XXIV
World´s Poultry Congress 5 - 9
August - 2012 • Salvador - Bahia - Brazil
The broiler breeder paradox from an ethical,
genetic and physiological perspective and
suggestions for solutions
1
Department of Biosystems, Division LivestockNutrition-Quality, KU Leuven, Kasteelpark Arenberg
30, 3001 Leuven, Belgium
2
Centre of Science, Technology & Ethics, KU Leuven.
Kasteelpark Arenberg 1, 3001 Leuven, Belgium
3
Department of Biosystems, Division Gene
Technology, KU Leuven, Kasteelpark Arenberg 30,
3001 Leuven, Belgium
Modified after a paper published in British Poultry
Science 51(5): 569-579.
Summary
D
ue to intensive selection, broiler chickens
became the most efficient meat producing
animals because of their fast growth,
supported by a virtually unlimited voluntary
feed intake. These characteristics cause a lot of
problems in the management of broiler breeder
hens, since a negative correlation between muscle
growth and reproduction effectiveness is observed.
This problem, namely the ‘fast muscle growth versus
reproduction health’-paradox induces another
paradox, namely: ‘acceptable reproduction and
health versus hunger stress and impaired welfare’
because broiler breeder hens require dedicated
programs of feed restriction to a) maximize egg
and chick production and b) to avoid metabolic
disturbances and mortality in broiler breeders.
Given that poultry selection is a global largescale business and since chickens are prolific species,
the only improvement in profit can be obtained by
selecting on feed conversion and/or higher breast
Introduction about the
nature of the problem
E. Decuypere et al.
*Eddy Decuypere, Kasteelpark Arenberg 30, B-3001 Leuven,
Belgium, Fax +32 (0) 16 32 19 94, Tel +32 (0) 16 32 17 34,
[email protected]
meat percentage which will intensify the broiler
breeder paradox. New feeding strategies are
being studied, but it is questionable if the paradox
can be solved by management tools alone. Since
breeding and selection are long-term processes,
involving animals, farmers, consumers, industry,
environment…, a more sustainable breeding goal
needs to be determined by pluridisciplinarity and
an open debate between several actors in the
discussion. Using dwarf broiler breeder hens could
be one alternative, because dwarf hens combine a
relatively good reproductive fitness with ad libitum
feeding. Another possibility is to accept lower
broiler productivity by assigning economic values to
welfare and integrity-traits included in an extended
breeding goal.
World increase of consumption of animal
products is estimated at ± 7% per year between 2005
and 2015 and a similar increase is expected until
2025 or later. This is true for animal food production
in general and may be even more pronounced for
chicken meat production as this sector is growing
relatively faster than that of the other meat species.
At the top of the animal production pyramid, animal
breeding and reproduction play an influential role
on the animals that are available for food production
(Fabre technology platform, 2005). Genetic selection
has increased production levels and efficiency, but
animals that have been selected for high production
efficiency seem to be more at risk for behavioural,
physiological and immunological problems. Genetic
selection is often still a black box if we do not
understand the underlying physiological processes
and may lead to loss of homeostatic balance,
resulting in the occurrence of pathologies and
consequently in impaired welfare (Rauw et al.,
1998). Our efforts to breed for higher production
efficiency may raise concerns regarding both animal
welfare and animal integrity. The reflection on the
Area: Chicken Breeder and Broiler Production • August 08
1
XXIV
E. Decuypere et al.
ethical significance of breeding goals can help us
to evaluate these breeding goals according to their
potential to affect animal welfare and integrity
(Mepham, 1995). This may force us to recognize
our moral responsibility and to discuss the limits of
acceptability. Applied and practical ethics provide
us with tools and with a framework of values and
principles guiding our reflection.
Animal breeding has traditionally focused on
cumulative short-term genetic changes because
breeding goals were set in a purely economic
framework. As a consequence, animal breeding
may have and has led to unwanted side effects that
are in conflict with sustainable animal husbandry
(Olesen et al., 2000). To counteract some of the
negative effects, selection goals should not be only
expressed in terms of production efficiency, but also
in characteristics which are linked to the health and
welfare of the animals. Therefore, the concept of
‘robustness’ (Star et al., 2008) can be used. A broad
definition was already given by Kitano (2004): “the
maintenance of specific functionalities of the system
against perturbations, and it often requires the
system to change its mode of operation in a flexible
way”. Knap (2005) mentions robust pigs as “pigs that
combine high production potential with resilience
to external stressors, allowing for unproblematic
expression of high production potential in a wide
variety of environmental conditions”. From this,
one can conclude that the qualifying elements
in the definition of ‘robustness’ are: production
efficiency and functioning in a broad variability
of environmental conditions. This functioning
encompasses both physiological, behavioural and
immunological characteristics. Robust animals will
be less susceptible for disease stress and will recover
faster, if needed (better health). From a welfare
point of view, robustness as a selection goal should
lead to animals with ameliorated ‘coping abilities’,
leading to a better adaptation to the management
system. If the animals dispose of this flexibility,
their welfare is increased. Finally, also integrity is a
precondition for robustness. Decreasing or harming
the telos of an animal (Rollin, 1995) is not consistent
with robustness. Lack of integrity is the case in
broiler breeding and forms the heart of the broiler
breeder paradox.
Sustainable breeding, besides profitability,
also needs equilibrium between production level,
efficiency, and the physiology (which encompasses
welfare, behaviour, health, reproduction … in other
words the functioning of an animal). Therefore, more
knowledge about basic biology of selection traits
and their correlation is needed. A strong negative
2
Area: Chicken Breeder and Broiler Production • August 08
World´s Poultry Congress 5 - 9
August - 2012 • Salvador - Bahia - Brazil
relationship is observed between body weight and
reproductive efficiency in poultry, and the strength
of this relationship is evidenced by the existence of
two types of chickens of commercial significance
which show extreme opposites in body weight
and reproductive performance. Concomitant with
improvements in growth rate of broiler chickens,
the ability of meat-type parent stocks to reproduce
has been severely reduced. Nevertheless, parents of
meat-type poultry must not only have the genetic
potential to exhibit fast and efficient meat growth,
but also be capable of reproducing.
