Optimum feed composition of broiler breeder diets to maximise progeny performance
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1 Optimum feed composition of broiler breeder diets to maximise progeny performance P. M. Hocking* Genetics and Genomics, Roslin Institute, Roslin, Midlothian EH25 9PS, UK *Corresponding author: Recent research to define a measure of chick quality has evaluated the effects of incubation conditions, breeder age and genotype on progeny growth and survival. Nutritional research has focused on defining the optimum concentration of maternal dietary nutrients for progeny growth, mortality and immune status. There is a research requirement to bring these two areas together to better understand optimum maternal nutrition for maximum chick quality. Recent research suggests that nutritional concentrations for vitamin D are higher for optimum progeny performance than for egg production. Research also suggests that increased breeder dietary concentrations of zinc, manganese and selenium may benefit progeny performance. Low energy density diets improved progeny growth in young broiler breeders and liveability in offspring of older broiler breeders. There is evidence that different broiler breeder genotypes may have different responses to maternal nutrient concentrations. Further research to quantify the relationships between broiler growth, mortality and immune status in relation to maternal dietary nutrient concentrations in different broiler breeder genotypes is warranted. Keywords: chick quality; broiler; growth; breeder; nutrition Introduction The profitability of a broiler production enterprise is ultimately related to the performance of the hatched chick and depends on liveability, growth rate to slaughter, feed efficacy and carcass value. Taken together these traits combined define the potential value of the chick and are the best measure of chick quality. Traditionally much research has been focussed on identifying the nutrients and allowances that maximise the production and hatchability of eggs from broiler breeders and there are several reviews of this aspect of breeder nutrition (e.g. Wilson, 2007). More recently there have been renewed efforts to define chick quality and its relationship to breeder hen genotype and age, incubation practices (Hulet, 2007) and the role of some minerals and vitamins. A comprehensive review of nutritional factors affecting progeny performance was provided by Kidd (2003) and Kemp et al., (2001). The purpose of this paper is to update these publications with special reference to maternal vitamin D 3, organic minerals and the role of low energy and low protein diets on chick quality. Measuring chick quality Tona et al., (2003a) devised a descriptive scheme based on the characteristics of the hatched chick for assessing chick quality (Table 1). Different traits were defined and weighted by a subjective score based on interviews with people familiar with broiler chicks. The maximum total score was 100 and a series of experiments was conducted to investigate the relationship between chick quality and post hatching performance. Weight gains from 1 to 7 d post hatch were lower in chicks with a score <100 in each of three genotypes studied (Table 2, Tona et al., 2004). In two experiments it was shown that day-old chick weight was comparatively poorly correlated (R 2 <0.35) with relative growth and was less useful for predicting broiler performance compared with the quality score. However, there was a clear effect of other factors such as age of breeder flock, storage time, incubation conditions and hatching time on growth of chicks with the same quality score. In a study of chicks from 8 broiler lines, 16th European Symposium on Poultry Nutrition 101
2 Table 1. Measuring chick quality (from Tona et al., (2003a) Parameters Assessment Characteristics Scores Activity Speed of righting from back. Good/weak 6/0 Appearance Dry/clean vs. wet or dirty. Clean, dry/wet/dirty, wet 10/8/0 Retracted yolk Height/hardness of abdomen. Normal/large, hard 12/0 Eyes Bright and wide Bright/dull/closed 16/8/0 Legs Upright stance; inflammation. Normal/1 infeceted/2 infected 16/8/0 Navel Closure colour. Normal/open/open, discoloured 12/6/0 Membrane Size of remaining membrane. None/small/large/very large 12/8/4/0 Yolk Size of remaining yolk. Small/medium/large/very large 16/12/8/0 Wolanski et al., (2006) reported that shank length and body length at hatch correlated more strongly with body weight at 14 d than did hatch weight. These results collectively suggest that intrinsic factors other than chick weight and size influence day-old chick quality. Tona et al. (2005) showed that the navel area was the most significant factor determining chick quality and was closely correlated with