bone mineral content, and
improved bone strength in hens later housed in conventional cages as adults (Hester et al., 2013a,b). This is
important because keel bone damage in adult birds is
correlated with poor bone strength (Rodenburg et al.,
2014). Existing studies thus suggest that pullets should
be provided with perches throughout rearing if they are
expected to use perches as adults.

Perches

Substrate and Its Quality

Pullets are highly motivated to perch and prefer to

use the highest perches available, suggesting that this
anti-predator behavior is highly conserved despite many
generations of domestication (Newberry et al., 2001).

Early experience with litter has significant effects

on the development of pecking behavior, as indicated
by a large number of experimental studies. The provision of sand and straw compared with wire from

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water nipples, perches, and nest boxes are normally

located, and to fly and jump more often than floorreared hens throughout the laying period (Colson et al.,
2005). They also lay fewer eggs outside of nests,
potentially reducing the risk of cloacal cannibalism
(Colson et al., 2005). Rearing in aviaries with feed and
water provided on elevated platforms (aviary rows),
when compared with provision of feed on the floor,
increases the use of elevated aviary levels at adulthood, results in a higher accuracy of long flights and
jumps, reduces mortality during rearing, and increases
the number of eggs laid in nest boxes (Colson et al.,
2008). Indeed, the mortality rate of floor-reared hens
is higher than that of aviary-reared hens with feeders located on platforms both before and after transfer
from the rearer to the producer (Colson et al., 2008).
Aviary-reared birds are also better at solving spatial
tasks, as indicated by their better working memory in
hole-board tasks (Tahamtani et al., 2015). They have
bones with better load bearing capability and stiffness
(Regmi et al., 2015) compared to cage-reared birds. It
has thus been clearly demonstrated that hens destined
for aviaries should be reared in aviaries.

REARING EFFECTS ON LAYING HEN WELFARE

of litter during the first 4 weeks of rearing was predictive of an elevated incidence of feather pecking during
the laying period (Bestman and Wagenaar, 2003).
The importance of early developmental processes in
determining the incidence of feather pecking is emphasized by positive associations between measures of severe feather pecking as early as 5 weeks of age, fear of
humans during rearing, and feather damage at 40 weeks
of age in aviary-housed laying hens in conventional systems (de Haas et al., 2014a). It is emphasized that even
relatively brief interruptions in access to a substrate
during rearing may have detrimental consequences for
birds that normally have access to substrate (de Haas
et al., 2014b).

Outdoor Access during Rearing for Organic

Systems
Only a few studies have tested the effects of access to
outdoor areas during rearing. This may be important
because usually only a small proportion of adult hens
use outside ranges in organic systems at any particular
time (Bubier and Bradshaw, 1998; Zeltner et al., 2004;
Hegelund et al., 2005; Keeling et al., 1988). It is likely
that early experience with outdoor areas during rearing
influences the use of outdoor areas in adult birds. Birds
that were both handled and exposed to an outdoor area
from 12 to 20 weeks of age emerged more quickly from
a test box placed outside, and also moved further away
from the box, than birds that were only handled or
were neither handled nor exposed to an outdoor area
(Grigor et al., 1995). A more recent study indicates that
6-week-old layer chicks exposed to one week of access
to an outdoor area were less fearful and learned to find
a food reward significantly faster than controls without
outdoor access (Krause et al., 2006). Taken together,
these studies suggest that early exposure to an outside
area during rearing should increase the use of outdoor
space by adult hens in organic production.

Enrichment, Brooders, and Noise

There is evidence that the provision of enrichment
during rearing reduces fearfulness in both pullets and
adult laying hens. For example, birds reared in pens
containing brightly colored plastic bottles, balls, and
rattles, and exposed to human voices from a radio during daylight hours, as well as human handling, had
lower levels of potentially damaging fear reactions and
incurred fewer knocks against the cage during depopulation than non-enriched birds (Reed et al., 1993).
Chicks raised with a variety of objects are reported
to be more mobile and to feed and vocalize more in
open field tests. They also take less time to emerge
into an open area in hole-in-the-wall tests (Jones, 1982)
than birds without an enriched environment. Access
to environmental enrichment in the form of peckable
strings during the rearing period has been shown to

