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Effects of timing and duration of feed restriction during rearing on reproductive characteristics in broiler breeder females
PHYSIOLOGY AND REPRODUCTION Effects of Timing and Duration of Feed Restriction During Rearing on Reproductive Characteristics in Broiler Breeder Females V. BRUGGEMAN,*,1 O. ONAGBESAN,* E. D’HONDT,† N. BUYS,* M. SAFI,* D. VANMONTFORT,* L. BERGHMAN,† F. VANDESANDE,† and E. DECUYPERE* *Laboratory for Physiology and Immunology of Domestic Animals, Catholic University of Leuven, Kardinaal Mercierlaan 92, 3001 Heverlee, Belgium and †Laboratory for Neuroendocrinology and Immunological Biotechnology, Zoological Institute, Catholic University of Leuven, Naamsestraat 59, 3000 Leuven, Belgium ing rearing changed the growth curves of the birds. Feed restriction from 7 to 15 wk followed by either ad libitum or restricted feeding led to improved reproductive performance, suggesting that long-term feed restriction may not be necessary to attain good reproductive performance. The birds restricted from 7 to 15 wk of age had higher proportional weights of ovary (≥1.7%) and oviduct (≥1.58%) at age of sexual maturity. The cLHRH-I levels in the median eminence and gonadotrophin contents in the pituitary followed that of growth in response to feeding levels and timing of feeding and could be related to the timing of the onset of lay. At age of first egg, all groups had similar levels of cLHRH-I, LH, and FSH. However, no clear effect of level of feed intake or time period of restriction could be observed for plasma LH or FSH concentrations.
(Key words: broiler breeder, feeding level, critical period, egg production, reproductive axis) 1999 Poultry Science 78:1424–1434
The management practice of broiler breeder females includes the restriction of feed allowance during both rearing and breeding to limit body weight gains, reduce the incidence of obesity, and improve egg production. Although restricted feeding prolongs the time to reach sexual maturity (Leeson and Summers, 1982), the added values in terms of increased egg production, increased fertility, hatchability, egg quality, reduced number of double-yolked or malformed eggs, and reduced mortality (McDaniel et al., 1981; Leeson and Summers, 1982; Katanbaf et al., 1989; Hocking et al., 1987, 1989; Fattori et al., 1991; Yu et al., 1992a; Hocking, 1993) far outweigh this delay in starting lay. The amount of restriction and the timing or duration of restriction, however, vary between operators, and, most certainly, the amount of gain differs. The duration of feed restriction to broiler breeder chickens
has now become an important issue of animal welfare because feed restriction can act as a stressor on the animal (FAWC, 1998). Research reports also seem to disagree on the best timing of restricted feeding. McDaniel et al. (1981) and Yu et al. (1992a,b) have suggested that restriction should cover almost the entire period of rearing (4 to 18 wk) and also breeding. Pym and Dillon (1974) contended that restriction was only necessary during the rearing period. Robbins et al. (1986, 1988) demonstrated that ad libitum feeding during part or all of the laying period increased egg production. Hocking (1993) concluded that restricted feeding of broiler breeder females after 14 wk of age decreased the incidence of multiple ovulations, thus leading to increased egg production. Several studies (Brody et al., 1980; Bornstein and Lev, 1982; Bornstein et al., 1984; Soller et al., 1984; Katanbaf et al., 1989; Yu et al., 1992b) have related the timing and size of growth of certain organs with feeding levels and level of egg pro-
Received for publication December 2, 1998. Accepted for publication July 1, 1999. 1 To whom correspondence should be addressed: [email protected]
Abbreviation Key: cLHRH-I = chicken luteinizing hormone releasing hormone-I; FSH = follicle-stimulating hormone; LH = luteinizing hormone.
INTRODUCTION
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ABSTRACT The objective of this study was to determine whether there exists a critical period during rearing when restricted feeding of broiler breeder hens can be most beneficial on subsequent egg production. Broiler breeder pullets were subjected to combinations of either ad libitum or restricted feeding during three periods before sexual maturity. Body weight gain, feed intake, and egg production were recorded. Ovary and oviduct weights were noted at age of first oviposition. At 15 and 18 wk of age and at age of first oviposition, chicken luteinizing hormone releasing hormone-I (cLHRH-I) in the median eminence and the levels of luteinizing hormone (LH) and follicle-stimulating hormone (FSH) in the pituitary and plasma were determined. The results demonstrated that alternation between ad libitum and restricted feeding dur-
RESPONSE OF BROILER BREEDER FEMALES TO FEED RESTRICTION
MATERIALS AND METHODS General Management of Animals Five hundred 1-d-old female Hybro G broiler breeder chicks (Euribrid, Boxmeer, The Netherlands) were raised in floor pens littered with wood shavings and supplied with suspended drinkers. The photoperiod was 23 h light (L) and 1 h dark (D) during the first week. Thereafter, light was decreased by 3 to 4 h/wk to 8 L:16 D at Week 6. Birds were photostimulated from 19 wk of age onward by increasing the photoperiod by 2 h weekly to reach 14 L:10 D at 21 wk of age. Birds were fed a standard broiler starter diet from 0 to 3 wk of age (2,800 kcal/kg metabolizable energy, 18% crude protein) followed by chick grower pellet (2,700 kcal/kg metabolizable energy, 15% crude protein). Three weeks before the expected start of egg laying, the birds were fed prelay feed (2,750 kcal/kg metabolizable energy, 14% crude protein), followed by a breeder layer mash (2,750 kcal metabolizable energy, 17% crude protein). The amount of feed allowance to birds depended on the experimental protocol. All birds had unrestricted access to water.
Experimental Design During the 1st wk, all birds consumed feed for ad libitum intake. At 7 d of age, birds were divided into two groups: one group had ad libitum access to feed, and the second group was fed a restricted quantity of feed according to breeder company recommendations. At 7 wk of age, these two groups were each subdivided into two groups: one of each group was allowed feed for ad libitum intake, and the other was fed a restricted quantity of feed. A similar subdivision was made in each of the four groups at the age of 16 wk, resulting finally in eight experimental
FIGURE 1. Schematic presentation of the division of the broiler breeder hens in feeding groups, resulting in eight groups at Week 16. The bold letter in italic indicates the feeding level during the corresponding period. Res (R) = restricted feeding; Ad lib (A) = ad libitum access to feed.
groups. One-half of each group was either fed for ad libitum intake or feed restricted. This feeding regimen was continued until just after the first oviposition. Birds of each treatment group were divided into two pens randomly distributed in the housing facility. A flow diagram of the feeding schedule is shown in Figure 1. Table 1 presents the amount of feed provided to the restricted birds and the weights of feed consumed by birds that were allowed ad libitum access to feed. Precautionary measures were taken such that birds did not develop crop problems during transition from restricted to ad libitum feeding. The change of feeding level from restricted to ad libitum at end of 15 wk was by the gradual increase in amount of feed over 7 d. At 18 wk of age, birds of all groups were individually caged to observe the date of first oviposition and to continue keeping egg laying records until 50 wk of age. During the laying period, all birds consumed layer feed ad libitum; this period began just after the first oviposition. From 2 wk onward, body weight was recorded weekly by weighing 15 birds randomly chosen from each treatment group. Feed intakes of each of the ad libitum fed groups were recorded. At Weeks 15 and 18 and at age of first oviposition, eight birds per group were killed by cervical dislocation. Blood samples were collected and centrifuged, and plasma was stored at −20 C until assayed for LH (luteinizing hormone) and FSH (follicle-stimulating hormone). The median eminences were collected for cLHRH-I (chicken luteinizing hormone releasing hormone-I) determination. The pituitaries were also excised for LH and FSH content determinations at 15 wk of age and at age of first oviposition. At the age of first oviposition, ovaries and oviducts were collected and weighed. Laying performance was followed until 50 wk of age. Eggs produced were sorted into settable and defective eggs (soft-shell, shell-less, cracked, double-yolked eggs).
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duction. These reports suggest that there are critical periods within either the rearing period or breeding period when restricted feeding imparts its effect to improve reproductive performance. The aim of this study was to determine whether there exists a critical period during rearing when restricted feeding of broiler breeder hens can be most beneficial on subsequent egg production. For this purpose, the rearing period was subdivided into three parts during which ad libitum and restricted feeding were alternated, and these birds were compared with those fed for ad libitum intake or feed restricted throughout the three periods. The choice of this division was based on the aforementioned literature on effects of feeding levels during rearing on growth and reproductive characteristics and on previous results (Bruggeman et al., 1997; Bruggeman, 1998a). These findings showed that from 2 to 7 wk, significant changes occurred in plasma metabolic hormones as an effect of restricted feeding compared with full feeding. The period around Week 16 appeared to be important for initiating the development and functioning of the reproductive axis in broiler breeder females.