appearance, membrane, retracted yolk, chick weight and relative growth to 7 d. A simpler system based on a score for the navel area was used to systematically measure chick quality on large numbers of chicks under semi-commercial production constraints. Chick quality was assessed on a 3-point scale as Good (navel closed and clean), Medium (navel not closed) and Bad (navel not closed and discoloured) in a large replicated field trial (Bouchot and Picard, 2005). Assessment of the performance of commercial chicks from 5 broiler lines classified in this way are summarised in Table 3. Male chicks exhibited better quality scores than female chicks. Good quality chicks had lower Table 2. Body weights (means ± SEM) of 1, 7 and 41 d old broilers of three lines classified by chick quality score (Tona et al., 2004). Broiler % chicks Quality Body weight (g) at different ages 1 parent score = 100 scores 1 d 7 d 41 d Label 24.9 < ± d ± 1.7 1,605 e ± ± c ± 2.0 1,734 d ± 37 Dwarf 25.9 < ± c ± 2.4 2,006 c ± ± b ± 2.7 2,132 b ± 37 Normal 25.7 < ± b ± 1.9 2,123 b ± ± a ± 2.2 2,2560 a ± 45 1 Means followed by different letters are significantly different (P<0.05) within each column. Table 3. Mean performance of broiler chicks of different quality (from Bouchard and Picard, 2005). Trait Factor Chick Quality 1 Good (%) Medium (%) Bad (%) Sex (%) Female 24.5 x 66.6 x 8.8 x Male 32.9 y 60.0 y 7.2 y Mortality (%) 0-3 wk 4.4 a 5.6 ab 6.7 b 3-6 wk Body weight (g) 1 d 40.1 a 40.5 b 40.9 c 35 d Means followed by different letters are significantly different (P<0.05) within a column for chick quality within each trait and across rows for each trait th European Symposium on Poultry Nutrition
3 mortality than bad quality chicks during the first 3 weeks after hatch. Chicks with high navel quality were lighter than the medium and low navel quality chicks: an observation that may explain the low correlation between chick weight and early growth rate. There were no significant effects of chick quality on mortality from 3 to 5 wk or body weight and carcass quality at 6 wk. Differences in early mortality and numerical differences in leg conformation suggest that unhealed navels predispose to the risk of infection. Maternal mineral and vitamin nutrition and progeny performance Pearson (1982) pointed out that the gross composition of the hen s egg is relatively constant and must contain all the nutrients required for successful development of the embryo to hatching and its first feed. In fact there are small but biologically important changes in the composition of the egg with age of the hen and the proportion of yolk and shell in particular change with time. In contrast to the energy and protein composition of the egg, the vitamin and mineral content is dependent on the maternal diet and deficiencies, excesses and imbalances can affect hatchability, chick viability and growth (e.g. Whitehead et al., 1985). The mineral and vitamin content of the egg may vary over a fairly wide range suggesting that requirements of the dam for her maintenance and productivity may not match those of the embryo. There is increasing evidence on the beneficial role of higher maternal vitamin and mineral nutrition on measures of the immune system in broilers (Rebel et al., 2004). Kidd (2003) published a comprehensive review of the effect of maternal vitamin and mineral nutrition on progeny performance. More recent research evaluated the role of vitamin D 3 in maternal diets on progeny growth and skeletal development. Progeny weight gain was greatest when broiler breeders were fed the highest maternal dietary concentrations of 2000 or 4000 IU vitamin D 3 /kg and the incidence of tibial dyschondroplasia in progeny were improved in the offspring of young (30, 37 week) but not older (45, 57 week) broiler breeders (Atencio et al., 2005a). These concentrations are similar to recommended commercial supplements (3000 IU/kg, Kemp et al., 2001) and the authors own recommended supplement of 2,800 IU/kg (Atencio et al., 2006). Atencio et al. (2005b) showed that 25-hydroxycholecalciferoal (25-OH-D 3 ) had very high biological potency at low dietary concentrations of vitamin D 3 and that the relative biological value of 25-OH-D 3 was higher for embryos than for hens. These results suggest that further research is required to determine the optimum maternal nutritional concentrations of vitamin D and its metabolites for overall economic performance. There is increasing interest in the role of maternal nutrition on the antioxidant status of offspring (Surai, 2000). In general experiments have reported indirect measures of liveability and performance at hatch or during early growth and it is not clear how these relate to final weight, carcass quality or overall mortality. Karadas et al. (2005) showed