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Interrelationship between environmental temperature and dietary nonphytate phosphorus in laying hens
Interrelationship Between Environmental Temperature and Dietary Nonphytate Phosphorus in Laying Hens M. E. Persia, P. L. Utterback, P. E. Biggs, K. W. Koelkebeck, and C. M. Parsons1 Department of Animal Sciences, University of Illinois, Urbana, Illinois 61801 Experiment 3 was similar to experiments 1 and 2 except that constant HS was implemented. Both constant HS and low dietary NPP reduced feed intake and egg production, and there was no significant interaction between HS and dietary NPP level. In experiment 4, hens were fed 0.10 or 0.45% NPP diets and exposed to a more severe HS (38°C) for 8 h. Hens fed the deficient NPP level showed a 16% incidence of severe heat distress (unable to stand, unresponsive). Our results generally indicated that there was no interaction between dietary NPP level and HS in laying hens. However, subjecting hens that had been fed a P-deficient diet to an acute HS of 38°C did increase the incidence of severe heat distress.
(Key words: egg production, heat stress, laying hen, nonphytate phosphorus, mortality) 2003 Poultry Science 82:1763–1768
INTRODUCTION Heat stress (HS) is a problem in large parts of the world, including many parts of United States. HS has been associated with decreases in feed intake, weight gain, egg production, nitrogen retention, protein digestibility, and total mineral retention (Siegel et al., 1974; Bonnet et al., 1997). In the latter area, several studies have reported that HS reduces P utilization. Phosphorus retention by birds exposed to HS is reduced with increased urinary P excretion (Belay et al., 1992; Belay and Teeter, 1996). Phosphorus absorption from the digestive tract is reduced in turkeys during HS (Wolfenson et al., 1987). HS has been shown to reduce plasma inorganic phosphate levels in broiler chicks and laying hens (Ait-Boulahsen et al., 1993; Usayran et al., 2001). Little research has focused on possible interactions between HS and low dietary P in laying hens. Hens fed only 0.22% available P showed increased mortality with increased temperature, especially when peak house temperatures reached 38°C and above (Garlich et al., 1978). In contrast, hens were fed 0.2, 0.3, 0.4, and 0.5% NPP diets and exposed to temperatures of 35°C without any affects on mortality (Usayran et al., 2001). Any adverse effects of HS on P
2003 Poultry Science Association, Inc. Received for publication January 13, 2003. Accepted for publication June 11, 2003. 1 To whom correspondence should be addressed: [email protected].
metabolism are becoming increasingly important as the poultry industry is being encouraged to reduce dietary P levels due to environmental concerns about excess P excreted in poultry manure. Indeed, several recent studies have suggested that laying hens have a NPP requirement that is lower than what is reported in the NRC (1994) and much lower than levels commonly fed by industry (Boling et al., 2000a,b). However, any negative interactions between HS and dietary P would need to be considered when feeding lower levels of NPP during times of high environmental temperature. The objectives of this study were to evaluate the interactions between chronic HS and dietary NPP on mortality, egg production, feed intake, tibia ash, egg specific gravity, and blood parameters in laying hens and to determine the effects of acute severe HS and dietary NPP level on severe heat distress (SHD) in laying hens.
MATERIALS AND METHODS General Procedures All animal procedures used in these experiments received approval from the University of Illinois Institutional Animal Care and Use Committee. Laying hens, either De-
Abbreviation Key: HS = heat stress; NPP = nonphytate phosphorus; pCO2 = partial pressure CO2; SHD = severe heat distress.
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ABSTRACT Four experiments were conducted to evaluate the effects of phosphorus nutrition on laying hens exposed to heat stress (HS). Hens were fed their respective diet for at least 3 wk prior to initiation of each experiment to allow the hens fed low-P diets to become P deficient. In most experiments, hens housed in non-HS conditions were pair-fed to the HS hens to maintain equal feed intake. In experiments 1 and 2, two levels of nonphytate P (NPP; deficient at 0.10 or 0.16% vs. control at 0.45%) and two temperatures (constant thermoneutral at 21°C or cyclic HS up to 35°C) were evaluated. Low NPP significantly reduced feed intake and hen-day egg production, but the cyclic heat treatment had no effect on hen performance.
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TABLE 1. Composition of corn-soybean meal diets varying in nonphytate phosphorus (NPP) content (experiments 1, 2, 3, and 4) Ingredient
0.10% NPP
0.16% NPP
0.45% NPP
(%) 65.30 23.95 9.80 — 0.40 0.20 0.15 0.10 0.05 0.05
65.18 23.95 9.60 0.32 0.40 0.20 0.15 0.10 0.05 0.05
64.51 23.95 8.40 1.89 0.40 0.20 0.15 0.10 0.05 0.05
16.7 3.80 0.10 2,861
16.7 3.80 0.16 2,857
16.6 3.80 0.45 2,834
Experiment 1
1 Provided per kilogram of diet: vitamin A (as retinyl A acetate), 1,514 µg; cholecalciferol (as activated animal sterol), 25 µg; vitamin E (as DLα-tocopheryl acetate), 11 mg; vitamin B12, 0.01 mg; riboflavin, 4.41 mg; D-pantothenic acid, 10 mg; niacin, 22 mg; menadione sodium bisulfite, 2.33 mg. 2 Provided per kilogram of diet: manganese, 75 mg from MnO; iron, 75 mg from FeSO4ⴢH2O; zinc, 75 mg from ZnO; copper, 5 mg from CuSO4ⴢ5H2O; iodine, 0.35 mg from ethylene diamine dihydroiodide; selenium, 0.2 mg from Na2SeO3.
