Explore

Communities in English

Advertise on Engormix

Optimizing nutrition in the rearing period: overview of the latest research

Published: March 19, 2019
By: Dr. R.A. van Emous / Wageningen Livestock Research, PO box 338, 6700 AH Wageningen, The Netherlands.
Summary

Nowadays, management issues in broiler breeders associated with nutrition and reproductive characteristics, are becoming increasingly challenging. Due to genetic selection on broilers, body composition of breeders has changed dramatically during the last 50 years to less fat and more breast muscle. Both male and female broiler breeders of these fast growing strains need to be fed restricted, both in the rearing and the production period, although the restriction level is most severe between 6 and 16 weeks of age. Feeding programmes as skip-a-day are applied as these should improve flock uniformity, however, recent research shows that every day feeding benefits on reproduction and welfare. Besides an improved uniformity, floor feeding also plays a positive role in immunity. It is postulated that a certain amount of body fat in broiler breeders at the onset of lay is necessary for maximum performance. Body composition of breeders can be influenced by different feed allowances during rearing, as well as by changes in nutrient composition of the diet. It can be concluded that feeding a low protein diet during rearing decreased breast muscle and increased abdominal fat pad. The higher abdominal fat pad content resulted in an increased hatchability during the first phase of lay and a larger number of eggs during the second phase of lay. On the other hand, a low daily protein intake during the rearing and first phase of lay can lead to a poor feather cover.

Introduction
The basis of the modern poultry meat industry dates back to the late 1950s and nowadays, poultry meat is one of the most important protein sources in human diet. Global poultry meat production in 2000 was 69 million tons and this has been increased to over 97 million tons in 2010 (Windhorst, 2011): an annual production of approximately 70 billion broilers originating from approximately 600 million broiler breeders. These data underline how a relatively small number of parent stock can have a major impact on following links in the poultry meat chain. The impressive growth of the poultry meat industry is supported by improvements in health, nutrition and environmental management (McKay, 2009). However, the major changes in broiler production can be attributed to genetic improvement of the birds as shown by Havenstein et al. (2003a,b). They estimated that the 6 fold increase in carcass yield, measured in a 2001 strain fed a 2001 diet compared to a 1957 strain fed a 1957 diet, was 85-90% due to genetics and 10-15% due to nutrition. This selection on growth efficiency is the result of decades of intensive genetic selection of broilers and consequently also broiler breeders. For example, ad libitum-fed standard broiler breeder pullets, from 11 to 24 wk of age, consumed 30% more feed compared to restricted fed pullets, resulting in a dramatic increase (5.4 vs. 2.2 kg) of BW and decreased reproductive performance (Heck et al., 2004). Ad libitum feeding compared to a restricted feed intake, can lead to a high mortality, decreased egg quality, lower peak production and lower egg production (Heck et al., 2004).
Modern-day broilers have approximately 9% more breast muscle, whereas the total fat percentage is approximately 7% lower than broilers 30 yr ago (de Beer, 2009). The results of selection, changed body composition of broilers and led to major changes in the growth potential of these birds (Havenstein et al., 2003a,b; Renema et al., 2007b). Not only have feed conversion ratio, growth rate, and body composition of broilers changed, but also of broiler breeders. At the onset of lay, modern broiler breeders have less fat and more breast muscle than a few decades ago, resulting in a delay of maturity (Decuypere et al., 2010). More breast muscle has resulted in an increased energy requirement to maintain this metabolically active tissue (de Beer, 2009). Some researchers suggest that a certain percentage of body fat in broiler breeders at the onset of lay is necessary for an adequate reproductive performance (Bornstein et al., 1984; Sun and Coon, 2005; de Beer, 2009; Mba et al., 2010). Yu et al. (1992a,b) hypothesized that a sufficient feed allowance and a minimum body fat content during the prebreeding period are important to promote sexual maturity in broiler breeders. Body composition can be affected by the use of different feed allowances during rearing (Fattori et al., 1993; Renema et al., 2001a; Robinson et al., 2007). On the other hand, body composition can also be influenced by differences in diet composition. Different energy or protein levels may affect the fat content of the breeder during rearing (Miles et al., 1997; Hudson et al., 2000) or laying (Pearson and Herron, 1981; Spratt and Leeson, 1987). Recently, Mba et al. (2010) showed that a low dietary protein level during rearing increased abdominal fat and decreased breast muscle of pullets at the onset of lay.
The main goal in broiler breeder production is to provide fertilized eggs to produce a maximum number of healthy and robust day-old broilers chicks (Zuidhof, et al., 2007). Important in relation to the management of adult breeders is maintaining the health status of the flock while keeping the egg production at a high level. Major criteria for monitoring birds for management purposes include body weight, body condition, egg production and hatching, hatchability and infertility, and egg weight (Leeson and Summers, 2000). In the rearing period, that comprises the age between 0 and 18-22 weeks, broiler breeder pullets are prepared for the production phase. The aim of the rearing period is to produce birds of ideal weight, uniformity, condition and stage of sexual maturity when they enter the production house (Leeson and Summers, 2000). Body weight and flock uniformity are important production indicators during the rearing period (Zuidhof et al., 2015).
Therefore, the overall objective of the present presentation is to give an overview of the research on the effects of nutrition during the rearing period on body composition, performance and behaviour.
 
