EDUCATION AND PRODUCTION. Does Excess Dietary Protein Improve Growth Performance and Carcass Characteristics in Heat-Exposed Chickens?

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1 EDUCATION AND PRODUCTION Does Excess Dietary Protein Improve Growth Performance and Carcass Characteristics in Heat-Exposed Chickens? S. Temim, A. M. Chagneau, S. Guillaumin, J. Michel, R. Peresson, and S. Tesseraud 1 Station de Recherches Avicoles, Institut National de la Recherche Agronomique, Centre de Tours-Nouzilly, Nouzilly, France ABSTRACT The effects of two environmental temperatures data, and bird responses were lower than at 22 C. We (22 and 32 C, constant) and five dietary protein contents (10 to 33% CP) were investigated in 4- to 6-wkold broiler chickens. High ambient temperature reduced growth rate, feed efficiency, and breast muscle proportion and increased abdominal fat proportion. Irrespective of ambient temperature, increasing dietary protein content improved growth performance and carcass characteristics. concluded that under conditions of chronic heat exposure, diets containing the highest protein levels, 28% and 33% compared with 20% CP, slightly improved chick performance. However, the effect was low and, in our experimental conditions, modifying dietary protein supply (variations in the total quantity of protein) is not sufficient to help broilers to withstand hot conditions. At 32 C, there was a greater heterogeneity of the (Key words: chronic heat exposure, dietary protein, growth, carcass characteristics, broiler) 2000 Poultry Science 79: INTRODUCTION The effect of high ambient temperatures on growth and feed intake of broiler chickens is well documented (reviews of Austic, 1985; Charles, 1986; Howlider and Rose, 1987; Geraert, 1991). In birds, heat loss is limited by feathering and by the lack of sweat glands, and there is evidence that heat exposure decreases feed intake to reduce metabolic heat production. This reduced feed consumption results in lower growth. However, the reduction in growth is greater than the reduction of feed intake, resulting in a depressed feed efficiency (Geraert et al., 1996a). Several nutritional strategies have been proposed to alleviate the adverse effects of high ambient temperatures (reviews of Austic, 1985; Leeson, 1986; Picard et al., 1993; Balnave, 1996; Daghir, 1996). With respect to dietary protein concentration, two opposite strategies can be invoked to alleviate the negative effects of high temperatures on growth. The first one consists of the use of low protein diets to limit the heat increment produced by the metabolism of protein or amino acids. Some authors have recommended a reduction in dietary protein content with suitable supplementation by essential amino acids (Wal- Received for publication February 1, Accepted for publication September 30, To whom correspondence should be addressed: tours. inra.fr. 2 Amino acid analyzer LC 5001, Eppendorf-Netherler Hinz G17BH, Division Biotronik, Hamburg, Germany. 3 Abacus Concepts, 1996, Inc., Berkeley, CA droup et al., 1976; Waldroup, 1982; Austic, 1985). However, Alleman and Leclercq (1997) showed that providing a low protein diet (16% CP with added lysine, methionine, threonine, arginine, and valine vs 20%) did not prevent the negative effects caused by heat with resulting poor performance. The second strategy recommends the use of high protein diets to offset the decreased protein intake related to the lower food consumption under heat exposure. In this way, increasing dietary protein level could be favorable during hot conditions (Temim et al., 1999). The objective of this study was to measure the response of male broilers to dietary protein supply under high or normal temperature conditions during 4 to 6 wk of age. MATERIALS AND METHODS Three hundred fifty day-old male broiler chicks (ISA JV15) were placed in heated battery compartments. They had free access to water. Up to 28 d of age, they received a standard laboratory diet that provided 3,100 kcal ME/ kg and 22% CP and had the following composition (grams per kilogram): corn 485, wheat 126, soybean meal 220, meat meal 41, fat 40, corn gluten 50, dicalcium phosphate 12.7, Ca CO , NaCl 4.0, L-lysine 2.0, DL-methionine 0.9, vitamins, and minerals 6. The lighting program 23 h of light:1 h dark cycle was maintained until the end of the experiment. The ambient temperature was gradually Abbreviation Key: FCR = feed conversion ratio. 312