It is well known that broiler breeders require
dedicated programs of feed restriction to maximize
egg and chick production (Costa, 1981). The
application of the restriction program in practice
implicates at the same time the importance of carryover effects of a specific feeding level during growth
on the development of the reproduction axis. The
emphasis for improving reproductive performance
of broiler breeders has always been more on
management than on genetic improvements. This
is linked with the low percentage of energy cost
for the breeder population in the total efficiency
of feed energy for broiler meat production,
including slaughter and breeder generation. Since
feed restriction during rearing of broiler breeders
is the most important management tool to avoid
metabolic disturbances and mortality in broiler
breeder rearing as well as to reach an acceptable
level of egg laying afterwards, it follows that the
“solution” for the problem namely the “fast growth
versus
reproduction-health”-paradox
induces
another: “acceptable reproduction – health versus
hunger-stress – impaired welfare”. Any sustainable
solution of the paradox as outlined here should
be based on a better understanding of the impact
of severeness and timing of feed restriction on
performance parameters such as growth, feed
efficiency, and reproductive performance, health
and welfare. Therefore, the physiology of the
nutrition-dependent reproductive ability of broiler
breeders needs to be better understood and will
be discussed in the third part. Finally, elements
discussed above will be reconsidered in the broader
framework and suggestions for solutions or further
debate and analysis will be given.
The broader framework
Sustainable animal production
In the evolution of animal production systems
since mankind has domesticated some animal
species for his own use and benefit, four phases are
XXIV
World´s Poultry Congress 5 - 9
August - 2012 • Salvador - Bahia - Brazil
distinguished by Olesen et al., (2000), starting with
“pioneering” (subsistence husbandry) followed
by “production” (maximalization of products),
“productivity” (optimization of production) and
“persistency” (the idea of sustainable production,
starting around 1970). Two aspects of philosophy
are important in our understanding of these different
perspectives or phases: the ontology, our belief
about what nature is and this can be approached in a
reductionistic or holistic way. The other aspect is the
epistemology, how we try to learn about nature or
our ways to analyze things and this can be done in a
rather subjective or objective way. The combination
of these two perspectives with both approaches
results in four categories of worldviews, including
our views about agriculture and animal production:
a cultural-social, an ecological, a personal-egocentric
and a technical worldview (Olesen et al., 2000).
Elements of sustainability as defined by Francis
and Callaway (1993) include profitability, resource
efficiency, productivity, environmental soundness
and social viability.
According to Sriskandarajah and Bawden
(1994), functional integrity has philosophical
priority over a resource sufficiency approach; the
latter favours a status quo, even if quality of life is
deteriorating, while analyzing livestock production
in terms of functional integrity enhances discussion
about priorities to give (e.g. productivity, resource
efficiency, vs. animal welfare and integrity).
Animal integrity goes beyond that of concern for
health or welfare. One of the observed differences
between both is that welfare can be affected not
only by humans but by natural circumstances
as well. In contrast, human action is required to
affect integrity, and thus integrity demands human
respect. It is defined as the intrinsic value of animals,
e.g. a naturally evolved, unharmed wholeness of an
individual, a species or a breed; therefore it is more
a philosophical than an empirical issue (Christiansen
and Sandoe, 2000).
In this context, broiler breeders are not naturally
evolved or unharmed as a population (individuals)
since, as a consequence of selection, they show
abnormalities and a high mortality rate, even before
attaining sexual maturity, when fed ad libitum. In
other words, broiler breeders seem to be reduced
to mere instruments for human interest: the
production of eggs and chicks with a genetic high
growth potential. In order to achieve this, their own
growth must be extremely reduced by severe feed
restriction, the severity of which having been ever
increased over the last decades (Robinson et al.,
2007). Therefore, this may be considered a violation
of animal integrity.
E. Decuypere et al.
Because of the often conflicting elements, it is
critical to weigh and give priorities to the different
objectives in the term; moreover it is clear that such
a definition of a sustainable animal production
system is based on a holistic philosophy, but this
can be approached methodologically in two ways
as pointed out by Thompson and Nardone (1994)
and Christiansen and Sandoe (2000): a resource
sufficiency or a functional integrity approach:
• The former relies to a large extent on inputs
and outputs and belongs to the evolutionary
phase of productivity (the mainstream view
of those involved in the animal husbandry
sector until now); it is more informed by an
objective epistemology and an ontology of
reductionism.
• The latter is focused more on long-term
“health” of a whole system and more
informed by a subjective epistemology and
an ontology of holism.
concepts; for example, it is too often assumed that
animal welfare can be measured objectively and
these measurements rely too much on physiological,
immune or behavioural measures that are often not
adequately validated (Rushen, 2003). This attitude
however countered the defensive tactic of asserting
that concerns about animal welfare were purely
“emotional” or anthropomorphic (Fraser, 1995).
Nevertheless, we will need more specific welfare
indicators to assess each type of specific challenge,
whether it is a housing, breeding, nutritional or
stockmanship challenge; there is no such thing as
a golden standard to measure objectively welfare in
general.
As a conclusion, weighing concerns against each
other implicates that all “parties” involved (being
animals, farmers, consumers, industry, environment
...) should be considered for a particular breeding
goal. Even though the policy that no harm to animals
must be done unless necessary, and the harm
must be outweighed by the benefits, balancing
good against bad, is an utilitarian approach, it is
recognizing that animals have intrinsic value and are
not purely instrumental to man (Brom and Schroten,
1993).
Animal welfare and integrity
Both animal welfare and integrity are hard to
define as a concept and moreover are changing
The risks and implications of a certain breeding
program must be assessed beforehand, based
Area: Chicken Breeder and Broiler Production • August 08
3
XXIV
on available scientific knowledge. However, the
overall interpretation and the priority we attach to
implications will be determined by our own ethical
view, by what we understand as the meaning of
animal welfare and/or integrity, by what we consider
good reasons, by how we weigh the interests of
animals against those of human beings (Sandøe and
Holtuy, 1998).
The genetic point of view
E. Decuypere et al.
Occurrence of negative correlation
between growth and reproduction
In domestic poultry, a strong negative relationship
is observed between body weight and reproductive
effectiveness. The strength of this relationship
is evidenced by the existence of two types of
chickens of commercial significance that show
extreme opposites in body weight and reproductive
performance: broiler type and layer type chickens.
Also empirical data further corroborate this negative
relationship between selection for fast meat growth
and reproduction, e.g. characterized as the ratio of
percentage daily production of normal eggs over
percentage of daily ovulation, DP/DO (Rauw et al.,
1998). This ratio was 0,84 for a high weight line
and 0,98 for a low weight line, and this was also
reported for other weight divergent lines (Jaap and
Muir, 1968; Antony et al., 1989; Liu et al., 1995).