Restricted feeding
Over the past 30 years, the growth potential of commercial broilers increased drastically (Renema et al., 2007b). Modern broiler strains grow 4.6 times the rate of a 1957 strain (Havenstein et al., 2003b). According to Havenstein (2003a) the 6 fold increase in carcass yield in 2001 stocks fed a 2001 diet compared to 1957 stocks fed a 1957 diet is 85-90% due to genetics, and 10-15% due to nutritional changes. This extreme increase in carcass yield is the result of increased growth potential of the broiler breeders. Ad libitum fed standard broiler breeder chicks consumed from 11 to 24 wk of age 48 g/d more feed (210 vs. 162 g/d) compared to restricted fed chicks, resulting in a dramatically increase (5.4 vs. 2.2 kg) of BW (Heck et al., 2004). As a result of this increased growth potential, to prevent serious health problems and to maintain a good production of eggs and chicks, broiler breeders have to be fed restrictedly at a young age. Over the past 30 years, broiler breeder BW targets have undergone change, although the degree of change is small compared to the large increases in growth potential. As a consequence, the ratio in BW between broiler breeders to broilers at 6 wk of age in female Hubbard birds decreased over the period from 1979 to 2005 from 52% to 27% (Renema et al., 2007). To realize target weights, the degree of feed restriction for maintaining broiler breeder BW targets had to be continuously increased.
Decades of selection for meat production traits have impaired the reproductive abilities of broiler breeders (Siegel and Dunnington, 1985). Ad libitum feeding of broiler breeders results in a low egg production which has been associated with multiple ovulations caused by the presence of more than one hierarchy of ovarian yellow follicles during early lay (Hocking et al., 1989). Feed intake during rearing and body weight at sexual maturity seem directly correlated with the number of yellow follicles in the ovary (Hocking, 1993). Therefore, feed restriction is necessary to obtain an acceptable reproductive performance in broiler breeders. Heck et al. (2004) compared ad libitum and restricted fed broiler breeders. Restricted feeding delayed sexual maturity by 6 weeks and the peak of lay by 7 to 8 weeks. The maximal laying rates, however, were 83.3% for restricted fed hens, versus 57% for ad libitum fed hens. The restricted fed birds showed a good persistency, whereas the rate of lay of the ad libitum fed group rapidly decreased to only 20 to 25% after peak production. A significantly higher proportion of eggs were laid with multiple-yolk, soft or broken shells by the ad libitum fed hens than by the restricted-fed hens, resulting in a reduced percentage of settable eggs in the former group. Mortality was dramatically increased to 40.4% in the ad libitum fed hens versus 5.6% in the restricted fed hens.
Already in the early ‘90s researchers described the effect of the restricted feeding program in broiler breeders on the welfare of the birds. Restricted fed broiler breeders show behavioural signs of stress and frustration, i.e. redirected oral behaviours resulting in stereotypic object pecking (and if directed at the drinker resulting in overdrinking), hyperactivity, pacing (stereotypic walking) (de Jong, et al., 2002; Hocking, 1993; Hocking et al., 1993; Hocking, et al., 1996; Savory and Maros, 1993; Savory, et al., 1993; Savory, et al., 1992; Savory, et al., 1996), increased aggression (Jones, et al., 2004) and increased feeding motivation (Savory and Lariviere, 2000). It has also been reported that physiological indicators of (chronic) stress were observed, such as increased plasma corticosterone levels and increased heterophil:lymphocyte ratios in the blood (de Jong, et al., 2003; Hocking, 1993; Hocking et al., 1996; Savory and Mann, 1997).
During the first 2 to 3 weeks of the rearing period, feed is provided unrestricted and thereafter a restricted feeding program is started. The period in which the most severe restriction is applied starts around 6-7 weeks of age and runs to 15-16 weeks of age (de Jong and Jones, 2006). Restriction levels were estimated to be 25-33% of the intake of ad libitum fed broiler breeders (de Jong et al., 2002) but there are no recent data on relative restriction level. It can be expected that due to the continuing selection for efficient growth of the progeny the relative restriction level has even been increased since then (Zuidhof, et al., 2014). It is calculated by van Emous (nonpublished data) that feed restriction level is increased to around 75 to 80% between by the end of the rearing period, from 16 weeks of age onwards, the daily feed allowance slightly increases to prepare the birds for the production period. Also during the production period restricted feeding is applied, but restriction levels are much less severe as compared to the rearing period. Restriction levels of 45-80 % of the ad libitum intake are applied until the peak of lay (Bruggeman, et al., 1999) and restriction levels to about 80 % of ad libitum intake are applied after peak of lay (Hocking, et al., 2002), although also here no recent data are available.
 
