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ENVIRONMENT, WELL-BEING, AND BEHAVIOR |
* Institute of Animal Science, The Volcani Center, Bet Dagan 50250, Israel; Department of Animal Sciences, Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot 76100, Israel; and Department of Poultry Science, North Carolina State University, Raleigh 27695-7608
2 Corresponding author: yahavs{at}agri.huji.ac.il
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: embryogenesis • thermal manipulation • broiler • thermotolerance • stress
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Being homeotherms, birds are able to maintain their body temperature within a narrow range. An increase in body temperature above the regulated range, as a result of exposure to the environmental conditions and excessive metabolic heat production that often characterize broiler chickens, may lead to a potentially lethal cascade of irreversible thermoregulatory events. Although broilers are typically maintained in environmentally controlled facilities that minimize fluctuations of ambient temperature, wild birds, as well as their eggs and neonates, have often been subjected to erratic environmental conditions. This is thought to be one of the reasons why wild birds have been better able to develop thermotolerance. Such exposure to temperature fluctuations during the perinatal period has been shown to lead to epigenetic temperature adaptation (Nichelmann et al., 1999; Tzschentke et al., 2001). The mechanism for this adaptation is based on the assumption that environmental factors, especially ambient temperature, have a strong influence on determining the set point for physiological control systems during critical developmental phases, first described as the "determination rule" (Dörner, 1974).
Recent studies have suggested that it is possible to improve the acquisition of thermotolerance (AT) in poultry by exposing them to high ambient temperatures during embryogenesis (Decuypere, 1984; Tzschentke et al., 2001; Janke et al., 2002; Tzschentke and Basta, 2002; Yahav et al., 2004a,b). However, these studies revealed the potential to cope with acute heat stress up to only 10 d posthatch. Furthermore, a recent study by Collin et al. (2007) showed that thermal manipulation of chick embryos applied during early or late embryogenesis, or during both periods, did not improve AT when the broilers were tested at 6 wk of age.
Selection of the critical phase during embryogenesis for the application of thermal manipulation (TM) to improve AT was based on the hypothesis that the set point, or "response threshold," of controlling systems could be altered most efficiently during the development or maturation of the hypothalamus-hypophysis-thyroid axis (thermoregulation) and the hypothalamus-hypothesis-adrenal axis (stress). This study aimed to elucidate the effect of TM during the development of the thyroid and adrenal axes of broiler embryos on the AT potential of broilers, as evidenced by the ability to withstand acute thermal stress at marketing age.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The procedures in this study were carried out in accordance with the accepted ethical and welfare standards of the Israeli ethics committee (IL-005/05). A total of 504 fertile Cobb broiler hatching eggs (62.5 ± 2.5 g) were obtained from one breeder flock of hens at 39 wk of age. The eggs were incubated in 2 automatic incubators (Type 65Hs, Masalles, Barcelona, Spain), the control and the TM incubators. Three treatments were applied in the experiment: 1) control, under standard conditions of 37.8°C, 56% RH, and at a turning frequency of 1/h (Bruzual et al., 2000); 2) TM of 39.5°C and 65% RH continuously from embryonic day (E)7 to E16 (180 to 408 h of incubation; 24H); 3) TM during the same period but for only 12 h/ d (12H). From E0 to E7 and from E17 to E18, all eggs were incubated in the control incubator. On E7, eggs in the 2 TM treatments were transferred to the TM incubator. The 24H eggs were kept in this incubator until E16 (inclusive), whereas those in the 12H treatment were transferred every 12 h to the TM incubator and back to the control incubator. On E18, eggs were transferred to hatching trays and maintained under the same conditions of 37.5°C and 56% RH. The beginning of the incubation was defined as E0. At E6, eggs were candled to remove nonfertile eggs and early dead embryos.
Relative humidity in the TM treatment was elevated to 65% to avoid excessive water loss from the eggs as a result of the increase in incubation temperature. The RH elevation caused a slight decline in the partial pressure of oxygen (pO2) by 7.1 mmHg.
During hatching, the number of chicks hatched was recorded every hour. Nonhatched eggs or those that were externally pipped were also recorded. After the feathers of each chick had dried (approximately 2 h after hatching), each was taken out of the incubator for immediate measurement of body temperature (Tb) with a digital thermometer (Super Speed Digital Thermometer, Procare Measure Technology Co. Ltd., San Chung City, Taipei, Taiwan) accurate to ±0.1°C, BW measurement, and sex identification.
After the measurements were completed, chicks from each treatment and sex were randomly divided into non-challenged and thermally challenged subtreatments (70 chicks in each group) and were placed in cages (5 chicks per cage) that measured 40 x 28 x 45 cm (length, width, and height), with a 2-cm wire mesh floor. The cages were situated in 3 computer-controlled environmental rooms that maintained a constant temperature with an accuracy of ±1.0°C, RH at ±2.5%, air velocity at ±0.25 m/s, and under continuous fluorescent illumination. A similar number of chicks from each treatment and subtreatment were housed in each of the environmentally controlled rooms. Chicks were raised under these standard conditions to 21 d of age. At 21 d of age, each chicken was placed in a single cage and ambient temperature was maintained at 25.0 ± 1.0°C to 35 d of age. Water and feed in mash form were supplied ad libitum. The diet was designed according to NRC (1994) recommendations. At weekly intervals, BW and feed intake were recorded for both individuals and groups (15 individuals per group), respectively.
