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Sulfur Amino Acid Requirement of Broiler Chicks from Fourteen to Thirty-Eight Days of Age.
METABOLISM AND NUTRITION Sulfur Amino Acid Requirement of Broiler Chicks from Fourteen to Thirty-Eight Days of Age. 1. Performance and Carcass Yield J. B. SCHUTTE TNO-Institute of Animal Nutrition and Physiology (ILOB), P.O. Box 15, 6700 AA Wageningen, The Netherlands M. PACK
ABSTRACT Two experiments were conducted to evaluate increasing dietary levels of methionine and TSAA on broiler performance and carcass yield. In Experiment 1, the corn-soybean basal diet contained .75% TSAA, to which increasing dose levels of DL-methionine were added, providing at the highest supplemental level .95% TSAA. The experimental diets were fed for 20 d, covering the age period of 14 to 34 d. In Experiment 2, a corn-soybean basal diet containing .70% TSAA was used along with DL-methionine supplements to determine TSAA requirement during the age period of 14 to 38 d. The highest supplemental level of DL-methionine in this experiment provided .94% TSAA. The TSAA requirement was found to be higher for maximum efficiency of feed utilization and breast meat yield than for obtaining maximum weight gain. Based on feed conversion efficiency and breast meat yield, the requirement for TSAA was estimated to be at least .88% for the age period of 14 to 34 or 38 d. It was calculated that the estimated TSAA requirement was equivalent to approximately .75% apparent digestible SAA or .78% true digestible SAA. (Key words: broiler chick, methionine, sulfur amino acids, performance, carcass yield) 1995 Poultry Science 74:480-487
INTRODUCTION The requirement of broiler chicks for methionine and total sulfur amino acids (TSAA) during early life (0 to 2 or 3 wk) is well established. Regarding this age period, the dietary levels recommended by the NRC (1994) of .50% methionine and .90% TSAA are generally accepted. However, limited information is available for the requirement after 3 wk of age. Recent reports in literature indicate that the NRC (1994) recommendation of .38% methionine and .72% TSAA for the age period of 3 to 6 wk is too low for obtaining
Received for publication February 22, 1994. Accepted for publication October 12, 1994.
maximum broiler performance (Jensen et al., 1989; Mendonca and Jensen, 1989; Hickling et al, 1990; Skinner et al, 1992). In determining the levels to be applied in commercial feeds, the criteria used for evaluation of the methionine and TSAA requirement become of concern. In most studies the criteria are growth rate and feed conversion efficiency. Recently, carcass composition of broiler chicks as affected by individual amino acids is receiving considerable attention as a result of further processing of the birds by the industry. There is an emphasis on increasing the breast meat yield and decreasing the content of abdominal fat of the broiler carcass. It has been demonstrated that increasing the dietary lysine content results in an increase of breast meat yield
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Degussa AG, Applied Technology Feed Additives, P.O. Box 1345, D-63403, Hanau, Germany
SULFUR AMINO ACID REQUIREMENT OF BROILERS
MATERIALS AND METHODS Experimental Design Two experiments were conducted with chicks of a commercial broiler strain (Ross). The sexed day-old chicks were randomly assigned to litter floor pens (4.3 m2) in an insulated broiler house with concrete floors. Sixty males or 60 females were placed in each of 48 pens for each trial. From 0 to 14 d posthatch, birds in both trials were fed a standard diet containing 22.1% CP, 3,150 kcal of ME/kg, and .90% SAA. At 14 d of age, the birds were individually weighed and selected to have similar average starting weights for each pen with males or females, respectively. In Experiment 1 the mean starting weight per pen with males or females was 400 and 390 g, respectively. Corresponding weights for males and females in Experiment 2 at this time were 402 and 388 g, respectively. In Experiment 1 each experimental diet was fed to three pens with 43 males each and three pens with 43 females each for a period of 20 d (14 to 34 d of age). In Experiment 2 each experimental diet was fed to four pens with 50 males each and four pens with 50 females each for a period of 24 d (14 to 38 d of age).
Each pen was equipped with a tube feeder and an automatic waterer. Incandescent lights were used to provide the birds with 24 h light/d. Temperature was regulated by thermostatically controlled gas brooders and ventilation fans. Broilers had free access to feed as pellets and water. The basal diets used were based on corn and soybean meal (Table 1) and analyzed to contain 21.2% CP (Experiment 1) and 22.7% CP (Experiment 2) as determined by the Kjeldahl method (Association of Official Analytical Chemists, 1984). Both diets were calculated to be adequate in all essential amino acids except methionine and TSAA. Amino acid contents were verified by analysis. The analyzed contents of the most important essential amino acids are presented in Table 1. Amino acids were determined by ion-exchange chromatography (Beck et al, 1978) after hydrolysis of the samples with 6 M HC1 for 24 h. Methionine and cystine were determined by ionexchange chromatography as methionine sulphone and cysteic acid, respectively, after oxidation with performic acid. In Experiment 1, seven additions of DLmethionine (.02, .04, .07, .10, .13, .16, and .20%) to a basal diet containing .75% TSAA were tested to provide TSAA levels of .77 to .95%. Experiment 2 was designed to test the effect of five additions of DL-methionine (.03, .07, .12, .18, and .24%) to a basal diet containing .70% TSAA, providing TSAA levels varying between .73 to .94%. The additions of DL-methionine were verified by analysis. These values corresponded well with the calculated contents. At the end of the trials, birds were weighed individually and feed intake of each pen was recorded. After termination of Experiment 2,15 males per pen were chosen at random to determine carcass yield. Each of these birds was deprived of feed for 12 h, and individually weighed just prior to slaughter. The birds were slaughtered and cut into parts by a trained team according to a standardized procedure (Uijttenboogaart and Gerrits, 1982).
Statistical Analysis The results of both experiments were analyzed by means of ANOVA as a randomized block design (Cochran and Cox,
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(Moran, 1988; Hickling et al, 1990; Moran and Bilgili, 1990; Holsheimer and Veerkamp, 1992). Similarly, increasing dietary methionine levels have shown to reduce abdominal fat content (Jensen et al, 1989; Mendonca and Jensen, 1989; Jeroch and Pack, 1992) and increase breast meat yield (Hickling et al, 1990; Huyghebaert et al, 1994). Considering the literature, it seems that the TSAA requirement of broiler chicks has been studied mainly during the growth phases of 0 to 3 and 3 to 6 or 7 wk of age, respectively. In European practice, however, diet composition is commonly changed at 14 and 34 or 38 d of age, respectively. The purpose of the present investigations was to study the effect of dietary additions of DL-methionine to practical diets on broiler performance in the age period of 14 to 34 and 14 to 38 d, respectively, and its effect on carcass quality.