kalb Sigma or Hy-Line W-98, were fed 0.10 or 0.45% NPP diets for at least 3 wk before initiation of each experiment. Feeding the 0.10% NPP diet was done to allow hens to deplete body stores of P and to begin to show P deficiency signs. In experiments 1 to 3, hens were randomly transferred to one of two side-by-side environmentally controlled chambers. Each of the first three experiments was set up as a 2 × 2 factorial with two levels of dietary NPP and two temperature treatments. Eight replicate groups of four hens were penned in cages in each chamber for both dietary NPP treatments in all three experiments. Thus, a total of 128 hens were used in each of the first three experiments. Hens were allowed 7 or 12 d to adjust to the environ-
The first experiment was designed to test the effects of cyclic HS on Dekalb Sigma laying hens from 56- to 59-wkof-age fed different levels of NPP. Treatments were set up in a 2 × 2 factorial arrangement with 0.16 and 0.45% NPP diets (Table 1) and two temperatures, a constant 21°C and a 12-h cyclic 35 or 26°C. During the 14-d experimental period, temperature and RH values for the non-HS chamber ranged from 20 to 22°C and 33 to 96%, respectively. The temperature for the HS chamber during the hot period was 35°C with 36 to 85% RH and 24 to 27°C with 40 to 97% RH during the cool period. The HS period was applied from 0800 to 2000 h, allowing the birds 5 h of light without HS. During the experimental period, the birds kept in the non-HS chamber were pair-fed the amount of feed that the HS hens on the same NPP level had consumed the previous day to eliminate any differences in feed and P intake, within NPP level, due to HS.
Experiment 2 The second experiment was designed to test the effects of a more severe cyclic HS on Dekalb laying hens from 64 to 67 wk of age that were fed different levels of NPP.
TABLE 2. Performance and tibia ash of laying hens fed various nonphytate phosphorus (NPP) levels and exposed to different temperatures (experiment 1)1 Temperature (°C)
NPP level (%)
Adjustment2 (1 to 7 d)
21
Experimental (8 to 21 d)
21
0.16 0.45 0.16 0.45 0.16 0.45
Period
Heat stress3 Pooled SEM ANOVA NPP Temperature NPP × temperature 1
Feed intake (g/hen per d) 87 87 83 89 85 91 2 0.01 0.27 0.79
Hen-day egg production (%) 70 92 64 83 70 80 4 Probability 0.01 0.74 0.28
Tibia ash (%) — — 44 45 44 46 1 0.23 0.89 0.81
Means of eight groups of four Dekalb Sigma laying hens, 56 to 59 wk. Hens were allowed 7 d to adjust to the environmental chambers (21°C) before the 14-d experimental period. The adjustment period data were not included in statistical analysis. The hens had been fed the diets varying in NPP for 3 wk before being moved into the environmental chambers. 3 Cyclic heat stress (12 h at 35°C followed by 12 h at 25°C). 2
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Ground corn Soybean meal Ground limestone Dicalcium phosphate Salt Vitamin mix1 Trace mineral mix2 DL-Met Choline chloride Larvadex/solka floc Calculated composition CP Ca NPP MEn (kcal/kg)
mental chambers before the 14-d experimental period was initiated. The environmental temperature was maintained at 21°C during the adjustment period. All hens were allowed access to feed and water ad libitum during adjustment periods and were maintained on a daily 17-h light period (0530 to 2230 h) for the duration of all experiments. Hens were caged in 46 cm × 46 cm × 46 cm pens with four hens per cage. Mortality, feed intake, and egg production were measured daily during the adjustment and experimental periods. At the end of experiments 1 to 3, eight hens from each treatment (one per replicate group) were randomly selected and euthanized with CO2 gas to determine tibia ash values as outlined by Boling et al. (2000a).
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HEAT STRESS AND PHOSPHORUS IN LAYING HENS TABLE 3. Performance and tibia ash of laying hens fed various nonphytate phosphorus (NPP) levels and exposed to different temperatures (experiment 2)1 Temperature (°C)
NPP level (%)
Adjustment2 (1 to 7 d)
21
Experimental (8 to 21 d)
21
0.10 0.45 0.10 0.45 0.10 0.45
Period
Heat stress3
Feed intake (g/hen per d) 74 98 61 88 61 87 2
75 82 44 77 44 75 4 Probability
0.01 0.77 0.88
0.01 0.88 0.79
Tibia ash (%) — — 50 55 51 54 1 0.01 0.88 0.40
1
Means of eight groups of four Dekalb Sigma laying hens, 64 to 67 wk. Hens were allowed 7 d to adjust to the environmental chambers (21°C) before the 14-d experimental period. The adjustment period data were not included in statistical analysis. The hens had been fed the diets varying in NPP for 2 wk before being moved into the environmental chambers. 3 Cyclic heat stress (16 h at 35°C followed by 8 h at 30°C). 2
Treatments were again arranged as a 2 × 2 factorial arrangement with 0.10 and 0.45% NPP diets (Table 1) and two temperatures, a constant 21°C and a cyclic 16 h at 35°C and 8 h at 30°C. During the experimental period, temperature and RH values for the non-HS chamber ranged from 20 to 22°C and 60 to 99%, respectively. The temperature for the HS chamber during the hot period was 35°C with 32 to 80% RH and 30 to 31°C with 38 to 90% RH during the cool period. The HS period was applied from 0600 to 2000 h, allowing the birds 1 h of light without HS. During the 14-d experimental period, the birds kept in the nonHS chamber were pair-fed the amount of feed that the HS
hens on the same NPP level had consumed the previous day.
