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The Effect of Low-Density Broiler Breeder Diets on Performance and Immune Status of their Offspring

H. Enting^*,1, W. J. A. Boersma, J. B. W. J. Cornelissen, S. C. L. van Winden^*,, M. W. A. Verstegen and P. J. van der Aar^*,2

^* Schothorst Feed Research, 8200 AM Lelystad, the Netherlands; Animal Sciences Group, Wageningen University, 8200 AB Lelystad, the Netherlands; Royal Veterinary College, University of London, Hatfield, Hertfordshire AL9 7TA, UK; and Animal Nutrition Group, Wageningen University, 6700 AH Wageningen, the Netherlands

² Corresponding author: pvdaar{at}schothorst.nl

	ABSTRACT

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Effects of low-density broiler breeder diets on offspring performance and mortality were studied using 2,100 female and 210 male Cobb 500 breeders. Breeder treatments involved 4 experimental groups and a control group with normal density diets (ND, 2,600 kcal of AME/kg during rearing and 2,800 kcal of AME/kg during laying). In treatment 2, nutrient densities were decreased by 12% (LD12) and 11% (LD11) during the rearing and laying periods, respectively, whereas in treatment 3, nutrient densities were decreased by 23% (LD23) and 21% (LD21) during the rearing and laying periods, respectively. The nutrient density in these treatments was decreased through inclusion of palm kernel meal, wheat bran, wheat gluten feed, and sunflower seed meal in the diets. Treatment 4 included diets with the same nutrient densities as in treatment 2 but included oats and sugar beet pulp (LD12^OP and LD11^OP). In treatment 5, the same low-density diet was given to the breeders as in treatment 2 during the rearing period, but it was followed by a normal density diet during the laying period (LD12-ND). Treatments were applied from 4 to 60 wk of age. On low-density diets, offspring showed an increased 1-d-old weight. As compared with offspring of breeders that received ND, the d 38 live weight of chickens from 29-wk-old breeders fed LD11 was improved. Mortality was reduced in offspring from 60-wk-old parent stock given low-density diets. The IgM titers in 35-d-old offspring from eggs with a lower-than-average weight were reduced when 29-wk-old broiler breeders were fed low-density diets. In offspring from eggs with a higher-than-average weight from 60-wk-old parent stock given LD11 or LD21 diets, IgM titers were higher compared with ND. It was concluded that low-density broiler breeder diets can improve offspring growth rates, reduce mortality, and reduce or increase immune responses, depending on breeder age and egg weight.

Key Words: broiler breeder • nutrient density • offspring performance

	INTRODUCTION

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Broiler chicken performance is highly dependent on the genetic potential of these birds (Havenstein et al., 1994). Besides genetic potential, breeder age, level of feed intake, and dietary composition of breeder feeds may also influence offspring performance (Triyuwanta et al., 1992; Kidd et al., 1993; Lopez and Leeson, 1994, 1995; Hossain et al., 1998; Peebles et al., 1998, 1999a, Peebles et al., b).

Shanawany (1984), Yannakopoulos and Tserveni-Gousi (1987), Applegate and Lilburn (1996), and Christensen et al. (1996) observed a higher embryo development rate and embryo weight with increasing breeder age. Egg weight and yolk:albumen increase with age (Fletcher et al., 1981; Al Bustany and Elwinger, 1987; Etches, 1996), and offspring performance of young broiler breeders (<35 wk of age) is generally poorer than that of older broiler breeders of >35 wk of age (McNaughton et al., 1978; Lopez and Leeson, 1995; Peebles et al., 1999a).

Based on effects of breeder age on offspring performance, it can be hypothesized that an increase in egg weight and yolk:albumen can improve embryonic development and broiler chicken performance. Enting et al. (unpublished data) observed an increase in egg weight and a more advanced embryonic development in terms of an increase in vitellina externa surface area and higher embryo weight when young breeders were fed low-density diets. Moreover, they found an increase in albumen:yolk. These observed effects may raise the question as to what extent these changes can improve offspring performance.