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hatch until 4 weeks of age results in increased plumage

quality, reduced feather pecking, reduced expression of
fear-related behavior in a tonic immobility test, and reduced mortality in adult birds later housed on straw
(Johnsen et al., 1998). This is consistent with an earlier study indicating that rearing on substrate instead
of wire results in less feather pecking in adult birds
housed in pens (Blokhuis and van der Haar, 1989) and
has been confirmed by a later study showing that a
lack of substrate in the first 4 weeks of life is related
to increased feather pecking in adulthood (Bestman
et al., 2009). Rearing chicks on litter or sand as opposed to wire has a preventive effect on the development of feather pecking even when the hens are later
moved to a barren environment (Vestergaard et al.,
1997). Beneficial effects on feather pecking may be particularly clear after the provision of long straw (HuberEicher and Wechsler, 1998; Blokhuis, 1991), but the
provision of sand and peat during rearing also reduces
plumage deterioration in adult birds (Nrgaard-Nielsen
et al., 1993).
There is also ample documentation on the importance of early experience with litter from large on-farm
studies. In aviary systems, early access to litter lowers mortality (Aerni et al., 2005) and access to woodshavings for a minimum of 10 days during the rearing
period reduces feather pecking compared with keeping
hens continually on wire throughout the rearing and
adult periods (Nicol et al., 2001). The latter study however indicated that the current substrate was of great
importance, and adult hens housed on wood-shavings
performed significantly more ground pecking and less
feather pecking than birds housed on wire, regardless
of previous experience. A Swiss study used data from
aviary-reared birds housed on plastic grids or having access to litter in rows for the first 2 weeks of life (HuberEicher and Seb
o, 2001). All groups were later housed
under identical conditions with unrestricted access to
litter. The results indicated that birds reared on litter
spent more time foraging at 5 weeks of age and less
time feather pecking at 5 and 14 weeks (Huber-Eicher
and Seb
o, 2001). The first observation is crucial, as a
higher proportion of hens foraging is associated with
a lower incidence of severe feather pecking during the
rearing period in organic and indoor loose housing systems (Gilani et al., 2013). A recent study of 47 rearing flocks in the Netherlands showed that disruption of
access to litter from 7 to 10 days post-hatch, and limitation of litter supply in the aviary rows, increases the
incidence of severe feather pecking and feather damage,
and increases fearfulness during the rearing period (de
Haas et al., 2014b). This illustrates the previous argument that moving birds from a system with a better
to a poorer substrate quality may be instrumental in
causing the development of damaging feather pecking
behavior. The study by de Haas et al. (2014b) is striking
in indicating significant benefits of substrates as simple
as paper soiled with feces and feed. In a study of 28 commercial organic flocks in the Netherlands, the absence

JANCZAK AND RIBER

Effects of Feeding-Related Factors

An experimental study has suggested that pullets
fed pellets have more plumage damage than pullets
fed mashed feed (Savory et al., 1999). Other experimental studies suggest that provision of whole grain in

the substrate during the rearing period increases foraging directed to the floor, and reduces damage due to
feather pecking in adult birds (Blokhuis, 1991; Blokhuis
and van der Haar, 1992). A study of 34 flocks from 29
rearing farms indicates that an increasing number of
diet changes during rearing increases the incidence of
feather-pecking outbreaks in adult birds (Gilani et al.,
2013). A study including 22 free-range and organic laying farms (Drake et al., 2010) indicated that the presence of chain feeders, compared with feed hoppers, was
associated with an earlier onset of severe feather damage. This could possibly be explained by higher feed
intake in pullets fed using a chain feeder as increased
feed intake in pullets is also associated with a risk of
earlier development of severe feather damage (Drake
et al., 2010).
Few studies have addressed effects of the feeder space
provided during rearing. Existing studies were conducted more than 20 years ago (Anderson and Adams,
1994a,b) and may therefore no longer be valid, as the
genetic lines used today are different and for example,
body size and feed intake have changed (Anderson and
Jones, 2012). However, one recent study reports that
the rate of severe feather-pecking is lower when more
than one feeder type is used, and higher when compartmentalized pans are used, as opposed to the sole use of
chain feeders (Gilani et al., 2014). In summary, the provision of mashed or crumbled feed rather than pellets
is one approach to reducing the risk of feather pecking.