Experiment 3 The third experiment was designed to test the effects of constant HS on Hy-Line W-98 laying hens from 58 to 61 wk of age that were fed different levels of NPP. Treatments were arranged as an unbalanced 2 × 2 × 2 factorial arrangement with 0.10 and 0.45% NPP diets (Table 1), two temperatures (constant 25 and 35°C), and two feeding programs in the non-HS chamber (pair-fed to HS birds and ad libitum
TABLE 4. Performance and tibia ash of laying hens fed various nonphytate phosphorus (NPP) levels and exposed to different temperatures (experiment 3)1
Period
T (°C)
NPP level (%)
Feeding program
Adjustment2 (1 to 12 d)
25
Ad libitum
Experimental (13 to 27 d)
25
0.10 0.45 0.10 0.45 0.10 0.45 0.10 0.45
353
Pooled SD
Ad libitum Limit4 Ad libitum
Feed intake (g/hen per d) 93 108 91 118 69 79 69 75 17
ANOVA NPP Temperature Program NPP × temperature NPP × program
Hen-day egg production (%) 84 84 78 82 71 74 64 73 10
Tibia ash (%) — — 54 57 52 55 52 55 3
Probability 0.01 0.01 0.01 0.01 0.01
0.11 0.01 0.55 0.13 0.96
0.03 0.29 0.38 0.97 0.99
1 Adjustment period data and experimental period data for 35°C are means of eight groups of four Hy-Line W-98 laying hens from 58 to 61 wk. Experimental period data for 25°C (ad libitum and limit) are means of four groups of four Hy-Line W-98 laying hens. 2 Hens were allowed 12 d to adjust to the environmental chambers before the 14-d experimental period. Adjustment period data were not included in statistical analysis. 3 Constant 35°C. 4 Hens were pair-fed to maintain equal feed intake with hens exposed to the 35°C treatment and fed the same NPP level.
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Pooled SEM ANOVA NPP Temperature NPP × temperature
Hen-day egg production (%)
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PERSIA ET AL. TABLE 5. Egg specific gravity and selected blood parameters of laying hens fed various levels of nonphytate phosphorus (NPP) with acute exposure to different temperatures (experiment 3)1 Temperature (°C) 25
35
NPP level (%)
Feeding program
0.10 0.45 0.10 0.45 0.10 0.45
Ad libitum Limit3 Ad libitum
pH
3 4 4 4 8 8
7.40 7.38 7.44 7.40 7.46 7.44 0.05
43.5 45.5 41.7 44.8 40.4 40.1 5.8
0.16 0.01 0.32 0.84 0.72
HCO3− (mmol/L)
27.0 27.0 27.8 27.3 28.4 27.0 1.8 Probability
0.50 0.12 0.68 0.65 0.86
0.30 0.41 0.60 0.41 0.79
Specific gravity (g/cm3) 1.078 1.080 1.080 1.079 1.069 1.068 0.006 0.81 0.01 0.94 0.32 0.50
1 Data for blood parameters are means of blood samples taken from the laying hens 6 h after starting the 14d experimental period. Data for egg specific gravity are means for eggs collected on d 1 and 2 of the experimental period. 2 Partial pressure CO2. 3 Hens were pair-fed to maintain equal feed intake with hens exposed to the 35°C treatment and fed the same NPP diet.
feed intake). During the experimental period, temperature and RH values for the non-HS chamber ranged from 24 to 25°C and 45 to 88%, respectively. The temperature for the HS chamber during the heat period was 35°C with 25 to 65% RH. During the 14-d experimental period, four of the replicate groups of birds kept in the non-HS chamber were pair-fed the amount of feed the HS hens on the same NPP level had consumed the previous day, whereas the remaining four groups were allowed access to feed ad libitum. On d 1 and 14 of the experimental period, blood samples were obtained from the wing vein of one hen randomly selected each day from each pen and used to determine blood parameters. Blood samples were immediately analyzed for pH, partial pressure CO2 (pCO2), and HCO3− using the CG4+ cartridge and an i-STAT blood analyzer.2 Eggs were collected on d 1 and 2 and d 10 to 14 to determine specific gravity as described by Boling et al. (2000b).
Experiment 4 The fourth experiment was designed to test the effects of severe acute HS on 71-wk-old Hy-Line W-98 laying hens fed different levels of NPP. This experiment was set up with two dietary treatments, 0.10 and 0.45% NPP (Table 1) and 8 h of exposure to 38°C. The temperature and RH for the HS chamber during the heat exposure was 38°C with 48 to 58% RH. Hens were fed the experimental diets for 4 wk prior to initiation of acute HS, and the environmental room was preheated to 38°C prior to moving the hens into it. Eight replicate groups of four caged hens were assigned to each dietary treatment. Birds showing signs of SHD (unable to stand, lying on side, and generally unre-
2
i-STAT Corporation, Princeton, NJ.
sponsive) were recorded and immediately removed from the experiment and euthanized with CO2 gas.
Statistical Analysis Data from the first three experiments were subjected to ANOVA for completely randomized designs employing the appropriate factorial arrangement of treatments using SAS software (SAS Institute, 1985). Data for the adjustment period in each experiment were not included in the statistical model but were provided for reference. The SHD data from experiment 4 were subjected to ANOVA for completely randomized designs employing Fisher’s least significant difference test to determine significance (Steel and Torrie, 1980). Chick mortality, SHD, and tibia ash percentage data were arcsin transformed prior to statistical analysis for all experiments. In experiment 3, pH data were log transformed prior to statistical analysis. In experiments 1, 2, and 4, data are presented as means with a pooled SEM. Data collected from experiment 3 are reported as means with a SD due to unequal replication.