Broiler breeders are fed a restricted amount of feed to prevent health and reproductive disorders (Katanbaf et al., 1989). Current feed restriction levels can result in hunger and chronic stress (De Jong et al., 2002, 2003). In humans, food shortage that results in hunger can result in retarded offspring development (Barker, 1995). Chronic stress during pregnancy has been shown to increase the mortality rate of offspring in rats (Lordi et al., 2000). Smulders and Enting (Schothorst Feed Research, unpublished data) observed a significant reduction in the mortality rate of broiler chickens when breeders were fed low-density diets. Because Zuidhof et al. (1995) found indications of a reduction in chronic stress when broiler breeders were fed diets that were diluted by oat hulls, it can be hypothesized that low-density diets can affect offspring mortality due to a reduced stress level in parent stock. Due to the immunosuppressive effect of stress hormones (Griffin, 1989), offspring immune status might be affected as well.

Based on the observation of Enting et al. (unpublished data) that low-density broiler breeder diets increased egg weight, albumen:yolk, and embryo weight and the possible effect of low-density diets on hunger and chronic stress in parent stock, offspring performance of breeders given diets with different nutrient densities was determined at different breeders ages.

	MATERIALS AND METHODS

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Broiler Breeder Treatments
The protocol for the experiments was in agreement with standards for animal experiments and was approved by the Ethical Committee of Schothorst Feed Research. The broiler breeder experiment involved, in total, 2,700 Cobb 500 female birds during the rearing period and 2,100 Cobb 500 female and 210 Cobb 500 male breeders during the laying period. These birds were housed in 30 floor pens of 4.5 x 3 m, with 90 female birds per pen during the rearing period. In the laying period, 70 female and 7 male birds were housed per pen. Male birds were obtained at 25 wk of age from a rearing company (De Kuikenaer Opfok, Delden, the Netherlands).

The broiler breeders were subjected to 5 different treatments, in which each treatment included 6 replicates with 1 treatment pen per block. Treatment 1 was the control group, in which normal density diets were fed during the rearing and laying period (ND, 2,600 and 2,800 kcal of AME/kg, respectively). In treatments 2 and 3, the levels of energy, digestible Lys, Ca, available P, Na, and linoleic acid were decreased by 12 and 23% in the rearing period (LD12 and LD23) and by 11 and 21% in the laying period (LD11 and LD21). These nutrient densities were decreased by inclusion of palm kernel meal, wheat bran, wheat gluten feed, and sunflower seed meal in the diets. Treatment 4 included diets with the same nutrient density as in treatment 2, but in this treatment, the lower nutrient density was reached by the inclusion of oats and sugar beet pulp (LD12^OP and LD11^OP). Treatment 5 included a diet with a 12% lower nutrient density in the rearing period and a ND diet in the laying period (LD12-ND). The composition and calculated contents of the broiler breeder diets are shown in Table 1 for the rearing period and in Table 2 for the laying period.

Birds and Housing Broiler Experiments.
At 29, 41, and 60 wk of broiler breeder age, in total, 10,000 eggs were collected (approximately 330 per pen) during 8, 8, and 11 d, respectively, weighed, and separated in 2 weight classes with higher- and lower-than-average egg weights of the particular pen by a commercial egg packing station (FrisianEgg, Drachten, the Netherlands). This resulted in 60 groups of about 167 hatching eggs each (30 pens of broiler breeders x 2 egg weight classes per pen). Eggs were stored in a separate room at 15°C before incubation. Eggs were incubated per pen and per weight class according to a randomized design by Animal Sciences Group. Eggs were incubated at a constant eggshell temperature of 37.8°C during the entire incubation period.

After hatching, broiler chickens were feather-sexed and transported to Schothorst Feed Research. Each experiment in which broiler chicken performance was determined included a total of 6,800 birds. Birds were placed in 40 pens of 4.95 x 2.05 m with 85 male and 85 female birds per pen, giving 8 replicates per treatment with 4 replicates per egg weight class.

In all broiler chicken experiments, light was provided 23 h per day. Temperature started at 32°C at d 0 and was gradually decreased to 20°C from d 28 on. Birds were vaccinated against Newcastle disease, infectious bronchitis, and infectious bursal disease according to recommendations of a broiler chicken integrator (De Kuikenaer, Wezep, the Netherlands). Feed and water were provided for ad libitum consumption. Wood shavings were used as bedding material.