Effects of Stocking Density and Flock Size

European Union legislation allows a maximum density of 18 birds/m2 during rearing in barren cages, and
13 birds/m2 during rearing in furnished cages (CEC,
1999, Council Directive, 1999/74/EC). No maximum
stocking density is defined for birds reared in aviary systems. There are few studies testing the effects of stocking density and flock size during rearing. A few studies
were performed more than two decades ago (Anderson
and Adams, 1992; Carey, 1987), but it is difficult to
apply these results today as modern hens are different
from the lines used at that time, and housing conditions have also changed. Results from earlier studies of
stocking density must also be interpreted with care as
in most studies, especially the older ones, stocking density was altered by adjusting the number of birds in a
cage or pen, thereby also affecting feeder and drinker
space allowances.
A study of 64 Swiss flocks indicated that rearing at a
lower stocking density (<10 pullets/m2 ) reduces the occurrence of feather pecking in adults (Huber-Eicher and
Audige, 1999). Hansen and Braastad (1994) found that
rearing at 6.5 pullets/m2 rather than 13 pullets/m2 reduces the occurrence of feather pecking during rearing,
but not during the laying period. However, the plumage
condition was better in the laying period in hens reared
at the lower density.

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reduce feather pecking in both the rearing and the laying periods, with the effect on the rearing period being
most pronounced if the objects were introduced from
the time of hatching (McAdie et al., 2005). In contrast,
the introduction of strings during the laying period is
ineffective for reducing feather pecking in adult laying
hens (Glatz, 2000).
Dark brooders are warm, dark, and enclosed areas
that may simulate the effects of a brooding hen. Fourweek-old chicks reared in dark brooders expressed lower
levels of severe feather-pecking than those brooded under heat lamps in experimental conditions (Johnsen
and Kristensen, 2001). Dark brooders were also found
to have long-term preventive effects on severe featherpecking and cannibalism in an experimental study
(Jensen et al., 2006). At 23 weeks of age, hens with intact beaks reared in brooders had better plumage and
skin condition, and reduced mortality compared with
control birds. Data collected from a large on-farm study
found a reduced prevalence of severe feather-pecking
and improved plumage condition in intact birds over
the period from brooder placement to 35 weeks of age,
with no adverse effect on growth, body-weight uniformity, or mortality to the end of rearing (Gilani et al.,
2012). Dark brooders are also reported to improve behavioral synchrony between birds, reduce disturbances
during resting, and result in calmer birds (Riber et al.,
2007b; Gilani et al., 2012).
Whereas exposure to audio stimulation from a radio
has beneficial effects, this does not apply to high sound
levels in general. A study of 34 flocks from 29 rearing
farms in the UK indicates that the probability of severe
feather-pecking at 35 weeks is increased when the range
of sound levels in the house at the end of rear is high
(mean 7.8 dB, range 0 to 18 dB; Gilani et al., 2013).
Furthermore, higher average sound levels during rearing
(mean 58.3 dB, range 32 to 66 dB) are associated with
increased feather damage at 35 weeks of age (Gilani
et al., 2013). This is corroborated by another study of
22 free-range and organic laying farms which identified
higher sound levels during rearing (mean 59.4 dB, range
14.3 to 80.0 dB) as risk a factor for the earlier onset of
severe feather damage (Drake et al., 2010). Between
15 and 17 weeks of age, each 10 dB increase in sound
level was associated with a 25.5% reduction in the time
to reach a cutoff point at which the average plumage
condition of the flock was defined as poor, and between
17 and 20 weeks, with a 7.9% reduction in the time
to reach the cutoff point for poor plumage condition
(Drake et al., 2010). Investment in the development of
quieter systems is therefore likely to be beneficial.

