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PRODUCTION, MODELING, AND EDUCATION |
* Institut Technique de l’Aviculture, BP1, 37380 Nouzilly, France; Institut National de la Recherche Agronomique (INRA), UR83 Recherches Avicoles, 37380 Nouzilly, France; and INRA, UMR85 Physiologie de la reproduction et du comportement, 37380 Nouzilly, France
1 Corresponding author: bouvarel.itavi{at}tours.inra.fr
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: sequential feeding • growth performance • protein • energy • feeding behavior
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Sequential feeding with distinct dietary concentrations of energy and amino acids on alternate days has resulted in a similar efficiency compared with a complete feed; this might provide new opportunities to modulate growth (Bouvarel et al., 2004) and to adapt the diet to short-term temperature variations (Lozano et al., 2006). The first research into sequential feeding dates from the 1970s. Gous and Du Preez (1975) found that when broilers were offered 2 feeds with different amino acid compositions for alternate 6-h periods, the birds were able to adjust their intakes to receive a balanced amino acid intake, but with 12-h alternate feeding there was a deleterious effect on growth rate. Rosebrough et al. (1989) fed broiler chicks high- and low-protein feeds during alternate 24-h periods and observed a decrease in growth. More recently, Bouvarel et al. (2004) showed in a series of experiments that extreme differences between the composition of the 2 sequential feeds (CP = 300 and 90 g/kg) at 24 h compared with a 48-h cycle of feed distribution had deleterious effects on growth and body composition. In the same studies, experimentations on sequential feeding in 48-h cycles showed that this technique had no negative effect on performance and digestibility of nutrients and very limited effects on muscle and fat deposition in broiler chickens, if the consumption of the sequential feeds provided an energy and amino acid intake similar to the control diet. Lastly, a field trial with 8 flocks of broilers confirmed that feeding high-protein low-energy and low-protein high-energy feeds on alternate days resulted in similar performance to that from feeding a complete feed, despite large day-to-day variations in protein intake. It emerges from these experiments (Bouvarel et al., 2004) that sufficient intake of distinct feeds is essential to reach an overall nutritional balance with sequential feeding.
The present study aimed 1) at evaluating the main effects of energy and protein contents on feed intake during several feeding cycles, 2) to quantify the adaptation of chickens exposed to sequential feeding at different ages, and 3) to quantify time spent in the major behavioral patterns and the occurrence of abnormal gait in the birds. In fact, the occurrence of leg abnormalities may be reduced with alternation of diets varying in energy and protein content (Bouvarel et al., 2004).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Nine hundred 1-d-old male broiler chicks (Ross PM3) were wing-banded and randomly distributed into 45 pens (1.6 x 1.75 m, 20 chicks per pen, 9 pens per treatment) in an environmentally controlled poultry shed at the Poultry Research Center in Nouzilly, France. The floor was covered with wood shavings. Lighting was reduced from daily 24L:0D to 14L:10D after the age of 2 d and was then increased to daily 16L:8D at the age of 7 d. Environmental temperature was progressively reduced from 32 to 23°C, and then maintained at this temperature after the age of 27 d. Feed was provided in linear feeders. All the chickens received the same starter diet (2,900 kcal/kg of ME, 21% CP). From 10 to 29 d of age, chickens were given control or sequential treatments.
Seven diets were used during the sequential feeding period (Table 1
). The control treatment was complete feed (3,000 kcal/kg of ME, 19.5% CP). Two diets were isoenergetic with differences in protein and essential amino acid contents: the high-protein feed (P+ = 23.4% CP) and the low-protein feed (P– = 15.6% CP). Two diets were isoproteic with differences in ME content: the low-energy feed (E– = 2,800 kcal/kg of ME) and the high-energy feed (E+ = 3,200 kcal/kg of ME). Two diets had differences in both protein and energy contents: the high-protein and low-energy feed (P+E–) and the low protein and high-energy feed (P–E+). Diets (i.e., P+ and P–, E– and E+, and P+E– and P–E+) were formulated to provide on average (50/50) the same nutrient intake as the control feed.
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All the chickens received the same feed during the withdrawal period (30 to 35 d of age) (3,050 kcal/kg of ME, 17.5% CP).
Physical Characteristics of Feeds
The diets were manufactured on a semiindustrial scale by the experimental feed mill at the Poultry Research Center in Nouzilly. They were pelleted using a steam pelleter (Ø = 2.5 mm, L = 47 mm).