Dietary Treatments and Diet Composition.
The broiler chickens were given the same starter, grower, and finisher diets in all treatments of the experiments. Starter diets were provided from d 0 to 15, grower diets from d 15 to 30, and finisher diets from d 30 to 38. The diets had wheat, corn, and soybean meal as main ingredients. The starter diet contained 2,900 kcal of AME and 202 g of CP/kg. The grower and finisher diets contained 3,050 kcal of AME and 193 g of CP/kg. Diets were formulated according to recommendations used in Dutch practice (Centraal Veevoeder Bureau, 2003). The diets did not contain an antibiotic, but 0.5% of formic acid as antimicrobial growth promoter. The starter diet contained 3 mg/kg of halofuginone (Hoechst, Frankfurt, Germany), and the grower diets contained 60 mg/kg of salinomycin Na (Intervet, Boxmeer, the Netherlands) as coccidiostat. All diets were milled through a 3.2-mm screen and were given as pellets with a diameter of 2.5 mm in the starter period and 3.0 mm in the grower and finisher phases.

Measurements.
Weight of the collected eggs was recorded per pen and per weight class. During incubation, number of fertile and hatched eggs were recorded for each group. In each broiler chicken experiment, live weight and feed intake of the birds was determined per broiler pen at d 0, 15, 30, and 38. Mortality was recorded daily.

Immunization experiments were carried out with a total of 200 female broiler chickens per experiment. Birds originated from the same batches of hatched eggs as birds in the performance experiments. Broiler chickens were placed in pens of 1.40 x 1.25 m with 10 birds per pen. Each treatment included 4 replicates per treatment with 2 replicates per egg weight class. At 10 and 30 d of age, broiler chickens in the vaccination experiments were vaccinated with 200 µg of 2,4,6-trinitrophenyl-keyhole limpet hemocyanin (KLH-TNP) in 0.1 and 0.2 mL of saline solution, respectively. At 17 and 35 d of age, blood samples of at least 0.5 mL were taken. In blood serum, IgG, and IgM anti-TNP titers as a result of the immunizations with KLH-TNP were determined in an ELISA system using BSA-TNP as a coating and specific antibody conjugates for detection (Koenen et al., 2004). Serum samples were stored at –20°C until use.

Statistical Analysis.
Data of the broiler chicken experiments were subjected to ANOVA (GLM procedure of GenStat 7.1, GenStat Committee, 2003). The statistical model included block (replicate), treatment, and egg weight class within treatment as factors. Parameters were tested for normal distributions before statistical analysis. Output data are given as means with SEM. Significant differences among treatments were detected by a least significant differences procedure (Snedecor and Cochran, 1967). Differences among treatments were considered significant at P 0.05.

	RESULTS

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The percentages of fertile and hatched eggs were not different among treatments (not shown). Eggs from the heavy weight class led to higher 1-d-old chicken weights than eggs from the light weight class at all breeder ages (Table 3). Eggs from 29-wk-old breeders fed LD21 or LD11^OP resulted in higher weights than both ND and LD11. Weight of 1-d-old chickens was higher when breeders were fed LD11^OP than when ND, LD21, or LD12-ND were fed at this age. A higher weight was found for eggs of 41-wk-old breeders fed LD11, LD21, or LD11^OP as compared with breeders fed ND. Also 1-d-old chick weight was higher when 41-wk-old breeders were fed LD11, LD21, LD11^OP, or LD12-ND as compared with ND. In wk 60, eggs from breeders provided LD21 and LD11^OP had a higher weight than when ND was fed. One-day-old chicken weight was lower when breeders were fed LD12-ND instead of ND, LD11, LD21, or LD11^OP at this breeder age. Weight of 1-d-old chickens of 60 wk-old breeders fed LD11^OP was higher as compared with that of other breeder treatments.

At 29 wk of breeder age, offspring live weight at 15 and 30 d was higher when breeders were fed LD11 or LD11^OP as compared with breeders fed ND (Table 4). At 38 d of age, live weight was higher when breeders were fed LD11 instead of ND or LD21. Feed intake from d 0 to 15 and 0 to 30 was higher when breeders were fed LD11, LD21, LD11^OP, or LD12-ND than when breeders were fed ND. From d 0 to 38, feed intake was higher when breeders were given LD11, LD11^OP, or LD12-ND instead of ND.

When broiler breeders were 60 wk of age, the live weight of 15- and 30-d-old chickens was higher when breeders were fed LD21 as compared with breeders fed ND. Feed intake from d 0 to 15 was higher when breeders were fed LD21, LD11^OP, or LD12-ND instead of ND. From d 0 to 30, feed intake was higher when parents were fed LD11, LD21, or LD12-ND as compared with parents provided ND. In broiler chickens of 60-wk-old breeders, feed intake from d 0 to 38 was higher when breeders were fed LD21 or LD12-ND instead of ND.