At the age of 35 and 36 d, male and female chickens, respectively, from the thermally challenged group were exposed to 35.0°C and low RH (
30%) for 5 h, whereas the nonchallenged chicks continued under the standard conditions. During the last hour of thermal challenge, Tb was measured in 20 individuals per treatment as described above, and blood samples were drawn from the brachial vein of 10 individuals per treatment. Identical measurements and samplings were conducted with the nonchallenged chicks.
Blood Analysis
Radioimmunoassays of total thyroxin (T4) and total triiodothyronine (T3) were applied to plasma samples with commercial RIA kits (Diagnostic Products Corporation DCP, Los Angeles, CA). The intraassay and interassay CV of the T3 assay were 7.0 and 9.4%, respectively, and those of the T4 assay were 5.0 and 7.5%, respectively. Plasma corticosterone concentrations were measured with an RIA kit with the ImmuChem Double Antibody Corticosterone RIA kit (ICN Biomedical Inc., Diagnostics Division, Orangeburg, NY). The intraassay and interassay CV of the corticosterone assay were 4.7 and 6.5%, respectively.
Statistical Analysis
The data were subjected to one-way ANOVA and to the all-pairs Tukey-Kramer honestly significant difference test by means of JMP software (SAS Institute, 2002). Hatchability, external pipping, nonabsorbed yolk sacs, and rough navals were analyzed with the chi-square test. Means were considered significantly different at P 
0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The effect of TM during embryogenesis on hatchability is summarized in Table 1
. Hatchability after 501 h of incubation was 83.3 and 79.4% for the control and 12H TM, respectively, whereas that of the 24H TM was only 50.6%. The initiation of hatching differed among the treatments and was 474, 472, and 479 h for the control, 12H, and 24H treatments, respectively. A significant delay in reaching 50% hatching was observed for the 24H TM compared with the control and 12H TM groups (Figure 1). In the 24H treatment, 60% of the nonhatched embryos could not complete external pipping, compared with only 33 and 23% in the 12H and control treatments, respectively. Moreover, the percentage of hatched chicks with a rough navel or nonabsorbed yolk sac in the 24H TM reached 34%, compared with 14 and 5% in the 12H and control treatments, respectively. The BW at hatching was significantly lower for both sexes in the 24H TM than in the control and 12H treatments (Table 2; Figure 2). The BW of both sexes of the 12H TM chickens was similar to that of the control chickens during the 35 d of growth and development (Figure 2), whereas the BW of the 24H TM chickens was significantly lower throughout this period.
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and Figure 3. The Tb was significantly lower in the 12H TM-treated birds than in the control birds, and the Tb of the 24H TM birds was significantly lower than those of both other treatments.
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). In females, the Tb of the TM birds was significantly lower than that of control birds for the entire 5 wk of growth. Thermal Challenge
Thermal challenge (35°C for 5 h) of male broilers at 35 d of age resulted in a significant and dramatic development of hyperthermia in all 3 treatments (Table 3). How-ever, by the end of the challenge, the distribution of Tb among treatments differed (Figure 4, upper panel). Of the 12H TM chickens, 32% exhibited a Tb ranging between 43 and 44°C, whereas only 19 and 20% of the control and 24H birds, respectively, had Tb in the same temperature range.
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). Plasma corticosterone concentration increased significantly in all treatments as a result of thermal challenge, but remained significantly lower in the 12H and 24H TM chickens as compared with the control birds. Both the 12H and 24H TM chickens exhibited half as much mortality as the control chickens during thermal challenge (Table 3).
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). The Tb distribution, which ranged between 43 and 44°C and between 44 and 45°C by the end of the exposure, was 20, 37, and 44%, and 60, 37, and 44% for the control, 12H, and 24H treatments, respectively (Figure 4, lower panel).
The plasma concentration of T4 increased during thermal challenge and was significantly lower in the 24H than in the 12H and control treatments. Plasma T3 concentration was significantly higher in the nonchallenged control females compared with the treated birds (Table 4). Thermal challenge caused a significant decline in plasma T3 concentrations in all treatments, but the concentration in the 24H TM-treated chickens was significantly lower than that of the control birds, and that of the 12H TM-treated birds was significantly lower than that of the 24H TM broilers (Table 4). A significant increase in plasma corticosterone concentration occurred in all treatments as a result of thermal challenge; however, the 12H and 24H TM broilers exhibited a significantly lower concentration than was exhibited by the controls. No female mortality was recorded during thermal challenge (Table 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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It was previously reported that exposing embryos to high or low temperatures during incubation improved their capacity to adapt to hot or cold environments, respectively, in the posthatch phase (Decuypere, 1984; Iqbal et al., 1989; Nichelmann et al., 1994; Tzschentke and Basta, 2002; Moraes et al., 2003; Yahav et al., 2004a,b; Shinder et al., 2007). Continued genetic selection has caused a significant increase in heat production. Furthermore, studies that were conducted during the 1980s and 1990s were carried out with broilers that differed to some extent from present-day birds. The latter studies challenged the broilers only at a young age or tested their potential with mild heat stress. A recent study that evaluated the potential of broilers to cope with severe heat stress at marketing age (Collin et al., 2007) after TM at E8 to E10, E16 to E18, or a combination of the 2 treatments during embryogenesis could demonstrate no advantage of TM in the birds’ ability to cope with deleterious environmental temperatures, mainly because TM was not applied during the most critical phase period.