2 PROTEIN SUPPLY IN HEAT-EXPOSED CHICKENS 313 TABLE 1. Composition of basal diets (%) Diet Ingredients 10% 33% Corn Corn starch 18.6 Corn gluten meal (62% CP) 10.0 Wheat 11.7 Soybean meal (48% CP) Soybean protein 3.6 Rapeseed oil Calcium carbonate Dicalcium phosphate Salt Trace minerals Vitamins DL-methionine Lysine-HCl Threonine 0.08 Valine 0.09 Tryptophan Leucine 0.08 Calculated composition ME (kcal/kg) 3,098 3,096 Crude protein Tesseraud et al. (1996). decreased from 32 C when the birds were 1 d old to 22 C when 28 d old. At 4 wk of age, chickens were weighed, and 216 of them were selected to form 10 groups (n = 20 to 22) of similar body weight (1141 ± 15 g). These chickens were placed in individual battery cages in controlled environment rooms maintained at a constant temperature of either 32 or 22 C; relative humidity was maintained at about 55%. They were fed one of the five experimental diets made by mixing graded proportions of two basal diets, a low protein diet and a high protein diet (Table 1). These diets were calculated to provide 10, 15, 20, 28, and 33% CP and to have the same proportions of amino acids in relation to lysine content (Table 2). All the diets were isoenergetic and in pellet form (2.5-mm diameter). Dietary nitrogen (protein) was measured by the Kjeldahl procedure (Procedure V18-100; AFNOR, 1985). Dietary amino acid content was determined by ion-exchange chromotography on an autoanalyzer 2 using the Procedure V (AFNOR, 1993). More precisely, amino acid content was determined after 23 h acid hydrolysis with 6 N hydrochloric acid at 115 C. The analyzed values of protein and amino acid contents were in good agreement with calculated values, except for the sulfur amino acid content of the 33% CP diet (Table 2). Growth performances were determined during the experimental period, 28 to 42 d of age. Body weights were recorded after an overnight (16 h) feed-deprivation period. Feed consumptions were individually measured every 3 d. At 6 wk of age, carcass characteristics were measured in 14 to 15 chickens per treatment using the methods described by Ain Baziz et al. (1996). The selected chickens exhibited growth performances similar to the group mean. They were slaughtered and plucked mechanically. Abdominal fat and breast muscles were anatomically excised and weighed. Statistical Analysis Values are given as SEM. Homogeneity of the variance between treatments was tested by Bartlett s test. Because heat exposure increased the variability of growth performances and carcass characteristics, data were analyzed using Kruskal-Wallis s nonparametric test (Kruskal and Wallis, 1952), and means were compared by the Mann- Whitney U test (Mann and Whitney, 1947). These analyses were performed using the StatView software program. 3 RESULTS Performance was always significantly depressed at 32 C as compared with that at 22 C (Table 3). Moreover, chronic heat exposure decreased weight gain 25 to 35% and feed intake 15 to 20%, therefore feed conversion ratio (FCR) was significantly higher at 32 than at 22 C (10 to 30%). Increased dietary protein content clearly improved growth performance at 22 and 32 C (Table 3). In comparison of the responses of chickens at the two experimental temperatures, the results first showed a greater dispersion of individual data at 32 C than at 22 C because higher SEM values were recorded at 32 C, at least for the 28 and 33% CP diets. Furthermore, increase of the dietary protein content from 10 to 33% exhibited a less pronounced effect in hot conditions; the increase of daily body weight gain was equal to 13.7 vs 26.8 g/d at 32 C and 22 C, respectively; the reduction of FCR was equal to 1.15 vs 1.36 points, TABLE 2. Crude protein and amino acid concentrations of experimental diets (%), as measured and calculated 10% 15% 20% 28% 33% Diet Measured Calculated Measured Measured Measured Measured Calculated CP (%) Lysine Methionine Cystine Threonine Valine Leucine Isoleucine Arginine