One sample of each prepared diet was used for the following measurements. Fine particles were weighed (±0.1 g) after screening 200 g of diet on a 0.6-mm screen. Two replicate measurements were taken for each diet. The percentage of fine particles in the pellets was very low, being 0.6% on average and similar between treatments. Pelleted feed resistance to abrasion was measured using a SABE (SABE Distribution, Chauche, France) durabilimeter with 500-g samples treated for 20 s using a 2-mm screen. Durability was expressed as the percentage of pelleted particles that resisted abrasion by weighing the fine particles (±0.01 g). Resistance to abrasion for the control feed was 86.0% and ranged from 60.4 to 95.2 for the experimental diets (Table 1
). Hardness was measured in 100 pellets of each diet using an Instron 5543 machine (Instron, Guyancourt Cedex, France). Hardness was expressed as the maximum load necessary to break the outer surface of the particle (MPa). Hardness of pellets ranged from 0.80 (soft) to 2.13 MPa (hard) for the experimental diets, the control diet was intermediate (1.26 Mpa; Table 1). Pellet length was measured individually using calipers (200 repetitions/feed). They varied from 4.1 to 5.2 mm, with the control diet being of an intermediate length (4.5 mm). Color was measured using a Commission International d’Eclairage L*a*b*c* Hunterlab spectrocolorimeter (Socemi, Metz, France). Mean L* and C* parameters varied from 54.7 to 58.4 and 26.9 to 34.6, respectively (Table 1). Physical characteristics were dependent on the composition of the feed. A high level of energy obtained by adding oil decreased hardness, resistance to abrasion, length of pellets, and modified color.
Measurements Performed on Broiler Chicks
Chicken BW was individually measured at 9, 17, 30, and 35 d of age. From 10 to 29 d, feed intake was recorded each day by weighing uneaten feed in each feeder. After exposure to the new feed, and after 2 and 6 h, the percentage of time allocated to 1) eating, 2) standing, 3) pecking, scratching on the floor, or both was measured for the third and seventh cycles. Each pen was observed for 40 s, at 10-min intervals, by 3 different observers.
Each bird was observed in its pen at 34 d of age and assigned into different categories of walking ability by 2 observers, according to a classification adapted from Kestin et al. (1992). There were 5 categories of gait score, from 0, corresponding to a bird that walked normally with no detectable abnormality, to 4 designating a bird that had a severe gait defect but was still capable of walking with difficulty and only when strongly motivated. A score of 5 was not included because birds with such a gait score would no longer have been able to walk and would have been culled beforehand. Birds with a gait score of 3 and 4 were considered to have abnormal gait.
At 35 d of age, 4 or 5 chickens per pen whose weights were closest to the pen mean weight were slaughtered (40 broilers per treatment). Breast muscle and abdominal fat weights were recorded. At 24 h postmortem, the ultimate pH (pHu) of the pectoral muscle was measured with a portable pH meter (model 506, Crison Instruments, Barcelona, Spain) by inserting a glass electrode directly into the thickest part of the pectoralis major muscle.
Statistical Analysis
All data were analyzed using STATVIEW program version 5. Tested factors were considered as significantly different if P < 0.05. All the data were expressed per pen as an experimental unit.
A 3-way ANOVA was performed on the variables
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where Ri = treatment effect (i = 1, 2, 3, 4 between 10 to 17 d and 1, 2, 3, 4, 5 after 17 d). Treatment SEPB was considered as a control for 10 to 17 d period. Bj = row-block effect; Ck = line-block effect; and 
ijkl= residual.
When significant (P < 0.05) the treatment means were tested using Newmann and Keul’s test. A repeated-measure analysis was performed to test the changes in the proportion of feed eaten on the first day of each cycle compared with the second day during each period.
Behavior pattern and gait score were analyzed with nonparametric tests. Cycle day effects were tested with the Wilcoxon test and treatment effects with the Kruskall Wallis and Mann-Whitney U-tests. The frequency of birds with abnormal gait was tested with a 
2 test.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Ten chickens died or were culled during the experiment, of which 3 of 180 were controls, and 7 of 720 were sequentially fed. Compared with the control diet, there were no differences in total feed intake with the sequential treatments for the first (10 to 17 d of age) or second period (18 to 29 d of age; Table 2). Although the total feed intake was similar across all treatments over the experimental period, chicks did not eat the same proportion of both diets. For the first period, the proportion of feed eaten on days with the E– or P+E– sequential treatment was lower than for the control diet. Chickens overconsumed E+ or P–E+ the second day of the cycle. However, the proportion of feed eaten on days with the P+ was similar to the control diet. For the second period, the proportion of feed eaten on the first days of the cycle was lower for all sequential feeds than for the control diet. The proportion of P+ (46.8%) was the closest to the control diet (48.5%). The proportion of P+E– eaten was lower when sequential feeding began from 10 d compared with 18 d of age (43.2 vs. 44.5%, P < 0.05). The proportion of feed eaten on the first days for the first period was similar for the different cycles. For the second period, a significant effect of time was observed, due to the gradual/progressive decrease of the proportion of P+E– feed intake for SEPA and SEPB (P < 0.01).