RESULTS AND DISCUSSION Table 2 shows feed intake hen-day egg production and tibia ash data for experiment 1. The feed intake values for the adjustment and experimental periods were similar, indicating only mild HS. In the experimental period, feeding the lower NPP level reduced feed intake and egg production (P ≤ 0.01). There were no significant differences in egg production due to HS, and there were no significant interactions between dietary NPP and temperature for egg production. Dietary NPP and temperature treatments had no effects on hen mortality (P > 0.05; data not shown). Tibia ash was not affected by NPP level or temperature. The lack of effect of the HS on egg production might have been due
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Pooled SD ANOVA NPP Temperature Program NPP × temperature NPP × program
n
pCO22 (mm of Hg)
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HEAT STRESS AND PHOSPHORUS IN LAYING HENS TABLE 6. Egg specific gravity and selected blood parameters of laying hens fed various levels of nonphytate phosphorus (NPP) with chronic exposure to different temperatures (experiment 3)1 Temperature (°C)
NPP level (%)
Feeding program
0.10 0.45 0.10 0.45 0.10 0.45
Ad libitum
25
35
Limit3 Ad libitum
pH
4 4 4 4 8 8
7.37 7.37 7.35 7.39 7.39 7.37 0.06
48.1 47.8 57.3 48.7 46.1 47.7 8.5
0.92 0.78 0.76 0.92 0.37
0.37 0.78 0.24 0.80 0.33
HCO3− (mmol/L)
29.3 27.5 31.0 29.5 27.4 27.0 2.4 Probability 0.17 0.20 0.09 0.46 0.91
Specific gravity (g/cm3) 1.072 1.073 1.072 1.077 1.071 1.071 0.003 0.13 0.22 0.32 0.84 0.72
1 Data for blood parameters are means of blood samples taken from the laying hens 14 d after starting the 14-d experimental period. Data for egg specific gravity are means for eggs collected on d 10 to 14 of the experimental period. 2 Partial pressure CO2. 3 Birds were pair-fed to maintain equal feed intake with hens exposed to the 35°C treatment and fed the same NPP diet.
to the hens being able to maintain feed intake during the 5 h of light in which there was no increased environmental temperature. In experiment 2, feed intake was lower during the experimental period than the adjustment period, suggesting a more severe HS than in experiment 1 (Table 3). As in experiment 1, decreased dietary NPP reduced feed intake and egg production (P ≤ 0.01). The HS had no effect on egg production and no interaction between dietary NPP and temperature was observed. There were no differences in mortality (P > 0.05; data not shown) among treatments. The finding that cyclic HS with maximum temperatures of 35°C in experiments 1 and 2 did not increase mortality in laying hens fed a low-P diet agrees with the previous study by Usayran et al. (2001). The lower NPP diet did produce a decrease in tibia ash (P ≤ 0.01). This decrease in tibia ash seen with a low-P diet agrees with Boling et al. (2000a) where hens fed 0.10 and 0.15% available P diets showed decreased tibia bone ash in comparison to hens fed 0.45% available P diets. The increased temperature did not affect tibia ash in the current study. In a previous report, de Andrade et al. (1977) showed no significant decreases in TABLE 7. Severe heat distress (SHD) of laying hens fed various levels of nonphytate phosphorus (NPP) and exposed to acute heat stress (38°C) for 8 h (experiment 4) NPP level (%) 0.10 0.45 Pooled SEM
SHD (%) 16a 0b 4
a,b Means without a common superscript letter are significantly different (P ≤ 0.05). 1 Means of eight groups of four 71-wk-old Hy-Line W-98 laying hens per treatment. Hens were fed experimental diets for 4 wk prior to heat stress. Mean egg production for the week prior to initiation of heat stress was 48 and 82% for the hens fed 0.10 and 0.45% NPP, respectively.
bone ash for laying hens subjected to 12 wk of cyclic HS. No interaction between NPP and temperature was observed for tibia ash values in the current study. Dietary NPP, temperature, and feeding program all affected feed intake (P ≤ 0.01) in experiment 3 (Table 4). Feed intake was markedly reduced by the constant HS treatment. There was a dietary NPP by temperature interaction (P < 0.01) for feed intake as the constant HS reduced feed intake more severely for the ad libitum 0.45% NPP treatment than for the ad libitum 0.10% NPP treatment. Consequently, the NPP by feeding program interaction (P ≤ 0.01) at 25°C resulted because limit or pair feeding caused a greater decrease in feed intake at 0.45% NPP than for hens fed 0.10% NPP. Egg production of hens fed 0.10% NPP was numerically, but not significantly, reduced (P = 0.11). Constant HS reduced egg production (P ≤ 0.01). No significant interaction was observed between dietary NPP and temperature. No differences in mortality (P > 0.05; data not shown) were noted even with a constant 35°C HS for the 14-d period. As mentioned earlier, these mortality data are consistent with reports from Usayran et al. (2001) that showed no interaction between dietary NPP level and environmental temperature when hens were exposed to a 35°C HS. Tibia ash was reduced (P ≤ 0.03) by the 0.10% NPP diet, but no other treatment main effects or interactions were significant in experiment 3. Tables 5 and 6 show selected blood parameters for hens fed various levels of NPP and exposed to HS for 6 h or 14 d, respectively, in experiment 3. During the acute response to HS (6 h), hens at 35°C had increased blood pH (P ≤ 0.01) compared to hens at 25°C. An increase in blood pH and a decrease in pCO2 during acute HS have been previously reported (Bottje and Harrison, 1985; Koelkebeck and Odom, 1994). Dietary NPP level had no significant effect on blood pH, pCO2 or HCO3−. Because P or P-containing compounds are important as buffers and in regulating
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Pooled SD ANOVA NPP Temperature Program NPP × temperature NPP × program
n
pCO22 (mm of Hg)
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ACKNOWLEDGMENTS This study was funded by a grant from the Illinois Council for Food and Agricultural Research (C-FAR). The authors also express their appreciation to J. L. Snow, A. C.
Martinez, K. A. Rafacz, A. M. Schafer, and K. L. Formas for their contributions during blood sampling and analysis.