REARING EFFECTS ON LAYING HEN WELFARE

Effects of Lighting
Older studies suggest that high light intensities during rearing results in pullets with a poorer plumage
condition (e.g. see Hughes and Duncan, 1972). Similar results from more recent studies also indicate that
high light intensity during rearing (30 lux vs. 3 lux) increases the prevalence of severe feather-pecking at 10
and 45 weeks of age, but not at 28 weeks of age (Kjaer
and Vestergaard, 1999). In this study, the increased
incidence of severe feather-pecking negatively affected
plumage condition at 11 weeks of age, but not at 28 or
46 weeks of age. High light intensity during rearing also

tends to have a long-term negative impact on mortality from 16 to 46 weeks (Kjaer and Vestergaard, 1999).
Smaller differences in light intensities (3 lux or 10 lux)
do not appear to influence the development of feather
pecking or cannibalism (Kjaer and Srensen, 2002). Another study indicates that a high light intensity (5 lux
vs. 60 to 80 lux) during rearing does not influence the
incidence of cannibalism during the pre-laying period
or the early laying period (Hartini et al., 2002).
A study of 22 free-range and organic laying farms
identified high light intensities during rearing as a risk
factor for the earlier onset of severe feather damage;
each 100-lux increase was associated with a 12.2% reduction in latency to reach a cutoff point where the average plumage condition of the flock was defined as poor
(Drake et al., 2010). In contrast, the absence of daylight
at the age of 7 to 17 weeks, in combination with not having litter at the age of 1 to 4 weeks, was found to be a
significant predictor of feather damage during the laying period in an on-farm study run in The Netherlands
(Bestman et al., 2009). Another recent study compared
the percentage of loose-housed flocks with or without
plumage damage according to whether they were exposed to daylight through windows (23 flocks) or not
(58 flocks; Yngvesson et al., 2011). Thirty percent of
flocks with windows had damaged plumage compared
to 50% of flocks not exposed to daylight, suggesting
that daylight exposure is not associated with increased
risk of plumage damage.
Gentle feather-pecking may increase in pullets reared
with low light intensities (3 lux vs. 30 lux), suggesting that low light intensity may impair the ability to
identify environmental cues (Kjaer and Vestergaard,
1999). This may also explain why Gilani et al. (2013)
found that a larger variation in light intensity within
the house was associated with a reduced frequency of
gentle feather-pecking during rearing. A light intensity
above 5 lux is necessary for proper inspection of birds
by the farmers. At intensities below 5 lux, light does
not pass directly through the skull and cranial tissues
to the pineal gland, where it would normally suppress
the production and release of serotonin and melatonin
(Zawilska et al., 2004). This is important, because melatonin modulates growth in poultry (Zeman et al., 1999),
and low serotonin levels may increase feather pecking
(van Hierden et al., 2002, 2004), aggression (Shea et al.,
1990), and fear (Newberry and Blair, 1993).
A comparison of farms providing photoperiods ranging from 9.8 to 24 h/d indicates that the risk of severe
feather-pecking during rearing, but not laying, is increased with shorter photoperiods (Gilani et al., 2013).
The length of the photoperiod may also indirectly affect
the prevalence of cloacal cannibalism. An onset of lay
prior to 20 weeks of age has been related to an increased
risk of vent pecking (Potzsch et al., 2001). Since the
timing of sexual maturation can be controlled by using
short photoperiods followed by increasing day length
(Lewis et al., 1998), the risk of cloacal cannibalism can
potentially be reduced by using a lighting schedule that

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Similarly, a Dutch study of 28 rearing flocks, split into