that high maternal supplements of carotenoids resulted in high progeny concentrations to 7 d but no measures of antioxidant properties or immunity were conducted. Pappas et al. (2005) showed that high dietary breeder intakes affected progeny selenium concentrations at 28 d but there were no measures of performance. There are now several reports of the beneficial effects of using organic forms of some minerals including selenium. Kemp et al., (2001) referred to unpublished commercial trials that together indicated small but economically important improvements in fertility, hatchability and mortality to 10 d when organic selenium replaced sodium selenite. These results are consistent with the observation that progeny of hens fed high organic selenium had higher tissue concentrations of docosahexaenoic acid up to 14 d post hatch (Pappas et al., 2006). Early research on the role of zinc in progeny growth was reviewed by Kidd (2003) who concluded that higher than recommended zinc supplements improved cellular immune function and early survival. Hudson et al. (2004a; 2004b) fed high levels of maternal dietary zinc with additional zinc in organic or inorganic form or as a mixture. There was no effect of the additional zinc supplements and whereas organic zinc improved one measure of immune function and feed conversion compared with the same intake of zinc as zinc sulphate, there were many measured responses and the differences may be statistical artefact. In a similar experiment with additional zinc and manganese, Viridin et al. (2003; 2004) reported that broilers from hens fed on diets with organic zinc and manganese had higher liveability from hatch to 34 d, and some immune parameters and measures of cardiac function were higher in progeny of dams fed higher dietary nutrients. Taken together there is evidence that 16th European Symposium on Poultry Nutrition 103
4 substantially higher maternal dietary concentrations of selenium, zinc and manganese than are typically recommend may improve immune function and liveability. Whether there is a significant benefit from feeding the organic compared with the conventional inorganic forms of these minerals is uncertain, although they may be benefit to the environment if greater availability facilitates the formulation of breeder diets with lower concentrations of these elements. Dietary protein and energy concentrations In a review of the literature on dietary protein and energy allowances Kidd (2003) concluded that low maternal dietary protein concentrations and allowances had no effect on progeny performance at slaughter. Even though very low protein diets resulted in low egg and chick weights there was no statistical effect on final body weight or carcass quality at 30 weeks but at 52 weeks male and female broilers from hens fed on 120g crude protein/kg were significantly heavier than those fed 100 or 160 g crude protein/kg (Lopez and Leesen 1995). The experiment was too small to detect statistically significant treatment differences in carcass weight and quality. Lopez and Leesen (1995) concluded that dietary crude protein concentrations for broiler breeders may be lowered provided amino acid intakes could be maintained. In practice differences in chick weight and chick quality might affect early survival and larger experiments are required to clarify the role of maternal protein intakes on progeny performance. Research by Peebles and colleagues demonstrated an effect of fat type and concentration on carcass quality in some (Peebles et al., 1999a, b) but not all (Peebles et al., 2002) experiments. Further research to clarify the role of maternal fat on progeny growth and carcass quality and particularly on the immune status of the chick is justified. In practice the effects of restricting feed (energy) to control body weight gain is critical to maximise egg production in broiler breeders and there is limited scope for increasing energy intake. Recent research has concentrated on feeding high fibre (low energy and protein) to broiler breeders during the rearing and laying periods to increase the apparent welfare of feed restricted birds (Savory et al., 1996; Hocking et al., 2004). Most of these reports did not consider progeny performance (Hocking et al., 2002; Tolkamp et al., 2005; Hocking, 2006). Hocking (2006) fed diets that were diluted with 0, 200 or 400 g oat hulls/kg and found lower drinking behaviour and water intake and better litter quality in broilers fed on the experimental treatments but no change in other indexes of welfare. de Jong et al (2005) reported behavioural evidence for less stress in breeders fed high fibre diets at 6 and 10 weeks of age but higher heterophil-lymphocyte ratios during lay compared with conventional diets. In a very large replicated