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Compared with the control diet, there were no differences in BW with the sequential treatments at 17, 30, and 35 d of age (Table 3). Feed:gain ratio, energy conversion ratio (kilocalories of ME:grams of weight gain), and protein conversion ratio (grams of CP:grams of weight gain) were similar for all treatments from 9 to 17 d of age. Feed:gain ratio and energy conversion ratio increased for SP, SEPA, and SEPB compared with C and SE from 18 to 30 d of age (P < 0.01), and protein conversion ratio was higher for SEPB compared with SE. Between 0 and 35 d of age, feed:gain ratio for SEPA and SEPB were the highest (P < 0.01; data not shown).
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The proportion of chickens standing was significantly increased between d 1 and 2 for cycles 3 and 7 for SP, and for cycle 7 for SEPA and SEPB (data not shown, similar to SEPA), 2 and 6 h after distribution of feed in the morning (Figure 1). No differences were observed for C and SE. The proportion of chickens eating increased significantly between d 1 and 2 for cycles 3 and 7 for SE and SEPA and for cycle 7 for SEPB (data not shown, similar to SEPA). This difference appeared immediately after feed distribution for the 3 regimens and again 2 h after for SE. The proportion of chickens pecking, scratching, or both was modified between d 1 and 2 only for SP and SE. For SP, it increased immediately and 6 h after feed distribution the second day for cycle 3 only. For SE, it decreased 2 h after feed distribution for cycles 3 and 7.
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). Mean gait scores averaged 1.71 and were not significantly different among treatments. Carcass Conformation
Breast yield and abdominal fat did not differ between treatments (Table 3). The pHu of breast meat was significantly lower for chickens receiving diets varying in protein contents (5.9) than other treatments (>6.0). The highest pHu of breast meat was obtained with the control treatment.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The independent effects of energy and protein contents on feed intake were evaluated in this experiment (Table 2). The proportion of high-protein feed intake was similar to the controls in the early period. In the second period, the proportion of high-protein feed was lower than the control group, with a similar protein intake. Thus, chickens regulated day to day their protein intake, as if they progressively distinguished high-protein from low-protein feeds. Protein deficiency was perceived early by chickens. Indeed, the proportion of chickens pecking, scratching, or both was higher at an early age when chickens received low-protein feed, as if they were searching for complementary nutriments (Figure 1). These findings are in agreement with data obtained by Bizeray et al. (2002) with alternation of low- and normal-specific amino acid (lysine) diets during the day. At an older age, chickens compensated their feed intake from one day to another and exploration behavior disappeared, as shown by Bizeray et al. (2002). Picard et al. (1999) reported that broiler chicks fed alternately a diet deficient in essential amino acids and a supplemented diet, with change of feed every day needed 1 wk to identify the diets, the distribution pattern, or both. The question is how chickens learn to distinguish the different feeds. In fact, growing broiler chickens can compensate well for periods of access to only a low-protein feed by subsequent intake of a high-protein feed as long as they are able to gauge the sensory properties of the feeds (Forbes and Shariatmadari, 1996). Chickens associate postingested effects with physical characteristics or with temporal change of feed. Feed flavor, digestive tract, and metabolic signals are combined with visual and tactile cues to build progressively the identity of the feed (Picard et al., 2002). Thus, we hypothesize that the long learning period in our experiment (a week) could be explained because physical characteristics (hardness and color) of both feeds varying in protein contents were relatively similar compared with those in other treatments (Table 1). During the first week, feed, energy, and protein efficiencies were similar in sequential feeding compared with the control, when sequential feeding was introduced at an early age (10 d of age). The feed to gain ratio and energy efficiency slightly decreased at 18 to 30 d of age, unlike the protein efficiency. This implies a high metabolism capacity to compensate for the alternation of high- and low-protein, with buffer storage of nutrients such as amino acids for over 24 h and effective short-term adaptation of protein metabolism to extreme nutritional status. The decrease in energy efficiency could be explained by higher energy utilization, particularly for heat production. For example, the higher activity of chickens when receiving low protein feed (standing, pecking, and scratching; Figure 1) may contribute to an increased heat production. There is also evidence that chickens subjected to variations in dietary protein supply exhibited high responses in terms of metabolism [e.g., protein turn-over (Muramatsu et al., 1987; Muramatsu, 1990) and lipogenesis (Rosebrough et al., 1989)]. The consequence of such changes on energy expenditure is unknown in chickens. The available data give controversial results since nutrient synchrony [i.e., the matching of nutrient availability with body and tissue requirements within a day did not have the same effects on heat production in preruminant calves and pigs (van den Borne et al., 2006, 2007)]. Nevertheless, according to Buyse et al. (1992), Kita et al. (1993), and Swennen et al. (2004) when comparing isoenergetic diets varying in protein contents, the excessive energy relative to protein intake results in increased heat production and even energy retention as fat. In the present study and in Bouvarel et al. (2004), no changes in abdominal fat levels with sequential feeding were observed. However, the pHu of breast meat was lower with diets varying in protein contents than other treatments, which in the range of values observed in the present study could be an advantage for the industry because high muscle pH (>6) produces conditions that make fillets a dark color and more susceptible to bacterial spoilage (Allen et al., 1997). This decrease in breast pHu suggests a higher muscle glycogen content at death, pHu being inversely related to this parameter (Berri et al., 2005) and, thus, a higher energy storage in the muscles.