3 314 TEMIM ET AL. respectively. Finally, as at thermoneutrality, providing excess protein in hot conditions (28 or 33% CP compared with 20% CP) did not worsen performance. On the contrary, it improved growth rate and feed conversion ratio by about 10%. It should be noted that, in our experimental conditions, data were similar with diets containing 28 and 33% CP. Thus, a maximal response could be reached at the highest protein levels. The percentage of abdominal fat was increased by heat exposure with diets containing 20, 28, or 33% CP (16, 38, and 36%, respectively) (Table 4). On the contrary, breast muscle weight and its proportion were reduced in hot conditions. Again, this effect appeared greater with diets containing 20, 28, or 33% CP (reduction by approximately 25 g for breast muscle weight and by 10% for breast muscle proportion). Increased dietary protein content improved carcass characteristics at 22 and 32 C. However, as reported for growth performance, this effect seemed lower in hot conditions. Similarly, excess protein did not damage carcass characteristics at 32 as at 22 C. In particular, the highest dietary CP diet (33%) allowed an increase in the weight of breast muscles (11% at both ambient temperatures) and its proportion (7 to 8%) and a reduction in the proportion of abdominal fat (26 and 14% at 22 and 32 C, respectively), compared with the diet containing 20% CP. To take into account the heat-induced reduction in feed intake, growth rate, FCR, and carcass characteristics were plotted against dietary protein intake (data shown only for growth rate, Figure 1). Increasing dietary protein in- take improved growth performance at both rearing temperatures, but this effect seemed less pronounced in hot conditions. Regarding the linear part of the graph, the slope was approximately 2.5-fold lower at 32 C than at 22 C for growth rate (Figure 1), and for breast muscle proportion, the slope was approximately threefold lower at 32 than at 22 C. Concerning FCR and the proportion of abdominal fat, slopes seemed lower and responses smaller at 32 C than at 22 C, even though the differences between the two ambient temperatures were less clear than those obtained for growth rate. DISCUSSION In this study, the response of chickens to dietary protein supply at high (32 C) and control (22 C) ambient temperatures were compared. A wide range of protein concentrations (10 to 33% CP) was tested. The experimental model used was previously defined in our laboratory (Geraert et al., 1996a) and consisted of a 2-wk exposure of broilers to a constant temperature of 32 or 22 C from 4 to 6 wk of age. The constant heat exposure without cool periods do not allow birds to recover as in cyclic-exposure to high temperatures. As expected, chronic heat exposure reduced feed intake, depressed growth, and thus increased FCR, as previously reported in our studies (Geraert et al., 1996a; Temim et al., 1999). Moreover, chronic heat exposure reduced breast muscle proportion (approximately 10% with diets containing at least 20% CP), in good agreement with previous results of Howlider and Rose (1989) and Aïn Baziz et al. (1996). TABLE 3. Effect of dietary protein level and environmental temperature on growth performances of male broiler chickens from 4 to 6 wk of age Dietary protein LW 3 LW Daily body Feed intake intake 2 4 wk 6 wk weight gain Temperature Diet n 1 (g/d) (g/d) (g) (g) (g/d) FCR 4 22 C 10% ab g 1,146 1,849 c 46.9 d b (3.7) (0.41) (15) (31) (1.6) (0.066) 15% a e 1,145 2,073 b 61.9 c d (2.3) (0.34) (15) (25) (1.1) (0.026) 20% bc d 1,144 2,190 a 69.7 b f (2.8) (0.55) (16) (31) (1.5) (0.019) 28% cd b 1,145 2,262 a 74.4 a g (2.3) (0.64) (14) (27) (1.2) (0.023) 33% de a 1,140 2,247 a 73.7 a g (1.7) (0.57) (14) (24) (1.2) (0.025) 32 C 10% ef h 1,137 1,681 e 36.3 f a (3.8) (0.42) (16) (24) (1.4) (0.067) 15% fg f 1,141 1,751 de 40.6 ef c (3.3) (0.49) (15) (36) (2.0) (0.092) 20% g e 1,140 1,810 cd 44.6 de d (2.9) (0.58) (15) (28) (2.0) (0.092) 28% g c 1,131 1,868 c 49.2 d de (3.0) (0.84) (15) (40) (2.4) (0.086) 33% g b 1,143 1,890 c 50.0 d ef (3.2) (1.07) (15) (44) (2.8) (0.091) a-h Means (SEM) within columns with no common superscript differ significantly (P < 0.05). 1 Number of chicks. 2 Dietary protein intake calculated from measured dietary CP content. 3 LW = Live weight. 4 Feed conversion ratio.