Feeding programmes rearing
Although in Europe daily feeding is commonly applied, in North America skip-a-day feeding programmes are applied as these should improve flock uniformity (de Beer and Coon, 2007). Feed restriction basically consists of adjusting the amount of feed consumed by broiler breeder pullets during rearing and production in order to avoid obesity, high mortality and other problems derived from ad libitum feeding. Parent stock of fast growing broiler chickens is subjected to feed restriction during the rearing period (e.g., de Jong and Guemene, 2011; EFSA, 2010). Also, water provision may be restricted (Hocking, et al., 1993). Feed can be either provided daily or a skip-a-day feeding regime may be applied (EFSA, 2010). Skip-a-day feeding regimes can be in the form of 6/1, 5/2 or 4/3 feeding programmes (1, 2 or 3 days without feed each week and a larger portion on the feeding days). In Europe, usually, daily feeding is applied as legislation does not allow skip-a-day feeding programmes.
Research of de Beer and Coon (2007), Montiel (2016) and Zuidhof et al. (2015) showed new insights into the effects of every day (ED) feeding. De Beer and Coon (2007) compared four different feeding programmes (SAD, 4-3, 5-2, and ED) and concluded that breeder pullets fed every day during rearing produced more settable eggs and consumed 8% less feed to reach the same body weight and sexual maturity. Mortality, fertility and hatchability were not affected by the feeding systems used. Egg production and egg weights are not significantly different in birds fed SAD or skip two days. Skip two days restriction programs, although not commonly used in the industry, have been attempted experimentally, resulting in lower body weights, increased age at the first egg, higher plasma corticosterone and glucose levels after feeding (Bartov et al., 1988). Every day (ED) feeding produced less stress than SAD feeding evidenced by lower cortisone and insulin-like factor plasma levels (Ekmay et al., 2010). Research of Montiel (2016) confirms the previous research results of de Beer and Coon (2007). They concluded that every feeding during rearing was as good or better than the SAD feeding programs which is the accepted feed restriction method for most broiler breeder rearing around the world. Additional, an improved feed efficiency and comparable uniformity was found by Zuidhof et al. (2015) when applying every day feeding.
 
Floor feeding
Another approach to implementing restriction used in a number of countries in Europe and America is by changing the feed delivery method, broadcasting feed in the litter instead of conventional mechanical feeder administration. This system increased activity and feeding space, decreased abdominal fat and produce larger eggs (Chu, 1979). Feed distribution is typically automated by means of mechanical feeders, most commonly offered in trough type feeders (mechanical chain feeders) or feeding pans to improve speed and to uniformly distribute the daily ration throughout the flock. More recently, broadcasting feed on the litter has been adopted as a feed distribution method (de Jong et al., 2005; Zuidhof et al., 2015; Montiel, 2016) in several countries showing good performance results, less mortality, less leg problems, improved litter condition and more uniform body weights (Aviagen, 2018).
De Jong et al. (2005b) tested whether increasing the feeding frequency from once to twice a day, or scattering feed in the litter would reduce stress or hunger in the rearing period. They did not find any positive effects of both these methods on the behaviour and physiological indicators of stress. In general, it is advised to use mash feed instead of pellets to increase feeding time in broiler breeders, although this has not any effect on feelings of hunger. Further, it is important to provide sufficient space at the feeders to prevent aggression in the birds at the time of feeding, as aggression around feeding may result in increased levels of feather and skin damage. Finally, the speed to which feed is distributed is very important to promote equal feed consumption between individuals, to promote flock uniformity, and to prevent aggression between birds.
Recently Montiel (2016) observed improved innate immune responses in broiler breeder pullets when they were fed on the floor. They found that pullets fed ED (on the litter) cleared E.coli faster than the SAD and ED (in feeders) groups and exhibited lower SE colonization rates towards the end of the restriction period (17-22 weeks of age). This together suggests that feeding programs including off-feed days such as SAD have a negative impact on innate immune responses. They postulated that this is possibly derived from feed competition and available feeding space in the SAD or ED (in feeders) programs and perhaps due to fasting during off-feed days in the SAD program or insufficient feed amounts delivered daily in the ED (in feeders) fed birds.
A uniform flock is easier to manage than a variable one because birds in a similar physiological state will respond more uniformly to management factors (Aviagen, 2018). On the other hand, an extreme good uniformity (low CV%) is probably not really necessary and maybe even contra productive. Zuidhof et al. (personal communication) developed a precision feeding system for breeder pullets to increase broiler breeder lifetime reproductive performance through improved flock uniformity. At photo stimulation, pullet fed via the precision feeding system had a BW CV of 2 versus 14% in standard-fed pullets. Egg production in birds fed via the precision was 27% decreased compared to the standard fed pullets. They hypothesized that metabolic changes in precision fed pullets provided an insufficient metabolic trigger for sexual maturation.
 