51 laying-hen flocks, indicated that a higher number of
pullets per square meter (range 15 to 53 pullets/m2 )
in the first 4 weeks of life was associated with an increased incidence of feather damage during the rearing
period (Bestman et al., 2009). However, the researchers
noted that it was difficult to differentiate the influence of stocking density from the influence of a lack
of litter during the first 4 weeks, as most of the highdensity flocks also lacked litter during this period. In
contrast, another comparable on-farm study indicated
no association between stocking density during rearing
and feather pecking during the rearing or production
phases (Gilani et al., 2013). Spindler et al. (2013) used
a planimetric method to compare the effects of space allowance in alternative housing systems for laying hens.
The floor space covered by the pullets was determined
using a software program calculating the animal area
from color contrast photographs of standing and sitting pullets. This was done at regular intervals from the
6th week of life until the pullets were 18 or 20 weeks
old. A correlation between floor space covered by the
pullets in the standing position and the live weight was
found. The authors concluded that the maximum stocking density for pullets at the age of 16 weeks should be
between 11 and 14 birds/m2 , depending on the genetic
line used (Lohmann Traditional: 11 birds/m2 ; Lohmann
Brown: 12 birds/m2 ; Lohmann Selected Leghorns: 13
birds/m2 ; and Dekalb White: 14 birds/m2 ). However,
they also recommended that these suggested maximum
stocking densities should be verified by further investigations using observations of behavior.
The few existing studies testing the effects of flock
size involve flocks that are significantly smaller than
those used on commercial farms today (Meuniersalaun
et al., 1984). Stocking density, total area, and enrichment are thought to have a greater effect on welfare
than flock size. An exception is found for the effects of
flock size on the use of outdoor areas. The percentage of
pullets that use an outdoor range is higher for smaller
flocks (flock size range 92 to 15,848; Gilani et al., 2014),
and this corresponds to findings for laying hens (Bubier and Bradshaw, 1998; Zeltner et al., 2004; Hegelund
et al., 2005).

10

JANCZAK AND RIBER

Gas Concentrations and Air Quality

A large on-farm study indicates that elevated concentrations of carbon dioxide (range 43 to 2000) and
ammonia (range 0 to 100 parts per million (ppm))
are risk factors for the earlier onset of severe feather
damage (Drake et al., 2010). In this study, between
the ages of 15 and 17 weeks, every 15 ppm increase
in NH3 recorded was associated with a 10.1% reduction
in the time taken to reach a threshold score for severely
damaged plumage. A lower ceiling height in the rearing
house (range 0.7 to 3.1 m) is associated with a higher
prevalence of severe feather-pecking during rearing, but
not during lay (Gilani et al., 2013). This latter finding
could be related to increased ammonia and carbon dioxide concentrations resulting from poorer ventilation in
poultry houses with low ceilings.

Effects of Staff Competence

Lambton et al. (2013) in the UK tested the protective effects of a farm management package aimed
at reducing the development of damaging pecking in
loose-housed laying hens. Fifty-three treatment flocks,
in which the producers were advised in the use of preventative strategies against feather pecking, were compared with 47 that were not instructed in the use of preventative measures. The study revealed that the implementation of the management package, including measures directed at the rearing period, significantly reduced levels of injurious pecking during the laying phase
(Lambton et al., 2013). Another study of 34 UK flocks
from 29 rearing farms supported the interpretation that
the degree of experience of the staff caring for birds
during the rearing period contributed significantly to a
reduction in feather pecking during lay (Gilani et al.,
2013).
Managing growth to avoid the production of underweight pullets reduces the risk of uterine prolapse and
hence cloacal cannibalism, as uterine prolapse may trigger cloacal cannibalism (Glatz, 2005). It is also commonly thought that avoiding underweight pullets, and
increasing uniformity, may lower the risk of feather
pecking and cannibalism. However, research into this
area seems to be very sparse. One study of Danish rearing flocks (both conventional and organic) showed that
the lower the mean weight at 15 weeks of age in flocks of
both white (n = 222) and brown strains (n = 158), the
higher the mortality in the rearing period (Mrch et al.,
2012). For the brown strains, uniformity of the flock also
affected mortality; the less uniform flocks having the
highest mortality in the rearing period. A tendency was
found for flocks (n = 39) of Lohmann Selected Leghorn
(LSL) hens housed in cages (conventional cages and furnished cages) with a uniformity above 90% at 15 weeks
of age to have a lower mortality during the laying period than flocks with uniformity between 85 to 90% or
below 85%. In contrast, the body weight at 15 weeks of