REFERENCES Ait-Boulahsen, A., J. D. Garlich and F. W. Edens. 1993. Calcium deficiency and food deprivation improve the response of chickens to acute heat stress. J. Nutr. 123:98–105. Arima, Y., F. B. Mather, and M. M. Ahmad. 1976. Response of egg production and shell quality to increases in environmental temperature in two age groups of hens. Poult. Sci. 55:818–820. Belay, T., and R. G. Teeter. 1996. Effects of ambient temperature on broiler mineral balance partitioned into urinary and faecal loss. Br. Poult. Sci. 37:423–433. Belay, T., C. J. Wiernusz, and R. G. Teeter. 1992. Mineral balance and urinary and fecal mineral excretion profile of broilers housed in thermoneutral and heat-distressed environments. Poult. Sci. 71:1043–1047. Boling, S. D., M. W. Douglas, M. L. Johnson, X. Wang, C. M. Parsons, K. W. Koelkebeck, and R. A. Zimmerman. 2000a. The effects of dietary available phosphorus levels and phytase on performance of young and older laying hens. Poult. Sci. 79:224–230. Boling, S. D., M. W. Douglas, R. B. Shirley, C. M. Parsons, and K. W. Koelkebeck. 2000b. The effects of various dietary levels of phytase and available phosphorus on performance of laying hens. Poult. Sci. 79:535–538. Bonnet, S., P. A. Geraert, M. Lessire, B. Carre, and S. Guillaumin. 1997. Effect of high ambient temperature on feed digestibility in broilers. Poult. Sci. 76:857–863. Bottje, W. G., and P. C. Harrison. 1985. The effect of tap water, carbonated water, sodium bicarbonate, and calcium chloride on blood acid-base balance in cockerels subjected to heat stress. Poult. Sci. 64:107–113. de Andrade, A. N., J. C. Rogler, W. R. Featherston, and C. W. Alliston. 1977. Interrelationships between diet and elevated temperatures (cyclic and constant) on egg production and shell quality. Poult. Sci. 56:1178–1188. Garlich, J. D., F. W. Edens, and C. R. Parkhurst. 1978. The phosphorus requirement of laying hens with special reference to high environmental temperature. Proc. 16th World’s Poult. Congress IV-EF:598–609. Harrison, P. C., and H. V. Biellier. 1969. Physiological response of domestic fowl to abrupt changes of ambient air temperature. Poult. Sci. 48:1034–1045. Koelkebeck, K. W. and T. W. Odom. 1994. Laying hen responses to acute heat stress and carbon dioxide supplementation: I. Blood gas changes and plasma lactate accumulation. Comp. Biochem. Physiol. 107A:603–606. National Research Council. 1994. Nutrient Requirements of Poultry. 9th rev. ed. National Academy Press, Washington, DC. Persia, M. E., and C. M. Parsons. 2003. Interrelationship between environmental temperature and dietary nonphytate phosphorus in chicks. Poult. Sci. 82:1616–1623. SAS Institute. 1985. SAS User’s Guide: Statistics. Version 5 ed. SAS Institute Inc., Cary, NC. Siegel, H. S., L. N. Drury, and W. C. Patterson. 1974. Blood parameters of broilers grown in plastic coops and on litter at two temperatures. Poult. Sci. 53:1016–1024. Steel, R. G. D., and J. H. Torrie. 1980. Principles and Procedures of Statistics. A Biometrical Approach. 2nd ed. McGraw-Hill, New York, NY. Wolfenson, D., D. Sklan, Y. Graber, O. Kedar, I. Bengal, and S. Hurwitz. 1987. Absorption of protein, fatty acids and minerals in young turkeys under heat and cold stress. Br. Poult. Sci. 28:739–742. Usayran, N., M. T. Farran, H. H. O. Awadallah, I. R. Al-Hawi, R. J. Asmar, and V. M. Ashkarian. 2001. Effects of added dietary fat and phosphorus on the performance and egg quality of laying hens subjected to a constant high environmental temperature. Poult. Sci. 80:1695–1701.
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blood acid/base balance, we hypothesized that a dietary NPP deficiency might impair a hen’s ability to regulate blood pH, CO2, and HCO3 during acute HS. No such effect, however, was observed in experiment 3. Egg specific gravity was reduced (P ≤ 0.01) during the first 2 d of heat exposure (Table 5). This response has been demonstrated previously, with decreases in egg breaking strength and specific gravity with onset of HS (Harrison and Biellier, 1969; Arima et al., 1976; de Andrade et al., 1977). After the 14-d exposure to HS no significant differences among treatments were observed in any blood parameters, suggesting that the hens were able to adapt to the HS (Table 6). Egg specific gravity for the eggs collected from d 10 to 14 were not different among treatments, also suggesting adaptation (Table 6). Harrison and Biellier (1969) also reported an adaptive response to HS, where after an initial HS induced decrease, egg specific gravity gradually increased in hens exposed to chronic HS. The incidence of SHD in hens previously fed different levels of dietary NPP and exposed to a severe acute HS is shown in Table 7. Egg production for the week prior to HS initiation was 48 and 82% for the 0.10 and 0.45% NPP treatments, respectively. This difference indicated that the hens fed the 0.10% NPP diets were very deficient in P at the time of HS exposure. Hens fed the diet containing 0.10% NPP showed 16% incidence of SHD, which was higher (P ≤ 0.03) than that for hens fed 0.45% NPP. This increased SHD at 38°C for hens fed the 0.10% NPP diet is in accordance with earlier research by Garlich et al. (1978) that suggested laying hens fed a low-P diet are more adversely affected by temperatures of 38°C and above. In summary, neither cyclic nor constant chronic HS (35°C) affected mortality and did not interact with dietary NPP level. Although NPP level and HS often affected egg production, there were generally no significant interactions between the treatment variables. An acute exposure to a severe HS (38°C) did result in an increased incidence of SHD in hens fed a 0.10% NPP diet. This NPP level is much lower than the levels fed in practical situations. Consequently, it seems that a potential adverse interaction between feeding lower NPP diets and increased environmental temperature is of little concern for commercial laying hens. In contrast, another study from our laboratory (Persia and Parsons, 2003) showed that acute HS (35 to 38°C) caused high mortality and SHD in 22-d-old broiler chicks fed a low-P diet (0.2% NPP). The latter results suggest that broiler chicks are more susceptible to an interaction of dietary NPP and HS than are laying hens. Thus, an interrelationship between dietary P and HS does exist in poultry, and some caution should be exercised when feeding lower NPP diets during periods of elevated environmental temperature.