experiment Enting et al. (2007) fed broiler breeders on diets that contained 12 or 23 % less energy and other nutrients by dietary dilution with high fibre ingredients. The diets were fed in higher amounts to provide the same daily intake on all 4 treatments. The diet with 12 % dilution based on oat hulls produced larger eggs and chicks at 29, 41 and 60 weeks of age (Table 4) whereas differences at 38 d were small (29 weeks) or not significant (41 and 60 weeks). Mortality was not affected by maternal dietary treatments at 29 and 41 weeks whereas mortality at 60 weeks was highest in the offspring of breeders fed the conventional diet and lowest in broilers from dams fed on the -12 % diet during rearing and a conventional diet during lay (Table 4). The authors concluded that low density diets could enhance progeny growth and mortality but that this probably resulted from increased nutrient intake in the breeders rather than a diminution of the stress of feed restriction. Taken together the results from feeding low density, high fibre diets suggest that because of the higher feed intakes welfare improvements may be seen up to 10 or 12 weeks of age but not thereafter. However, low density feed does appear to result in lower progeny mortality in older breeders. It would be interesting to know if this effect in older breeders persisted if the feed allowance after 40 weeks was decreased i.e. if the greater feed intake in birds fed low density diets resulted in increased nutrient absorption or less stress that was reflected in higher egg and chick quality. In contrast to these results, Peebles et al. (2002) reported higher broiler 43 d weight in male offspring of breeders fed on a low energy ration where the high energy was obtained from added fat th European Symposium on Poultry Nutrition
5 Table 4. Progeny weight at 38 d and mortality form hatch to 38 d in broilers from breeders fed on diets of conventional nutrient density (Control), 12 (LD1) or 23 (LD2) % less during rearing and breeding or 12 % less during rearing and the Control diet during lay (LD3) (from Enting et al., 2007). Trait Age, wk Control LD1 LD2 LD3 SEM Chick weight, g * * * Weight at 38 d, g * Mortality, % * * Significant differences P<0.05. Conclusions Much of the literature reviewed by Kidd (2003) were fairly old and the question must be asked as to how reliable these data are for modern genotypes and commercial conditions. Modern broiler dam genotypes require less feed and are restricted to a smaller proportion of mature body weight than breeders of 20 to 40 years ago. Furthermore there are significant differences between modern commercial broiler genotypes in body size, composition (Hocking and Robertson, 2005; Wolanski et al., 2006) and rate of egg production that may affect nutrient requirements of the breeder hen. More research to clarify the role of mineral and vitamin supplementation of maternal diets above current recommendations is warranted particularly as it affects immune status and early mortality in broiler chicks. As the time to slaughter becomes annually ever shorter, the effects of dam nutrition on chick quality and the immune status of the chick in the first d become increasingly significant as a proportion of the lifetime of the bird if slaughter age continues to decrease by one day per year. The importance of chick liveability justifies further research to clarify the factors that affect the very different performance of chicks of the same quality as measured by Tona et al. (2003b) s chick quality index. Measures of immune function might usefully incorporate recent information on the genetics of the immune system to clarify the effects of maternal nutrition on chick quality. The beneficial effects of feeding organic forms of Se, Zn and Mn for improving some aspects of immune function compared with the inorganic elements, is supported by some but not all published data. The greater efficiency of utilisation of organic forms of minerals may permit the feeding of lower dietary concentrations and lead to less environmental pollution by faecal contamination. A dramatic illustration of this phenomenon was provided by Plumstead et al. (2007) who showed that phytase released the equivalent amount of phosphorus in an unsupplemented diet as in birds fed on the conventional diet and that phosphorus in the litter was decreased by 42 %. Further use of enzymes to release poorly digested organic sources may become more important in future but is unlikely to affect progeny performance in non-limiting circumstances. Because so many maternal nutritional factors interact on broiler chick quality and this in turn is assessed by performance in different environments, evaluating optimum maternal nutrition will be complex. Research has shown that there exists