The percentage of chromosomal abnormalities was
higher in a high body weight line (14,5%) versus a
low body weight line (6,2%) (Reddy and Siegel, 1977)
and consequently hatch of fertile eggs decreased.
Reproductive effectiveness can be characterized
by a combination of phenotypes including egg
production, libido, sperm and oocyte quality, sperm
storage by the hen, gamete-gamete interactions,
genetic compatibility and hatchability, not to
mention the potential interactions among the
phenotypes (Decuypere et al., 2003). Regardless
of mechanism, the ability of meat-type parent
stocks to reproduce has been severely reduced. It
may however be mentioned here that inconsistent
results as for effects of selection for body weight
on male sperm characteristics have been obtained
(Siegel, 1963; Marini and Goodman, 1969; Edens et
al., 1973; Nestor, 1977).
Biological explanation for the occurrence
of this negative genetic correlation
This question has been addressed for more than
half a century and Lerner (1954) puts forward the
theory of genetic homeostasis. Heterozygosity,
stabilizing selection and negative genetic correlations
4
Area: Chicken Breeder and Broiler Production • August 08
World´s Poultry Congress 5 - 9
August - 2012 • Salvador - Bahia - Brazil
will all result in intermediate optima in order to
maintain homeostasis, in other words maintain
additive variance which acts as a buffering effect to
a wide range of environments at a population level.
The competition for resources by two characters
may result in negative genetic correlations (Rendel,
1963) and this led to the “Resource Allocation
Theory” (Goddard and Beilharz, 1977). If the
responses are limited, fitness will decrease with
an increased allocation of resources to a particular
trait of fitness; in order to maximize fitness (health,
reproductive longevity ...) an optimal partitioning of
resources is accomplished by allocating intermediate
proportions to the different traits contributing
to fitness. As experienced in broiler breeders,
undesirable side effects may and will increasingly
appear with ongoing selection for growth and feed
efficiency of broilers. Therefore, broiler and broiler
breeder selection may be considered as a forerunner
for similar problems in other species. With selection,
the “optimal” situation is shifted towards high
(growth, meat) production and fewer resources are
left to respond adequately to other demands (Rauw
et al., 1998). Therefore, the breeding goal has to be
redefined into a broader perspective or alternatively
the resource situation has to be increased, if possible.
Why these rather unidirectional selection
goals in broiler production?
Poultry breeding is a competitive business
and success in poultry breeding business not only
depends on efficient pedigree programmes in
order to maximize annual genetic gains or efficient
multiplication of the commercial products, but
also on defining the correct or right breeding goal.
Its definition is an essential starting point for any
successful breeding programme (Emmerson, 2003).
For long, the ultimate measure of performance for
poultry meat output was the meat output per chick,
but since the early 1990’s, it has become clear that
meat output per breeder animal has become a
dominant indicator of success (e.g. Pollock, 1999),
an indication that both growth and reproduction
are important. The meat output per breeder is
composed of at least three parameters: 1) growth
of the broiler, 2) feed conversion of the broiler and
3) breeder effectiveness.
Any assessment of the efficiency of feed energy
utilisation for growth in meat animals must consider
not only the feed conversion in the slaughter
generation, but also the cost of maintaining an
effective breeder population. In prolific species such
as poultry, the majority of feed is consumed by the
slaughter generation (approximately 95% vs. 5%
for the breeder generation). Therefore, selection
XXIV
World´s Poultry Congress 5 - 9
August - 2012 • Salvador - Bahia - Brazil
goals will be directed predominantly towards traits
that favour growth, feed conversion efficiency and
carcass quality in the slaughter generation, with
much less emphasis on reproductive traits of the
breeder (Decuypere et al., 2003). In slow-reproducing
species such as cows, the metabolizable energy (ME)
intake is distributed approximately equally between
breeder and slaughter generations and therefore
it is theoretically as profitable to manipulate traits
relating to the efficiency of the breeding cow as it
is to manipulate growth in the slaughter animals
(Webster, 1989). The rather low impact of breeding
for broiler breeder reproductive efficiency, linked
with the low percentage of energy cost for the
breeder population in total efficiency of feed energy
for broiler meat production (including slaughter and
breeder generation) was also calculated in terms of
profitability by Emmerson (2003).
Of course these figures are market and price
dependant and they will also change with market
weight of the broiler: as this increases, the relative
contribution of day-old chick cost, and hence of
egg production by the breeder and hatchability will
decrease. In the content Emmerson (2003) describes,
the broiler day-old chick cost is about 20% of a
broiler at slaughter age at a body weight of 1,8 kg
and 12,5% of a broiler at body weight of 3 kg. From
foregoing it is clear that breeding goals in the broiler
industry have focussed and will continue to focus
on growth, carcass quality and feed efficiency and
much less, if at all, on reproductive efficiency.
Therefore, improvement of reproductive
performance of broiler breeders has been focussed
more on management than on genetic improvement
and empirically it is well known that broiler breeders
require dedicated programmes of feed restriction to
maximize egg and chick production. This of course
is at the heart of the broiler breeder paradox: the
apparent impossibility of reconciling production
requirements (good reproductive performance,
good health and low mortality of the female broiler
breeder; satisfactory growth and performance
of the offspring) without recourse to severe feed
Importance of defining breeding goals for
broiler breeders
Defining breeding goals is an essential starting
point for any successful breeding programme
(Emmerson, 2003). Moreover, breeding goals
become increasingly a blend of economics,
consumer preferences and social concerns (including
ethical concerns) and therefore these goals
become diversified and increase in number. One
consequence of this evolution is that correlations
between traits associated with breeding goals must
be considered; if genetic correlations between traits
are positive and high, economic considerations
will not compete markedly with selection for traits
relevant for welfare or ethics, at most it will slow
down a bit the speed of genetic improvement for
single production related traits. However, traits
will compete with each other if genetic correlation
is low or even negative and this will slow down
significantly the overall achieved genetic gain (Mills
and Beilharz, 1997). Although it is difficult to assign
an economic value to considerations such as welfare
and integrity, breeders will be expected (or forced?)
to define them in terms of production if it has to be
taken into account in breeding plans.
A second consequence is the diversity of this
broader economic, socio-cultural and ethical
framework and the differences between regions
or continents. In view of the internationalisation
of poultry breeding companies (and also for other
production animal species) and their worldwide
trade, differentiation in breeding goals is the logical
consequence and at the same time diversity is a
goal on itself for maintenance of genetic variability.