(Key words: egg production, heat stress, laying hen, nonphytate phosphorus, mortality) 2003 Poultry Science 82:1763–1768
INTRODUCTION Heat stress (HS) is a problem in large parts of the world, including many parts of United States. HS has been associated with decreases in feed intake, weight gain, egg production, nitrogen retention, protein digestibility, and total mineral retention (Siegel et al., 1974; Bonnet et al., 1997). In the latter area, several studies have reported that HS reduces P utilization. Phosphorus retention by birds exposed to HS is reduced with increased urinary P excretion (Belay et al., 1992; Belay and Teeter, 1996). Phosphorus absorption from the digestive tract is reduced in turkeys during HS (Wolfenson et al., 1987). HS has been shown to reduce plasma inorganic phosphate levels in broiler chicks and laying hens (Ait-Boulahsen et al., 1993; Usayran et al., 2001). Little research has focused on possible interactions between HS and low dietary P in laying hens. Hens fed only 0.22% available P showed increased mortality with increased temperature, especially when peak house temperatures reached 38°C and above (Garlich et al., 1978). In contrast, hens were fed 0.2, 0.3, 0.4, and 0.5% NPP diets and exposed to temperatures of 35°C without any affects on mortality (Usayran et al., 2001). Any adverse effects of HS on P
2003 Poultry Science Association, Inc. Received for publication January 13, 2003. Accepted for publication June 11, 2003. 1 To whom correspondence should be addressed: [email protected].
metabolism are becoming increasingly important as the poultry industry is being encouraged to reduce dietary P levels due to environmental concerns about excess P excreted in poultry manure. Indeed, several recent studies have suggested that laying hens have a NPP requirement that is lower than what is reported in the NRC (1994) and much lower than levels commonly fed by industry (Boling et al., 2000a,b). However, any negative interactions between HS and dietary P would need to be considered when feeding lower levels of NPP during times of high environmental temperature. The objectives of this study were to evaluate the interactions between chronic HS and dietary NPP on mortality, egg production, feed intake, tibia ash, egg specific gravity, and blood parameters in laying hens and to determine the effects of acute severe HS and dietary NPP level on severe heat distress (SHD) in laying hens.
MATERIALS AND METHODS General Procedures All animal procedures used in these experiments received approval from the University of Illinois Institutional Animal Care and Use Committee. Laying hens, either De-
Abbreviation Key: HS = heat stress; NPP = nonphytate phosphorus; pCO2 = partial pressure CO2; SHD = severe heat distress.
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ABSTRACT Four experiments were conducted to evaluate the effects of phosphorus nutrition on laying hens exposed to heat stress (HS). Hens were fed their respective diet for at least 3 wk prior to initiation of each experiment to allow the hens fed low-P diets to become P deficient. In most experiments, hens housed in non-HS conditions were pair-fed to the HS hens to maintain equal feed intake. In experiments 1 and 2, two levels of nonphytate P (NPP; deficient at 0.10 or 0.16% vs. control at 0.45%) and two temperatures (constant thermoneutral at 21°C or cyclic HS up to 35°C) were evaluated. Low NPP significantly reduced feed intake and hen-day egg production, but the cyclic heat treatment had no effect on hen performance.
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TABLE 1. Composition of corn-soybean meal diets varying in nonphytate phosphorus (NPP) content (experiments 1, 2, 3, and 4) Ingredient
0.10% NPP
0.16% NPP
0.45% NPP
(%) 65.30 23.95 9.80 — 0.40 0.20 0.15 0.10 0.05 0.05
65.18 23.95 9.60 0.32 0.40 0.20 0.15 0.10 0.05 0.05
64.51 23.95 8.40 1.89 0.40 0.20 0.15 0.10 0.05 0.05
16.7 3.80 0.10 2,861
16.7 3.80 0.16 2,857
16.6 3.80 0.45 2,834
Experiment 1
1 Provided per kilogram of diet: vitamin A (as retinyl A acetate), 1,514 µg; cholecalciferol (as activated animal sterol), 25 µg; vitamin E (as DLα-tocopheryl acetate), 11 mg; vitamin B12, 0.01 mg; riboflavin, 4.41 mg; D-pantothenic acid, 10 mg; niacin, 22 mg; menadione sodium bisulfite, 2.33 mg. 2 Provided per kilogram of diet: manganese, 75 mg from MnO; iron, 75 mg from FeSO4ⴢH2O; zinc, 75 mg from ZnO; copper, 5 mg from CuSO4ⴢ5H2O; iodine, 0.35 mg from ethylene diamine dihydroiodide; selenium, 0.2 mg from Na2SeO3.