Our results indicate that the proportion of low-energy feed intake depended on the energy content of the feed with an attraction for high-energy feed and a day to day balance (Table 2). Addition of fat usually improves palatability of a diet, which may be more powerful than the metabolic effects in stimulating intake (Forbes, 1988). Moreover, the proportion of chickens eating was higher for at least the first 2 h of feed distribution when chickens received high-energy feed (Figure 1). On the other hand, the proportion of chickens pecking, scratching, or both was higher when chickens received a low-energy diet, as if they were in search of high-energy feed, which indicates their great attraction to high-energy feed. For all the periods, feed, energy, and protein efficiencies were similar in sequential feeding and the controls (Table 3). However, dietary protein efficiency was higher for diets varying in energy, and this difference reached statistical significance when compared with SEPB (i.e., protein-energy diet treatment introduced later). This may explain why these birds had a heavier BW than the other treatments at 30 d of age. Whole-body protein degradation and especially protein synthesis have been shown to rise curvilinearly with increasing ME intake or CP intake, thereby improving protein deposition (Kita et al., 1993). In our case, for diets varying in energy contents, the energy to protein ratios of both feeds were less limiting than the other sequential feeding regimens and allowed a good protein dietary efficiency.
The use of the treatment with variations in both protein and energy contents led to results in line with those observed when dissociating the effects of energy and protein. The interest of the present experiment was also to study the adaptation of chickens with sequential feeding introduced at 2 different ages. When sequential feeding was introduced early (i.e., treatment SEPA), the proportion of high-protein-low-energy-feed intake was similar to the proportion of low-energy-feed intake alone (SE) for the first period (10 to 17 d), but was lower for the second (18 to 24 d; Table 2). When sequential feeding was introduced later (i.e., treatment SEPB), it was similar again to the proportion of low-energy feed intake (SE). Chickens seemed to adapt their consumption initially according to energy content (SEPA period 1, SEPB), and then also to protein content (SEPA period 2). Age introduction of sequential feeding did not modify the feed to gain ratio and energy conversion ratio. Conversely, later introduction had a deleterious effect on the protein conversion ratio, suggesting birds adapted their protein metabolism more easily when experiencing early sequential feeding (Table 3). To our knowledge, the effect of age on protein metabolism adaptation has not yet been investigated. However, the fact that the responsiveness to the nutritional status of muscle protein synthesis is particularly pronounced in young animals and decreases with age (Davis et al., 2002) could indicate that such adaptation of protein metabolism is possible in the chicken and should be studied.
These results suggest that chickens were able to modify feed intake when energy concentrations differed between 2 sequential feeds, but were less able to do so for the protein concentrations studied. Indeed, in this study, chickens modified feed intake according to the energy to protein ratios just after 1 wk of distribution. When diets varied both in protein and energy contents, chickens adapted their feed intake to energy concentrations first and then to protein levels. Finally, Ross PM3 broiler chickens adapted to sequential feeding during 48-h cycles with diets varying in protein, energy contents, or both, particularly when sequential feeding began early. Chickens were able to make appropriate choices when energy or protein concentrations, or both, differed between 2 sequential feeds. The adaptation in feeding behavior induced only slight changes in locomotor behavior and no improvement of gait score. The equivalent growth performances and carcass conformation suggest this method achievable in field conditions.
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ACKNOWLEDGMENTS |
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Received for publication May 24, 2007. Accepted for publication September 8, 2007.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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