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BRUGGEMAN ET AL. TABLE 1. The amount of feed (g) provided to the feed restricted (R) birds or taken in by the birds fed for ad libitum intake (A) on a daily basis per individual and per week1 Period 1 Week 2 3 4 5 6
R
A 22 34 53 93 122
RR
RA
AR
AA
47 55 57 59 61 62 65 67 69
155 154 237 152 203 196 118 177 190
47 55 57 59 61 62 65 67 69
178 126 229 144 218 215 134 224 175
Period 3 Week
RRR
RRA
RAR
RAA
ARR
ARA
AAR
AAA
16 17 18 19 20 21 22 23 24 25
75 80 85 90 100 110 120 130 140 150
117 232 230 231 240 285 324 207 243 217
75 80 85 90 100 110 120 130 140 150
174 184 201 221 208 259 139 198 204 211
75 80 85 90 100 110 120 130 140 150
117 206 203 199 207 241 275 254 293 261
75 80 85 90 100 110 120 130 140 150
175 183 214 203 219 131 203 219 205 214
Period 2 Week 7 8 9 10 11 12 13 14 15
1 For group abbreviations see Figure 1. The bold letter in italic indicates the feeding level during the corresponding period.
Hormone Assays Chicken Luteinizing Hormone Releasing HormoneI Assay. Chicken luteinizing hormone releasing hormone-I was determined by RIA as previously described by Bruggeman et al. (1998a). Luteinizing Hormone Assay. Luteinizing hormone was measured using a homologous RIA (Krishnan et al., 1994). Reagents, including cLH, were kindly donated by USDA Animal Hormone Program2. Chicken LH was radioiodinated by the chloramine-T procedure according to the procedure of Proudman and Opel (1981). The iodinated protein was separated by gel filtration on a PD10 column3. The assay was performed according to the recommendations supplied with the RIA kit. Separation of bound and free radioactivity was achieved by incubation with a second antibody-coated cellulose suspension4, centrifugation, and removal of the supernatant by aspiration. The lowest detectable level of LH was 0.1 ng/ml. Cross-reactivity of the antibody used with cFSH was <3% and <0.9% for turkey prolactin, cGH, or recombinant cGH. The intra- and interassay coefficients of variation were 3.3 and 7.6%, respectively.
2
ARS, Beltsville, MD 20705. Pharmacia Biotech Benelux, 4704 AT Roosendaal, The Netherlands. Innogenetics, 9000 Gent, Belgium.
3 4
Follicle-Stimulating Hormone Assay. Follicle-stimulating hormone was measured using a homologous RIA. The chicken FSH RIA kit provided by the USDA Animal Hormone Program2 included a highly purified preparation of FSH (USDA-cFSH-K-I; Krishnan et al., 1992), used as a standard, and a polyclonal rabbit antiserum (USDAAcFSH-16). The FSH was iodinated by the chloramine-T procedure according to the procedure of Proudman and Opel (1981). The iodinated protein was separated on a PD-10 column3 followed by further purification on Sephadex G-75 column3. The RIA was carried out according to the instructions that came with the RIA kit. The detection level of the assay was 60 pg/tube. The antiserum used showed no cross-reaction with different purified preparations of LH, turkey LH, cGH, and turkey prolactin. The intra- and interassay coefficients of variation were 4.8 and 8.4%, respectively.
Statistical Analysis Data are expressed as means ± SEM. Results were analyzed by ANOVA with group and age as factors. Statistical differences were assessed by Duncan’s multiple range test (General Linear Models procedure; SAS Institute, 1985). Relationships among hormones were analyzed by the Pearson correlation procedure (SAS Institute, 1985). P-values <0.05 were considered statistically significant.
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FIGURE 2. Body weight curves from 2 until 32 wk of age of broiler breeder hens fed under different feeding regimens during rearing. For group abbreviations, see Figure 1. R = restricted; A = ad libitum access to feed.
Body Weights Figure 2 shows the body weight curves of the eight groups of birds fed at different feeding levels from 2 wk of age up to 32 wk. The curves show that between 7 and 15 wk of age, the body weight curves of the RA and AA (R = restricted fed; A = ad libitum feeding) groups on the one hand, and those of the RR and AR on the other, were steeply divergent. At the end of this period of the feeding regimen, the body weights of ad libitum groups (RA and AA) were about twice as high as those of the restricted groups (RR and AR). Between 16 and 24 to 26 wk, ad libitum feeding resulted in a steep compensatory body weight gain in birds that had been restricted in the preceeding period (ARA and RRA). Restriction during this final period following previous restriction (ARR and RRR) reduced growth rate, leading to significantly lower weight in these birds compared with their counterparts fed for ad libitum intake during this period. Chickens fed for ad libitum intake or feed restricted during this period caused only a moderate increase in BW of chickens that had been fed for ad libitum intake during the previous period (RAA, RAR, AAA, or AAR).
Age, Body Weight, Ovary Weight, and Oviduct Weight at First Egg Table 2 summarizes the results for body weight at 6, 15, and 18 wk and at age at first egg. It also shows the age and ovary and oviduct weights at first egg for the eight groups of chickens. Age at first egg was earliest for the RAA group and latest for the RRR group. Ages at first egg were negatively correlated with body weights at first egg in the AAA/RAA and ARR/RRR groups. The feeding level during the first period did not affect age at first oviposition. An interaction (P < 0.04) between the first and the second period was found. The data show that feeding during the second and third periods is a more important determinant of age or body weight at first egg. Restriction during the third period in these birds
after restriction during the second period led to reduced body weights and later age at first egg (RRR or ARR). Ad libitum or restricted feeding during the third period following a previous ad libitum feeding during the middle period lowered age at first egg (RAA, RAR and AAA, AAR). At the age of first oviposition, absolute weights of the ovary in the eight groups did not differ. This finding probably indicates that a threshold of ovary weight must be achieved before sexual maturity is attained, whatever the feeding regimen that might have been applied. However, as a percentage of body weight, there were significant differences among the groups. Interactions between the second and third periods of feeding were observed for ovary weights (P < 0.0001). Birds that were restricted during all three periods (RRR) of feeding showed the highest value. Birds that consumed feed for ad libitum intake during the second period followed by ad libitum intake or restricted feeding during the third period showed the lowest ovary weights as a percentage of body weight (AAA, AAR, RAA, or RAR), with the exception of the RRA group. Those that consumed feed for ad libitum intake or were restricted after a restriction during the second period and ad libitum feeding during the first period showed intermediate values (ARA and ARR). Oviduct weights expressed as percentage of body weights followed a trend similar to ovary weights in percentages. An interaction between the second and third period of feeding on oviduct weight was also observed (P < 0.0001). The highest values were found in the RRR, RRA, ARR, ARA, and RAR groups. The values for the AAA, RAA, and AAR groups were lower.
Egg Production The analysis of egg production data is presented in Table 3. The average number of eggs per week per bird, the cumulative egg production, and settable eggs from onset of lay to 50 wk of age are presented for the eight groups of birds. Generally, chickens restricted during the middle period (ARA, RRR, RRA, and ARR) showed the highest average weekly egg production. The group fed
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RESULTS
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TABLE 2. Body weights at 6, 15, and 18 wk of age and at age at first egg. Body weights, ovary, and oviduct weights are presented at age at first egg for the broiler breeder hens fed under different feeding regimens during rearing1 Feeding regimen R Week 6 Body weight, g
A 929
± 87a RAR
1,840
RR Week 15 Body weight, g
1,705 RRR
Week 18 Body weight, g Age at first egg, d At first egg Body weight, g Ovary weights, g Ovary weights, % of body weight Oviduct weights, % of body weight
± 67b RRA
3,570
RAA
ARR
± 40a AR ± 75b ARA
AA 3,610
± 114a AAR
AAA
2,122 179.4
± 118d ± 7.5a
2,792 176.9
± 87c ± 9.8a
3,500 169.1
± 98b ± 11.4ab
4,090 154.6
± 102a ± 7.3b
2,005 174.4
± 70d ± 2.6a
2,800 166.7
± 62c ± 9.7ab
3,845 171.8
± 129ab ± 8.0ab
4,405 161.2
± 132a ± 14.8ab
3,393
± 85b
4,290
± 127a
4,487
± 208a
4,633
± 125a
3,177
± 108b
4,288
± 130a
4,656
± 144a
4,710
± 157a
68.8
± 3.7
a
66.7
± 5.9
a
70.4
± 7.2
a
72.3
± 6.5
a
56.3
± 3.9
a
73.5
± 7.3
a
70.5
± 3.3
a
62.9
± 4.3a
2.03 ± 0.11a
1.55 ± 0.13bc
1.56 ± 0.13bc
1.56 ± 0.14bc
1.75 ± 0.10ab
1.70 ± 0.14abc
1.52 ± 0.06bc
1.35 ± 0.10c
1.69 ± 0.09a
1.58 ± 0.09ab
1.55 ± 0.11ab
1.21 ± 0.05c
1.58 ± 0.11ab
1.58 ± 0.08ab
1.35 ± 0.04bc
1.26 ± 0.08c
Means within a row lacking a common superscript differ (P < 0.05). Values are expressed as means ± SEM (n = 8). For group abbreviations, see Figure 1. R = restricted feeding; A = ad libitum access to feed.
a–d 1
BRUGGEMAN ET AL.
± 19b RA
459
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for ad libitum intake throughout the periods (AAA) showed the lowest egg production per week. Those fed for ad libitum intake during the middle period followed by either ad libitum or restricted feeding were intermediate. The highest cumulative egg production was attained by the ARA group (124.38 ± 3.67 eggs/bird; P < 0.05). The birds on the ad libitum regimen from Week 7 to 15, except the AAR, had significantly lower egg production throughout the laying period compared with their restricted counterparts. A similar trend was observed for the cumulative settable eggs per birds; the group restricted between 7 to 15 wk was the better producing group. The highest number of settable eggs was observed in the ARA group (103.43 ± 3.40 eggs/bird), and the lowest was observed in the AAA group (69.59 ± 3.24 eggs/bird).