No differences in mortality rate were observed among treatments in offspring from 29- and 41-wk-old broiler breeders and between broilers from light or heavy eggs (Table 5). At a breeder age of 60 wk of age, a lower mortality rate was found from d 0 to 15 and 0 to 38 when breeders were fed LD21 or LD12-ND as compared with breeders provided ND. Offspring mortality from breeders fed LD11^OP was lower in the period from d 0 to 15 and tended to be lower from d 0 to 15 (P = 0.06) as compared with ND. From d 0 to 30, mortality in offspring of breeders fed LD12-ND was lower than in offspring of breeders provided ND.

The IgM titers in broiler chickens from the heavy egg weight class from 60-wk-old breeders were higher in broiler chickens from breeders provided LD11 or LD21 as compared with titers in broiler chickens from breeders fed ND. In broiler chickens from eggs with a lower-than-average weight, IgM titers were higher than in broiler chickens from breeders fed LD11^OP instead of ND at a breeder age of 60 wk. No significant interaction between diet and egg weight class was observed.

In offspring from eggs with a lower-than-average weight from young, 29-wk-old breeders, the IgG titers in broilers derived from breeders that received LD11^OP were significantly lower as compared with titers in broiler chickens from breeders fed ND or LD21 (Table 7). The IgG titers were significantly higher in broiler chickens from 60-wk-old breeders given LD21 instead of ND when broiler chickens originated from eggs with a higher-than-average weight.

	DISCUSSION

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According to Larbier (1973), Leclercq (1966), and Triyuwanta et al. (1992), an increased egg weight caused by increased dietary amino acid and linoleic acid levels or by an increased feed allowance can improve offspring growth rate. Based on the findings of Lopez and Leeson (1994, 1995), this might be particularly true for early broiler chicken growth. Because egg weight of breeders fed LD11 was lower than that of breeders fed LD11^OP and because the difference in live weight among egg weight classes was equal to that between ND and LD11, other factors than egg weight seem to affect offspring performance, too. Results of Leclercq (1966), Larbier (1973), and Triyuwanta et al. (1992) indicate that nutrient intake levels of parent stock per se might also play a role in offspring performance. Enting et al. (unpublished data) observed a higher-than-expected digestibility of the LD11 diet, which resulted in a higher daily nutrient intake in this treatment as compared with ND, LD21, or LD11^OP. According to Gardner and Young (1972) and Shafer et al. (1996), who found higher CP levels in eggs when dietary amino acid levels were increased, the higher digestible nutrient level in LD11 could have resulted in higher nutrient levels in eggs as compared with the other treatments. This may have provided the increased live weight of offspring when breeders received LD11 instead of ND. McDevitt et al. (2004) reported that broiler chickens of a fast-growing strain had a higher ability to digest feed when their parents were fed diets that were supplemented with a carbohydrate-hydrolyzing enzyme. This could have resulted in a higher nutritional value of the breeder diet. The possible importance of nutrient intake levels of breeders might also be illustrated by the fact that the largest improvement in live weight gain was observed in broiler chickens from eggs with a lower-than-average weight when breeders were fed LD11 instead of ND at 29 wk of age (from 2,074 to 2,162 g vs. from 2,176 to 2,209 g for broiler chickens from the high egg weight class; data not shown in Table 4). However, this interaction was not significant.

Enting et al. (unpublished data) observed an increase in egg weight, albumen:yolk, and embryonic development when breeders received LD21 instead of ND. However, these changes did not result in increased final live weights of broiler chickens. Therefore, to obtain a high feed intake and growth rate in broiler chickens, changes in albumen:yolk and embryonic development might be of less importance than digestible nutrient intake levels in broiler breeders.

