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. Tesseraud1
Station de Recherches Avicoles, Institut National de la Recherche Agronomique,
Centre de Tours-Nouzilly, 37380 Nouzilly, France
data, and bird responses were lower than at 22 C. We
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.
ABSTRACT The effects of two environmental temperatures (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. At 32 C, there was a greater heterogeneity of the
(Key words: chronic heat exposure, dietary protein, growth, carcass characteristics, broiler)
2000 Poultry Science 79:312–317
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.
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-
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 CO3 12.4, 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
Received for publication February 1, 1999.
Accepted for publication September 30, 1999.
1
To whom correspondence should be addressed: tesserau@ tours.
inra.fr.
2
Amino acid analyzer LC 5001, Eppendorf-Netherler Hinz G17BH,
Division Biotronik, Hamburg, Germany.
3
Abacus Concepts, 1996, Inc., Berkeley, CA 94704-1014.
Abbreviation Key: FCR = feed conversion ratio.
312
313
PROTEIN SUPPLY IN HEAT-EXPOSED CHICKENS
TABLE 1. Composition of basal diets (%)
Diet
Ingredients
10%
33%
Corn
Corn starch
Corn gluten meal (62% CP)
Wheat
Soybean meal (48% CP)
Soybean protein
Rapeseed oil
Calcium carbonate
Dicalcium phosphate
Salt
Trace minerals1
Vitamins1
DL-methionine
Lysine-HCl
Threonine
Valine
Tryptophan
Leucine
Calculated composition
ME (kcal/kg)
Crude protein
41.78
18.6
29.91
10.0
11.7
11.9
5.0
7.9
2.0
0.45
0.1
0.5
0.025
0.045
3,098
10.51
45.9
3.6
6.0
1.16
1.85
0.4
0.1
0.5
0.212
0.113
0.08
0.09
0.005
0.08
3,096
33.22
1
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 autoanalyzer2 using the
Procedure V18-113 (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 MannWhitney 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
10.91
0.54
0.22
0.21
0.44
0.53
1.06
0.44
0.67
10.51
0.52
0.20
0.20
0.39
0.52
0.95
0.46
0.64
15.16
0.79
0.32
0.27
0.67
0.79
1.50
0.63
0.96
19.85
1.07
0.40
0.33
0.89
0.98
2.02
0.87
1.28
28.13
1.50
0.55
0.41
1.23
1.39
2.90
1.20
1.77
33.27
1.77
0.67
0.49
1.43
1.64
3.37
1.45
2.13
33.22
1.82
0.75
0.61
1.33
1.79
3.33
1.61
2.18
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 Aı̈n 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
Temperature
Diet
n1
22 C
10%
20
15%
20
20%
19
28%
21
33%
22
10%
15
15%
18
20%
19
28%
19
33%
20
32 C
Feed intake
(g/d)
Dietary protein
intake2
(g/d)
LW3
4 wk
(g)
LW
6 wk
(g)
Daily body
weight gain
(g/d)
FCR4
146.4ab
(3.7)
150.9a
(2.3)
141.7bc
(2.8)
134.2cd
(2.3)
131.7de
(1.7)
124.2ef
(3.8)
116.8fg
(3.3)
111.7g
(2.9)
111.7g
(3.0)
109.4g
(3.2)
16.07g
(0.41)
22.95e
(0.34)
28.17d
(0.55)
37.85b
(0.64)
43.82a
(0.57)
13.63h
(0.42)
17.77f
(0.49)
22.20e
(0.58)
31.49c
(0.84)
36.42b
(1.07)
1,146
(15)
1,145
(15)
1,144
(16)
1,145
(14)
1,140
(14)
1,137
(16)
1,141
(15)
1,140
(15)
1,131
(15)
1,143
(15)
1,849c
(31)
2,073b
(25)
2,190a
(31)
2,262a
(27)
2,247a
(24)
1,681e
(24)
1,751de
(36)
1,810cd
(28)
1,868c
(40)
1,890c
(44)
46.9d
(1.6)
61.9c
(1.1)
69.7b
(1.5)
74.4a
(1.2)
73.7a
(1.2)
36.3f
(1.4)
40.6ef
(2.0)
44.6de
(2.0)
49.2d
(2.4)
50.0d
(2.8)
3.152b
(0.066)
2.444d
(0.026)
2.035f
(0.019)
1.805g
(0.023)
1.791g
(0.025)
3.445a
(0.067)
2.943c
(0.092)
2.564d
(0.092)
2.337de
(0.086)
2.285ef
(0.091)
Means (SEM) within columns with no common superscript differ significantly (P < 0.05).
Number of chicks.
2
Dietary protein intake calculated from measured dietary CP content.
3
LW = Live weight.
4
Feed conversion ratio.
a-h
1
315
PROTEIN SUPPLY IN HEAT-EXPOSED CHICKENS
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
Temperature
Diet
n1
22 C
10%
14
15%
15
20%
15
28%
15
33%
15
10%
15
15%
14
20%
15
28%
14
33%
15
32 C
LW2
(g)
1,848.6c
(17.9)
2,039.8b
(20.1)
2,187.9a
(34.4)
2,266.6a
(17.9)
2,250.0a
(24.2)
1,681.1e
(24.0)
1,719.3d
(26.7)
1,806.6c
(26.6)
1,872.1c
(32.9)
1,885.3c
(53.9)
AF3
(g)
AF/BW
(%)
BM4
(g)
BM/BW
(%)
64.4a
(3.4)
57.2a
(2.6)
42.7bc
(2.2)
36.5cd
(1.8)
32.5e
(1.8)
3.5a
(0.2)
2.8b
(0.1)
1.9cd
(0.1)
1.6de
(0.1)
1.4e
(0.1)
226.3e
(5.4)
268.8c
(4.5)
328.3b
(8.9)
361.4a
(6.5)
364.2a
(8.3)
12.2d
(0.2)
13.2c
(0.2)
15.0b
(0.2)
15.9a
(0.2)
16.2a
(0.2)
61.5a
(2.8)
49.6b
(3.2)
38.8cd
(2.5)
40.9cd
(2.6)
35.1de
(2.7)
3.6a
(0.1)
2.9b
(0.2)
2.2c
(0.1)
2.2c
(0.1)
1.9cd
(0.1)
207.2f
(4.7)
227.3ef
(5.2)
249.5d
(6.9)
258.2cd
(5.7)
277.9cd
(10.6)
12.3d
(0.2)
13.2c
(0.2)
13.8c
(0.3)
13.8c
(0.2)
14.7b
(0.3)
Means (SEM) within columns with no common superscript differ significantly (P < 0.05).
Number of chicks.
2
LW = Live weight.
3
AF = Abdominal fat.
4
BM = Breast muscles.
a-f
1
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 (䉭) or 32 C
(▲). 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 = 14.59 + 2.00 x; r2 = 0.89. At 32 C body weight gain = 24.49
+ 0.80 x, r2 = 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
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.
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