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breast meat yield using a nonlinear regression procedure. Exponential response curves were fitted to the experimental data points using the following equation:
Y = a + b[l -
-c(x - d)
]
where Y = weight gain, feed conversion or breast meat yield; a = intercept; b = maximum improvement from added DLmethionine; c = curvature steepness; x = TSAA level, experimental diets (percentage), and d = TSAA level, basal diet (percentage). Tentative values for SAA requirements were calculated at 95% of maximum response. This value was chosen arbitrarily. In the nonlinear regression analysis, the combined performance data for weight gain. There were numerical im-
TABLE 1. Composition of the basal diets Ingredients Corn Animal fat Soybeans, toasted (36.5% CP) Soybean meal (44.5% CP) Soybean meal (48.2% CP) Feather meal (85.7% CP) Meat meal tankage (48.0% CP) Peas (22.8% CP) Molasses Ground limestone Dicalcium phosphate Iodized salt Vitamin-mineral premix1 DL-methionine L-lysine HC1 Analyzed contents Crude protein ME, calculated, kcal/kg2 Calcium Phosphorus Methionine Methionine + cystine Lysine Arginine Threonine Valine Isoleucine Leucine
Experiment 1 51.87 6.0 6.15 26.8 2.2 1.0 2.0 1.0 1.6 .3 1.0 .03 .05
21.2 3,160 .89 .65 .33 .75 1.16 1.44 .84 1.08 .91 1.82
Experiment 2 43.61 6.0 9.5 28.0 .7 2.0 5.0 2.0 1.2 .6 .3 1.0 .09
22.7 3,210 .93 .64 .34 .70 1.32 1.57 .87 1.09 .96 1.85
Supplied per kilogram of diet: riboflavin, 4 mg; niacinamide, 40 mg; D-pantothenic acid, 12 mg; choline chloride, 500 mg; cobalamin, 15 mg; menadione, 5 mg; DL-a-tocopheryl acetate, 25IU; retinyl acetate, 10,000 IU; cholecalciferol, 2,000 IU; biotin, .1 mg; folic acid, .75 mg; FeS04-7H20,300 mg; Mn02,100 mg; CuS04-5H20,100 mg; ZnS0 4 H 2 0,150 mg; Na2Se03,15 mg; antioxidant ("Ethoxyquin"), 100 mg; Avoparcin, 100 mg; Monensin (up to 5 d before slaughtering), 100 mg. 2 Values calculated from data provided by the Dutch Bureau of Livestock Feeding (1991).
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1957). The computer program GENSTAT 5 (Payne et ah, 1987) was used to calculate the ANOVA. The treatment factors were dietary level of SAA and sex. No significant sex by treatment interaction was observed. Therefore, only the combined results for males and females are presented. Because male birds of Experiment 2 were involved in carcass yield measurements, performance results of the males of this experiment are also presented separately. The significance of differences between treatment means was tested by using the least significance difference test (Snedecor and Cochran, 1980). All statements of significance are based on a probability of less than .05. The SAA requirements were estimated from weight gain, feed:gain ratio, and
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SULFUR AMINO ACID REQUIREMENT OF BROILERS TABLE 2. Effects of dietary DL-methionine supplementation on broiler performance, Experiment 1 (14 to 34 d of age) Treatment1
Added DL-methionine
Dietary SAA level
- (%)
—
(g)
(g/bird/d) 108.9* 107.9*= 109.2» 107.4*= 106.8"=d 105.8=d 105.0d 106.0=d .8
Feed:gain (g:g) 1.788* 1.756b 1.740b= 1.726=d 1.709
*-fMean values within a column with no common superscript differ significantly (P ^ .05). 1 Each treatment consisted of six replicates of 43 birds each.
male and female chicks were also evaluated, as the response curves for weight gain and feed conversion efficiency for both sexes followed a similar pattern. RESULTS
Mortality rate in both experiments was very low, being .5% in Experiment 1 and .7% in Experiment 2. No appreciable differences in mortality among the treatments were observed. Performance data of Experiment 1 are summarized in Table 2. Weight gain was improved significantly up to a dietary TSAA of .79%. A further increase of the TSAA content had hardly any effect on provements in feed conversion efficiency up to the highest supplemented level of
.20% DL-methionine, resulting in a dietary TSAA level of .95%. Feed conversion efficiency of birds fed the diet containing .95% TSAA was significantly better than those fed the diet containing .85% TSAA. There was a trend of a decreased daily feed intake when the dietary TSAA level was increased from .79 to .91%. Performance data of Experiment 2 are presented in Tables 3 and 4. In Table 3 these data relate to the combined results for both sexes and those in Table 4 to the male chicks separately. There were numerical improvements in weight gain for all increments in dietary TSAA, but the effects were not significant above a TSAA level of .77%. Feed conversion efficiency was improved up to a dietary TSAA level of .88%. However, these improvements
TABLE 3. Effects of dietary DL-methionine supplementation on broiler performance, Experiment 2 (14 to 38 d of age) Treatment1
Added DL-methionine ( % )
1 0 2 .03 3 .07 4 .12 5 .18 6 .24 Pooled SEM (df 36)
Dietary SAA level —
•
.70 .73 .77 .82 .88 .94
Weight gain
Feed intake
(g)
(g/bird/d) 120.5 121.3 121.9 120.9 120.8 121.3 .8
1,566= 1,613" 1,643* 1,651* 1,658* 1,666* 15
'-''Means within a column with no common superscript differ significantly (P S .05). iEach treatment consisted of eight replicates of 50 birds each.
Feed:gain 1.855* 1.812b 1.792"= 1.769=d 1.759d 1.760d .010
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Feed intake
1,221= l,230b= 1,257* 1,248* 1,251* 1,252* 1,249* 1,265* 8
.75 .77 .79 .82 .85 .88 .91 .95
1 0 2 .02 3 .04 4 .07 5 .10 6 .13 7 .16 8 .20 Pooled SEM (df 32)
Weight gain
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SCHUTTE AND PACK TABLE 4. Effects of dietary DL-methionine supplementation on male broiler performance, Experiment 2 (14 to 38 d of age)
Treatment1
Added DL-methionine
Weight gain
Feed intake
(g)
(g/bird/d) 129.5 129.3 130.1 129.8 129.4 130.5
Dietary SAA level
(%) • 1 0 2 .03 3 .07 4 .12 5 .18 6 .24 Pooled SEM (df 36)
— .70 .73 .77 .82 .88 .94
1,736= l,780b= 1,840* 1,852= 1,862= 1,875= 21
Feed:gain
teg) 1.792= 1.744b 1.697= 1.683= 1.668= 1.670= .015
1.1
Means within a column with no common superscript differ significantly (P < .05). Each treatment consisted of four replicates of 50 birds each.