1
a–d
Means within a row lacking a common superscript differ (P < 0.05). Values are expressed as means ± SEM (n = 8). For group abbreviations, see Figure 1. R = restricted feeding; A = ad libitum access to feed.
69.59 ± 3.24d 83.32 ± 3.07c 103.43 ± 3.40a 69.77 ± 3.88d Cumulative settable eggs/bird
91.15 ± 2.92b
92.73 ± 2.72b
80.39 ± 3.63c
96.08 ± 3.26ab
83.07 ± 3.51d 108.62 ± 3.58b 124.38 ± 3.67a 91.48 ± 4.13c 108.21 ± 2.68b Cumulative egg production/bird
111.03 ± 2.72b
94.90 ± 4.19c
113.64 ± 3.01b
3.08 ± 0.13d 4.25 ± 0.14ab 4.75 ± 0.14a 4.53 ± 0.12ab 3.40 ± 0.15c 3.54 ± 0.16c 4.49 ± 0.11ab 4.44 ± 0.11ab Average number of eggs/week per bird
AAR ARA ARR RAA RAR RRA RRR
Feeding regimen
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Chicken Luteinizing Hormone Releasing Hormone-I Levels in Median Eminence Chicken luteinizing hormone releasing hormone-I contents in the median eminence increased with age in all groups (P < 0.02) (Figure 3). At Week 15, cLHRH-I contents were lower in the RR and AR groups than in their ad libitum fed counterparts (RA and AA) (P < 0.0001). Ad libitum feed consumption by birds during the third period, following restriction during the second period (ARA and RRA), resulted in higher cLHRH-I contents at Week 18 compared with those of their restricted counterparts (ARR and RRR). This upsurge in cLHRH-I was most pronounced in RRA compared with RRR, two groups that were restricted during the first two periods. The content of cLHRH-I remained low in the RRR and ARR groups until 18 wk but increased thereafter up to the age at first egg (P < 0.0001). In the four groups that were fed for ad libitum intake during the second period (AAA, AAR, RAA and RAR), the increase in cLHRH-I with age was less pronounced. Chicken LHRH-I in these groups at 15 and 18 wk and at age of first egg did not significantly differ. At the age of first oviposition, there were no differences in the content of cLHRH-I in the median eminence among groups.
Pituitary Luteinizing Hormone and Follicle-Stimulating Hormone Content Figure 4 shows the LH and FSH contents of the pituitaries of the eight groups. Significant group effects were observed for pituitary LH content at 15 wk and age at first egg. Feeding ad libitum during the second period increased LH significantly, but restriction kept it low. At Week 15, LH content of the RR and AR groups was lower than that of the ad libitum groups (P < 0.0001). Luteinizing hormone content at first egg was significantly lower also in the RRR group than in the AAA, AAR, and RAA groups. No significant differences were found among the other groups. Chicken LHRH-I contents in the median eminence correlated well with pituitary contents of LH, with an overall correlation coefficient of 0.42 (P < 0.0001).
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TABLE 3. Average number of total and settable eggs per bird per week and cumulative egg production (total and settable)from onset of lay to 50 wk of age1
AAA
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BRUGGEMAN ET AL.
Plasma Luteinizing Hormone and Follicle-Stimulating Hormone
DISCUSSION
FIGURE 3. Chicken luteinizing hormone releasing hormone-I (cLHRH-I) content in the median eminences of broiler breeder hens (mean ± SEM; n = 8) fed under different feeding regimens during rearing. Different letters indicate differences between groups (P < 0.05). For group abbreviations, see Figure 1. R = restricted; A = ad libitum access to feed.
Pituitary content of FSH in the AA group at 15 wk of age was higher than that of other groups (AR, RA, or RR) (P < 0.0001). At age at first egg, however, no group differences in FSH levels were observed. Although FSH levels increased with age until age at first egg, the greatest increase during the third period of feeding occurred in the groups on restricted feeding during the second period (ARA, ARR, RRA, and RRR). Again, cLHRH-I content in the median eminence showed a good correlation with pituitary FSH (r = 0.45; P < 0.0001).
The results of this study show clearly that there are relationships between the levels of feeding during the rearing period, the period of the application of any particular level of feeding, and the subsequent reproductive performance of the broiler breeder females used in this study. Subjecting pullets to combinations of either ad libitum or restricted feeding during the three experimental periods before sexual maturity influenced body weights at sexual maturation, the development of the reproductive apparatus (oviduct and ovary), reproductive hormone levels (cLHRH-I, LH, and FSH), age at first egg, and the subsequent number of eggs produced. The major aim of this study was to detect the best combinations of feeding regimens that would result in increased reproductive performance in terms of settable egg production; the data from this work suggest that restricted feeding during the middle period (between 7 and 15 wk of age) led to increased productivity compared with ad libitum feeding during the same period. The degree of improvement in egg production depended also on the feeding level during the third period following restriction. Ad libitum feeding during the third period yielded a better performance than restricted feeding. Chickens fed for ad libitum intake throughout the three periods had the lowest total and settable eggs, although they reached sexual maturity earliest. Although the level of feeding during each of the three periods had an effect, very significant interactions were found between the second and third periods on many of the parameters measured. The beneficial effect of restricting feed allowance to broiler breeder females has previously been reported (McDaniel et al., 1981; Leeson and Summers, 1982; Katanbaf et al., 1989; Hocking et al., 1987, 1989; Fattori et al., 1991; Yu et al., 1992a; Hocking,
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Figure 5 shows the concentration of LH and FSH in the plasma of chickens at 15 and 18 wk and at age of sexual maturity. Luteinizing hormone levels at the end of the second period showed no consistent changes between feeding groups, although LH levels tended to be higher in the groups fed for ad libitum intake during this period. At 18 wk, there were no significant differences among the eight feeding groups. Ad libitum feeding during the third period up to age at first egg increased LH levels in birds that were feed restricted during the second period (ARA and RRA). No changes in plasma LH concentrations were observed in other groups. No differences were observed in the level of plasma FSH in the four groups at the end of the second period of feeding or at the age at first egg; however, plasma FSH levels differed between groups at wk 18, with the lowest level in the RAR group (P < 0.0001). There were no correlations between cLHRH-I and plasma LH or FSH. Similarly, no correlations could be established between pituitary and plasma LH or FSH.
RESPONSE OF BROILER BREEDER FEMALES TO FEED RESTRICTION
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1993). However, the question had always been the best timing for restriction to attain the best reproductive performance. Yu et al. (1992a) showed that restriction from 4 until 18 wk of age resulted in the best egg production. Hocking (1993) concluded that feed restriction should be continued until the onset of lay because multiple ovulations are a major source of lost egg production when they are not reduced from 15 wk of age onward. The data in the present study narrowed the critical period, which may be between Weeks 7 and 15 when restricted feeding could be applied to obtain improved reproductive performance in broiler breeder females. This finding suggests that the current practice of long-term feed restriction may not be necessary for improved reproductive performance, which is especially important in view of recent concerns about the effect of long-term feed restriction on the welfare of the animals (FAWC, 1998). The physiological basis on which feed restriction modifies reproductive performance is not understood. The effects of feed intake on body weight gain and body composition during rearing or breeding have been reported
(Katanbaf et al., 1989; Yu et al., 1992b). A minimum age, body weight, lean body mass, shank length, or body fat composition before sexual maturation has been postulated (Brody et al., 1980; Bornstein et al., 1984; Soller et al., 1984). Yu et al. (1992b) stressed that controlling feed intake and growth from 4 to 18 wk is more important in determining age at sexual maturity than feed intake and changes in body composition from Week 18 until onset of lay. Feed restriction also modifies the development of the hypothalamo-pituitary axis, which produces the cLHRH-I, LH, and FSH that are important for development of the reproductive apparatus (Bruggeman et al., 1998a). The data in this study demonstrate that feed restriction modifies, in concert, many parameters that have consequences on the subsequent reproductive performance of the broiler breeder pullet. The results demonstrate that restricted feeding throughout the three periods reduced body weight, delayed age of sexual maturation, and produced the proportionally highest ovary and oviduct weight. Pullets that consumed feed for ad libitum intake throughout had the
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FIGURE 4. Luteinizing hormone (LH) and follicle-stimulating hormone (FSH) contents in the pituitaries of broiler breeder hens (mean ± SEM; n = 8) fed under different feeding regimens during rearing at 15 wk of age (upper panel) and at age at first egg (lower panel). Different letters indicate differences between groups (P < 0.05). For group abbreviations, see Figure 1. R = restricted; A = ad libitum access to feed.