4 PROTEIN SUPPLY IN HEAT-EXPOSED CHICKENS 315 TABLE 4. Effect of dietary protein level and environmental temperature on body weight and carcass composition of male broiler chickens at 6 wk of age LW 2 AF 3 AF/BW BM 4 BM/BW Temperature Diet n 1 (g) (g) (%) (g) (%) 22 C 10% 14 1,848.6 c 64.4 a 3.5 a e 12.2 d (17.9) (3.4) (0.2) (5.4) (0.2) 15% 15 2,039.8 b 57.2 a 2.8 b c 13.2 c (20.1) (2.6) (0.1) (4.5) (0.2) 20% 15 2,187.9 a 42.7 bc 1.9 cd b 15.0 b (34.4) (2.2) (0.1) (8.9) (0.2) 28% 15 2,266.6 a 36.5 cd 1.6 de a 15.9 a (17.9) (1.8) (0.1) (6.5) (0.2) 33% 15 2,250.0 a 32.5 e 1.4 e a 16.2 a (24.2) (1.8) (0.1) (8.3) (0.2) 32 C 10% 15 1,681.1 e 61.5 a 3.6 a f 12.3 d (24.0) (2.8) (0.1) (4.7) (0.2) 15% 14 1,719.3 d 49.6 b 2.9 b ef 13.2 c (26.7) (3.2) (0.2) (5.2) (0.2) 20% 15 1,806.6 c 38.8 cd 2.2 c d 13.8 c (26.6) (2.5) (0.1) (6.9) (0.3) 28% 14 1,872.1 c 40.9 cd 2.2 c cd 13.8 c (32.9) (2.6) (0.1) (5.7) (0.2) 33% 15 1,885.3 c 35.1 de 1.9 cd cd 14.7 b (53.9) (2.7) (0.1) (10.6) (0.3) a-f Means (SEM) within columns with no common superscript differ significantly (P < 0.05). 1 Number of chicks. 2 LW = Live weight. 3 AF = Abdominal fat. 4 BM = Breast muscles. In this experiment, the two basal diets (10 and 33% CP) contained corn, soybean meal, and corn gluten meal, which are considered to have high amino acid digestibility (NRC, 1994). They were formulated using CP and amino acid contents of the feed ingredients and then analyzed. For CP and for most amino acids, analyzed and calculated values were close to each other. However, FIGURE 1. Body weight gain as a function of protein intake in male broiler chickens kept between 4 and 6 wk of age at 22 C ( ) or32c ( ). At 22 C, regressions were established excluding data from diets containing 28 and 33% CP because these led to a nonlinear response (n = 59). At 32 C, calculations included all data (n = 91). At 22 C body weight gain = x; r 2 = At 32 C body weight gain = x, r 2 = 0.46, and x = protein intake. methionine and cystine contents determined in the 33% CP diet were lower than those expected and resulted in a slight imbalance in amino acid proportion. Consequently, the 20% CP diet obtained from the two basal diets appeared slightly deficient in sulfur amino acids compared with the NRC-recommended (1994) amino acid levels. This could explain the improved growth performance by increasing protein supply from 20 to 28% at 22 C. In the present experiment, increase of protein supply from 10 to 33% improved growth performance and carcass characteristics in hot conditions as at thermoneutrality. Therefore, we found that, at 32 C, excess protein did not damage chicken performances or carcass characteristics. These results are in good agreement with our previous findings (Temim et al., 1999) that in 4- to 6-wk old heat-exposed chickens, growth and feed efficiency were improved by increasing the dietary protein content from 20 to 25%. In this way, it is important to choose ingredients containing high quality proteins. Indeed, increase of the dietary protein level with low digestible protein materials could accentuate the negative heat effects (Picard et al., 1993). Moreover, the effect of protein supply under heat exposure could be also dependent on the genotype. Effectively, chickens with different growth rates and fatness respond differently to dietary protein level during hot conditions (Cahaner et al., 1995). Interestingly, it should be noted that a stimulation of heat production by excess amino acids should be questionable in hot conditions. Indeed, MacLeod (1992) found that the dietary protein content did not modify the heat production of broilers at high temperatures. Similarly, at