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delays the onset of lay. Birds reared with 23 h of continuous light and 1 h of darkness are reported to react less
fearfully in a tonic immobility test, and to be easier to
handle than those reared with a lighting program that
changes from 6 to 23 h of light depending on the age of
birds (Newberry and Blair, 1993). Another study indicates that chicks reared in 16 h of light have a higher
lymphocyte count and a more active lymphocyte response than chicks reared in 8 h of light, indicating an
enhanced immune response in birds exposed to a longer
photoperiod (Mashaly et al., 1988).
Other aspects of light may potentially affect the welfare of pullets. The ability of adult laying hens and
broilers to detect flickering depends on the color temperature of the light and the light intensity although
detection of flickering above 105 Hz has not been documented (Nuboer et al., 1992; Jarvis et al., 2002).
Even when poultry have been shown to perceive flickering, few studies indicate that this is aversive to birds
(see review by Prescott et al., 2003). The light source
and spectrum, or color, of the light are also important features. Some studies have shown a preference for
alternatives to incandescent lighting (biolux lighting,
Kristensen et al., 2007; fluorescent lighting, Widowski
et al., 1992); however incandescent lighting is in the process of being phased out in favor of more energy-efficient
lighting. Light-emitting diodes (LED) are thought to
be the light source that will be most commonly used in
poultry houses in the near future.
Research on LED and other light sources has mainly
been concentrated on broilers, and positive effects of
LED have been found on performance and welfare
(Mendes et al., 2013; Riber, 2014). One useful feature
of LED is that they are produced in all monochromatic
colors and all possible polychromatic color temperatures. It is therefore possible to adjust the spectrum
of the light to meet the birds preferences. Studies on
the effects of flickering, different light sources, and different color temperatures on pullet welfare are limited
(but see Gunnarsson et al., 2008a). It is, however, likely
that the findings for adult birds are applicable to pullets.
In pullets reared for a laying system with access to an
outdoor range, the light conditions during rearing may
affect the use of the outdoor area, both during rearing and laying. The percentage of the flock observed on
the range during the combined rearing and laying period increases with a higher light intensity in the house
(mean 123 lux, range 2 to 687 lux; Gilani et al., 2014).
Pullets reared for a production system with access to
outdoor areas should be reared with access to natural light, as pullets reared with access to natural light
show a higher preference for natural light at the age of
14 weeks than pullets reared without access to natural
light (Gunnarsson et al., 2008a). In addition, pullets
reared with access to natural light tend to start nighttime perching at an earlier age, which may reduce the
prevalence of cannibalism (Gunnarsson et al., 2008b).

REARING EFFECTS ON LAYING HEN WELFARE

age had no effect on mortality during the laying period

(Mrch et al., 2012).

Effects of Bird Hybrid and Interactions with

the Environment

may be large and therefore selective breeding against

fear within lines could be beneficial. Group housed birds
selected against mortality associated with feather pecking were more active in an open field test at 5 to 6 weeks
of age than randomly selected control birds (Rodenburg
et al., 2009). Higher activity in an open field test indicates lower levels of fearfulness and this result therefore
suggests positive associations between fearfulness and
feather pecking that could be utilized in selection programs (Rodenburg et al., 2009). De Haas et al. (2014a)
also found positive associations between measures of severe feather pecking as early as 5 weeks of age and fear
of humans during rearing in aviaries, emphasizing that
the relationship between fearfulness and feather pecking
is not experiment-specific. A recently published review
by Muir et al. (2014) highlights breeding as an effective
tool for improving poultry welfare and eliminating the
need for beak trimming.

DISCUSSION
This review summarizes existing knowledge about
rearing-related risk factors for poor welfare and productivity in laying hens. On this basis the following
recommendations can be made.

r In countries in which beak trimming is still permit-

ted, rearers should apply best practice. This would

involve beak trimming using a gentler method (for
example IR trimming), removal of as little of the
beak as possible, and performance of the operation as early as possible. Because of the adverse effects of beak trimming on bird welfare, alternative
strategies for reducing feather pecking (listed below) are preferable. In addition it is possible to reduce the need for beak trimming by using a hybrid
that functions better than others in loose housing
systems.
r Rearers should house pullets in environments that
are as similar as possible to the production environment to ensure optimal utilization of resources
and to avoid frustration and associated injurious
pecking.
r Starting shortly after hatching, pullets should
have constant access to an appropriate substrate throughout both the rearing and production
phases. For adult laying hens housed in furnished
cages, the industry as a whole should address the
common practice of infrequent substrate provision
in order for substrate provision to pullets to be effective in reducing problems with feather pecking.
The substrate provided should be of a quality similar to that which the birds will have access to as
adults.
r Perches should be provided from 7 days of age at
the latest to ensure optimal perch use in the adult
birds.