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FIGURE 5. Luteinizing hormone (LH) and follicle-stimulating hormone (FSH) plasma concentrations of broiler breeder hens (mean ± SEM; n = 8) fed under different feeding regimens during rearing at 15 (upper panel) and 18 wk of age (middle panel) and at age at first egg (lower panel). Different letters indicate differences between groups (P < 0.05). For group abbreviations, see Figure 1. R = restricted; A = ad libitum access to feed.
highest body weights, the youngest age at first egg, but the smallest proportional ovary and oviduct weights. Alternation between ad libitum and restricted feeding during the three periods changed the growth curves of the different groups during these periods. The growth spurt observed in pullets fed for ad libitum intake during the second period (7 to 15 wk) was shifted to the third period (18 to 24 wk) for pullets that were restricted during the second period but fed for ad libitum intake during the third. Birds that consumed feed for ad libitum intake during the second period but were restricted during the third
period did not significantly decrease their body weight; they had similar weights to those fed for ad libitum intake throughout the rearing period. Despite the late compensatory growth between Weeks 16 to 22 by pullets restricted at 7 to 15 wk, they never reached the body weights of those that consumed feed for ad libitum intake during the middle period (7 to 15 wk). The data suggest that the excessive body weights, which probably adversely affected their reproductive performance, was added during the 7 to 15 wk of rearing age. Furthermore, growth during this period may be unconnected with the development
RESPONSE OF BROILER BREEDER FEMALES TO FEED RESTRICTION
plasma LH or FSH concentrations during the period before the onset of lay. A similar result has been reported previously (Bruggeman et al., 1998a) and suggests a disconnection between cLHRH-I and gonadotrophin storage in the pituitary on the one hand, and between cLHRH-I and gonadotrophin release on the other. These data on hormone levels have shown that feeding levels and their timing influence the development of the hypothalamopituitary axis. Secretions of the axis are known to influence the development and functioning of the ovary and oviduct (Etches, 1993) and, subsequently, egg production. The results of the present study show that this axis matures earlier in full-fed birds and is delayed by feed restriction. Moreover, the development of the axis under the different regimens seemed to fall within the period of rapid growth. The delay in the maturation of this axis until 18 to 22 wk in birds restricted at 7 to 15 wk of age may be more appriopiate and preferential for the development of the reproductive apparatus to attain subsequently improved egg production. In conclusion, the results show that the feeding level, timing, and duration of application during the period before the attainment of sexual maturity has important repercussions on growth parameters and the maturation of the reproductive axis (hypothalamic-pituitary and ovary-oviduct development). Moreover, these two axes are closely linked to one another in determining age at first oviposition in broiler breeder females when threshold levels of body weight, body composition, and age were attained. The age at the onset of lay was stringently related to the developmental changes at the hypothalamic-pituitary level. The effects of restricted feeding during rearing were carried over to the laying period with clear effects on the functioning of the reproductive axis (egg production). Our data suggest that restriction applied at 7 to 15 wk of age followed by either ad libitum feeding or continued feed restriction were best for improving reproductive performance in broiler breeder females.
ACKNOWLEDGMENTS We are grateful to J. A. Proudman for providing the USDA FSH RIA kit. Veerle Bruggeman was supported by Grant Number 942009 of the Vlaams Instituut voor de bevordering van het Wetenschappelijk-Technologisch onderzoek in de industrie (IWT). This research was supported by Het Onderzoeksfonds (OT-project OT/95/19). Luc Berghman was supported by the Fund for Scientific Investigation (FWO).
REFERENCES Bornstein, S., and Y. Lev, 1982. The energy requirements of broiler breeders during the pullet-layer transition period. Poultry Sci. 61:755–765. 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. 17:215–223. Brody, T., Y. Eitan, M. Soller, I. Nir, and Z. Nitsan, 1980. Compensatory growth and sexual maturity in broiler females
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of organs of reproduction. This lack of connection is suggested by the fact that, although absolute ovary weights were similar, when stated as a percentage of body weights, feed-restricted birds had higher ovary and oviduct weights than did birds fed for ad libitum intake. This higher proportional weight of the ovary and oviduct possibly indicates that adequate and preferential development of reproductive organs instead of other organs occurs between 16 to 24 wk to attain improved reproductive performance rather than at 7 to 15 wk of age. The consequence of this delayed growth was an extension of the age at which sexual maturity was attained in these groups compared with their counterparts fed for ad libitum intake at 7 to 15 wk, which matured earlier. For an assessment of a good reproductive performance, our data suggest that ovary and oviduct weight should be above 1.70 and 1.58% of body weight respectively at day of first egg. The cLHRH-I levels in the median eminence of groups followed that of growth in response to feeding levels and the timing of feeding. Levels in pullets fed for ad libitum intake at 7 to 15 wk were significantly higher than those in feed-restricted birds. At 18 wk of age, ad libitum feeding from 16 wk following feed restriction from 7 to 15 wk increased the cLHRH-I level, but it remained low in feedrestricted birds. However, at age at first egg, all groups had similar levels of cLHRH-I in the median eminence. The groups that exhibited late increases in cLHRH-I levels correspond with those with the highest egg production, highest proportional ovary and oviduct weights, latest age at first egg, and with late compensatory growth (between 18 and 24 wk). The results confirm the finding that the onset of sexual maturation is associated with increased levels of hypothalamic cLHRH-I in layers (Sharp et al., 1990) and broiler breeder females (Bruggeman et al., 1998a). Pituitary contents of LH and FSH mimic the trend of cLHRH-I levels in the median eminence at 15 wk and age at first egg. However, levels of FSH were lower than LH levels, especially at 15 wk, indicating that the stimulation of LH synthesis by LHRH-I at this age is probably higher than that of FSH. Despite the differences in body weights between groups at sexual maturation, cLHRH-I levels were similar. Pituitary LH or FSH levels were also equal; yet, there were differences in laying rate. This result suggests the formation of certain factors in the reproductive apparatus that were influenced by the hypothalamic-pituitary axis during the rearing period. The effects of these factors are carried forward to influence reproductive performance after sexual maturation and may constitute the regulator of sensitivity of the ovary or oviduct to LH or FSH. Moreover, we have already shown that feeding levels can modify the sensitivity of the pituitary to cLHRHI, and possibly to gonadal hormones, in differently fed broiler breeder hens (Bruggeman et al., 1998b). It was suprising that no correlation was observed between cLHRH-I and plasma LH or FSH levels. In contrast to the significant depressing effect of feed restriction on LHRH-I and pituitary LH, no clear effect of the level of feed intake or period of restriction was observed on
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BRUGGEMAN ET AL. Krishnan, K. A., J. A. Proudman, and J. M. Bahr, 1994. Purification and partial characterization of isoforms of luteinizing hormone from the chicken pituitary gland. Comp. Biochem. Physiol. 108B:253–264. Leeson, S., and J. D. Summers, 1983. Consequence of increased feed allowance for growing broiler breeder pullets as a means of stimulating early maturity. Poultry Sci. 62:6–11. McDaniel, G. R., J. Brake, and R. D. Bushong, 1981. Factors affecting broiler breeder performance. 1. Relationship of daily feed intake level to reproductive performance of pullets. Poultry Sci. 60:307–312. Proudman, J. A., and H. Opel, 1981. Turkey prolactin: Validation of a radioimmunoassay and measurement of changes associated with broodiness. Biol. Reprod. 25:573–580. Pym, R.A.E., and J. F. Dillon, 1974. Restricted food intake and reproductive performance of broiler breeder pullets. Br. Poult. Sci. 15:245–259. Robbins, K. R., S. F. Chin, G. C. McGhee, and K. D. Roberson, 1988. Effect of ad libitum versus restricted feeding on body composition and egg production of broiler breeders. Poultry Sci. 67:1001–1007. Robbins, K. R., G. C. McGhee, P. Osei, and R. E. Beauchene, 1986. Effect of feed restriction on growth, body composition and egg production of broiler females through 68 weeks of age. Poultry Sci. 65:2226–2231. SAS Institute 1985. SAS/STAT威 Guide for Personal Computers. Version 6 Edition. SAS Insitute Inc., Cary, NC. Sharp, P. J., I. C. Dunn, G. M. Main, R. J. Sterling, and R. T. Talbot, 1990. Gonadotropin-releasing hormones: Distribution and function. Pages 31–42 in: Endocrinology of Birds. M. Wada, S. Ishii, and C. G. Scanes, ed. Springer-Verlag, Tokyo, Japan. Soller, M., Y. Eitan, and T. Brody, 1984. Effect of diet and early quantitative feed restriction on the minimum weight requirement for the onset of sexual maturity in White Rock broiler breeders. Poultry Sci. 63:1255–1261. Yu, M. W., F. E. Robinson, R. G. Charles, and R. Weingardt, 1992a. Effect of feed allowance during rearing and breeding on female broiler breeders. 2. Ovarian morphology and production. Poultry Sci. 71:1750–1761. Yu, M. W., F. E. Robinson, and A. R. Robblee, 1992b. Effect of feed allowance during rearing and breeding on female broiler breeders. 1. Growth and carcass characteristics. Poultry Sci. 71:1739–1749.