The possible genotype x environment interactions
worldwide, as well as the uncertainty and associated
risks about future circumstances, are incentives
to differentiate between breeding goals and to
maintain different breeding stocks (Olesen et al.,
2000). Moreover, establishment of breeding goals
is a process that must be regularly reviewed and reevaluated which creates on its turn opportunities to
include also some of the more “ethical oriented”
aspects in these goals (Emmerson, 2003).
E. Decuypere et al.
Indeed, in an integrated broiler breeder-broiler
business, the percentage of improvement in profit
resulting from a 1% improvement in the following
trait performances was:
• For egg production of the breeders: 0,23
• For hatchability in the hatchery:
0,46
• For broiler weight:
0,32
• For broiler mortality:
0,42
• For feed conversion:
1,31
• For breast meat percentage:
3,10
restriction (Decuypere et al., 2006; Renema et al.,
2007; Zuidhof et al., 2007). The idea that both
ad libitum and heavily restricted broiler breeders
have impaired welfare, but for different reasons,
constitutes the welfare/welfare paradox.
However, coming back to the heart of the
broiler breeder paradox, in broiler selection for
increased growth and feed efficiency, the welfare
of broiler breeders has been questioned in light
Area: Chicken Breeder and Broiler Production • August 08
5
XXIV
E. Decuypere et al.
of the severity of food restriction increasing every
year, with a proportional increase in growth
performances of the progeny obtained by genetic
selection (Karunajeewa, 1987). Physiological stress
is associated with restricted feeding on the one
hand and the excessive body weight for ad libitumfed broiler breeders on the other hand. Both are
questionable according to several welfare parameters
(Hocking et al., 1993). Unrestricted animals are
overweight and display several pathologies, leading
to unnecessary suffering and/or death. Although
severe feed restriction prevents these syndromes,
thereby improving welfare, it has been said that feed
restriction is cruel because animals cannot eat to
satisfy their hunger. The dilemma facing the broiler
breeder industry is thus a production/welfare and
welfare/welfare paradox. There is a need to balance
those problems inherent to excess intake against
those that accompany severe feed restriction.
Before changing selection goals or finding new
strategies in management for an altered balance as
mentioned above, the fundamental question is if
there is any causal or functional link between fast
growth and extreme lean tissue growth potential
on the one hand versus reproductive effectiveness
of the broiler breeder on the other hand. So, from
a genetic perspective, this question can be phrased
in the context of the genetic and phenotypic
correlations among the phenotypes. Therefore,
a next paragraph will discuss this dilemma from a
functional or physiological point of view
The physiological point of
view
The control of growth rate in broiler breeders
is one of the most important management tools,
together and interacting with light simulation,
to ensure the best reproductive performance
(Decuypere et al., 2003; Bruggeman et al., 2010).
In females, three key points are essential. First, the
rate of growth must be predetermined so that the
desired body weight is attained a few weeks before
onset of lay. The desired body weight is established
by giving the birds a certain amount of feed, which
is at some ages up to 70% restriction compared to
their unrestricted counterparts.
Second, it is important to synchronize growth
and sexual maturity. Reaching sexual maturity is not
accomplished just by gaining weight, but also body
fat (Bornstein et al., 1984), body fat-free mass or lean
body mass (Soller et al., 1984), photoperiod (Costa,
6
Area: Chicken Breeder and Broiler Production • August 08
World´s Poultry Congress 5 - 9
August - 2012 • Salvador - Bahia - Brazil
1981) and age (Brody et al., 1984) are important
factors. Katanbaf et al., (1989) observed that fullfed broiler breeders are dependent upon reaching a
critical age to start laying, while feed-restricted hens
are dependent upon attaining a critical body weight
and carcass fat stores. Yu et al., (1992 a, b) suggested
that feed intake and changes in body composition
(minimum fat level) during the pre-breeding period
are the most important factors in the determination
of the age of sexual maturity in broiler breeders. A
further reduction in fat content as expected by a
further selection for FCR (feed conversion ratio) may
therefore result in later maturity of breeder hens,
because the required body composition for sexual
maturity is not reached at an acceptable age. This
may even be aggravated because of the need for
a more severe feed restriction in breeders selected
for fast growth, so that both selection for leanness
and more stringent feed restriction act together to
delay the minimal fat stores needed to reach sexual
maturity.
The third essential key point in females, an
accurate feeding based on production rate, is
necessary at the start of and throughout the laying
period. Not only the level, but also the timing and
duration of severe feed restriction during rearing
could be important in controlling reproductive
performance in later life of the broiler breeders.
Results from Bruggeman et al., (1999) have shown
the existence of critical periods during rearing in
which feeding levels have repercussions on different
reproductive parameters (e.g. restriction from week
2 – 15 for delaying age at first egg, from week 7 –
15 for increasing total and servable egg production,
from week 2 – 6 for decreasing egg weight, from
week 16 – 24 for decreasing multiple follicles sets at
age of first egg).
Male broiler breeders that have a very high
growth potential also have to follow prescribed
growth curves, taking into account the size and
maturity of the females at the age of sexual maturity
in order to optimize mating and to reduce aggressive
behaviour towards the females. A lower crude
protein (12% vs. 17%) during rearing of males from
2 – 26 weeks (which occurs separately from the
females) improved their fertility in reproductive life
(Romero-Sanchez et al., 2007a), and a slow male
feed program from 16 – 26 weeks of age not only
made them more efficient but also improved their
fertility in later life. Moreover it allowed an increasing
male feed allocation during the production period
which further improved fertility (Romero-Sanchez et
al., 2007b) and this was paralleled with an improved
broiler progeny performance. This suggests that the
XXIV
World´s Poultry Congress 5 - 9
August - 2012 • Salvador - Bahia - Brazil
males with the greatest genetic potential were not
adequately mating when feed allocation during the
production is not adequate and too low (RomeroSanchez et al., 2008).
Physiological effects of feed
restriction on reproduction
in female breeders
Besides these changes at the ovarian level,
changes in the concentrations and/or pulsatility of
luteinizing hormone (LH) and follicle-stimulating
hormone (FSH) may be important factors explaining
the alterations in follicular development and
ovulation between broiler breeders fed different
amounts of feed. Plasma LH/FSH ratio was increased
by restricted feeding (Bruggeman, 1998; Onagbesan
et al., 2006). Moreover, the sensitivity of the pituitary
to luteinising hormone releasing hormone (LHRH)
as well as to ovarian feedback factors (Hicroids)
is influenced by the nutritional level. After sexual
maturation and establishment of lay, the longterm feed-restricted animals showed the highest
responsiveness to both LHRH-A and ovarian factors,
compared to animals fed ad libitum (Decuypere et
al., 1999). It is possible that this increased sensitivity
at the hypothalamic-pituitary level in feed-restricted
animals may as well contribute to the difference
in laying performance between ad libitum-fed and
restricted broiler breeder females (Bruggeman et
al., 1998). However, the growth factors such as IGF
and BMP’s e.g. regulating the responsiveness of the
ovary to the effect of LH and FSH, are likely more
important in controlling rate of ovulation and laying
rate of the hen (Onagbesan et al., 2006; Wang and
Johnson, 1993).