J
were of no importance in excess of .12% added methionine, providing .82% TSAA (Table 3). Carcass yield results of the male birds are presented in Table 5. A positive response on breast meat yield was achieved by increased dietary methionine. Breast meat yield of birds fed the diet containing .88% TSAA was significantly higher than that of birds fed diets containing .70 and .73% TSAA. In addition a decreased abdominal fat deposition by increasing dietary methionine up to a level of .12%, providing .82% TSAA, was observed. Abdominal fat deposition of birds fed the diet containing .82% TSAA was
significantly lower than that of birds fed diets with .70 and .73% TSAA. A summary of the TSAA requirements estimated from the exponential response curves is presented in Table 6. Based on these analyses the estimated TSAA requirements for obtaining m a x i m u m weight gain were similar in both experiments, being .83%. For obtaining maximum efficiency of feed utilization, the requirement for TSAA was estimated to be .88% in Experiment 2. The results of Experiment 1 suggest a higher requirement for TSAA for obtaining maximum efficiency of feed utilization, which was
TABLE 5. Effect of dietary DL-methionine supplementation on carcass yield characteristics (in percentage of body weight) of male broilers at 38 d of age, Experiment 2 Pooled SEM (df 18)
Treatments 1 Variable Added DL-methionine, % Dietary SAA level, % Body weight at slaughter, g Slaughter weight, 2 % BW Oven-ready,3 % BW Edible organs, % BW Breast meat, 4 % BW Abdominal fat, % BW a_
1
2
3
4
5
6
.70
.03 .73
.07 .77
.12 .82
.18 .88
2,071 85.1* 72.9b 3.7= 15.9= 2.9=
2,115 85.1* 73.0b 3.6= 16.3b= 2.7=b
2,128 85.2= 73.2=b 3.6= 16.7* 2.6b=
2,170 84.7b 72.9b 3.6= 16.8* 2.4=
2,183 85.1* 73.5= 3.4b 17.0= 2.5=
0
.24 .94 2,167 84.9=b 73.2=b 3.4b 16.9= 2.5=
=Means within a row with no common superscript differ significantly (P <, .05). n = 60 birds per treatment. 2 Body weight minus blood, feather, head, and feet. 3 Carcass including neck, neck skin, and abdominal fat. 4 Without bones and skin. x
32.1 .13 .17 .05 .18 .08
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a_c
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SULFUR AMINO ACID REQUIREMENT OF BROILERS TABLE 6. Summary of the estimated TSAA requirements from exponential response curves Experiment
Variable
Exponential response curve
1 Table 2
Weight gain Feed:gain
y = 1,219 + 35.3[l-e _ 3 6 3 ( x " 7 5 ) ] y = 1.78 - .117[l _ e - la9 < x " 75>]
2 Tables 3 and 5
Weight gain Feed:gain Breast meat^
y = 1,567 + 95.8[l - e"217(x " 7 0 ) ] y = 1.85 - .097[l-e~16-5(x~70)~ y = 21.9 - 1.30[l-e~ 160(x_70) '
Estimated requirements1 .83 >.952 .84 .88 .89
Calculated at 95% of maximum response. Estimated requirement of 1.02% exceeded the range of TSAA levels tested. Percentage of slaughter weight.
DISCUSSION Generally, in estimating amino acid requirements from growth studies two types of methods are used; the linear (broken line) model and the nonlinear models. As was pointed out by Fisher et al. (1973), the use of a linear response u p to a maximum level usually leads to an underestimation of requirements. On the other hand, use of curves based on exponential equations may lead to overestimation of the response in which practical decisions are made. From a comparison of the two models, Robbins et al. (1979) concluded that the nonlinear models are preferable. However, nonlinear curves do not define a fixed requirement, which led us to the approach to derive a tentative figure at 95% of the maximum response. Although this is an arbitrary choice, the procedure does give a good idea of the dietary amino acid level to support close to maximum performance. The results of these experiments demonstrate that the chicken's need for methionine and TSAA is higher for obtaining maximum efficiency of feed utilization than for maximum weight gain. This finding is supported by others (Adams et al, 1962; Bornstein and Lipstein, 1964, 1966; Van Weerden et al, 1976). The results of Experiment 1 suggest that this
phenomenon may be explained partly because methionine regulates feed intake, as proposed by Chee and Polin (1978). In this experiment there was a trend suggesting that birds have the ability to compensate for a marginal deficiency of methionine by consuming more feed. Similar effects were observed in previous studies with laying hens (Schutte and Van Weerden, 1978; Schutte et al, 1983, 1984), also indicating that at marginal deficiencies of methionine birds ate more feed in an attempt to meet their requirement. In Experiment 2, however, a regulating action by methionine on feed intake was not observed. From the results of both trials it was estimated that the TSAA requirement of broiler chicks in the age period of 14 to 34 or 38 d is at least .88% in a diet containing about 3,180 kcal ME/kg for obtaining maximum efficiency of feed utilization. A similar dietary requirement level of TSAA was estimated for obtaining maximum yield of breast meat in male broiler chicks. Literature data about the TSAA requirement of broiler chicks for the age period of 14 to 34 or 38 d are not available. Our estimation for TSAA requirement during this age period is somewhat lower than the dietary level recommended by NRC (1994) of .90% TSAA for the age period of 0 to 3 wk, but distinctly higher than their recommendation of .72% TSAA for 3 to 6 wk of age. Based on the results of the present studies, a dietary TSAA level of approximately .80% as reported by Jensen et al (1989), Mendonca and Jensen (1989), and Jeroch and Pack (1992) seems to be a
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calculated to be higher than the maximum level of .95% TSAA tested in the experiment. Maximum response on breast meat yield was estimated at a TSAA level of .89%.