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The genetic makeup of the birds may interact with

environmental parameters and thereby influence bird
welfare during both the rearing and laying periods.
Strains may differ in their propensity to perform injurious pecking or to express exaggerated fear responses.
Genetic selection against feather pecking may be a viable and more ethically acceptable alternative to beak
trimming.
Genetic selection against abnormal behavior has been
shown to be possible with regards to both feather pecking (Su et al., 2005) and cannibalism (Craig and Muir,
1993; Muir and Craig, 1998). Both types of behavior are
heritable and can be reduced using breeding. The heritability of feather pecking has been estimated to range
from 0.09 to 1.04, depending on the selection method
and variable measured (reviewed by Jensen et al., 2008);
whereas a single study reports a heritability for cannibalism of 0.65 (Craig and Muir, 1993). Breeding companies apparently select against feather pecking and cannibalism but the specifics are not published. Experimental lines of laying hens differing in their propensity
to feather peck have been created using individual selection, but these lines have been used only for experimental research (Kjaer et al., 2001).
Selection for reduced fearfulness, which can be defined as the propensity to express fear reactions to dangerous or potentially dangerous stimuli, is complicated
by its multifactorial nature and the plethora of methods
available for measurement. Fear responses may also be
stimulus-specific, meaning that selection for responses
to one stimulus may be unrelated to responses to other
stimuli. Furthermore, a bird may show active fear responses in the form of panicky flight, or passive fear
responses in the form of tonic immobility. Tonic immobility as measured in a tonic immobility test (one
example of a standardized fear test) has a heritability ranging from 0.18 to 0.32 (Craig and Muir, 1989;
Campo and Carnicer, 1993).
Some studies indicate breed differences in fearfulness.
For example, two lines of commercial floor-reared pullets subjected to several fear tests at 5 different times
from hatching to 30 weeks of age illustrated strain-byage interactions in response to the tonic immobility test
(Hocking et al., 2001). Albentosa et al. (2003) obtained
mixed results when comparing responses of four different strains in three different fear tests. Strain did
not influence behavior in the novel object test or the
open field test but White Leghorns reacted more fearfully than the other strains in the tonic immobility test.
Two studies indicate a lack of differences in fearfulness
between different genetic stocks (Hocking et al., 2004;
Anderson and Jones, 2012). The variation within lines

11

12

JANCZAK AND RIBER

r Pullets should be fed mashed or crumbled feed, and
r

r
r

r
r

This review identifies a number of topics that are

not well understood. Despite ongoing debate in many
European countries regarding whether beak trimming
should be practiced or not, no recent study clearly
documents the benefits of, or necessity for, this practice. This review presents convincing evidence of the
advantages associated with rearing hens in an environment similar to the one in which they will later
live as adults. However, the lack of detailed knowledge
regarding the mechanisms underlying the detrimental
effects of rearing in one system and producing in another means that further study is required. As an example, the basis of the contradictory welfare consequences
(Tahamtani et al., 2014) of combining rearing in an
aviary system with production in furnished cages is
poorly understood. The welfare effects of age at transfer
between rearing and production facilities should also be
studied further. Relative to their apparent importance
for both welfare and productivity, the welfare consequences of growth rate during rearing, as well as body
weight and uniformity at the initiation of lay, have also
been sparsely studied. Other neglected areas of research
are how welfare during the rearing and laying phases
is affected by bird density, feeder distribution, and
lighting (light source, flickering, and spectrum) during
rearing.

ACKNOWLEDGMENTS
This work was funded by Aarhus University, the
Norwegian Foundation for Research Levy on Agricultural Products (FFL), the Norwegian Agricultural
Agreement Research Fund (JA), the Norwegian Meat
and Poultry Research Centre (Animalia), and NMBU
School of Veterinary Science. Norwegian funding was
administrated through The Research Council of Norway grant number 207739. Marlene Furnes Bagley and
Tone Beate Hansen, of Animalia, Oslo, Norway, provided helpful comments on the manuscript. We acknowledge the two anonymous reviewers that provided
advice leading to important revision of the manuscript.

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