E. Decuypere et al.
Reproductive processes in females are the
result of controlled interaction between the
hypothalamus-pituitary and the ovary, and are
influenced by environmental, selection or nutritional
effects (Decuypere et al., 1999). A well-described
effect of feed restriction in broiler breeder females
is the reduction of ovary weight, the number of
yellow follicles during lay, and the incidence of
erratic ovipositions, defective eggs and multiple
ovulations (Hocking et al., 1989; Hocking, 1993; Yu
et al., 1992). Unrestricted access to feed leads to
a low egg production rate and fewer suitable eggs
for incubation. This is evidence that the observed
disturbances in follicular growth, differentiation,
and ovulations in animals fed ad libitum could be
attributed to changes in the steroid-producing
capacity and in the sensitivity of the follicles to
locally produced growth factors in interaction with
each other and with gonadotrophins (Decuypere
et al., 1999; Onagbesan et al., 2006). There is now
overwhelming evidence that the avian ovary is a site
of production and action of several growth factors
that have also been implicated in the functioning
of the mammalian ovary. Several members of the
Insulin-like growth factor family (IGF), the Epidermal
growth factor family (EGF), the bone morphogenetic
protein system (BMP-BMPR), the Transforming
growth factor- family (TGF-α), Fibroblast growth
factors (FGF), the Tumour necrosis factor-α (TNFα) and others have been identified either in the
granulosa and/or their compartments of ovarian
follicles and in the embryonic and juvenile ovary
(reviewed by Onagbesan et al., 2009). From our
results (Decuypere et al., 2006; Onagbesan et
al., 1999, 2003, 2006) it became clear that for
both BMP’s and IGF’s, feed restriction enhances
the interaction between growth factors and
gonadotrophins for the production of ovarian
steroids as well as the proliferation of granulate
cells. The interaction may explain the differential
yellow follicle number and (partly) egg production
rate between restricted and ad libitum fed broiler
breeders. Granulosa cells from feed-satiated broiler
breeder hens appear susceptible to apoptosis and
follicles undergo follicular atresia and prolonged
retention of follicles within the hierarchy.
Hyperphagia, enhanced adiposity and increased
hepatic lipogenesis, lipogenic dysregulation and
changed endocrine signals may result in the
accumulation of excess triglycerides and fatty acids
in non-adipocytes, hence in lypotoxicity and ovarian
dysfunction and cell death (Chen et al., 2006).
Effect of broiler selection on the
physiology of reproduction in female
breeders
It was found in many experimental selection
models that obesity in hens was associated with
poor egg production (Leclercq et al., 1985; Cahaner
et al., 1986) and hatchability of eggs produced by
lean broiler breeders is higher than that of fat birds
(Cahaner et al., 1986). Although comparisons of
reproductive performances between fat and lean
adult breeder hens are reported in several papers,
a straightforward comparison between selection
strategies or even between different lines for similar
selection procedures is not easy in view of the
different feeding programmes used (Buyse et al.,
1999). Since lean and fat lines are characterized by a
different appetite, even as adult hens, comparisons
of reproductive traits under ad libitum feeding
conditions can be quite different from restricted
Area: Chicken Breeder and Broiler Production • August 08
7
XXIV
E. Decuypere et al.
conditions, and restriction conditions will be
differential for lean and fat lines if the restriction
is not imposed as a percentage of the ad libitum
uptake for both lines what is often not realised.
In a study of Onagbesan et al., (1999a), a growth
selected line (GL or fat line) and a feed conversion
selected line (FC or lean line) were reared under ad
libitum and restricted conditions (75% of the ad
libitum condition). The average number of yellow
follicles/ovary decreased, egg production increased
and atresia of yellow follicles decreased under
restricted feeding. The effects of restrictions were
more pronounced for the FC than for the GL-line.
Moreover, in vitro P4 (progesterone) production
of granulosa cells as a response to different doses
of LH showed no differences for F1 and F2 follicles
for ad libitum fed GL hens, while feed restriction
made them respond like the FC-line. The latter is
similar to laying hens where P4-production by F1granulosa cells is greater than that of F2-granulosa
cells. Similar observations were made for the effects
of several growth factors on granulosa cells from
both lines and feeding regimens. Taken together,
these data indicate that correlated responses in
reproductive abilities with selection for rapidly
growing and hence fat birds cannot simply be
explained in energetic or mechanistic terms. This
selection affects endocrine/paracrine mechanisms
that, at least partly, are involved in the selection
goals (N-retention and growth, protein and lipid
metabolism) but because of the multiple effects
of hormones and the interrelationship of these
hormonal parameters with other endocrine systems,
this may be the basis of a number of correlated
responses (Decuypere et al., 2003).
Concluding remarks and
suggestions for solutions
The foregoing discussion, firstly, leads to the main
concrete question: can the growth requirement of
broiler breeder hens be allied with good reproductive
performance, good health, and welfare, either by a
feed restriction programme which does not cause
undue hunger, or by innovative genetic selection?
Therefore, further breeding should consider not
only how to increase production and production
efficiency, but also how to alleviate correlated
side effects by extending or changing selection
goals for obvious economic reasons as well as for
the unacceptability of some correlated responses
to an increasing number of people. Whether the
8
Area: Chicken Breeder and Broiler Production • August 08
World´s Poultry Congress 5 - 9
August - 2012 • Salvador - Bahia - Brazil
selection goals have to be extended by additional
criteria or changed to settle for lower productivity
levels will depend on the answer to the questions
asked as to what extent the dilemmas discussed
here are merely hazards from a selection policy as
applied until now or are causally linked and hence
inevitable consequences of the applied selection
goals. More and more data in literature illustrate
that fast and efficient growth of the broilers and
efficient reproduction of the broiler breeder are
mutually exclusive selection goals, suggesting that
there is a causal negative biological relation. Indeed,
changes in growth related hormones or factors, as
a consequence of selection for fast and efficient
growth seem to be linked to changes of the same
growth factors in the ovary of broiler breeders,
resulting in gonadal dysfunction. If that is true, then
one has to make choices in future broiler breeder
management and/or breeding goals.