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REFERENCES Adams, R. L., F. N. Andrews, J. C. Rogler, and C. W. Carrick, 1962. The sulfur amino acid requirement of the chick from 4 to 8 weeks of age as affected by temperature. Poultry Sci. 41: 1801-1806. Association of Official Analytical Chemists, 1984. Official Methods of Analysis. 14th ed. Association of Official Analytical Chemists, Washington, DC. Beck, A., H. Schmidtborn, M. Spindler, and H. Tanner, 1978. Die Bestimmung von gebundenen und supplementierten Aminosauren in Futtermitteln u n d Mischfuttern mit Hilfe der lonenaustausch-Chromatographie. Kraftfutter 3: 118-124. Bornstein, S., and B. Lipstein, 1964. Methionine supplementation of practical broiler rations. 1. The value of added methionine in diets of varying fish meal levels. Br. Poult. Sci. 5: 175-186. Bornstein, S., and B. Lipstein, 1966. Methionine supplementation of practical broiler rations. III. The value of added methionine in broiler finisher rations. Br. Poult. Sci. 7:273-284. Chee, K. M., and D. Polin, 1978. Effect of methionine and methods of feeding on feed intake. Poultry Sci. 57:1126.(Abstr.) Cochran, W. G., and G. M. Cox, 1957. Experimental Designs. 2nd ed. John Wiley and Sons, Inc., New York, NY. Degussa, 1992. Digestible Amino Acids in Feedstuffs for Poultry. Degussa AG, Hanau, Germany. Dutch Bureau of Livestock Feeding, 1991. Chemical Composition, Digestibility and Energy Value of
Feed Ingredients. Bureau of Livestock Feeding, Lelystad, The Netherlands. Fisher, C , T. R. Morris, and R. C. Jennings, 1973. A model for the description and prediction of the response of laying hens to amino acid intake. Br. Poult. Sci. 14:469-484. Hickling, D., W. Guenter, and M. E. Jackson, 1990. The effect of dietary methionine and lysine on broiler chicken performance and breast meat yield. Can. J. Anim. Sci. 70:673-678. Holsheimer, J. P., and C. H. Veerkamp, 1992. Effect of dietary energy, protein, and lysine content on performance and yields of two strains of male broiler chicks. Poultry Sci. 71:872-879. Huisman, J., P.H.U. de Vries, E. J. van Weerden, and H. L. Bertram, 1985. The availability of synthetic methionine in pigs. J. Anim. Physiol. Anim. Nutr. 55:267-272. Janssen, W.M.M.A., K. Terpstra, F.F.E. Beeking, and A.J.N. Bisalsky, 1979. Feeding Values for Poultry. 2nd ed. Spelderholt Publication 303, Beekbergen, The Netherlands. Huyghebaert, G., M. Pack, and G. de Groote, 1994. Influence of protein concentration on the response of broilers to supplemental DLmethionine. Arch. Gefltlgelkd. 58(l):23-29. Jensen, L. S., C. L. Wyatt, and B. I. Fancher, 1989. Sulfur amino acid requirement of broiler chicks from 3 to 6 weeks of age. Poultry Sci. 68: 163-168. Jeroch, H., and M. Pack, 1992. Influence of protein content in feed on sulphur amino acid requirements of broiler chicks. Pages 601-605 in: Proceedings of the 19th World's Poultry Congress. Ponsen and Looyen, Wageningen, The Netherlands. Mendonca, C. X., and L. S. Jensen, 1989. Influence of protein concentration on the sulphur-containing amino acid requirement of broiler chicks. Br. Poult. Sci. 30:889-898. Moran, E. T., 1988. Dietary lysine and broiler meat yield. Pages 46-52 in: Proceedings of the California Animal Nutrition Conference, Fresno, CA. Moran, E. T., and S. F. Bilgili, 1990. Processing losses, carcass yield quality, and meat yields of broiler chickens receiving diets marginally deficient to adequate in lysine prior to marketing. Poultry Sci. 69:702-710. National Research Council, 1994. Nutrient Requirements of Poultry. 9th rev. ed. National Academy Press, Washington, DC. Pack M., and J. B. Schutte, 1995. Sulfur amino acid requirement of broiler chicks from 14 to 34 or 38 days of age. 2. Economical evaluation. Poultry Sci. 74:488—493. Payne, R. W., P. W. Lane, A. E. Ainsley, K. E. Bicknell, P.G.N. Digby, S. A. Harding, P. K. Leech, H. R. Simpson, A. D. Todd, P. J. Verrier, and R. P. White, 1987. Genstat 5 Reference Manual, Oxford University Press, New York, NY. Robbins, K. R., H. W. Norton, and D. H. Baker, 1979. Estimation of nutrient requirements from growth data. J. Nutr. 109:1710-1714. Schutte, J. B., and E. J. van Weerden, 1978. Requirement of the hen for sulphur containing amino acids. Br. Poult. Sci. 19:573-581. Schutte, J. B., E. J. van Weerden, and H. L. Bertram, 1983. Sulphur amino acid requirement of laying
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more reasonable requirement figure for the age period of 3 to 6 wk. Janssen et al. (1979) determined the content and digestibility of amino acids of various feedstuffs used in the formulation of poultry diets. From their data it was calculated that the content of apparent digestible SAA in the basal diet used in Experiment 1 was .62% and .57% in the basal diet used in Experiment 2. Assuming that digestibility of DL-methionine can be set at 100% (Huisman et al, 1985), it can be calculated that the current estimated requirement for TSAA (.88%) for the age period of 14 to 34 or 38 d corresponds with approximately .75% apparent digestible SAA. In terms of true digestible amino acids, the two basal diets were calculated to contain .65 and .60% digestible SAA, respectively (Degussa, 1992). Based on this criterion, the estimated requirement for TSAA corresponds with approximately .78% true digestible SAA. The economics of feeding increasing SAA levels must be considered in evaluating the results of the present studies. This has been done in an additional paper (Pack and Schutte, 1994).
SULFUR AMINO ACID REQUIREMENT OF BROILERS hens and the effects of excess dietary methionine on laying performance. Br. Poult. Sci. 24: 319-326. Schutte, J. B., E. J. van Weerden, and H. L. Bertram, 1984. Protein and sulphur amino acid nutrition of the hen during the early stage of laying. Arch. Gefltlgelkd. 48(5):165-170. Skinner, J. T., A. L. Waldroup, and P. W. Waldroup, 1992. Interaction of methionine and cystine needs of broilers 21 to 42 days of age. Poultry Sci. 71(Suppl. l):110.(Abstr.)