kalb Sigma or Hy-Line W-98, were fed 0.10 or 0.45% NPP diets for at least 3 wk before initiation of each experiment. Feeding the 0.10% NPP diet was done to allow hens to deplete body stores of P and to begin to show P deficiency signs. In experiments 1 to 3, hens were randomly transferred to one of two side-by-side environmentally controlled chambers. Each of the first three experiments was set up as a 2 × 2 factorial with two levels of dietary NPP and two temperature treatments. Eight replicate groups of four hens were penned in cages in each chamber for both dietary NPP treatments in all three experiments. Thus, a total of 128 hens were used in each of the first three experiments. Hens were allowed 7 or 12 d to adjust to the environ-
The first experiment was designed to test the effects of cyclic HS on Dekalb Sigma laying hens from 56- to 59-wkof-age fed different levels of NPP. Treatments were set up in a 2 × 2 factorial arrangement with 0.16 and 0.45% NPP diets (Table 1) and two temperatures, a constant 21°C and a 12-h cyclic 35 or 26°C. During the 14-d experimental period, temperature and RH values for the non-HS chamber ranged from 20 to 22°C and 33 to 96%, respectively. The temperature for the HS chamber during the hot period was 35°C with 36 to 85% RH and 24 to 27°C with 40 to 97% RH during the cool period. The HS period was applied from 0800 to 2000 h, allowing the birds 5 h of light without HS. During the experimental period, the birds kept in the non-HS chamber were pair-fed the amount of feed that the HS hens on the same NPP level had consumed the previous day to eliminate any differences in feed and P intake, within NPP level, due to HS.
Experiment 2 The second experiment was designed to test the effects of a more severe cyclic HS on Dekalb laying hens from 64 to 67 wk of age that were fed different levels of NPP.
TABLE 2. Performance and tibia ash of laying hens fed various nonphytate phosphorus (NPP) levels and exposed to different temperatures (experiment 1)1 Temperature (°C)
NPP level (%)
Adjustment2 (1 to 7 d)
21
Experimental (8 to 21 d)
21
0.16 0.45 0.16 0.45 0.16 0.45
Period
Heat stress3 Pooled SEM ANOVA NPP Temperature NPP × temperature 1
Feed intake (g/hen per d) 87 87 83 89 85 91 2 0.01 0.27 0.79
Hen-day egg production (%) 70 92 64 83 70 80 4 Probability 0.01 0.74 0.28
Tibia ash (%) — — 44 45 44 46 1 0.23 0.89 0.81
Means of eight groups of four Dekalb Sigma laying hens, 56 to 59 wk. Hens were allowed 7 d to adjust to the environmental chambers (21°C) before the 14-d experimental period. The adjustment period data were not included in statistical analysis. The hens had been fed the diets varying in NPP for 3 wk before being moved into the environmental chambers. 3 Cyclic heat stress (12 h at 35°C followed by 12 h at 25°C). 2
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Ground corn Soybean meal Ground limestone Dicalcium phosphate Salt Vitamin mix1 Trace mineral mix2 DL-Met Choline chloride Larvadex/solka floc Calculated composition CP Ca NPP MEn (kcal/kg)
mental chambers before the 14-d experimental period was initiated. The environmental temperature was maintained at 21°C during the adjustment period. All hens were allowed access to feed and water ad libitum during adjustment periods and were maintained on a daily 17-h light period (0530 to 2230 h) for the duration of all experiments. Hens were caged in 46 cm × 46 cm × 46 cm pens with four hens per cage. Mortality, feed intake, and egg production were measured daily during the adjustment and experimental periods. At the end of experiments 1 to 3, eight hens from each treatment (one per replicate group) were randomly selected and euthanized with CO2 gas to determine tibia ash values as outlined by Boling et al. (2000a).
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HEAT STRESS AND PHOSPHORUS IN LAYING HENS TABLE 3. Performance and tibia ash of laying hens fed various nonphytate phosphorus (NPP) levels and exposed to different temperatures (experiment 2)1 Temperature (°C)
NPP level (%)
Adjustment2 (1 to 7 d)
21
Experimental (8 to 21 d)
21
0.10 0.45 0.10 0.45 0.10 0.45
Period
Heat stress3
Feed intake (g/hen per d) 74 98 61 88 61 87 2
75 82 44 77 44 75 4 Probability
0.01 0.77 0.88
0.01 0.88 0.79
Tibia ash (%) — — 50 55 51 54 1 0.01 0.88 0.40
1
Means of eight groups of four Dekalb Sigma laying hens, 64 to 67 wk. Hens were allowed 7 d to adjust to the environmental chambers (21°C) before the 14-d experimental period. The adjustment period data were not included in statistical analysis. The hens had been fed the diets varying in NPP for 2 wk before being moved into the environmental chambers. 3 Cyclic heat stress (16 h at 35°C followed by 8 h at 30°C). 2
Treatments were again arranged as a 2 × 2 factorial arrangement with 0.10 and 0.45% NPP diets (Table 1) and two temperatures, a constant 21°C and a cyclic 16 h at 35°C and 8 h at 30°C. During the experimental period, temperature and RH values for the non-HS chamber ranged from 20 to 22°C and 60 to 99%, respectively. The temperature for the HS chamber during the hot period was 35°C with 32 to 80% RH and 30 to 31°C with 38 to 90% RH during the cool period. The HS period was applied from 0600 to 2000 h, allowing the birds 1 h of light without HS. During the 14-d experimental period, the birds kept in the nonHS chamber were pair-fed the amount of feed that the HS
hens on the same NPP level had consumed the previous day.