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reared under severe food restriction from day of hatching. Br. Poult. Sci. 21:437–446. Bruggeman, V., E. D’Hondt, L. Berghman, O. Onagbesan, D. Vanmontfort, F. Vandesande, and E. Decuypere, 1998a. The effect of food intake from 2 to 24 weeks of age on LHRH-I content in the median eminence and gonadotrophin levels in pituitary and plasma in female broiler breeder chickens. Gen. Comp. Endocrinol. 112:200–209. Bruggeman, V., O. Onagbesan, D. Vanmontfort, L. Berghman, G. Verhoeven, and E. Decuypere, 1998b. The effect of longterm food restriction on pituitary sensitivity to cLHRH-I in broiler breeder females. J. Reprod. Fertil. 114:267–276. Bruggeman, V., D. Vanmontfort, R. Renaville, D. Portetelle, and E. Decuypere, 1997. The effect of food intake from two weeks of age to sexual maturity on plasma growth hormone, insulin-like growth factor-I, insulin-like growth factor-binding proteins, and thyroid hormones in female broiler breeder chickens. Gen. Comp. Endocrinol. 107:212–220. Etches, R. J., 1993. Reproduction in poultry. Pages 493–530 in: Reproduction in Domesticated Animals. World Animal Science B9. Elsevier Science Publishers, Amsterdam, The Netherlands. Fattori, T. R., H. R. Wilson, R. H. Harms, and R. D. Miless, 1991. Response of broiler breeder females to feed restriction below recommended levels. 1. Growth and reproductive performance. Poultry Sci. 70:26–36. FAWC, 1998. Report on the welfare of broiler breeders. Farm Animals Welfare Council (FAWC), Surbiton, Surrey, U.K. Hocking, P. M., 1993. Effects of body weight at sexual maturity and the degree and age of restriction during rearing on the ovarian follicular hierarchy of broiler breeder females. Br. Poult. Sci. 34:793–801. Hocking, P. M., A. B. Gilbert, M. Walker, and D. Waddington, 1987. Ovarian follicular structure of White leghorns fed ad libitum and dwarf and normal birds fed ad libitum or restricted to point of lay. Br. Poult. Sci. 28:493–506. Hocking, P. M., D. Waddington, M. A. Walker, and A. B. Gilbert, 1989. Control of the development of the follicular hierarchy in broiler breeder pullets by food restriction during rearing. Br. Poult. Sci. 30:161–174. Katanbaf, M. N., E. A. Dunnington, and P. B. Siegel, 1989. Restricted feeding in early and late-feathering chickens. 2. Reproductive responses. Poultry Sci. 68:352–358. Krishnan, K. A., J. A. Proudman, and J. M. Bahr, 1992. Purification and characterization of chicken follicle-stimulating hormone. Comp. Biochem. Physiol. 102B:67–75.
(Key words: broiler breeder, feeding level, critical period, egg production, reproductive axis) 1999 Poultry Science 78:1424–1434
The management practice of broiler breeder females includes the restriction of feed allowance during both rearing and breeding to limit body weight gains, reduce the incidence of obesity, and improve egg production. Although restricted feeding prolongs the time to reach sexual maturity (Leeson and Summers, 1982), the added values in terms of increased egg production, increased fertility, hatchability, egg quality, reduced number of double-yolked or malformed eggs, and reduced mortality (McDaniel et al., 1981; Leeson and Summers, 1982; Katanbaf et al., 1989; Hocking et al., 1987, 1989; Fattori et al., 1991; Yu et al., 1992a; Hocking, 1993) far outweigh this delay in starting lay. The amount of restriction and the timing or duration of restriction, however, vary between operators, and, most certainly, the amount of gain differs. The duration of feed restriction to broiler breeder chickens
has now become an important issue of animal welfare because feed restriction can act as a stressor on the animal (FAWC, 1998). Research reports also seem to disagree on the best timing of restricted feeding. McDaniel et al. (1981) and Yu et al. (1992a,b) have suggested that restriction should cover almost the entire period of rearing (4 to 18 wk) and also breeding. Pym and Dillon (1974) contended that restriction was only necessary during the rearing period. Robbins et al. (1986, 1988) demonstrated that ad libitum feeding during part or all of the laying period increased egg production. Hocking (1993) concluded that restricted feeding of broiler breeder females after 14 wk of age decreased the incidence of multiple ovulations, thus leading to increased egg production. Several studies (Brody et al., 1980; Bornstein and Lev, 1982; Bornstein et al., 1984; Soller et al., 1984; Katanbaf et al., 1989; Yu et al., 1992b) have related the timing and size of growth of certain organs with feeding levels and level of egg pro-
Received for publication December 2, 1998. Accepted for publication July 1, 1999. 1 To whom correspondence should be addressed: [email protected]
Abbreviation Key: cLHRH-I = chicken luteinizing hormone releasing hormone-I; FSH = follicle-stimulating hormone; LH = luteinizing hormone.
INTRODUCTION
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ABSTRACT The objective of this study was to determine whether there exists a critical period during rearing when restricted feeding of broiler breeder hens can be most beneficial on subsequent egg production. Broiler breeder pullets were subjected to combinations of either ad libitum or restricted feeding during three periods before sexual maturity. Body weight gain, feed intake, and egg production were recorded. Ovary and oviduct weights were noted at age of first oviposition. At 15 and 18 wk of age and at age of first oviposition, chicken luteinizing hormone releasing hormone-I (cLHRH-I) in the median eminence and the levels of luteinizing hormone (LH) and follicle-stimulating hormone (FSH) in the pituitary and plasma were determined. The results demonstrated that alternation between ad libitum and restricted feeding dur-
RESPONSE OF BROILER BREEDER FEMALES TO FEED RESTRICTION
MATERIALS AND METHODS General Management of Animals Five hundred 1-d-old female Hybro G broiler breeder chicks (Euribrid, Boxmeer, The Netherlands) were raised in floor pens littered with wood shavings and supplied with suspended drinkers. The photoperiod was 23 h light (L) and 1 h dark (D) during the first week. Thereafter, light was decreased by 3 to 4 h/wk to 8 L:16 D at Week 6. Birds were photostimulated from 19 wk of age onward by increasing the photoperiod by 2 h weekly to reach 14 L:10 D at 21 wk of age. Birds were fed a standard broiler starter diet from 0 to 3 wk of age (2,800 kcal/kg metabolizable energy, 18% crude protein) followed by chick grower pellet (2,700 kcal/kg metabolizable energy, 15% crude protein). Three weeks before the expected start of egg laying, the birds were fed prelay feed (2,750 kcal/kg metabolizable energy, 14% crude protein), followed by a breeder layer mash (2,750 kcal metabolizable energy, 17% crude protein). The amount of feed allowance to birds depended on the experimental protocol. All birds had unrestricted access to water.
Experimental Design During the 1st wk, all birds consumed feed for ad libitum intake. At 7 d of age, birds were divided into two groups: one group had ad libitum access to feed, and the second group was fed a restricted quantity of feed according to breeder company recommendations. At 7 wk of age, these two groups were each subdivided into two groups: one of each group was allowed feed for ad libitum intake, and the other was fed a restricted quantity of feed. A similar subdivision was made in each of the four groups at the age of 16 wk, resulting finally in eight experimental
FIGURE 1. Schematic presentation of the division of the broiler breeder hens in feeding groups, resulting in eight groups at Week 16. The bold letter in italic indicates the feeding level during the corresponding period. Res (R) = restricted feeding; Ad lib (A) = ad libitum access to feed.
groups. One-half of each group was either fed for ad libitum intake or feed restricted. This feeding regimen was continued until just after the first oviposition. Birds of each treatment group were divided into two pens randomly distributed in the housing facility. A flow diagram of the feeding schedule is shown in Figure 1. Table 1 presents the amount of feed provided to the restricted birds and the weights of feed consumed by birds that were allowed ad libitum access to feed. Precautionary measures were taken such that birds did not develop crop problems during transition from restricted to ad libitum feeding. The change of feeding level from restricted to ad libitum at end of 15 wk was by the gradual increase in amount of feed over 7 d. At 18 wk of age, birds of all groups were individually caged to observe the date of first oviposition and to continue keeping egg laying records until 50 wk of age. During the laying period, all birds consumed layer feed ad libitum; this period began just after the first oviposition. From 2 wk onward, body weight was recorded weekly by weighing 15 birds randomly chosen from each treatment group. Feed intakes of each of the ad libitum fed groups were recorded. At Weeks 15 and 18 and at age of first oviposition, eight birds per group were killed by cervical dislocation. Blood samples were collected and centrifuged, and plasma was stored at −20 C until assayed for LH (luteinizing hormone) and FSH (follicle-stimulating hormone). The median eminences were collected for cLHRH-I (chicken luteinizing hormone releasing hormone-I) determination. The pituitaries were also excised for LH and FSH content determinations at 15 wk of age and at age of first oviposition. At the age of first oviposition, ovaries and oviducts were collected and weighed. Laying performance was followed until 50 wk of age. Eggs produced were sorted into settable and defective eggs (soft-shell, shell-less, cracked, double-yolked eggs).
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duction. These reports suggest that there are critical periods within either the rearing period or breeding period when restricted feeding imparts its effect to improve reproductive performance. The aim of this study was to determine whether there exists a critical period during rearing when restricted feeding of broiler breeder hens can be most beneficial on subsequent egg production. For this purpose, the rearing period was subdivided into three parts during which ad libitum and restricted feeding were alternated, and these birds were compared with those fed for ad libitum intake or feed restricted throughout the three periods. The choice of this division was based on the aforementioned literature on effects of feeding levels during rearing on growth and reproductive characteristics and on previous results (Bruggeman et al., 1997; Bruggeman, 1998a). These findings showed that from 2 to 7 wk, significant changes occurred in plasma metabolic hormones as an effect of restricted feeding compared with full feeding. The period around Week 16 appeared to be important for initiating the development and functioning of the reproductive axis in broiler breeder females.