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Snedecor, G. W., and W. G. Cochran, 1980. Statistical Methods. 7th ed. The Iowa State University Press, Ames, IA. Uijttenboogaart, T. G., and A. R. Gerrits, 1982. Method of dissection of broiler carcasses and description of parts. Spelderholt Report 370. Beekbergen, The Netherlands. Van Weerden, E. J., J. B. Schutte, and J. E. Sprietsma, 1976. Relation between methionine and inorganic sulphate in broiler rations. Poultry Sci. 55: 1476-1481.
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ABSTRACT Two experiments were conducted to evaluate increasing dietary levels of methionine and TSAA on broiler performance and carcass yield. In Experiment 1, the corn-soybean basal diet contained .75% TSAA, to which increasing dose levels of DL-methionine were added, providing at the highest supplemental level .95% TSAA. The experimental diets were fed for 20 d, covering the age period of 14 to 34 d. In Experiment 2, a corn-soybean basal diet containing .70% TSAA was used along with DL-methionine supplements to determine TSAA requirement during the age period of 14 to 38 d. The highest supplemental level of DL-methionine in this experiment provided .94% TSAA. The TSAA requirement was found to be higher for maximum efficiency of feed utilization and breast meat yield than for obtaining maximum weight gain. Based on feed conversion efficiency and breast meat yield, the requirement for TSAA was estimated to be at least .88% for the age period of 14 to 34 or 38 d. It was calculated that the estimated TSAA requirement was equivalent to approximately .75% apparent digestible SAA or .78% true digestible SAA. (Key words: broiler chick, methionine, sulfur amino acids, performance, carcass yield) 1995 Poultry Science 74:480-487
INTRODUCTION The requirement of broiler chicks for methionine and total sulfur amino acids (TSAA) during early life (0 to 2 or 3 wk) is well established. Regarding this age period, the dietary levels recommended by the NRC (1994) of .50% methionine and .90% TSAA are generally accepted. However, limited information is available for the requirement after 3 wk of age. Recent reports in literature indicate that the NRC (1994) recommendation of .38% methionine and .72% TSAA for the age period of 3 to 6 wk is too low for obtaining
Received for publication February 22, 1994. Accepted for publication October 12, 1994.
maximum broiler performance (Jensen et al., 1989; Mendonca and Jensen, 1989; Hickling et al, 1990; Skinner et al, 1992). In determining the levels to be applied in commercial feeds, the criteria used for evaluation of the methionine and TSAA requirement become of concern. In most studies the criteria are growth rate and feed conversion efficiency. Recently, carcass composition of broiler chicks as affected by individual amino acids is receiving considerable attention as a result of further processing of the birds by the industry. There is an emphasis on increasing the breast meat yield and decreasing the content of abdominal fat of the broiler carcass. It has been demonstrated that increasing the dietary lysine content results in an increase of breast meat yield
480
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Degussa AG, Applied Technology Feed Additives, P.O. Box 1345, D-63403, Hanau, Germany
SULFUR AMINO ACID REQUIREMENT OF BROILERS
MATERIALS AND METHODS Experimental Design Two experiments were conducted with chicks of a commercial broiler strain (Ross). The sexed day-old chicks were randomly assigned to litter floor pens (4.3 m2) in an insulated broiler house with concrete floors. Sixty males or 60 females were placed in each of 48 pens for each trial. From 0 to 14 d posthatch, birds in both trials were fed a standard diet containing 22.1% CP, 3,150 kcal of ME/kg, and .90% SAA. At 14 d of age, the birds were individually weighed and selected to have similar average starting weights for each pen with males or females, respectively. In Experiment 1 the mean starting weight per pen with males or females was 400 and 390 g, respectively. Corresponding weights for males and females in Experiment 2 at this time were 402 and 388 g, respectively. In Experiment 1 each experimental diet was fed to three pens with 43 males each and three pens with 43 females each for a period of 20 d (14 to 34 d of age). In Experiment 2 each experimental diet was fed to four pens with 50 males each and four pens with 50 females each for a period of 24 d (14 to 38 d of age).
Each pen was equipped with a tube feeder and an automatic waterer. Incandescent lights were used to provide the birds with 24 h light/d. Temperature was regulated by thermostatically controlled gas brooders and ventilation fans. Broilers had free access to feed as pellets and water. The basal diets used were based on corn and soybean meal (Table 1) and analyzed to contain 21.2% CP (Experiment 1) and 22.7% CP (Experiment 2) as determined by the Kjeldahl method (Association of Official Analytical Chemists, 1984). Both diets were calculated to be adequate in all essential amino acids except methionine and TSAA. Amino acid contents were verified by analysis. The analyzed contents of the most important essential amino acids are presented in Table 1. Amino acids were determined by ion-exchange chromatography (Beck et al, 1978) after hydrolysis of the samples with 6 M HC1 for 24 h. Methionine and cystine were determined by ionexchange chromatography as methionine sulphone and cysteic acid, respectively, after oxidation with performic acid. In Experiment 1, seven additions of DLmethionine (.02, .04, .07, .10, .13, .16, and .20%) to a basal diet containing .75% TSAA were tested to provide TSAA levels of .77 to .95%. Experiment 2 was designed to test the effect of five additions of DL-methionine (.03, .07, .12, .18, and .24%) to a basal diet containing .70% TSAA, providing TSAA levels varying between .73 to .94%. The additions of DL-methionine were verified by analysis. These values corresponded well with the calculated contents. At the end of the trials, birds were weighed individually and feed intake of each pen was recorded. After termination of Experiment 2,15 males per pen were chosen at random to determine carcass yield. Each of these birds was deprived of feed for 12 h, and individually weighed just prior to slaughter. The birds were slaughtered and cut into parts by a trained team according to a standardized procedure (Uijttenboogaart and Gerrits, 1982).
Statistical Analysis The results of both experiments were analyzed by means of ANOVA as a randomized block design (Cochran and Cox,
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(Moran, 1988; Hickling et al, 1990; Moran and Bilgili, 1990; Holsheimer and Veerkamp, 1992). Similarly, increasing dietary methionine levels have shown to reduce abdominal fat content (Jensen et al, 1989; Mendonca and Jensen, 1989; Jeroch and Pack, 1992) and increase breast meat yield (Hickling et al, 1990; Huyghebaert et al, 1994). Considering the literature, it seems that the TSAA requirement of broiler chicks has been studied mainly during the growth phases of 0 to 3 and 3 to 6 or 7 wk of age, respectively. In European practice, however, diet composition is commonly changed at 14 and 34 or 38 d of age, respectively. The purpose of the present investigations was to study the effect of dietary additions of DL-methionine to practical diets on broiler performance in the age period of 14 to 34 and 14 to 38 d, respectively, and its effect on carcass quality.