Dietary broiler breeder treatments did not affect mortality of offspring of 29-and 41-wk-old broiler breeders, but low-density breeder diets resulted in a significant decrease in mortality rate of offspring of 60-wk-old breeders. At this breeder age, mortality in offspring of breeders provided ND was higher than at 29 and 41 wk of age. In an earlier study (Smulders and Enting, unpublished data), a significant reduction in broiler mortality of 3.3 and 2.7%, respectively, was observed with 26- and 40-wk-old broiler breeders given the same low-density diets as in this study. The results of the latter and the present study indicate that low-density breeder diets can result in a significant reduction in broiler chicken mortality. The results of the present study also indicate that feeding low-density diets during the rearing period of broiler breeders is essential. Results of the earlier study also stress this, because no reduction in mortality was found when low-density feeds were only provided during the laying period. It can be hypothesized that the importance of feeding low-density diets during the rearing period is related to a delay in reproductive tract development and to an increase in egg size and albumen:yolk due to changes in reproductive tract development, as was found by Enting et al. (unpublished data).

The significant differences in IgG and IgM titers in broiler chickens of 35 d of age indicate that low-density breeder diets can affect adaptive immune responses of offspring. No clear differences in IgG and IgM titers were observed at d 17 after the first KLH-TNP immunization at 10 d of age. It appeared, therefore, that effects of broiler breeder diets developed relatively late after hatching. However, immune responses in young broiler chickens are low, and biological variation may not allow detection of significant differences at that age (Praharaj et al., 1997).

Differences in adaptive immune responses in broiler chickens were observed at 35 d of age after a second immunization on 30 d of age. Primary responses (IgM) were significantly lower in broiler chickens from eggs with a lower-than-average weight of 29-wk-old breeders fed LD21, LD11^OP, or LD12-ND instead of ND. This effect was not observed in broiler chickens from eggs with a higher-than-average weight at 29 wk of breeder age.

In offspring of 41-wk-old breeders, no dietary effects were observed in broiler chickens from relatively light eggs. When breeders were fed LD11 or LD21 instead of ND, a significant increase in IgM titers was found in offspring from eggs with a higher-than-average weight. The results indicate that no clear differences in IgM response were observed in broiler chickens from eggs weighing about 59 to 65 g. Lower egg weights from young broiler breeders led to reduced responses when low-density diets were given. Higher egg weights (>68 g) gave higher IgM responses in broiler chickens derived from 60-wk-old breeders. Although Klasing and Calvert (1999) calculated that only small amounts of nutrients are required for the development of the innate and adaptive immune system, it might be hypothesized that a limited amount or availability of nutrients in eggs with a relatively low weight may be used for growth rather than for the preparation of the adaptive immune system of the young bird. The mechanism underlying this effect is not yet unraveled, but, nevertheless, this indicates that competition for vital functions may exist. This seems to be in line with the work of Cheema et al. (2003), who concluded that genetic selection for improved broiler performance has resulted in a decrease in the adaptive arm of the immune response.

Differences in IgG titers were similar to those observed for IgM titers. However, significant differences were only found in broiler chickens from the lowest egg weight class of 29-wk-old breeders provided LD11^OP (reduced titers) and in chickens from the highest egg weight class of 60-wk-old breeders fed LD21 (increased titers) instead of ND. This indicates that the priority of the IgG response in broiler chickens is less sensitive to events early in life (Tizard, 1982).

Differences in IgM and IgG titers seem to be more related to differences in egg weight and egg composition than to differences in nutrient intake of the breeders, because broiler chickens of breeders provided LD11 did not show the highest titers. De Jong et al. (2005) found no effects of low-density diets on corticosterone level and heterophil:lymphocyte in 26-wk-old broiler breeders. However, a significant increase in heterophil:lymphocyte was observed at 40 wk of age when breeders were fed LD21 as compared with breeders fed ND. Because significantly lower titers were observed in offspring of 29-wk-old breeders provided low-density diets and almost no differences in titers were found in offspring of 41-wk-old breeders, no indications were found that stress levels in broiler breeders affected offspring immune responses.

Based on the results of these studies, it can be concluded that low-density broiler breeder diets can improve offspring growth rate and mortality and can affect humoral immunity, depending on breeder age and egg weight. An increase in offspring growth rate seems to be mainly related to an increase in nutrient intake of parents. A reduced offspring mortality and changes in adaptive immunity might be related to an increased egg weight and albumen:yolk.

	ACKNOWLEDGMENTS

 
This project was funded by the Ministry of Agriculture, Nature and Food Quality, the Product Board for Livestock and Eggs, and the Product Board for Animal Nutrition.

	FOOTNOTES

 
¹ Present address: Nutreco PRRC, Ctra. CM-4004 Km. 10.5, 45950 Casarrubios del Monte, Spain.

Received for publication March 29, 2006. Accepted for publication October 9, 2006.

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