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BRUGGEMAN ET AL. TABLE 1. The amount of feed (g) provided to the feed restricted (R) birds or taken in by the birds fed for ad libitum intake (A) on a daily basis per individual and per week1 Period 1 Week 2 3 4 5 6
R
A 22 34 53 93 122
RR
RA
AR
AA
47 55 57 59 61 62 65 67 69
155 154 237 152 203 196 118 177 190
47 55 57 59 61 62 65 67 69
178 126 229 144 218 215 134 224 175
Period 3 Week
RRR
RRA
RAR
RAA
ARR
ARA
AAR
AAA
16 17 18 19 20 21 22 23 24 25
75 80 85 90 100 110 120 130 140 150
117 232 230 231 240 285 324 207 243 217
75 80 85 90 100 110 120 130 140 150
174 184 201 221 208 259 139 198 204 211
75 80 85 90 100 110 120 130 140 150
117 206 203 199 207 241 275 254 293 261
75 80 85 90 100 110 120 130 140 150
175 183 214 203 219 131 203 219 205 214
Period 2 Week 7 8 9 10 11 12 13 14 15
1 For group abbreviations see Figure 1. The bold letter in italic indicates the feeding level during the corresponding period.
Hormone Assays Chicken Luteinizing Hormone Releasing HormoneI Assay. Chicken luteinizing hormone releasing hormone-I was determined by RIA as previously described by Bruggeman et al. (1998a). Luteinizing Hormone Assay. Luteinizing hormone was measured using a homologous RIA (Krishnan et al., 1994). Reagents, including cLH, were kindly donated by USDA Animal Hormone Program2. Chicken LH was radioiodinated by the chloramine-T procedure according to the procedure of Proudman and Opel (1981). The iodinated protein was separated by gel filtration on a PD10 column3. The assay was performed according to the recommendations supplied with the RIA kit. Separation of bound and free radioactivity was achieved by incubation with a second antibody-coated cellulose suspension4, centrifugation, and removal of the supernatant by aspiration. The lowest detectable level of LH was 0.1 ng/ml. Cross-reactivity of the antibody used with cFSH was <3% and <0.9% for turkey prolactin, cGH, or recombinant cGH. The intra- and interassay coefficients of variation were 3.3 and 7.6%, respectively.
2
ARS, Beltsville, MD 20705. Pharmacia Biotech Benelux, 4704 AT Roosendaal, The Netherlands. Innogenetics, 9000 Gent, Belgium.
3 4
Follicle-Stimulating Hormone Assay. Follicle-stimulating hormone was measured using a homologous RIA. The chicken FSH RIA kit provided by the USDA Animal Hormone Program2 included a highly purified preparation of FSH (USDA-cFSH-K-I; Krishnan et al., 1992), used as a standard, and a polyclonal rabbit antiserum (USDAAcFSH-16). The FSH was iodinated by the chloramine-T procedure according to the procedure of Proudman and Opel (1981). The iodinated protein was separated on a PD-10 column3 followed by further purification on Sephadex G-75 column3. The RIA was carried out according to the instructions that came with the RIA kit. The detection level of the assay was 60 pg/tube. The antiserum used showed no cross-reaction with different purified preparations of LH, turkey LH, cGH, and turkey prolactin. The intra- and interassay coefficients of variation were 4.8 and 8.4%, respectively.
Statistical Analysis Data are expressed as means ± SEM. Results were analyzed by ANOVA with group and age as factors. Statistical differences were assessed by Duncan’s multiple range test (General Linear Models procedure; SAS Institute, 1985). Relationships among hormones were analyzed by the Pearson correlation procedure (SAS Institute, 1985). P-values <0.05 were considered statistically significant.
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19 24 29 34 40
RESPONSE OF BROILER BREEDER FEMALES TO FEED RESTRICTION
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FIGURE 2. Body weight curves from 2 until 32 wk of age of broiler breeder hens fed under different feeding regimens during rearing. For group abbreviations, see Figure 1. R = restricted; A = ad libitum access to feed.
Body Weights Figure 2 shows the body weight curves of the eight groups of birds fed at different feeding levels from 2 wk of age up to 32 wk. The curves show that between 7 and 15 wk of age, the body weight curves of the RA and AA (R = restricted fed; A = ad libitum feeding) groups on the one hand, and those of the RR and AR on the other, were steeply divergent. At the end of this period of the feeding regimen, the body weights of ad libitum groups (RA and AA) were about twice as high as those of the restricted groups (RR and AR). Between 16 and 24 to 26 wk, ad libitum feeding resulted in a steep compensatory body weight gain in birds that had been restricted in the preceeding period (ARA and RRA). Restriction during this final period following previous restriction (ARR and RRR) reduced growth rate, leading to significantly lower weight in these birds compared with their counterparts fed for ad libitum intake during this period. Chickens fed for ad libitum intake or feed restricted during this period caused only a moderate increase in BW of chickens that had been fed for ad libitum intake during the previous period (RAA, RAR, AAA, or AAR).
Age, Body Weight, Ovary Weight, and Oviduct Weight at First Egg Table 2 summarizes the results for body weight at 6, 15, and 18 wk and at age at first egg. It also shows the age and ovary and oviduct weights at first egg for the eight groups of chickens. Age at first egg was earliest for the RAA group and latest for the RRR group. Ages at first egg were negatively correlated with body weights at first egg in the AAA/RAA and ARR/RRR groups. The feeding level during the first period did not affect age at first oviposition. An interaction (P < 0.04) between the first and the second period was found. The data show that feeding during the second and third periods is a more important determinant of age or body weight at first egg. Restriction during the third period in these birds
after restriction during the second period led to reduced body weights and later age at first egg (RRR or ARR). Ad libitum or restricted feeding during the third period following a previous ad libitum feeding during the middle period lowered age at first egg (RAA, RAR and AAA, AAR). At the age of first oviposition, absolute weights of the ovary in the eight groups did not differ. This finding probably indicates that a threshold of ovary weight must be achieved before sexual maturity is attained, whatever the feeding regimen that might have been applied. However, as a percentage of body weight, there were significant differences among the groups. Interactions between the second and third periods of feeding were observed for ovary weights (P < 0.0001). Birds that were restricted during all three periods (RRR) of feeding showed the highest value. Birds that consumed feed for ad libitum intake during the second period followed by ad libitum intake or restricted feeding during the third period showed the lowest ovary weights as a percentage of body weight (AAA, AAR, RAA, or RAR), with the exception of the RRA group. Those that consumed feed for ad libitum intake or were restricted after a restriction during the second period and ad libitum feeding during the first period showed intermediate values (ARA and ARR). Oviduct weights expressed as percentage of body weights followed a trend similar to ovary weights in percentages. An interaction between the second and third period of feeding on oviduct weight was also observed (P < 0.0001). The highest values were found in the RRR, RRA, ARR, ARA, and RAR groups. The values for the AAA, RAA, and AAR groups were lower.
Egg Production The analysis of egg production data is presented in Table 3. The average number of eggs per week per bird, the cumulative egg production, and settable eggs from onset of lay to 50 wk of age are presented for the eight groups of birds. Generally, chickens restricted during the middle period (ARA, RRR, RRA, and ARR) showed the highest average weekly egg production. The group fed
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RESULTS
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TABLE 2. Body weights at 6, 15, and 18 wk of age and at age at first egg. Body weights, ovary, and oviduct weights are presented at age at first egg for the broiler breeder hens fed under different feeding regimens during rearing1 Feeding regimen R Week 6 Body weight, g
A 929
± 87a RAR
1,840
RR Week 15 Body weight, g
1,705 RRR
Week 18 Body weight, g Age at first egg, d At first egg Body weight, g Ovary weights, g Ovary weights, % of body weight Oviduct weights, % of body weight
± 67b RRA
3,570
RAA
ARR
± 40a AR ± 75b ARA
AA 3,610
± 114a AAR
AAA
2,122 179.4
± 118d ± 7.5a
2,792 176.9
± 87c ± 9.8a
3,500 169.1
± 98b ± 11.4ab
4,090 154.6
± 102a ± 7.3b
2,005 174.4
± 70d ± 2.6a
2,800 166.7
± 62c ± 9.7ab
3,845 171.8
± 129ab ± 8.0ab
4,405 161.2
± 132a ± 14.8ab
3,393
± 85b
4,290
± 127a
4,487
± 208a
4,633
± 125a
3,177
± 108b
4,288
± 130a
4,656
± 144a
4,710
± 157a
68.8
± 3.7
a
66.7
± 5.9
a
70.4
± 7.2
a
72.3
± 6.5
a
56.3
± 3.9
a
73.5
± 7.3
a
70.5
± 3.3
a
62.9
± 4.3a
2.03 ± 0.11a
1.55 ± 0.13bc
1.56 ± 0.13bc
1.56 ± 0.14bc
1.75 ± 0.10ab
1.70 ± 0.14abc
1.52 ± 0.06bc
1.35 ± 0.10c
1.69 ± 0.09a
1.58 ± 0.09ab
1.55 ± 0.11ab
1.21 ± 0.05c
1.58 ± 0.11ab
1.58 ± 0.08ab
1.35 ± 0.04bc
1.26 ± 0.08c
Means within a row lacking a common superscript differ (P < 0.05). Values are expressed as means ± SEM (n = 8). For group abbreviations, see Figure 1. R = restricted feeding; A = ad libitum access to feed.
a–d 1
BRUGGEMAN ET AL.