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breast meat yield using a nonlinear regression procedure. Exponential response curves were fitted to the experimental data points using the following equation:
Y = a + b[l -
-c(x - d)
]
where Y = weight gain, feed conversion or breast meat yield; a = intercept; b = maximum improvement from added DLmethionine; c = curvature steepness; x = TSAA level, experimental diets (percentage), and d = TSAA level, basal diet (percentage). Tentative values for SAA requirements were calculated at 95% of maximum response. This value was chosen arbitrarily. In the nonlinear regression analysis, the combined performance data for weight gain. There were numerical im-
TABLE 1. Composition of the basal diets Ingredients Corn Animal fat Soybeans, toasted (36.5% CP) Soybean meal (44.5% CP) Soybean meal (48.2% CP) Feather meal (85.7% CP) Meat meal tankage (48.0% CP) Peas (22.8% CP) Molasses Ground limestone Dicalcium phosphate Iodized salt Vitamin-mineral premix1 DL-methionine L-lysine HC1 Analyzed contents Crude protein ME, calculated, kcal/kg2 Calcium Phosphorus Methionine Methionine + cystine Lysine Arginine Threonine Valine Isoleucine Leucine
Experiment 1 51.87 6.0 6.15 26.8 2.2 1.0 2.0 1.0 1.6 .3 1.0 .03 .05
21.2 3,160 .89 .65 .33 .75 1.16 1.44 .84 1.08 .91 1.82
Experiment 2 43.61 6.0 9.5 28.0 .7 2.0 5.0 2.0 1.2 .6 .3 1.0 .09
22.7 3,210 .93 .64 .34 .70 1.32 1.57 .87 1.09 .96 1.85
Supplied per kilogram of diet: riboflavin, 4 mg; niacinamide, 40 mg; D-pantothenic acid, 12 mg; choline chloride, 500 mg; cobalamin, 15 mg; menadione, 5 mg; DL-a-tocopheryl acetate, 25IU; retinyl acetate, 10,000 IU; cholecalciferol, 2,000 IU; biotin, .1 mg; folic acid, .75 mg; FeS04-7H20,300 mg; Mn02,100 mg; CuS04-5H20,100 mg; ZnS0 4 H 2 0,150 mg; Na2Se03,15 mg; antioxidant ("Ethoxyquin"), 100 mg; Avoparcin, 100 mg; Monensin (up to 5 d before slaughtering), 100 mg. 2 Values calculated from data provided by the Dutch Bureau of Livestock Feeding (1991).
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1957). The computer program GENSTAT 5 (Payne et ah, 1987) was used to calculate the ANOVA. The treatment factors were dietary level of SAA and sex. No significant sex by treatment interaction was observed. Therefore, only the combined results for males and females are presented. Because male birds of Experiment 2 were involved in carcass yield measurements, performance results of the males of this experiment are also presented separately. The significance of differences between treatment means was tested by using the least significance difference test (Snedecor and Cochran, 1980). All statements of significance are based on a probability of less than .05. The SAA requirements were estimated from weight gain, feed:gain ratio, and
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SULFUR AMINO ACID REQUIREMENT OF BROILERS TABLE 2. Effects of dietary DL-methionine supplementation on broiler performance, Experiment 1 (14 to 34 d of age) Treatment1
Added DL-methionine
Dietary SAA level
- (%)
—
(g)
(g/bird/d) 108.9* 107.9*= 109.2» 107.4*= 106.8"=d 105.8=d 105.0d 106.0=d .8
Feed:gain (g:g) 1.788* 1.756b 1.740b= 1.726=d 1.709
*-fMean values within a column with no common superscript differ significantly (P ^ .05). 1 Each treatment consisted of six replicates of 43 birds each.
male and female chicks were also evaluated, as the response curves for weight gain and feed conversion efficiency for both sexes followed a similar pattern. RESULTS
Mortality rate in both experiments was very low, being .5% in Experiment 1 and .7% in Experiment 2. No appreciable differences in mortality among the treatments were observed. Performance data of Experiment 1 are summarized in Table 2. Weight gain was improved significantly up to a dietary TSAA of .79%. A further increase of the TSAA content had hardly any effect on provements in feed conversion efficiency up to the highest supplemented level of
.20% DL-methionine, resulting in a dietary TSAA level of .95%. Feed conversion efficiency of birds fed the diet containing .95% TSAA was significantly better than those fed the diet containing .85% TSAA. There was a trend of a decreased daily feed intake when the dietary TSAA level was increased from .79 to .91%. Performance data of Experiment 2 are presented in Tables 3 and 4. In Table 3 these data relate to the combined results for both sexes and those in Table 4 to the male chicks separately. There were numerical improvements in weight gain for all increments in dietary TSAA, but the effects were not significant above a TSAA level of .77%. Feed conversion efficiency was improved up to a dietary TSAA level of .88%. However, these improvements
TABLE 3. Effects of dietary DL-methionine supplementation on broiler performance, Experiment 2 (14 to 38 d of age) Treatment1
Added DL-methionine ( % )
1 0 2 .03 3 .07 4 .12 5 .18 6 .24 Pooled SEM (df 36)
Dietary SAA level —
•
.70 .73 .77 .82 .88 .94
Weight gain
Feed intake
(g)
(g/bird/d) 120.5 121.3 121.9 120.9 120.8 121.3 .8
1,566= 1,613" 1,643* 1,651* 1,658* 1,666* 15
'-''Means within a column with no common superscript differ significantly (P S .05). iEach treatment consisted of eight replicates of 50 birds each.
Feed:gain
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Feed intake
1,221= l,230b= 1,257* 1,248* 1,251* 1,252* 1,249* 1,265* 8
.75 .77 .79 .82 .85 .88 .91 .95
1 0 2 .02 3 .04 4 .07 5 .10 6 .13 7 .16 8 .20 Pooled SEM (df 32)
Weight gain
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SCHUTTE AND PACK TABLE 4. Effects of dietary DL-methionine supplementation on male broiler performance, Experiment 2 (14 to 38 d of age)
Treatment1
Added DL-methionine
Weight gain
Feed intake
(g)
(g/bird/d) 129.5 129.3 130.1 129.8 129.4 130.5
Dietary SAA level
(%) • 1 0 2 .03 3 .07 4 .12 5 .18 6 .24 Pooled SEM (df 36)
— .70 .73 .77 .82 .88 .94
1,736= l,780b= 1,840* 1,852= 1,862= 1,875= 21
Feed:gain
teg) 1.792= 1.744b 1.697= 1.683= 1.668= 1.670= .015
1.1
Means within a column with no common superscript differ significantly (P < .05). Each treatment consisted of four replicates of 50 birds each.