Effect rearing diets
Feather cover
A low protein diet during the rearing period, however, had a negative effect on feather cover quality (van Emous et al., 2014; 2015c). In the experiment of van Emous et al. (2014), feather cover was inferior on the low protein diet at 6 and 11 wk of age while this difference disappeared from 16 wk of age onward. In the experiment of van Emous et al. (2015c), feather coverage was inferior on the low protein diet during the entire rearing period. It is, therefore, suggested that the protein and amino acid levels of the diets in the studies were critical or deficient, in particular, those amino acids needed for feather growth and development. The effect of daily protein intake on feather growth in broilers was previously reported by Twining et al. (1976), Aktara et al. (1996), Melo et al. (1999) and Urdaneta-Rincon and Leeson (2004). The suggestion of protein deficiency was underlined by the malformed cover feathers on the wings in the current study what might be an indication of amino acids deficiency. Moran (1984) already showed that marginal dietary deficiencies of sulphur containing amino acids resulted in abnormal feathering. Data of van Emous et al. (2013) were used to analyse the linear relationships between the total crude protein intakes at different phases during the rearing period on feather cover score. The data show that the effect of a low total CP intake on feather cover score was much more pronounced between 2 and 6 wk of age than between 6 and 15 wk of age. It is, therefore suggested that total CP (and AA) is a critical factor in development of feathers cover during rearing till approximately 6 wk of age.
Behaviour
An experiment was conducted to determine the effects of different dietary protein levels during rearing in broiler breeder pullets on behavior and feather cover (van Emous et al., 2015c). A total of 2,880 Ross 308 14-d old broiler breeder pullets were fed between wk 2 to 22 a high or low CP diet. Average feed intake at 11 and 17 wk of age was 12.1% higher for the low CP diets birds compared to the high CP diets birds resulting in a 2.4 times longer eating time and 47% decreased eating rate. During the rearing period low CP diets birds spent 110% more time feeding, 171% more time sitting, 35% more time comfort, and 7% less time standing, 11% less time walking, 24% less time foraging, 70% less time stereotypic object pecking, and 75% less time bird pecking compared to the high CP diets birds. Van Emous et al. (2015c) concluded that providing a low protein diet during rearing improved breeder pullet welfare during the rearing period, as showed by increased sitting and comfort behavior. Moreover, these birds showed less stereotypic object pecking, which is a major indicator of reduced hunger and frustration.
Body composition
A, on average, 16% lower dietary CP during the rearing period in the studies reported by van Emous et al. (2013, 2015a) resulted in a decreased breast meat and increased abdominal fat pad content at 10 wk of age and at onset of lay (20 and 22 wk of age). This was in close agreement with Mba et al. (2010) who found the same effects of a 12.5% reduction in crude protein content of the diet (14 vs. 16%) on body composition at 12 and 23 wk of age. In fact, not the dietary crude protein or amino acid content influenced body composition, but the differences in daily or total intake of the macro nutrients. On average, in both experiments of this thesis, the 16% lower protein diets (low vs. high protein diet) resulted in 11% higher total energy, 5% lower total crude, protein, and 7% lower total amino acid intake during the rearing period. Average breast muscle (18.8 vs. 17.2%) and abdominal fat pad (1.0 vs. 0.4%) content at the end of the rearing period of all birds was relative higher in the study reported by van Emous et al. (2015a) than the study by van Emous et al. (2013). The differences between the experiments in breast muscle content might be explained by the differences in the higher total dietary protein and moreover, total digestible lysine intake (+4.5%) in the second compared to the first experiment. Particularly dietary lysine is known as the major essential amino acid for breast muscle deposition in broilers and thus also for broiler breeders (Leeson and Summers, 2005). The abdominal fat pad content roughly doubled in the study reported by van Emous et al. (2015a) compared to the study reported by van Emous (2013) could be explained by two different factors. Firstly, body composition at the end of the rearing period was determined at 20 (van Emous et al., 2013) and 22 (van Emous et al., 2015a) wk of age. In this pullet to breeder transition period, body composition or moreover fat content of the body changes dramatically. Secondly, the differences could be explained by the, on average, 4.5% higher cumulative energy intake in the study reported by van Emous et al. (2015a).
At 15 wk of age, no effects of dietary protein level on abdominal fat pad (% BW) were found while this was present at wk 10 (van Emous et al., 2013). This phenomenon was also reported by Mba et al. (2010) who observed a difference in abdominal fat pad affected by differences in dietary protein level at wk 12 while this disappeared at 19 wk of age. It seems that abdominal fat pad and fat contents of the body follows a specific pattern during rearing with aging. This pattern in body composition was previously reported by Bennet and Leeson (1990) who found a decreased total fat content between 2 and 14 wk of age but an increased fat content between 14 and 24 wk of age. Combining the data of different authors yields a quadratic relationship between age and abdominal fat pad content (% BW) during the rearing and pullet to breeder transition period (P < 0.001).