an optimum maternal dietary crude protein concentration for progeny performance and the same is likely for energy density. The available data suggests that optimum chick quality may come from feeding lower energy and protein concentrations during rearing and laying than is presently the case. Research into quantifying the effects of maternal nutrition on chick quality should examine dietary concentrations that are in excess of current recommendations rather than relying on assumed deficiencies to guarantee a response. In an ideal world we would have nutritional models to characterise the response to different nutrients in terms of both breeder and offspring performance in relation to different genotypes and environments (e.g. high vs. low health). In the absence of such models breeder diet formulation should be based on properly designed response experiments. In general there is little evidence to suggest that current recommendations are far off the mark but alternative forms of some minerals and vitamins may be more effective than traditional ones. Higher 16th European Symposium on Poultry Nutrition 105
6 dietary concentrations or availability of some minerals and vitamins may lead to enhanced immune function and disease resistance that might be commercially important in the early rearing phase from hatch to 21 d of age. Further investigation of these trends will require new small-scale experimental methods to assess the potential of these nutrients and larger field experiments to asses their practical utility. This will not be a trivial task. References ATENCIO, A., EDWARDS,H.M. and PESTI, G. M. (2005a). Effect of the level of cholecalciferol supplementation of broiler breeder hen diets on the performance and bone abnormalities of the progeny fed diets containing various levels of calcium or 25-hydroxycholecalciferol. Poultry Science 84: ATENCIO, A., EDWARDS, H.M., PESTI, G.M. and WARE, G. O. (2006). The vitamin d-3 requirement of broiler breeders. Poultry Science 85: ATENCIO, A., PESTI, G. M. and EDWARDS, H. M. (2005b). Twenty-five hydroxycholecalciferol as a cholecalciferol substitute in broiler breeder hen diets and its effect on the performance and general health of the progeny. Poultry Science 84: BOUCHOT, C. and PICARD, M. (2005). Broiler breeder paradox. DE JONG, I. C., ENTING, H., VAN VOORST,A. and BLOKHUIS, H. J. (2005). Do low-density diets improve broiler breeder welfare during rearing and laying? Poultry Science 84: ENTING, H., BOERSMA, W. J. A., CORNELISSEN, J., VAN WINDEN,S.C.L., VERSTEGEN,M.W. A. and VAN DER AAR, P. J. (2007). The effect of low-density broiler breeder diets on performance and immune status of their offspring. Poultry Science 86: HOCKING, P. M. (2006). High-fibre pelleted rations decrease water intake but do not improve physiological indexes of welfare in food-restricted female broiler breeders. British Poultry Science 47: HOCKING, P.M., BERNARD, R. and ROBERTSON, G. W. (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. British Poultry Science 43: HOCKING,P.M. and ROBERTSON, G. W. (2005). Limited effect of intense genetic selection for broiler traits on ovarian function and follicular sensitivity in broiler breeders at the onset of lay. British Poultry Science 46: HOCKING,P.M., ZACZEK, V., JONES,E.K.M. and MACLEOD, M. G. (2004). Different sources of fibre may enhance the welfare of female broiler breeders. British Poultry Science 44: HUDSON, B. P., DOZIER,W.A., FAIRCHILD,B.D., WILSON,J.L., SANDER, J. E. and WARD,T. L. (2004a). Live performance and immune responses of straight-run broilers: Influences of zinc source in broiler breeder hen and progeny diets and ambient temperature during the broiler production period. Journal of Applied Poultry Research 13: HUDSON, B. P., FAIRCHILD, B. D., WILSON, J.L., DOZIER, W. A. and BUHR, R. J. (2004b). Breeder age and zinc source in broiler breeder hen diets on progeny characteristics at hatching. Journal of Applied Poultry Research 13: HULET, R. (2007). Influence of egg shell embryonic incubation temperature and broiler breeder flock age on posthatch growth performance and carcass characteristics. Poultry Science 86: KARADAS, F., PAPPAS,A.C., SURAI,P.F. and SPEAKE, B. K. (2005). Embryonic development within carotenoid-enriched eggs influences the post-hatch carotenoid status of the chicken. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 141: th European Symposium on Poultry Nutrition