J
were of no importance in excess of .12% added methionine, providing .82% TSAA (Table 3). Carcass yield results of the male birds are presented in Table 5. A positive response on breast meat yield was achieved by increased dietary methionine. Breast meat yield of birds fed the diet containing .88% TSAA was significantly higher than that of birds fed diets containing .70 and .73% TSAA. In addition a decreased abdominal fat deposition by increasing dietary methionine up to a level of .12%, providing .82% TSAA, was observed. Abdominal fat deposition of birds fed the diet containing .82% TSAA was
significantly lower than that of birds fed diets with .70 and .73% TSAA. A summary of the TSAA requirements estimated from the exponential response curves is presented in Table 6. Based on these analyses the estimated TSAA requirements for obtaining m a x i m u m weight gain were similar in both experiments, being .83%. For obtaining maximum efficiency of feed utilization, the requirement for TSAA was estimated to be .88% in Experiment 2. The results of Experiment 1 suggest a higher requirement for TSAA for obtaining maximum efficiency of feed utilization, which was
TABLE 5. Effect of dietary DL-methionine supplementation on carcass yield characteristics (in percentage of body weight) of male broilers at 38 d of age, Experiment 2 Pooled SEM (df 18)
Treatments 1 Variable Added DL-methionine, % Dietary SAA level, % Body weight at slaughter, g Slaughter weight, 2 % BW Oven-ready,3 % BW Edible organs, % BW Breast meat, 4 % BW Abdominal fat, % BW a_
1
2
3
4
5
6
.70
.03 .73
.07 .77
.12 .82
.18 .88
2,071 85.1* 72.9b 3.7= 15.9= 2.9=
2,115 85.1* 73.0b 3.6= 16.3b= 2.7=b
2,128 85.2= 73.2=b 3.6= 16.7* 2.6b=
2,170 84.7b 72.9b 3.6= 16.8* 2.4=
2,183 85.1* 73.5= 3.4b 17.0= 2.5=
0
.24 .94 2,167 84.9=b 73.2=b 3.4b 16.9= 2.5=
=Means within a row with no common superscript differ significantly (P <, .05). n = 60 birds per treatment. 2 Body weight minus blood, feather, head, and feet. 3 Carcass including neck, neck skin, and abdominal fat. 4 Without bones and skin. x
32.1 .13 .17 .05 .18 .08
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a_c
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SULFUR AMINO ACID REQUIREMENT OF BROILERS TABLE 6. Summary of the estimated TSAA requirements from exponential response curves Experiment
Variable
Exponential response curve
1 Table 2
Weight gain Feed:gain
y = 1,219 + 35.3[l-e _ 3 6 3 ( x " 7 5 ) ] y = 1.78 - .117[l _ e - la9 < x " 75>]
2 Tables 3 and 5
Weight gain Feed:gain Breast meat^
y = 1,567 + 95.8[l - e"217(x " 7 0 ) ] y = 1.85 - .097[l-e~16-5(x~70)~ y = 21.9 - 1.30[l-e~ 160(x_70) '
Estimated requirements1 .83 >.952 .84 .88 .89
Calculated at 95% of maximum response. Estimated requirement of 1.02% exceeded the range of TSAA levels tested. Percentage of slaughter weight.
DISCUSSION Generally, in estimating amino acid requirements from growth studies two types of methods are used; the linear (broken line) model and the nonlinear models. As was pointed out by Fisher et al. (1973), the use of a linear response u p to a maximum level usually leads to an underestimation of requirements. On the other hand, use of curves based on exponential equations may lead to overestimation of the response in which practical decisions are made. From a comparison of the two models, Robbins et al. (1979) concluded that the nonlinear models are preferable. However, nonlinear curves do not define a fixed requirement, which led us to the approach to derive a tentative figure at 95% of the maximum response. Although this is an arbitrary choice, the procedure does give a good idea of the dietary amino acid level to support close to maximum performance. The results of these experiments demonstrate that the chicken's need for methionine and TSAA is higher for obtaining maximum efficiency of feed utilization than for maximum weight gain. This finding is supported by others (Adams et al, 1962; Bornstein and Lipstein, 1964, 1966; Van Weerden et al, 1976). The results of Experiment 1 suggest that this
phenomenon may be explained partly because methionine regulates feed intake, as proposed by Chee and Polin (1978). In this experiment there was a trend suggesting that birds have the ability to compensate for a marginal deficiency of methionine by consuming more feed. Similar effects were observed in previous studies with laying hens (Schutte and Van Weerden, 1978; Schutte et al, 1983, 1984), also indicating that at marginal deficiencies of methionine birds ate more feed in an attempt to meet their requirement. In Experiment 2, however, a regulating action by methionine on feed intake was not observed. From the results of both trials it was estimated that the TSAA requirement of broiler chicks in the age period of 14 to 34 or 38 d is at least .88% in a diet containing about 3,180 kcal ME/kg for obtaining maximum efficiency of feed utilization. A similar dietary requirement level of TSAA was estimated for obtaining maximum yield of breast meat in male broiler chicks. Literature data about the TSAA requirement of broiler chicks for the age period of 14 to 34 or 38 d are not available. Our estimation for TSAA requirement during this age period is somewhat lower than the dietary level recommended by NRC (1994) of .90% TSAA for the age period of 0 to 3 wk, but distinctly higher than their recommendation of .72% TSAA for 3 to 6 wk of age. Based on the results of the present studies, a dietary TSAA level of approximately .80% as reported by Jensen et al (1989), Mendonca and Jensen (1989), and Jeroch and Pack (1992) seems to be a
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calculated to be higher than the maximum level of .95% TSAA tested in the experiment. Maximum response on breast meat yield was estimated at a TSAA level of .89%.