The decreased abdominal fat pad weight around 12 wk of age is caused by the severe feed restriction levels (67 to 75%) between 7 and 16 wk of age, as described by de Jong and Guéméne (2011). It is likely that due to the severe feed restriction program during the midterm phase of rearing, pullets are required to use body (fat) reserves to meet energy requirements. This explains that the fat content of the body decreased during the severe feed restriction period while it increased again when energy intake increases substantially after 15 wk of age.
Production performance
An interesting significant carryover effect of dietary protein level during rearing on the number of total and settable egg production during the second phase of lay was observed by van Emous et al. (2015a). Pullets fed a low protein diet during rear produced between 45 and 60 wk of age 3.0 more total and 3.6 more settable eggs than pullets fed a high protein diet. The better persistency of lay of birds fed low-protein diet during lay might be explained by the higher proportion of abdominal fat and lower proportion of breast muscle at the end of rearing. Breeders with a higher body fat content are probably more able to mobilize energy reserves in periods of a negative energy balance (Renema et al., 2013) which probably prevent them for molting. The lower muscle content of the body may decrease the daily energy requirement for maintenance and increase the amount of energy that would be available for egg production (Ekmay et al., 2013).
Contrary to the study of van Emous et al. (2015a), Miles et al. (1997) did not find any effects of a low protein diet during rearing on total egg production. This may be caused by the different breeds, or moreover the different properties due to 15 years of advances in selection and breeding resulting in differences in body composition (Renema et al., 2013). On the other hand, when pullets were fed very low protein diets (approx. 10%) during rearing, total egg production was negatively affected (Hudson et al., 2000; Hocking et al., 2002).
Data of the experiment of van Emous et al. (2015a) was used to analyse the relationship between breast muscle and abdominal fat pad content at 22 wk of age on total number of settable eggs. It was concluded that the effect of body composition on egg production persistency has to be refined. The data show that the number of settable eggs during the second phase of lay was affected by abdominal fat pad content and not by breast muscle content. It also shows that either breast muscle or abdominal fat pad content at the end of the rearing period did not affect the number of settable eggs during the first phase of lay. Particularly, abdominal fat pad is the cause of this difference while breast muscle content has no effect on persistency of lay. Breeders with a higher body fat content are probably more able to mobilize energy reserves during periods of a negative energy balance (Renema et al., 2013) which may prevent them start moulting. On the other hand, breeders with a low body fat content lack energy to meet their energy requirements if dietary energy intake is limited and, thereby, may lose BW over time that finally initiate moulting as part of a natural process. It is observed that natural moulting starts with a voluntary reduction in food intake resulting in an approximately 20% BW loss (Mrosovsky and Sherry, 1980).
Mortality
Hocking et al. (2002) indicated that diets with a low CP (10%) content between 15 and 18 wk of age could result in a doubling of mortality during lay. In line with these results, mortality of pullets fed the low protein diet during rearing by van Emous et al. (2015a) showed a tendency to an increased mortality over the entire laying period (6.3 vs. 8.1%. It is hypothesized that feeding low protein levels during the rearing period may negatively affect the immune system due to the indispensable need for certain amino acids (arginine, glutamine, and cysteine) for the development of the immune system (Kidd, 2004).
Incubation traits
It was postulated by van Emous et al. (2015a) that differences in late embryonic mortality during the first phase of lay between birds fed different dietary protein levels during the rearing period were caused by differences in body composition at the onset of lay. Data of van Emous et al. (2015b) were used to analyse the relationship between breast muscle and abdominal fat pad content of the body at 22 wk of age on embryonic mortality during the first of the laying period. No effect on embryonic mortality was found during the second phase of lay. These data show that particularly abdominal fat pad content and not breast muscle content at the end of the rearing period seems to be an important factor to affect embryonic mortality during the first phase of lay. Thus a higher abdominal fat pad content at the end of rearing resulted in a decreased embryonic mortality. A sound explanation for this phenomenon may be that egg composition might be affected by the differences in abdominal fat pad content of the body.
 