7 KEMP, C., WYLIE, L. and FISHER, C. (2001). Broiler breeder nutrition, nutrient transfer and broiler performance. In 13th European Symposium on Poultry Nutrition, Blankenberghe, Belgium. KIDD, M. T. (2003). A treatise on chicken dam nutrition that impacts on progeny. Worlds Poultry Science Journal 59: LOPEZ, G. and LEESON, S. (1995). Response of broiler breeders to low-protein diets.2. Offspring performance. Poultry Science 74: PAPPAS, A.C., ACAMOVIC, T., SURAI, P.F. and MCDEVITT, R. M. (2006). Maternal organoselenium compounds and polyunsaturated fatty acids affect progeny performance and levels of selenium and docosahexaenoic acid in the chick tissues. Poultry Science 85: PAPPAS, A.C., KARADAS, F., SURAI, P.F. and SPEAKE, B. K. (2005). The selenium intake of the female chicken influences the selenium status of her progeny. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 142: PEARSON, R. A. (1982). Influence of nutritional factors on hatchability. In Recent advances in animal nutrition Studies in the Agriculurural and Food Scienes (ed. W. Haresign), pp Butterworth, London, Nottingham. PEEBLES,E.D., DOYLE,S.M., PANSKY, T., GERARD,P.D., LATOUR,M.A., BOYLE,C.R. and SMITH, T. W. (1999a). Effects of breeder age and dietary fat an subsequent broiler performance. 1. Growth, mortality, and feed conversion. Poultry Science 78: PEEBLES,E.D., DOYLE,S.M., PANSKY, T., GERARD,P.D., LATOUR,M.A., BOYLE,C.R. and SMITH, T. W. (1999b). Effects of breeder age and dietary fat on subsequent broiler performance. 2. Slaughter yield. Poultry Science 78: PEEBLES, E. D., ZUMWALT, C.D., GERARD, P.D., LATOUR, M. A. and SMITH, T. W. (2002). Market age live weight, carcass yield, and liver characteristics of broiler offspring from breeder hens fed diets differing in fat and energy contents. Poultry Science 81: PLUMSTEAD, P.W., ROMERO-SANCHEZ, H., MAGUIRE, R.O., GERNAT, A. G. and BRAKE, J. (2007). Effects of phosphorus level and phytase in broiler breeder rearing and laying diets on live performance and phosphorus excretion. Poultry Science 86: REBEL,J.M.J., VAN DAM,J.T.P., ZEKARIAS,B., BALK,F.R.M., POST, J., MINAMBRES,A.F. and TER HUURNE, A. (2004). Vitamin and trace mineral content in feed of breeders and their progeny: Effects of growth, feed conversion and severity of malabsorption syndrome of broilers. British Poultry Science 45: SAVORY, C.J., HOCKING, P.M., MANN, J.S. and MAXWELL, M. H. (1996). Is broiler breeder welfare improved by using qualitative rather than quantitative food restriction to limit growth rate? Animal Welfare 5: SURAI, P. F. (2000). Effect of selenium and vitamion e content of the maternal deit on the antioxidant system of the yolk and the developing chick. British Poultry Science 41: TOLKAMP, B.J., SANDILANDS, V. and KYRIAZAKIS, I. (2005). Effects of qualitative feed restriction during rearing on the performance of broiler breeders during rearing and lay. Poultry Science 84: TONA, K., BAMELIS, F., DE KETELAERE, B., BRUGGEMAN, V., MORAES, V.M.B., BUYSE, J., ONAGBESAN, O. and DECUYPERE, E. (2003a). Effects of egg storage time on spread of hatch, chick quality, and chick juvenile growth. Poultry Science 82: TONA, K., ONAGBESAN, O., DE KETELAERE, B., BRUGGEMAN, V. and DECUYPERE, E. (2005). Interrelationships between chick quality parameters and the effect of individual parameter on broiler relative growth to 7 days of age. Archiv Fur Geflugelkunde 69: TONA, K., ONAGBESAN, O., DE KETELAERE, B., DECUYPERE, E. and BRUGGERMAN, V. (2003b). Effects of turning duration during incubation on corticosterone and thyroid hormone levels, gas pressures in air cell, chick quality, and juvenile growth. Poultry Science 82: th European Symposium on Poultry Nutrition 107
8 TONA, K., ONAGBESAN, O. M., JEGO, Y., KAMERS, B., DECUYPERE, E. and BRUGGEMAN, V. (2004). Comparison of embryo physiological parameters during incubation, chick quality, and growth performance of three lines of broiler breeders differing in genetic composition and growth rate. Poultry Science 83: VIRDEN, W.S., YEATMAN, J.B., BARBER, S. J., WILLEFORD, K.O., WARD, T. L., FAKLER, T. M., WIDEMAN, R. F. and KIDD, M. T. (2004). Immune system and cardiac functions of progeny chicks from dams fed diets differing in zinc and manganese level and source. Poultry Science 83: VIRDEN, W.S., YEATMAN, J.B., BARBER, S.J., ZUMWALT, C.D., WARD, T.L., JOHNSON, A. B. and KIDD, M. T. (2003). Hen mineral nutrition impacts progeny livability. Journal of Applied Poultry Research 12: WHITEHEAD,C.C., PEARSON,R.A. and HERRON, K. M. (1985). Biotin requirements of broiler breeders fed diets of different protein content and effect of insufficient biotin on the viability of progeny. British Poultry Science 26: WILSON, H. R. (2007). Effects of maternal nutrition on hatchability. Poultry Science 76: WOLANSKI, N.J., RENEMA, R.A., ROBINSON, F. E., CARNEY, V. L. and FANCHERT, B.I. (2006). Relationship between chick conformation and quality measures with early growth traits in males of eight selected pure or commercial broiler breeder strains. Poultry Science 85: th European Symposium on Poultry Nutrition
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