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REFERENCES Adams, R. L., F. N. Andrews, J. C. Rogler, and C. W. Carrick, 1962. The sulfur amino acid requirement of the chick from 4 to 8 weeks of age as affected by temperature. Poultry Sci. 41: 1801-1806. Association of Official Analytical Chemists, 1984. Official Methods of Analysis. 14th ed. Association of Official Analytical Chemists, Washington, DC. Beck, A., H. Schmidtborn, M. Spindler, and H. Tanner, 1978. Die Bestimmung von gebundenen und supplementierten Aminosauren in Futtermitteln u n d Mischfuttern mit Hilfe der lonenaustausch-Chromatographie. Kraftfutter 3: 118-124. Bornstein, S., and B. Lipstein, 1964. Methionine supplementation of practical broiler rations. 1. The value of added methionine in diets of varying fish meal levels. Br. Poult. Sci. 5: 175-186. Bornstein, S., and B. Lipstein, 1966. Methionine supplementation of practical broiler rations. III. The value of added methionine in broiler finisher rations. Br. Poult. Sci. 7:273-284. Chee, K. M., and D. Polin, 1978. Effect of methionine and methods of feeding on feed intake. Poultry Sci. 57:1126.(Abstr.) Cochran, W. G., and G. M. Cox, 1957. Experimental Designs. 2nd ed. John Wiley and Sons, Inc., New York, NY. Degussa, 1992. Digestible Amino Acids in Feedstuffs for Poultry. Degussa AG, Hanau, Germany. Dutch Bureau of Livestock Feeding, 1991. Chemical Composition, Digestibility and Energy Value of
Feed Ingredients. Bureau of Livestock Feeding, Lelystad, The Netherlands. Fisher, C , T. R. Morris, and R. C. Jennings, 1973. A model for the description and prediction of the response of laying hens to amino acid intake. Br. Poult. Sci. 14:469-484. Hickling, D., W. Guenter, and M. E. Jackson, 1990. The effect of dietary methionine and lysine on broiler chicken performance and breast meat yield. Can. J. Anim. Sci. 70:673-678. Holsheimer, J. P., and C. H. Veerkamp, 1992. Effect of dietary energy, protein, and lysine content on performance and yields of two strains of male broiler chicks. Poultry Sci. 71:872-879. Huisman, J., P.H.U. de Vries, E. J. van Weerden, and H. L. Bertram, 1985. The availability of synthetic methionine in pigs. J. Anim. Physiol. Anim. Nutr. 55:267-272. Janssen, W.M.M.A., K. Terpstra, F.F.E. Beeking, and A.J.N. Bisalsky, 1979. Feeding Values for Poultry. 2nd ed. Spelderholt Publication 303, Beekbergen, The Netherlands. Huyghebaert, G., M. Pack, and G. de Groote, 1994. Influence of protein concentration on the response of broilers to supplemental DLmethionine. Arch. Gefltlgelkd. 58(l):23-29. Jensen, L. S., C. L. Wyatt, and B. I. Fancher, 1989. Sulfur amino acid requirement of broiler chicks from 3 to 6 weeks of age. Poultry Sci. 68: 163-168. Jeroch, H., and M. Pack, 1992. Influence of protein content in feed on sulphur amino acid requirements of broiler chicks. Pages 601-605 in: Proceedings of the 19th World's Poultry Congress. Ponsen and Looyen, Wageningen, The Netherlands. Mendonca, C. X., and L. S. Jensen, 1989. Influence of protein concentration on the sulphur-containing amino acid requirement of broiler chicks. Br. Poult. Sci. 30:889-898. Moran, E. T., 1988. Dietary lysine and broiler meat yield. Pages 46-52 in: Proceedings of the California Animal Nutrition Conference, Fresno, CA. Moran, E. T., and S. F. Bilgili, 1990. Processing losses, carcass yield quality, and meat yields of broiler chickens receiving diets marginally deficient to adequate in lysine prior to marketing. Poultry Sci. 69:702-710. National Research Council, 1994. Nutrient Requirements of Poultry. 9th rev. ed. National Academy Press, Washington, DC. Pack M., and J. B. Schutte, 1995. Sulfur amino acid requirement of broiler chicks from 14 to 34 or 38 days of age. 2. Economical evaluation. Poultry Sci. 74:488—493. Payne, R. W., P. W. Lane, A. E. Ainsley, K. E. Bicknell, P.G.N. Digby, S. A. Harding, P. K. Leech, H. R. Simpson, A. D. Todd, P. J. Verrier, and R. P. White, 1987. Genstat 5 Reference Manual, Oxford University Press, New York, NY. Robbins, K. R., H. W. Norton, and D. H. Baker, 1979. Estimation of nutrient requirements from growth data. J. Nutr. 109:1710-1714. Schutte, J. B., and E. J. van Weerden, 1978. Requirement of the hen for sulphur containing amino acids. Br. Poult. Sci. 19:573-581. Schutte, J. B., E. J. van Weerden, and H. L. Bertram, 1983. Sulphur amino acid requirement of laying
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more reasonable requirement figure for the age period of 3 to 6 wk. Janssen et al. (1979) determined the content and digestibility of amino acids of various feedstuffs used in the formulation of poultry diets. From their data it was calculated that the content of apparent digestible SAA in the basal diet used in Experiment 1 was .62% and .57% in the basal diet used in Experiment 2. Assuming that digestibility of DL-methionine can be set at 100% (Huisman et al, 1985), it can be calculated that the current estimated requirement for TSAA (.88%) for the age period of 14 to 34 or 38 d corresponds with approximately .75% apparent digestible SAA. In terms of true digestible amino acids, the two basal diets were calculated to contain .65 and .60% digestible SAA, respectively (Degussa, 1992). Based on this criterion, the estimated requirement for TSAA corresponds with approximately .78% true digestible SAA. The economics of feeding increasing SAA levels must be considered in evaluating the results of the present studies. This has been done in an additional paper (Pack and Schutte, 1994).
SULFUR AMINO ACID REQUIREMENT OF BROILERS hens and the effects of excess dietary methionine on laying performance. Br. Poult. Sci. 24: 319-326. Schutte, J. B., E. J. van Weerden, and H. L. Bertram, 1984. Protein and sulphur amino acid nutrition of the hen during the early stage of laying. Arch. Gefltlgelkd. 48(5):165-170. Skinner, J. T., A. L. Waldroup, and P. W. Waldroup, 1992. Interaction of methionine and cystine needs of broilers 21 to 42 days of age. Poultry Sci. 71(Suppl. l):110.(Abstr.)
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Snedecor, G. W., and W. G. Cochran, 1980. Statistical Methods. 7th ed. The Iowa State University Press, Ames, IA. Uijttenboogaart, T. G., and A. R. Gerrits, 1982. Method of dissection of broiler carcasses and description of parts. Spelderholt Report 370. Beekbergen, The Netherlands. Van Weerden, E. J., J. B. Schutte, and J. E. Sprietsma, 1976. Relation between methionine and inorganic sulphate in broiler rations. Poultry Sci. 55: 1476-1481.
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