Presented at AMEVEA Nutrition Seminary, Bogotá, Colombia. November 2018.

Aktare, S. S., A. G. Khan, J. K. Bhardwaj, and N. G. Paradkar. 1996. Effect of protein levels on carcass yield of commercial broiler progenies from dwarf dam × normal sire. Indian J. Poult. Sci. 32:226-228.

Aviagen. 2018. Parent stock management manual: Ross 308. Aviagen, Ltd., Huntsville, AL.

Bartov, I., S. Bornstein, Y. Lev, M. Pines, and J. Rosenberg, 1988. Feed restriction in broiler breeder pullets: skip-a-day versus skip-two-days. Poultry Science, 67(5), 809-813.

Bennett, C. D., and S. Leeson. 1990. Body composition of the broiler-breeder pullet. Poult. Sci. 69:715-720.

Bornstein, S., I. Plavnik, and Y. Lev. 1984. Body weight and/or fatness as potential determinants of the onset of egg production in broiler breeder hens. Br. Poult. Sci. 25:323-341.

Bruggeman, V., O. Onagbesan, E. D’Hondt, N. Buys, M. Safi, D. Vanmontfort, L. Berghman, F. Vandesande, and E. Decuypere. 1999. Effects of timing and duration of feed restriction during rearing on reproductive characteristics in broiler breeder females. Poult. Sci. 78:1424-1434.

Chu, S. S. W. 1979. The effect of feeding management during the growing and laying periods on productivity and the characteristics of adipose tissue of the broiler breeders. Master thesis. University of British Columbia.

de Beer, M., and C. N. Coon. 2007. The effect of different feed restriction programs on reproductive performance, efficiency, frame size, and uniformity in broiler breeder hens. Poult. Sci. 86:1927-1939.

de Beer, M. 2009. Current approaches to feeding broiler breeders. Pages 104-114 in Proc. 17th Eur. Symp. Poult. Nutr., Edinburgh, Scotland. World’s Poult. Sci. Assoc., Attleborough, United Kingdom.

Decuypere, E., V. Bruggeman, N. Everaert, Yue Li, R. Boonen, J. De Tavernier, S. Janssens, and N. Buys. 2010. The Broiler Breeder Paradox: ethical, genetic and physiological perspectives, and suggestions for solutions. Br. Poult. Sci. 51:569-579.

de Jong, I. C., S. van Voorst, D. A. Ehlhardt, and H. J. Blokhuis. 2002. Effects of restricted feeding on physiological stress parameters in growing broiler breeders. Br. Poult. Sci. 43:157-168.

de Jong, I. C., S. van Voorst, and H. J. Blokhuis. 2003. Parameters for quantification of hunger in broiler breeders. Physiol. Behav. 78:773-783.

de Jong, I. C., M. Fillerup, and H. J. Blokhuis. 2005a. Effect of scattered feeding and feeding twice a day during rearing on parameters of hunger and frustration in broiler breeders. Appl. Anim. Behav. Sci. 92:61-76.
 
de Jong, I. C., H. Enting, S. van Voorst, and H. J. Blokhuis. 2005b. Do low-density diets improve broiler breeder welfare during rearing and laying? Poult. Sci. 84:194-203.
 
de Jong, I. C., and B. Jones. 2006. Feed restriction and welfare in domestic birds. Pages 120-135 in Feeding in domestic vertebrates. From structure to behavior. V. Bels ed. CABI Publishing, Wallingford, UK.
 
de Jong, I. C., and D. Guémené. 2011. Major welfare issues in broiler breeders. World's Poult. Sci. J. 67:73-82.
 
Dixon, L. M., S. Brocklehurst, V. Sandilands, M. Bateson, B. J. Tolkamp, and R. B. D'Eath. 2014. Measuring Motivation for Appetitive Behaviour: Food-Restricted Broiler Breeder Chickens Cross a Water Barrier to Forage in an Area of Wood Shavings without Food. Plos One 9. doi 10.1371/journal.pone.0102322.
 
EFSA. 2010. Scientific Opinion on welfare aspects of the management and housing of the grand-parent and parent stocks raised and kept for breeding purposes. EFSA Journal 8:81. doi doi:10.2903/j.efsa.2010.1667
 
Eitan, Y., E. Lipkin, and M. Soller. 2014. Body composition and reproductive performance at entry into lay of anno 1980 versus anno 2000 broiler breeder females under fast and slow release from feed restriction. Poult. Sci. 93:1227-1235.
 
Ekmay, R. D., M. de Beer, R. W. Rosebrough, M. P. Richards, J. P. McMurtry, C. N. and Coon. 2010. The role of feeding regimens in regulating metabolism of sexually mature broiler breeders. Poult. Sci. 89:1171-1181.
 
Ekmay, R. D., M. De Beer, S. J. Mei, M. Manangi, and C. N. Coon. 2013. Amino acid requirements of broiler breeders at peak production for egg mass, body weight, and fertility. Poult. Sci. 92:992-1006.
 
Fattori, T. R., H. R. Wilson, R. H. Harms, F. B. Mather, R. D. Miles, and G. D. Butcher. 1993. Response of broiler breeder females to feed restriction below recommended levels. 3. Characterizing the onset of sexual maturity. Poult. Sci. 72:2044-2051.
 
Havenstein, G. B., P. R. Ferket, and M. A. Qureshi. 2003a. Growth, livability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult. Sci. 82:1500-1508.
 
Havenstein, G. B., P. R. Ferket, and M. A. Qureshi. 2003b. Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult. Sci. 82:1509-1518.
 
Heck, A., O. Onagbesan, K. Tona, S. Metayer, J. Puterflam, Y. Jego, J. J. Trevidy, E. Decuypere, J. Williams, M. Picard, and V. Bruggeman. 2004. Effects of ad libitum feeding on performance of different strains of broiler breeders. Br. Poult. Sci. 45:695-703.
 