1. Intense selection of broilers can be continued
with the known consequences of the need for
severe feed restriction of the breeders. This
becomes difficult to defend when taking into
account the animal welfare policy in some
societies. New feeding regimens/diets more
adapted to the animals’ needs, by diminishing
the duration or the intensity of feed restriction
or by introducing diets with energy dilution are
suggested and have been studied. However, a
search for the optimal balance welfare/growth
and reproduction goals still needs further
investigations and it is questionable if it can be
reached at all just by management tools.
2. Changing selection goals in the broiler industry,
thereby diminishing the need for severe feed
restriction in breeders by selection, but without
deterioration of the quality demands of the
broiler. Introduction of the dwarf broiler breeder
hens, which seem to maintain a relatively good
reproductive fitness even with ad libitum feed
allowances during growth (Hocking et al.,
1987; Triyuwanta et al., 1992) could be such an
alternative. The presence of the sex-linked dwarf
gene (dw) may reduce the need for feed reduction
in the breeder while allowing the production of
fast-growing offspring because of its sex-linkage
and recessiveness. However, one has to bear in
mind that this divergent selection leads to an
unnatural biological situation in which natural
mating can become very difficult because of
the extreme size differences between male and
female. The production of broilers depends on
artificial insemination in such cases, as in the turkey
industry. From an ethical point of view, and in the
light of foregoing discussion about integrity, such
development can and will be questioned.
XXIV
World´s Poultry Congress 5 - 9
August - 2012 • Salvador - Bahia - Brazil
3. In view of the possible unavoidable mechanistic
link between selection for fast and efficient
growth of the broilers and reproductive and
welfare problems of broiler breeders, an
increasing pressure to settle for lower bird
productivity levels (in broilers) in order to reach
acceptable productivity that can be combined
with acceptable management systems in broiler
breeders will be the consequence. Introduction
of new genetic lines of broiler breeder females
that would tolerate ad libitum feeding could
be such a possibility. The production of slowergrowing label chickens (France), for example,
has led to a practice of mating a heavy broiler
cockerel with a slow-growing label breeder hen.
The resulting broiler reaches market weight 10 –
12 days later than a standard broiler.
as welfare/integrity should be realized as much
as possible. In both aspects also political leaders
have their responsibility as consensus builders and
value keepers in our society, what at least they are
expected to be.
Although breeding is a competitive business and
breeding decisions are economically driven, it is also
a society sensitive sector because it involves changes
in the appearance, behaviour and sometimes welfare
of the animals (Fabre technology platform, 2005).
It means that a balance of food safety, quality,
biodiversity, efficiency, animal health and welfare
should be reached and this in an economic viable
way. The broiler breeder and broiler sector could be
a forerunner for similar problems in other species,
but the primary breeders will have to develop novel
approaches to help provide sustainable solutions to
the problems as mentioned, and of course those
problems have first to be defined and then agreed
upon. Establishment of breeding goals is indeed an
ongoing process that must be regularly reviewed and
re-evaluated; this creates on its turn opportunities
to include also some of the more “ethical oriented”
aspects of these goals. Therefore, future research,
even in the broad field of animal sciences, must
become even more pluridisciplinary and focus on
developing an integrative understanding of the
lifetime functioning of whole animals and their
interrelationships with the environment, and regular
evaluation of these steps with breeding reality
(Sefabar, 2005).
BRODY, T., SIEGEL, P.B. and CHERRY, J.A. (1984) Age,
body weight and body composition requirements
for the onset of sexual maturity of dwarf and normal
chickens. British Poultry Science 25:245-252.
ANTHONY, N.B., DUNNINGTON, E.A. and SIEGEL, P.B.
(1989) Egg production and egg composition of
parental lines and F1 and F2 crosses of White Rock
chickens selected for 56-day body weight. Poultry
Science 68:27-36.
BORNSTEIN, S., PLAVNIK, I. and LEV, Y. (1984) Body
weight and/or fatness as potential determinants of
the onset of egg production in broiler breeder hens.
British Poultry Science 17:215-223.
BROM, F.W.A. and SCHROTEN, E. (1993) Ethical questions
around animal biotechnology: the Dutch approach.
Livestock Production Science 36(1):99-107.
BRUGGEMAN, V. (1998) The effect of level and timing
of feed restriction on growth and reproductive
characteristics and their endocrine control in broiler
breeder females. Ph. D. Thesis, K.U. Leuven, Belgium.
BRUGGEMAN, V., D’HONDT, E., BERGHMAN, L.,
ONAGBESAN, O., VANMONTFORT, D., VANDESANDE,
F. and DECUYPERE, E. (1998) The effect of food
intake from 2 to 24 weeks of age on LHRH-1 content
in the median eminence and gonadotrophin levels
in pituitary and plasma in female broiler breeder
chickens. General and Comparative Endocrinology
112:200-209.
E. Decuypere et al.
Because some of the issues, raised by this new
perception on breeding, are fundamentally ethical
in nature, both scientists (who are mostly oriented
towards very narrow questions) and ethicists
(who are oriented to very broad, fundamental
and theoretical questions) must direct research at
levels of analysis appropriate to the issues (Fraser,
2001). Polarisation of the debate has to be avoided
because this could prevent a real ethical analysis
of important issues and consensus building, and
assigning economic value to considerations such
References
BRUGGEMAN, V., ONAGBESAN, O., D’HONDT, E., BUYS,
N., SAFI, M., VANMONTFORT, D., BERGHMAN, L.,
VANDESANDE, F. and DECUYPERE, E. (1999) Effects
of timing and duration of feed restriction during
rearing on productive characteristics in broiler breeder
females. Poultry Science 78:1424-1434.
BRUGGEMAN, V., ONAGBASAN, O., WITTERS, A. and
DECUYPERE, E. (2010) Chickens: Broiler Reproduction
Management. In: TAYLOR and FRANCIS, (Eds)
Encyclopedia of Animal Sciences, 2nd ed., in press.
BUYSE, J., LEENSTRA, F.R., ZEMAN, M., RAHIMI, G.
and DECUYPERE, E. (1999). A comparative study of
different selection strategies to breed leaner meattype poultry. Poultry and Avian Biology Reviews
10:121-142.