± 19b RA
459
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for ad libitum intake throughout the periods (AAA) showed the lowest egg production per week. Those fed for ad libitum intake during the middle period followed by either ad libitum or restricted feeding were intermediate. The highest cumulative egg production was attained by the ARA group (124.38 ± 3.67 eggs/bird; P < 0.05). The birds on the ad libitum regimen from Week 7 to 15, except the AAR, had significantly lower egg production throughout the laying period compared with their restricted counterparts. A similar trend was observed for the cumulative settable eggs per birds; the group restricted between 7 to 15 wk was the better producing group. The highest number of settable eggs was observed in the ARA group (103.43 ± 3.40 eggs/bird), and the lowest was observed in the AAA group (69.59 ± 3.24 eggs/bird).
1
a–d
Means within a row lacking a common superscript differ (P < 0.05). Values are expressed as means ± SEM (n = 8). For group abbreviations, see Figure 1. R = restricted feeding; A = ad libitum access to feed.
69.59 ± 3.24d 83.32 ± 3.07c 103.43 ± 3.40a 69.77 ± 3.88d Cumulative settable eggs/bird
91.15 ± 2.92b
92.73 ± 2.72b
80.39 ± 3.63c
96.08 ± 3.26ab
83.07 ± 3.51d 108.62 ± 3.58b 124.38 ± 3.67a 91.48 ± 4.13c 108.21 ± 2.68b Cumulative egg production/bird
111.03 ± 2.72b
94.90 ± 4.19c
113.64 ± 3.01b
3.08 ± 0.13d 4.25 ± 0.14ab 4.75 ± 0.14a 4.53 ± 0.12ab 3.40 ± 0.15c 3.54 ± 0.16c 4.49 ± 0.11ab 4.44 ± 0.11ab Average number of eggs/week per bird
AAR ARA ARR RAA RAR RRA RRR
Feeding regimen
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Chicken Luteinizing Hormone Releasing Hormone-I Levels in Median Eminence Chicken luteinizing hormone releasing hormone-I contents in the median eminence increased with age in all groups (P < 0.02) (Figure 3). At Week 15, cLHRH-I contents were lower in the RR and AR groups than in their ad libitum fed counterparts (RA and AA) (P < 0.0001). Ad libitum feed consumption by birds during the third period, following restriction during the second period (ARA and RRA), resulted in higher cLHRH-I contents at Week 18 compared with those of their restricted counterparts (ARR and RRR). This upsurge in cLHRH-I was most pronounced in RRA compared with RRR, two groups that were restricted during the first two periods. The content of cLHRH-I remained low in the RRR and ARR groups until 18 wk but increased thereafter up to the age at first egg (P < 0.0001). In the four groups that were fed for ad libitum intake during the second period (AAA, AAR, RAA and RAR), the increase in cLHRH-I with age was less pronounced. Chicken LHRH-I in these groups at 15 and 18 wk and at age of first egg did not significantly differ. At the age of first oviposition, there were no differences in the content of cLHRH-I in the median eminence among groups.
Pituitary Luteinizing Hormone and Follicle-Stimulating Hormone Content Figure 4 shows the LH and FSH contents of the pituitaries of the eight groups. Significant group effects were observed for pituitary LH content at 15 wk and age at first egg. Feeding ad libitum during the second period increased LH significantly, but restriction kept it low. At Week 15, LH content of the RR and AR groups was lower than that of the ad libitum groups (P < 0.0001). Luteinizing hormone content at first egg was significantly lower also in the RRR group than in the AAA, AAR, and RAA groups. No significant differences were found among the other groups. Chicken LHRH-I contents in the median eminence correlated well with pituitary contents of LH, with an overall correlation coefficient of 0.42 (P < 0.0001).
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TABLE 3. Average number of total and settable eggs per bird per week and cumulative egg production (total and settable)from onset of lay to 50 wk of age1
AAA
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Plasma Luteinizing Hormone and Follicle-Stimulating Hormone
DISCUSSION
FIGURE 3. Chicken luteinizing hormone releasing hormone-I (cLHRH-I) content in the median eminences of broiler breeder hens (mean ± SEM; n = 8) fed under different feeding regimens during rearing. Different letters indicate differences between groups (P < 0.05). For group abbreviations, see Figure 1. R = restricted; A = ad libitum access to feed.
Pituitary content of FSH in the AA group at 15 wk of age was higher than that of other groups (AR, RA, or RR) (P < 0.0001). At age at first egg, however, no group differences in FSH levels were observed. Although FSH levels increased with age until age at first egg, the greatest increase during the third period of feeding occurred in the groups on restricted feeding during the second period (ARA, ARR, RRA, and RRR). Again, cLHRH-I content in the median eminence showed a good correlation with pituitary FSH (r = 0.45; P < 0.0001).
The results of this study show clearly that there are relationships between the levels of feeding during the rearing period, the period of the application of any particular level of feeding, and the subsequent reproductive performance of the broiler breeder females used in this study. Subjecting pullets to combinations of either ad libitum or restricted feeding during the three experimental periods before sexual maturity influenced body weights at sexual maturation, the development of the reproductive apparatus (oviduct and ovary), reproductive hormone levels (cLHRH-I, LH, and FSH), age at first egg, and the subsequent number of eggs produced. The major aim of this study was to detect the best combinations of feeding regimens that would result in increased reproductive performance in terms of settable egg production; the data from this work suggest that restricted feeding during the middle period (between 7 and 15 wk of age) led to increased productivity compared with ad libitum feeding during the same period. The degree of improvement in egg production depended also on the feeding level during the third period following restriction. Ad libitum feeding during the third period yielded a better performance than restricted feeding. Chickens fed for ad libitum intake throughout the three periods had the lowest total and settable eggs, although they reached sexual maturity earliest. Although the level of feeding during each of the three periods had an effect, very significant interactions were found between the second and third periods on many of the parameters measured. The beneficial effect of restricting feed allowance to broiler breeder females has previously been reported (McDaniel et al., 1981; Leeson and Summers, 1982; Katanbaf et al., 1989; Hocking et al., 1987, 1989; Fattori et al., 1991; Yu et al., 1992a; Hocking,
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Figure 5 shows the concentration of LH and FSH in the plasma of chickens at 15 and 18 wk and at age of sexual maturity. Luteinizing hormone levels at the end of the second period showed no consistent changes between feeding groups, although LH levels tended to be higher in the groups fed for ad libitum intake during this period. At 18 wk, there were no significant differences among the eight feeding groups. Ad libitum feeding during the third period up to age at first egg increased LH levels in birds that were feed restricted during the second period (ARA and RRA). No changes in plasma LH concentrations were observed in other groups. No differences were observed in the level of plasma FSH in the four groups at the end of the second period of feeding or at the age at first egg; however, plasma FSH levels differed between groups at wk 18, with the lowest level in the RAR group (P < 0.0001). There were no correlations between cLHRH-I and plasma LH or FSH. Similarly, no correlations could be established between pituitary and plasma LH or FSH.
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1993). However, the question had always been the best timing for restriction to attain the best reproductive performance. Yu et al. (1992a) showed that restriction from 4 until 18 wk of age resulted in the best egg production. Hocking (1993) concluded that feed restriction should be continued until the onset of lay because multiple ovulations are a major source of lost egg production when they are not reduced from 15 wk of age onward. The data in the present study narrowed the critical period, which may be between Weeks 7 and 15 when restricted feeding could be applied to obtain improved reproductive performance in broiler breeder females. This finding suggests that the current practice of long-term feed restriction may not be necessary for improved reproductive performance, which is especially important in view of recent concerns about the effect of long-term feed restriction on the welfare of the animals (FAWC, 1998). The physiological basis on which feed restriction modifies reproductive performance is not understood. The effects of feed intake on body weight gain and body composition during rearing or breeding have been reported
(Katanbaf et al., 1989; Yu et al., 1992b). A minimum age, body weight, lean body mass, shank length, or body fat composition before sexual maturation has been postulated (Brody et al., 1980; Bornstein et al., 1984; Soller et al., 1984). Yu et al. (1992b) stressed that controlling feed intake and growth from 4 to 18 wk is more important in determining age at sexual maturity than feed intake and changes in body composition from Week 18 until onset of lay. Feed restriction also modifies the development of the hypothalamo-pituitary axis, which produces the cLHRH-I, LH, and FSH that are important for development of the reproductive apparatus (Bruggeman et al., 1998a). The data in this study demonstrate that feed restriction modifies, in concert, many parameters that have consequences on the subsequent reproductive performance of the broiler breeder pullet. The results demonstrate that restricted feeding throughout the three periods reduced body weight, delayed age of sexual maturation, and produced the proportionally highest ovary and oviduct weight. Pullets that consumed feed for ad libitum intake throughout had the
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FIGURE 4. Luteinizing hormone (LH) and follicle-stimulating hormone (FSH) contents in the pituitaries of broiler breeder hens (mean ± SEM; n = 8) fed under different feeding regimens during rearing at 15 wk of age (upper panel) and at age at first egg (lower panel). Different letters indicate differences between groups (P < 0.05). For group abbreviations, see Figure 1. R = restricted; A = ad libitum access to feed.