Hocking, P. M., D. Waddington, M. A. Walker, and A. B. Gilbert. 1989. Control of the development of the ovarian follicular hierarchy in broiler breeder pullets by food restriction during rearing. Br. Poultry Sci. 30:161-174.
 
Hocking, P. M. 1993. Welfare of broiler breeder and layer females subjected to food and water control during rearing: quantifying the degree of restriction. Br. Poultry Sci. 343:53-64.
 
Hocking, P. M., M. H. Maxwell, and M. A. Mitchell. 1993. Welfare assessment of broiler breeder and layer females subjected to food restriction and limited access to water during rearing. Br. Poult. Sci. 34:443-458.
 
Hocking, P. M., M. H. Maxwell, and M. A. Mitchell. 1996. Relationships between the degree of food restriction and welfare indices in broiler breeder females. Br. Poult. Sci. 37:263-278.
 
Hocking, P. M., R. Bernard, and G. W. Robertson. 2002. Effects of low dietary protein and different allocations of food during rearing and restricted feeding after peak rate of lay on egg production, fertility and hatchability in female broiler breeders. Br. Poult. Sci. 43:94-103.
 
Hudson, B. P., R. J. Lien, and J. B. Hess. 2000. Effects of early protein intake on development and subsequent egg production of broiler breeder hens. J. Appl. Poult. Res. 9:324-333.
 
Kidd, M. T. 2004. Nutritional modulation of immune function in broilers. Poult. Sci. 83:650-657.
 
Leeson, S., and J. D. Summers. 2005. Commercial poultry nutrition. 3rd Edition. University books, Guelph, Ontario.
 
Mba, E., R. A. Renema, A. Pishnamazi, and M. J. Zuidhof. 2010. Do dietary protein:energy ratios modify growth and frame size of young broiler breeder females? Poult. Sci. 89(Suppl. 1):122. (Abstr.)
 
McKay, J. C. 2009. The genetics of modern commercial poultry. Pages 3-9 in: Biology of Breeding Poultry. Poultry Science Series Vol. 29. P. M. Hocking ed. CABI. Wallingford, UK.
 
Melo, J. E., M. C. Miquel, G. Mallo, M. Ciacciariello, and E. Villar. 1999. Effects of dietary crude protein on slaughter yield of selected broiler stocks. J. Appl. Genet. 40:219-231.
 
Miles, R. D., H. R. Wilson, and R. H. Harms. 1997. Protein intake of broiler breeder replacements and its effect on body composition and subsequent performance. J. Appl. Anim. Res. 11:25-36.
 
Montiel, E.R. 2016. Influence of feeding programs on innate and adaptive immunity in broiler breeders. PhD Diss. The University of Georgia, Athens, Georgia.
 
Moran, E. T., Jr. 1984. Feathers and L-methionine substitutes. Feed Manage. (Jan.):46.
 
Mrosovsky, N., and D. Sherry. 1980. Animal anorexias. Sci. 207:837-842.
 
Pearson, R. A., and K. M. Herron. 1981. Effects of energy and protein allowances during lay on the reproductive performance of broiler breeder hens. Br. Poult. Sci. 22:227-239.
 
Renema, R. A., F. E. Robinson, and P. R. Goerzen. 2001a. Effects of altering growth curve and age at photostimulation in female broiler breeders. 1. Reproductive development. Can. J. Anim. Sci. 81:467-476.
 
Renema, R. A., M. E. Rustad, and F. E. Robinson. 2007b. Implications of changes to commercial broiler and broiler breeder body weight targets over the past 30 years. World’s Poult. Sci. J. 63:457-472.
 
Renema, R. A., T. G. V. Moraes, and M. J. Zuidhof. 2013. Effects of broiler breeder nutrition on chick quality and broiler growth. Pages 212-222 in Proc. 2nd Int. Poult. Meat Congress, Antalya, Turkey.
 
Robinson, F. E., M. J. Zuidhof, and R. A. Renema. 2007. Reproductive efficiency and metabolism of female broiler breeders as affected by genotype, feed allocation, and age at photostimulation. 1. Pullet growth and development. Poult. Sci. 86:2256-2266.
 
Savory, C. J., and K. Maros. 1993. Influence of degree of food restriction, age and time of day on behavior of broiler breeder chickens. Behav. Proc. 29:179-190.
 
Savory, C. J., K. Maros, and S. M. Rutter. 1993. Assessment of hunger in growing broiler breeders in relation to a commercial restricted feeding programme. Anim. Welf. 2:131-152.
 
Savory, C. J., P. M. Hocking, J. S. Mann, and M. H. Maxwell. 1996. Is broiler breeder welfare improved by using qualitative rather than quantitative food restriction to limit growth rate? Anim. Welf. 5:105-127.
 
Savory, C. J., and J. S. Mann. 1997. Is there a role for corticosterone in expression of abnormal behavior in restricted-fed fowls? Physiol. Behav. 62:7-13.
 