5 316 TEMIM ET AL. 32 C, heat production of genetically lean or fat chickens, when expressed as a proportion of ME intake, was even decreased by higher dietary protein content (23 vs 19% CP; Geraert et al., 1993). A possible explanation may be that, at 32 C, higher protein supply did not increase muscle protein turnover. Indeed, we previously found that under similar conditions of chronic heat exposure, a high protein diet (25 vs 20% CP) did not change muscle proteosynthesis or increase muscle proteolysis but tended to reduce the muscle proteolysis (Temim et al., 1998). As a result, the cost of protein deposition (i.e., the difference between protein synthesis and proteolysis) seems to be lower with a high protein diet during hot conditions. The reduced cost of protein deposition may entirely counterbalance the possible additional cost of nitrogen excretion resulting from an increased protein level, assuming the overriding quantitative importance of the cost of protein accretion relative to that of nitrogen excretion (MacLeod, 1997). Therefore, heat production may be unchanged or possibly decreased by increasing protein intake under high ambient temperatures. In the present study, increasing protein supply at 32 C was beneficial even though the effect was relatively low. It is possible that heat exposure changes specifically the requirements of some amino acids rather than protein requirements; in this case, diet formulation in amino acids could be not adapted to the hot conditions. This hypothesis is supported by the heat-related changes in plasma amino acid profiles recorded by Geraert et al. (1996b); the plasma concentrations of some amino acids were greatly decreased by heat exposure. This decrease could have depressive effects on protein synthesis and consequently on growth. Furthermore, whereas the requirement for first-limiting amino acids, i.e., lysine and sulfur amino acids, does not seem increased in hot conditions (Sinurat and Balnave, 1985; Balnave and Oliva, 1990; Han and Baker, 1993; D Mello, 1994; Mendes et al., 1997; Alleman and Leclercq, 1997), the optimum arginine:lysine ratio might be higher, as reported by Balnave (1996). Threonine supplementation under heat exposure could also be an interesting strategy according to Chung et al. (1996). The requirements for the different amino acids in hot conditions could, therefore, differ from those at thermoneutrality, and their reevaluation could be necessary. In conclusion, our results indicate that, at 32 C, excess protein did not depress growth performance. The increase of protein supply had a favorable, but relatively low, effect. In our conditions, varying the amount of protein in the diet was not an efficient way to alleviate the adverse effects of high ambient temperatures. ACKNOWLEDGMENTS We would like to thank K. Gerard for animal care. We are also grateful to B. Leclercq and M. Picard for helpful comments. REFERENCES AFNOR, Norme V Pages in: Recueil de Normes Françaises. Aliments des Animaux, Méthodes d Analyses Françaises et Communautaires. 2nd ed. Association Française de Normalisation, Paris, France. AFNOR, Norme V Association Française de Normalisation, Paris, France. Aïn Baziz, H., P. A. Geraert, J.C.F. Padilha, and S. Guillaumin, Chronic heat exposure enhances fat deposition and modifies muscle and fat partition in broiler carcasses. Poultry Sci. 75: Alleman, F., and B. Leclercq, Effect of dietary protein and environmental temperature on growth performance and water consumption of male broiler chickens. Br. Poult. Sci. 38: Austic, R. E., Feeding poultry in hot and cold climates. Pages in: Stress Physiology in Livestock. M. K. Youssef, ed. CRC Press, Boca Raton, FL. Balnave, D., Nutritional strategies for alleviating the adverse effects of heat stress. Pages in: Proceedings of the XXth World Poultry Congress WPSA, New-Delhi, India. Balnave, D., and A. Oliva, Responses of finishing broilers at high temperatures to dietary methionine source and supplementation levels. Aust. J. Agric. Res. 41: Cahaner, A., Y. Pinchasov, I. Nir, and Z. Nitsan, Effects of dietary protein under high ambient temperature on body weight, breast meat yield, and abdominal fat deposition of broiler stocks differing in growth rate and fatness. Poultry Sci. 74: Charles, D. R., Temperature for