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FIGURE 5. Luteinizing hormone (LH) and follicle-stimulating hormone (FSH) plasma concentrations of broiler breeder hens (mean ± SEM; n = 8) fed under different feeding regimens during rearing at 15 (upper panel) and 18 wk of age (middle panel) and at age at first egg (lower panel). Different letters indicate differences between groups (P < 0.05). For group abbreviations, see Figure 1. R = restricted; A = ad libitum access to feed.
highest body weights, the youngest age at first egg, but the smallest proportional ovary and oviduct weights. Alternation between ad libitum and restricted feeding during the three periods changed the growth curves of the different groups during these periods. The growth spurt observed in pullets fed for ad libitum intake during the second period (7 to 15 wk) was shifted to the third period (18 to 24 wk) for pullets that were restricted during the second period but fed for ad libitum intake during the third. Birds that consumed feed for ad libitum intake during the second period but were restricted during the third
period did not significantly decrease their body weight; they had similar weights to those fed for ad libitum intake throughout the rearing period. Despite the late compensatory growth between Weeks 16 to 22 by pullets restricted at 7 to 15 wk, they never reached the body weights of those that consumed feed for ad libitum intake during the middle period (7 to 15 wk). The data suggest that the excessive body weights, which probably adversely affected their reproductive performance, was added during the 7 to 15 wk of rearing age. Furthermore, growth during this period may be unconnected with the development
RESPONSE OF BROILER BREEDER FEMALES TO FEED RESTRICTION
plasma LH or FSH concentrations during the period before the onset of lay. A similar result has been reported previously (Bruggeman et al., 1998a) and suggests a disconnection between cLHRH-I and gonadotrophin storage in the pituitary on the one hand, and between cLHRH-I and gonadotrophin release on the other. These data on hormone levels have shown that feeding levels and their timing influence the development of the hypothalamopituitary axis. Secretions of the axis are known to influence the development and functioning of the ovary and oviduct (Etches, 1993) and, subsequently, egg production. The results of the present study show that this axis matures earlier in full-fed birds and is delayed by feed restriction. Moreover, the development of the axis under the different regimens seemed to fall within the period of rapid growth. The delay in the maturation of this axis until 18 to 22 wk in birds restricted at 7 to 15 wk of age may be more appriopiate and preferential for the development of the reproductive apparatus to attain subsequently improved egg production. In conclusion, the results show that the feeding level, timing, and duration of application during the period before the attainment of sexual maturity has important repercussions on growth parameters and the maturation of the reproductive axis (hypothalamic-pituitary and ovary-oviduct development). Moreover, these two axes are closely linked to one another in determining age at first oviposition in broiler breeder females when threshold levels of body weight, body composition, and age were attained. The age at the onset of lay was stringently related to the developmental changes at the hypothalamic-pituitary level. The effects of restricted feeding during rearing were carried over to the laying period with clear effects on the functioning of the reproductive axis (egg production). Our data suggest that restriction applied at 7 to 15 wk of age followed by either ad libitum feeding or continued feed restriction were best for improving reproductive performance in broiler breeder females.
ACKNOWLEDGMENTS We are grateful to J. A. Proudman for providing the USDA FSH RIA kit. Veerle Bruggeman was supported by Grant Number 942009 of the Vlaams Instituut voor de bevordering van het Wetenschappelijk-Technologisch onderzoek in de industrie (IWT). This research was supported by Het Onderzoeksfonds (OT-project OT/95/19). Luc Berghman was supported by the Fund for Scientific Investigation (FWO).
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of organs of reproduction. This lack of connection is suggested by the fact that, although absolute ovary weights were similar, when stated as a percentage of body weights, feed-restricted birds had higher ovary and oviduct weights than did birds fed for ad libitum intake. This higher proportional weight of the ovary and oviduct possibly indicates that adequate and preferential development of reproductive organs instead of other organs occurs between 16 to 24 wk to attain improved reproductive performance rather than at 7 to 15 wk of age. The consequence of this delayed growth was an extension of the age at which sexual maturity was attained in these groups compared with their counterparts fed for ad libitum intake at 7 to 15 wk, which matured earlier. For an assessment of a good reproductive performance, our data suggest that ovary and oviduct weight should be above 1.70 and 1.58% of body weight respectively at day of first egg. The cLHRH-I levels in the median eminence of groups followed that of growth in response to feeding levels and the timing of feeding. Levels in pullets fed for ad libitum intake at 7 to 15 wk were significantly higher than those in feed-restricted birds. At 18 wk of age, ad libitum feeding from 16 wk following feed restriction from 7 to 15 wk increased the cLHRH-I level, but it remained low in feedrestricted birds. However, at age at first egg, all groups had similar levels of cLHRH-I in the median eminence. The groups that exhibited late increases in cLHRH-I levels correspond with those with the highest egg production, highest proportional ovary and oviduct weights, latest age at first egg, and with late compensatory growth (between 18 and 24 wk). The results confirm the finding that the onset of sexual maturation is associated with increased levels of hypothalamic cLHRH-I in layers (Sharp et al., 1990) and broiler breeder females (Bruggeman et al., 1998a). Pituitary contents of LH and FSH mimic the trend of cLHRH-I levels in the median eminence at 15 wk and age at first egg. However, levels of FSH were lower than LH levels, especially at 15 wk, indicating that the stimulation of LH synthesis by LHRH-I at this age is probably higher than that of FSH. Despite the differences in body weights between groups at sexual maturation, cLHRH-I levels were similar. Pituitary LH or FSH levels were also equal; yet, there were differences in laying rate. This result suggests the formation of certain factors in the reproductive apparatus that were influenced by the hypothalamic-pituitary axis during the rearing period. The effects of these factors are carried forward to influence reproductive performance after sexual maturation and may constitute the regulator of sensitivity of the ovary or oviduct to LH or FSH. Moreover, we have already shown that feeding levels can modify the sensitivity of the pituitary to cLHRHI, and possibly to gonadal hormones, in differently fed broiler breeder hens (Bruggeman et al., 1998b). It was suprising that no correlation was observed between cLHRH-I and plasma LH or FSH levels. In contrast to the significant depressing effect of feed restriction on LHRH-I and pituitary LH, no clear effect of the level of feed intake or period of restriction was observed on
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reared under severe food restriction from day of hatching. Br. Poult. Sci. 21:437–446. Bruggeman, V., E. D’Hondt, L. Berghman, O. Onagbesan, D. Vanmontfort, F. Vandesande, and E. Decuypere, 1998a. The effect of food intake from 2 to 24 weeks of age on LHRH-I content in the median eminence and gonadotrophin levels in pituitary and plasma in female broiler breeder chickens. Gen. Comp. Endocrinol. 112:200–209. Bruggeman, V., O. Onagbesan, D. Vanmontfort, L. Berghman, G. Verhoeven, and E. Decuypere, 1998b. The effect of longterm food restriction on pituitary sensitivity to cLHRH-I in broiler breeder females. J. Reprod. Fertil. 114:267–276. Bruggeman, V., D. Vanmontfort, R. Renaville, D. Portetelle, and E. Decuypere, 1997. The effect of food intake from two weeks of age to sexual maturity on plasma growth hormone, insulin-like growth factor-I, insulin-like growth factor-binding proteins, and thyroid hormones in female broiler breeder chickens. Gen. Comp. Endocrinol. 107:212–220. Etches, R. J., 1993. Reproduction in poultry. Pages 493–530 in: Reproduction in Domesticated Animals. World Animal Science B9. Elsevier Science Publishers, Amsterdam, The Netherlands. Fattori, T. R., H. R. Wilson, R. H. Harms, and R. D. Miless, 1991. Response of broiler breeder females to feed restriction below recommended levels. 1. Growth and reproductive performance. Poultry Sci. 70:26–36. FAWC, 1998. Report on the welfare of broiler breeders. Farm Animals Welfare Council (FAWC), Surbiton, Surrey, U.K. Hocking, P. M., 1993. Effects of body weight at sexual maturity and the degree and age of restriction during rearing on the ovarian follicular hierarchy of broiler breeder females. Br. Poult. Sci. 34:793–801. Hocking, P. M., A. B. Gilbert, M. Walker, and D. Waddington, 1987. Ovarian follicular structure of White leghorns fed ad libitum and dwarf and normal birds fed ad libitum or restricted to point of lay. Br. Poult. Sci. 28:493–506. Hocking, P. M., D. Waddington, M. A. Walker, and A. B. Gilbert, 1989. Control of the development of the follicular hierarchy in broiler breeder pullets by food restriction during rearing. Br. Poult. Sci. 30:161–174. Katanbaf, M. N., E. A. Dunnington, and P. B. Siegel, 1989. Restricted feeding in early and late-feathering chickens. 2. Reproductive responses. Poultry Sci. 68:352–358. Krishnan, K. A., J. A. Proudman, and J. M. Bahr, 1992. Purification and characterization of chicken follicle-stimulating hormone. Comp. Biochem. Physiol. 102B:67–75.