CAHANER, A., NITZAN, Z. and NIR, I. (1986) Reproductive
performance of broiler lines divergently selected on
abdominal fat. Poultry Science 65:1236-1243.
CHEN, S.E., MC MURBRY, J.P. and WALZEM, R.L. (2006)
Overfeeding-induced ovarian dysfunction in broiler
breeder hens is associated with lipotoxity. Poultry
Area: Chicken Breeder and Broiler Production • August 08
9
XXIV
Science 85:70-81.
CHRISTIANSEN, S.B. and SANDOE, P. (2000) Bioethics:
limits to the interference with life. Animal Reproduction
Science 60-61:15-29.
COSTA, M.J. (1981) Fundamental principles of broiler
breeders nutrition and the design of feeding programs.
World’s Poultry Science Journal 37:177-192.
DECUYPERE, E., BRUGGEMAN, V., ONAGBESAN, O. and
SAFI, M. (1999) Endocrine physiology of reproduction
in the female chicken: old wine in new bottles.
Proceedings of the International Congress on Bird
Reproduction, Tours.
DECUYPERE, E., BRUGGEMAN, V., BARBATO, G.F. and
BUYSE, J. (2003) Growth and reproduction problems
associated with selection for increased broiler
meat production. “Poultry Genetics, Breeding and
Technology”, CABI-publishing, Wallingford.
DECUYPERE, E., HOCKING, P.M., TONA, K., ONAGBESAN, O.,
BRUGGEMAN, V., JONES, E. K. M., CASSY, S., RIDEAU,
N., METAYER, S., JEGO, Y., PUTTERFLAM, J., TESSERAUD,
S., COLLIN, A., DUCLOS, M., TREVIDY, J. J. and WILLIAMS,
J. (2006) Broiler breeder paradox: a project report. World’s
Poultry Science Journal 62:443-453.
E. Decuypere et al.
EDENS, F.W., VAN KREY, H.P. and SIEGEL, P.B. (1973).
Selection for body weight at eight weeks of age. 9.
Chickens spermatozoa respiration. Poultry Science
52:977-981.
EMMERSON, D. (2003) Breeding objectives and selection
strategies for broiler production. In: MUIR W. M. and
AGGREY S. E., (Eds) Poultry genetics, breeding &
biotechnology, CAB.
FABRE TECHNOLOGY PLATFORM (2005) Sustainable
Animal Breeding and Reproduction. A vision for 2025.
FRANCIS, C.A. and CALLAWAY, M.B. (1993) Crop
improvement for future farming systems. In:
CALLAWAY M. B. and FRANCIS C. A. (Eds.) Crop
improvement for sustainable agriculture, Univ.
Nebraska Press, Lincoln.
FRASER, D. (1995) Science, values and animal welfare:
exploring the inextricable connection. Animal Welfare
4:103-117.
FRASER, D. (2001) The ‘New Perception’ of animal
agriculture: legless cows, featherless chickens and a
need for genuine analysis. Journal of Animal Science
79:634-641.
GODDARD, M.E. and BEILHARZ, R.G. (1977) Natural
selection and animal breeding. Proceedings 3rd
International Congress S.A.B.R.A.O., Animal Breeding
Papers.
HOCKING, P.M. (1993) Effects of body weight at sexual
maturity and the degree and age of restriction during
rearing on the ovarian follicular hierarchy of broiler
breeder females. British Poultry Science 34:793-801.
HOCKING, P.M., WADDINGTON, D., WALKER, M.A. and
GILBERT, A.B. (1989) Control of the development of
the follicular hierarchy in broiler breeder pullets by
food restriction during rearing. British Poultry Science
30:161-174.
JAAP, R.G. and MUIR, F.V. (1968) Erratic oviposition and
10
Area: Chicken Breeder and Broiler Production • August 08
World´s Poultry Congress 5 - 9
August - 2012 • Salvador - Bahia - Brazil
egg defects in broiler-type pullets. Poultry Science
47:417-423.
KATANBAF, M.N., DUNNINGTON, E. A. and SIEGEL, P.B.
(1984) Restricted feeding in early and late-feathering
chickens. 2. Reproductive responses. Poultry Science
68:352-358.
KARUNAJEEWA, H. (1987). A review of current poultry
feeding systems and their potential acceptability to
animal welfarists. World’s Poultry Science Journal
43:20-32.
KITANO, H. (2004) Biological robustness. Nature Reviews
Genetics 5:826-837.
KNAP, P.W. (2005) Breeding robust pigs, Australian
journal of experimental agriculture 45:763-773.
LECLERCQ, B., KOVASSI-KOUAKOU, J. and SIMON, J.
(1985) Laying performance, egg composition and
glucose tolerance of genetically lean or fat meat-type
breeders. Poultry Science 64:1609-1616.
LERNER, I.M. (1954) Genetic homeostasis, John Wiley,
New York.
LIU, G., DUNNINGTON, E.A. and SIEGEL, P.B. (1995)
Correlated responses to long-term divergent selection
for eight-week body weight in chickens: growth,
sexual maturity and egg production. Poultry Science
74:1259-1268.
MARINNI, P.J. and GOODMAN, B.L. (1969) Semen
characteristics as influenced by selection for divergent
growth rate in chickens. Poultry Science 48:859-865.
MEPHAM, T.B. (1995) Ethical aspects of animal
biotechnology. Journal of the Agricultar Society 75:3-21.
MILLS, A.D. and BEILHARZ, R.G. (1997) “Genetic
selection”, In: APPLEBY M. C. and HUGHES B. O. (Eds)
Animal Welfare, CAB.
NESTOR, K.E. (1977) The influence of a genetic change
in egg production, body weight, fertility or response
to cold stress on semen yield in the turkey. Poultry
Science 56:421-425.
OLESEN, I., GROEN, A.F. and GJERDE, B. (2000) Definition
of animal breeding goals for sustainable production
systems. Journal of Animal Science 78:570-582.
ONAGBESAN, O., DECUYPERE, E., LEENSTRA, F. and
EHLHARDT, D.A. (1999a) Differential effects of amount
of feeding on cell proliferation and progesterone
production in response to gonadotrophins and insulinlike growth factors by ovarian granulose cells of broiler
breeder chickens selected for fatness or leanness.
Journal of Reproduction and Fertility 166:73-85.
ONAGBESAN, O., VLEUGELS, B., BUYS, N., BRUGGEMAN,
V., SAFI, M. and DECUYPERE, E. (1999b) Insulin-like
growth factors in the regulation of avian ovarian
functions. Domestic Animal Endocrinology 17:299313.