Savory, C. J., and Lariviere, J. (2000). Effects of qualitative and quantitative food restriction treatments on feeding motivational state and general activity level of growing broiler breeders. Appl. Anim. Behav. Sci. 69:135-147.
 
Siegel, P. B., and E. A. Dunnington. 1985. Reproductive complications associated with selection for broiler growth. Pages 59-72 in Poultry Genetics and Breeding, W. G. Hill, J. H. Manson, and D. Hewitt eds. Longman, Harlow, UK.
 
Spratt, R. S., and S. Leeson. 1987. Broiler breeder performance in response to diet protein and energy. Poult. Sci. 66:683-693.
 
Sun, J., and C. N. Coon. 2005. The effects of body weight, dietary fat, and feed withdrawal rate on the performance of broiler breeders. J. Appl. Poult. Res. 14:728-739.
 
Twining, P. V., O. P. Thomas, and E. H. Bossard. 1976. The number of feathers on litter; another criterion for evaluating the adequacy of broiler diets. Poult. Sci. 55:1200-1207.
 
Urdaneta-Rincon M., and S. Leeson. 2004. Effect of dietary crude protein and lysine on feather growth in chicks to twenty-one days of age. Poult. Sci. 83:1713-1717.
 
van Emous, R. A., R. P. Kwakkel, M. M. van Krimpen, W. H. Hendriks. 2013. Effects of growth patterns and dietary crude protein levels during rearing on body composition and performance in broiler breeder females during the rearing and laying period. Poult. Sci. 92:2091-2100.
 
van Emous, R. A., R. Kwakkel, M. van Krimpen, and W. Hendriks. 2014. Effects of growth pattern and dietary protein level during rearing on feed intake, eating time, eating rate, behavior, plasma corticosterone concentration, and feather cover in broiler breeder females during the rearing and laying period. Applied Animal Behaviour Science 150:44-54.
 
van Emous, R. A., R. P. Kwakkel, M. M. van Krimpen, and W. H. Hendriks. 2015a. Effects of dietary protein levels during rearing and different dietary energy levels during lay on body composition and reproduction in broiler breeder females. Poult. Sci. 94:1030-1042.
 
van Emous, R. A., R. P. Kwakkel, M. M. van Krimpen, H. van den Brand, and W. H. Hendriks. 2015b. Effects of growth patterns and dietary protein levels during rearing of broiler breeders on fertility, hatchability, embryonic mortality, and offspring performance. Poultry Science 94:681-691.
 
van Emous, R. A., R. Kwakkel, M. van Krimpen, and W. Hendriks. 2015c. Effects of different dietary protein levels during rearing and different dietary energy levels during lay on behaviour and feather cover in broiler breeder females. Applied Animal Behaviour Science 168:45-55.
 
Windhorst, H. W. 2011. Patterns and dynamics of global and EU poultry meat production and trade. Lohmann information. Vol. 46 (1), April 2011. Page 28. Cuxhaven. Germany.
 
Yu, M. W., F. E. Robinson, and A. R. Robblee. 1992a. Effect of feed allowance during rearing and breeding on female broiler breeders. 1. Growth and carcass characteristics. Poult. Sci. 71:1739-1749.
 
Yu, M. W., F. E. Robinson, R. G. Charles, and R. Weingardt. 1992b. Effect of feed allowance during rearing and breeding on female broiler breeders. 2. Ovarian morphology and production. Poult. Sci. 71:1750-1761.
 
Zuidhof, M. J., R. A. Renema, and F. E. Robinson. 2007. Reproductive efficiency and metabolism of female broiler breeders as affected by genotype, feed allocation and age at photostimulation. 3. Reproductive efficiency. Poult. Sci. 86:2278-2286.
 
Zuidhof, M. J., B. L. Schneider, V. L. Carney, D. R. Korver, and F. E. Robinson. 2014. Growth, efficiency, and yield of commercial broilers from 1957, 1978, and 2005. Poult. Sci. 93:2970-2982.
 
Zuidhof, M. J., D. E. Holm, R. A. Renema, M. A. Jalal, and F. E. Robinson. 2015. Effects of broiler breeder management on pullet body weight and carcass uniformity. Poult. Sci. 94:1389-1397. 
Related topics:
Authors:
Rick van Emous
Wageningen University & Research
Wageningen University & Research
Influencers who recommended :
Mohammad Afrouziyeh
Recommend
Comment
Share
Profile picture
Would you like to discuss another topic? Create a new post to engage with experts in the community.
Featured users in Poultry Industry
Lorena Ramos
Lorena Ramos
Cargill
United States
Shivaram Rao
Shivaram Rao
Pilgrim´s
PhD Director Principal de Nutrición y Servicios Técnicos de Pilgrim’s Pride Corporation
United States
Karen Christensen
Karen Christensen
Tyson
Tyson
PhD, senior director of animal welfare at Tyson Foods
United States
Join Engormix and be part of the largest agribusiness social network in the world.