broilers. World s Poult. Sci. J. 42: Chung, T. K., J. Khajarern, and S. Khajarern, Effect of dietary threonine on growth performance and carcass characteristics of broiler chickens raised at high temperatures. Page 145 in: Proceedings of the XXth World Poultry Congress WPSA, New-Delhi, India. Daghir, N. J., Nutrition and climatic stress. Pages in: Proceedings of the XXth World Poultry Congress WPSA, New-Delhi, India. D Mello, J.P.F., Responses of growing poultry to amino acids. Pages in: Amino Acids in Farm Animal Nutrition. J.P.F. D Mello, ed. CAB International, Wallingford, U.K. Geraert, P. A., Energy metabolism of broilers under hot environmental conditions (in French). INRA Prod. Anim. 4: Geraert, P. A., S. Guillaumin, and B. Leclerq, Are genetically lean broilers more resistant to hot climate? Br. Poult. Sci. 34: Geraert, P. A., J.C.F. Padilha, and S. Guillaumin, 1996a. Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: growth performance, body composition and energy retention. Br. J. Nutr. 75: Geraert, P. A., J.C.F. Padilha, and S. Guillaumin, 1996b. Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: biological and endocrinological variables. Br. J. Nutr. 75: Han, Y., and D. H. Baker, Effects of sex, heat stress, body weight, and genetic strain on the dietary lysine requirement of broiler chicks. Poultry Sci. 72: Howlider, M.A.R., and S. P. Rose, Temperature and the growth of broilers. World s Poult. Sci. J. 43: Howlider, M.A.R., and S. P. Rose, Rearing temperature and the meat yield of broilers. Br. Poult. Sci. 30: Kruskal, W. H., and W. A. Wallis, Use of ranks in onecriterion variance analysis. J. Am. Stat. Assoc. 47: Leeson, S., Nutritional considerations of poultry during heat stress. World s Poult. Sci. J. 42: MacLeod, M. G., Energy and nitrogen intake, expenditure and retention at 32 in growing fowl given diets with a wide range of energy and protein contents. Br. J. Nutr. 67: MacLeod, M. G., Effects of amino acid balance and energy:protein ratio on energy and nitrogen metabolism in male broiler chickens. Br. Poult. Sci. 38:

6 PROTEIN SUPPLY IN HEAT-EXPOSED CHICKENS 317 Mann, H. B., and D. R. Whitney, On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Stat. 18: Mendes, A. A., S. E. Watkins, J. A. England, E. A. Saleh, A. L. Waldroup, and P. W. Waldroup, Influence of dietary lysine levels and arginine:lysine ratios on performance of broilers exposed to heat or cold stress during the period of three to six weeks of age. Poultry Sci. 76: National Research Council, Nutrient requirements of poultry. 9th rev. ed. National Academy Press, Washington, DC. Picard, M., B. Sauveur, F. Fenardji, I. Angulo, and P. Mongin, Suitable technico-economic adjustments for poultry feeding in hot countries (in French). INRA Prod. Anim. 6: Sinurat, A. P., and D. Balnave, Effects of dietary amino acids and metabolisable energy on the performance of broilers kept at high temperatures. Br. Poult. Sci. 26: Temim, S., A. M. Chagneau, R. Peresson, J. Michel, S. Guillaumin, and S. Tesseraud, Muscle protein turnover in broiler chickens: effects of high ambient temperatures and dietary protein intake. Leres Journees Francophones de Nutrition, Paris, France. Reprod. Nutr. Dev. 38:190. Temim, S., A. M. Chagneau, S. Guillaumin, J. Michel, R. Peresson, P. A. Geraert, and S. Tesseraud, Effects of chronic heat exposure and protein intake on growth performance, nitrogen retention and muscle development in broiler chickens. Reprod. Nutr. Dev. 39: Tesseraud, S., R. Peresson, J. Lopes, and A. M. Chagneau, Dietary lysine deficiency greatly affects muscle and liver protein turnover in growing chickens. Br. J. Nutr. 75: Waldroup, P. W., R. J. Mitchell, J. R. Payne, and K. R. Hazen, Performance of chicks fed diets formulated to minimize excess levels of essential amino acids. Poultry Sci. 55: Waldroup, P. W., Influence of environmental temperature on protein and amino acid needs of poultry. Fed. Proc. 41:

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