In the present study, 3 critical parameters for TM during incubation were considered: a) the critical phase; b) the temperature level; and c) the duration of exposure. The determination of the critical phase during embryogenesis for the application of TM to improve AT was based on the hypothesis that the set point or response threshold of the controlling systems could be altered most efficiently during the development or maturation of the hypothalamus-hypophysis-thyroid axis (thermoregulation) and the hypothalamus-hypophysis-adrenal axis (stress).
Exposure of embryos to TM for 12H between E7 and E16 (inclusive) induced early hatching by 2 and 7 h, respectively, compared with hatching of the control and 24H-treated birds. This earlier hatching trend became more evident at 50% hatching, but differences diminished during the last 8 h. However, TM resulted in a dramatic decline in the hatchability of the 24H TM chickens, as was demonstrated previously (Piestun, Y., D. Shinder, O. Halevy, and S. Yahav, unpublished manuscript), and negatively affected the quality of the hatched chicks, as evidenced by poor yolk sac absorption and the presence of rough navels.
The continuous TM (24H) had a long-lasting effect on the BW of both males and females. From hatching to 35 d of age, the BW of the 24H TM chickens was significantly lower than those of the 12H TM and control chickens. The lower BW coincided with significantly lower feed intake as well (data not shown). One could speculate that this was related to a lower metabolic rate. However, it was clear from the Tb of the chickens during the growth period and from the thyroid hormones levels before heat challenge at 35 d of age that the metabolic rate of the 24H TM chickens was similar to that of the chickens in the 12H treatment, which maintained a BW similar to the control birds.
Both TM treatments (12H and 24H) had a long-lasting effect on the Tb of both males and females. This phenomenon was not observed previously when embryos were subjected to an elevated temperature between E8 and E10 or E16 and E18 (Collin et al., 2007). We speculated that in this study the fine tuning of all 3 critical parameters (sensitive phase, level of incubation temperature, and duration of exposure) caused the long-lasting response in Tb. This change in Tb also found expression during the thermal challenge.
The AT can be defined by several parameters. In this study it was examined by using Tb and thyroid and corticosterone hormones. Thermal challenge at 35 d of age induced severe hyperthermia in all treatments. However, when the distribution of Tb was examined, the advantage of 12H and 24H females was pronounced (Figure 4). The birds that had Tb in the range of 43 to 44°C were able to recover from hyperthermia in most cases, whereas the birds in the higher temperature range (44 to 45°C) would probably not be able to recover (Yahav, 2000). In the males, a pronounced advantage (Tb between 43 and 44°C) was demonstrated by the 12H TM broilers only.
The mortality of the males exhibited a similar resistance to thermal challenge induced by both TM treatments despite the pronounced Tb distribution of those in the 12H treatment. The lower mortality rate may be related to the reduced metabolic rate and stress of the TM birds, as evidenced by the thyroid and corticosterone plasma levels, respectively.
Thermal challenge caused a significant decrease in plasma T3 concentrations in all 3 treatments. However, T3 levels of the TM chickens decline significantly more than those of the control chickens. The decline in plasma T3 concentration as a result of thermal challenge was most probably caused by reduced peripheral deiodination of T4, especially in the liver (Reyns et al., 2003), and by increased T3 catabolism (Bianco et al., 2002). The reduction in peripheral deiodination as a result of increasing ambient temperature apparently resulted in an increase in plasma T4 concentration. Indeed, this was the case regarding the thermally challenged control birds and the 12H TM males and females. However, within the 24H TM treatment, a moderate increase in plasma T4 concentration was exhibited by males, but no such response was observed in females. It can be speculated that TM during embryogenesis may have reduced the activity of the thyroid gland when the chickens were later exposed to acute thermal stress. These details remain to be elucidated. Coupled with the alteration in thyroid hormones, a dramatic increase in plasma corticosterone concentration was exhibited by both sexes. In the males, the increase was 8- and 6-fold for the control and TM treatments, respectively, whereas in the females more moderate increases of 6-fold and 3- to 4-fold, respectively, were recorded. In both sexes, the lower level of stress experienced by the TM broilers may have contributed to their ability to cope better with the acute thermal challenge.
We concluded that TM during embryogenesis, when the thyroid and adrenal axis develop and mature, had a long-lasting effect and improved the AT of broiler chickens exposed to acute thermal stress at market age. Whereas intermittent TM had no significant effect on hatchability and performance parameters, continuous TM negatively affected these parameters.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Received for publication January 17, 2008. Accepted for publication April 15, 2008.
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