ONAGBESAN, O., BRUGGEMAN, V., VAN AS, P., TONA,
K., WILLIAMS, J. and DECUYPERE, E. (2003) BMPs
and BMPRs in the chicken ovary and the effects
of BMP-4 and -7 on granulose cell proliferation
and progesterone production in vitro. Journal of
Physiology, Endocrinology and Metabolism 285:973983.
XXIV
World´s Poultry Congress 5 - 9
August - 2012 • Salvador - Bahia - Brazil
ONAGBESAN, O., METAYER, S., TONA, K., WILLIAMS, J.,
DECUYPERE, E. and BRUGGEMAN, V. (2006) Effects
of genotype and feed allowance on plasma LH, FSH,
progesterone, estradiol levels, follicle differentiation
and egg production rates of broiler breeder hens.
Poultry Science 85:1245-1258.
ONAGBESAN, O., BRUGGEMAN, V. and DECUYPERE,
E. (2009) Intra-ovarian growth factors regulating
ovarian function in avian species: A review. Animal
Reproduction Science 111:121-140.
POLLOCK, D.L. (1999) A geneticist’s perspective from
within a broiler primary breeder company. Poultry
Science 78:414-418.
RAUW, W.M., KANIS, E., NOORDHUIZEN-STASSEN, E.W.
and GROMMERS, F. J. (1998) Undesirable side effects
of selection for high production efficiency. Livestock
Production Science 56:15-33.
REDDY, P.R.K. and SIEGEL, P.B. (1977) Chromosomal
abnormalities in chickens selected for high and low
body weight. Journal of Heredity 68:253-256.
RENDEL, J.M. (1963) Correlation between the number
of scutellar and abdominal bristles in Drosophila
melanogaster. Genetics 48:391-408.
RENEMA, R.A., ROBINSON, F.E. and ZUIDHOF, M.J.
(2007) Reproductive efficiency and metabolism of
female broiler breeders as affected by genotype, feed
allocation and age at photostimulation. 1. Sexual
maturation. Poultry Science 86:2267-2277.
ROLLIN, B.E. (1995) The Frankenstein Syndrome: Ethical
and social issues in the genetic engineering of animals.
Cambridge, NY, USA: Press syndicate.
SIEGEL, P.B. (1963) Selection for body weight at eight
weeks of age. 2. Correlated responses of feathering,
body weights and reproductive characteristics. Poultry
Science 42:896-905.
SOLLER, M., EITAN, Y. and BRODY, T. (1984) Effect of diet
and early quantitative feed restriction on the minimum
weight requirement for the onset of sexual maturity in
White Rock broiler breeders. Poultry Science 63:12551261.
SRISKANDARAJAH, N. and BAWDEN, R. (1994) Farming
as a human activity: An alternative world view.
Seminars on Achieving Results by Cooperation Within
Environmental Protection and Agriculture, Kookola,
Finland.
STAR, L., ELLEN, D., UITDEHAAG, K. and BROM, F.W.A.
(2007) A plea to implement robustness into a breeding
goal: poultry as an example. Journal of Agricultural
and Environmental Ethics 21:109-125.
THOMPSON, P.B. and NARDONE, A. (1999) Sustainable
livestock production: methodological and ethical
challenges. Livestock Production Science 61:111-119.
TRIYUWANTA, A., LETERRIER, C., BRILLARD, J.P. and NYS,
Y. (1992) Maternal body weight and feed allowance of
breeders affect performance of dwarf broiler breeders
and tibial ossification of their progeny. Poultry Science
71:244-254.
WANG, S.Y. and JOHNSON, P.A. (1993) Increase in
ovarian alpha-inhibin gene expression and plasma
immunoreactive inhibin level is correlated with a
decrease in ovulation rate in domestic hen. General
and Comparative Endocrinology 91:52-58.
WEBSTER, A. J. F. (1989) Bio-energetics, bio-engineering
and growth. Animal Production 48:249-269.
ROMERO-SANCHEZ, H., PLUMSTEAD, P.W. and BRAKE,
J. (2007a) Feeding broiler breeder males. 1. Effect of
feeding program and dietary crude protein during
rearing on body weight and fertility of broiler breeder
males. Poultry Science 86:168-174.
YU, M.W., ROBINSON, F.E., CHARLES, R.G. and
WEINGARDT, R. (1992a) Effect of feed allowance
during rearing and breeding on female broiler
breeders. 2. Ovarian morphology and production.
Poultry Science 71:1750-1761.
ROMERO-SANCHEZ, H., PLUMSTEAD, P.W. and BRAKE,
J. (2007b) Feeding broiler breeder males. 3. Effect
of feed allocation program from sixteen to twentysix weeks and subsequent feed increments during
the production period on body weight and fertility.
Poultry Science 86:775-781.
YU, M.W., ROBINSON, F.E. and ETCHES, R.J. (1992b)
Effect of feed allowance during rearing and breeding
on female broiler breeders. 2. Ovarian steroidogenesis.
Poultry Science 71:1762-1767.
ROMERO-SANCHEZ, H., PLUMSTEAD, P.W., LEKSISOMPONY,
N., BRANNAN, K.E. and BRAKE, J. (2008) Feeding broiler
breeder males. 4. Deficient feed allocation reduces
fertility and broiler progeny body weight. Poultry
Science 87:805-816.
E. Decuypere et al.
ROBINSON, F.E., ZUIDHOF, M.J. and RENEMA, R.A. (2007)
Reproductive efficiency and metabolism of female
broiler breeders as affected by genotype, feed allocation
and age at photostimulation. 1. Pullet growth and
development. Poultry Science 86:2256-2266.
Suppl., 29:51-58.
SEFABAR (2005) Code of Good Practice for Farm Animal
Breeding Organisations. Version 2005.
ZUIDHOF, J.M., RENEMA, R.A. and ROBINSON, F.E.
(2007) Reproductive efficiency and metabolism of
female broiler breeders as affected by genotype,
feed allocation and age at photostimulation. 1.
Reproductive efficiency. Poultry Science 86:22782286.
RUSHEN, J. (2003) Changing concepts of farm animal
welfare: bridging the gap between applied and basic
research. Applied Animal Behaviour Science 81:199214.
SANDØE, P. and HOLTUY, N. (1998) Ethical aspects
of biotechnology in farm animal production. Acta
Agriculturae Scandinavica, Section A - Animal Science
Area: Chicken Breeder and Broiler Production • August 08
11