Experiment 3 The third experiment was designed to test the effects of constant HS on Hy-Line W-98 laying hens from 58 to 61 wk of age that were fed different levels of NPP. Treatments were arranged as an unbalanced 2 × 2 × 2 factorial arrangement with 0.10 and 0.45% NPP diets (Table 1), two temperatures (constant 25 and 35°C), and two feeding programs in the non-HS chamber (pair-fed to HS birds and ad libitum
TABLE 4. Performance and tibia ash of laying hens fed various nonphytate phosphorus (NPP) levels and exposed to different temperatures (experiment 3)1
Period
T (°C)
NPP level (%)
Feeding program
Adjustment2 (1 to 12 d)
25
Ad libitum
Experimental (13 to 27 d)
25
0.10 0.45 0.10 0.45 0.10 0.45 0.10 0.45
353
Pooled SD
Ad libitum Limit4 Ad libitum
Feed intake (g/hen per d) 93 108 91 118 69 79 69 75 17
ANOVA NPP Temperature Program NPP × temperature NPP × program
Hen-day egg production (%) 84 84 78 82 71 74 64 73 10
Tibia ash (%) — — 54 57 52 55 52 55 3
Probability 0.01 0.01 0.01 0.01 0.01
0.11 0.01 0.55 0.13 0.96
0.03 0.29 0.38 0.97 0.99
1 Adjustment period data and experimental period data for 35°C are means of eight groups of four Hy-Line W-98 laying hens from 58 to 61 wk. Experimental period data for 25°C (ad libitum and limit) are means of four groups of four Hy-Line W-98 laying hens. 2 Hens were allowed 12 d to adjust to the environmental chambers before the 14-d experimental period. Adjustment period data were not included in statistical analysis. 3 Constant 35°C. 4 Hens were pair-fed to maintain equal feed intake with hens exposed to the 35°C treatment and fed the same NPP level.
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Pooled SEM ANOVA NPP Temperature NPP × temperature
Hen-day egg production (%)
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PERSIA ET AL. TABLE 5. Egg specific gravity and selected blood parameters of laying hens fed various levels of nonphytate phosphorus (NPP) with acute exposure to different temperatures (experiment 3)1 Temperature (°C) 25
35
NPP level (%)
Feeding program
0.10 0.45 0.10 0.45 0.10 0.45
Ad libitum Limit3 Ad libitum
pH
3 4 4 4 8 8
7.40 7.38 7.44 7.40 7.46 7.44 0.05
43.5 45.5 41.7 44.8 40.4 40.1 5.8
0.16 0.01 0.32 0.84 0.72
HCO3− (mmol/L)
27.0 27.0 27.8 27.3 28.4 27.0 1.8 Probability
0.50 0.12 0.68 0.65 0.86
0.30 0.41 0.60 0.41 0.79
Specific gravity (g/cm3) 1.078 1.080 1.080 1.079 1.069 1.068 0.006 0.81 0.01 0.94 0.32 0.50
1 Data for blood parameters are means of blood samples taken from the laying hens 6 h after starting the 14d experimental period. Data for egg specific gravity are means for eggs collected on d 1 and 2 of the experimental period. 2 Partial pressure CO2. 3 Hens were pair-fed to maintain equal feed intake with hens exposed to the 35°C treatment and fed the same NPP diet.
feed intake). During the experimental period, temperature and RH values for the non-HS chamber ranged from 24 to 25°C and 45 to 88%, respectively. The temperature for the HS chamber during the heat period was 35°C with 25 to 65% RH. During the 14-d experimental period, four of the replicate groups of birds kept in the non-HS chamber were pair-fed the amount of feed the HS hens on the same NPP level had consumed the previous day, whereas the remaining four groups were allowed access to feed ad libitum. On d 1 and 14 of the experimental period, blood samples were obtained from the wing vein of one hen randomly selected each day from each pen and used to determine blood parameters. Blood samples were immediately analyzed for pH, partial pressure CO2 (pCO2), and HCO3− using the CG4+ cartridge and an i-STAT blood analyzer.2 Eggs were collected on d 1 and 2 and d 10 to 14 to determine specific gravity as described by Boling et al. (2000b).
Experiment 4 The fourth experiment was designed to test the effects of severe acute HS on 71-wk-old Hy-Line W-98 laying hens fed different levels of NPP. This experiment was set up with two dietary treatments, 0.10 and 0.45% NPP (Table 1) and 8 h of exposure to 38°C. The temperature and RH for the HS chamber during the heat exposure was 38°C with 48 to 58% RH. Hens were fed the experimental diets for 4 wk prior to initiation of acute HS, and the environmental room was preheated to 38°C prior to moving the hens into it. Eight replicate groups of four caged hens were assigned to each dietary treatment. Birds showing signs of SHD (unable to stand, lying on side, and generally unre-
2
i-STAT Corporation, Princeton, NJ.
sponsive) were recorded and immediately removed from the experiment and euthanized with CO2 gas.
Statistical Analysis Data from the first three experiments were subjected to ANOVA for completely randomized designs employing the appropriate factorial arrangement of treatments using SAS software (SAS Institute, 1985). Data for the adjustment period in each experiment were not included in the statistical model but were provided for reference. The SHD data from experiment 4 were subjected to ANOVA for completely randomized designs employing Fisher’s least significant difference test to determine significance (Steel and Torrie, 1980). Chick mortality, SHD, and tibia ash percentage data were arcsin transformed prior to statistical analysis for all experiments. In experiment 3, pH data were log transformed prior to statistical analysis. In experiments 1, 2, and 4, data are presented as means with a pooled SEM. Data collected from experiment 3 are reported as means with a SD due to unequal replication.
RESULTS AND DISCUSSION Table 2 shows feed intake hen-day egg production and tibia ash data for experiment 1. The feed intake values for the adjustment and experimental periods were similar, indicating only mild HS. In the experimental period, feeding the lower NPP level reduced feed intake and egg production (P ≤ 0.01). There were no significant differences in egg production due to HS, and there were no significant interactions between dietary NPP and temperature for egg production. Dietary NPP and temperature treatments had no effects on hen mortality (P > 0.05; data not shown). Tibia ash was not affected by NPP level or temperature. The lack of effect of the HS on egg production might have been due
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Pooled SD ANOVA NPP Temperature Program NPP × temperature NPP × program
n
pCO22 (mm of Hg)
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HEAT STRESS AND PHOSPHORUS IN LAYING HENS TABLE 6. Egg specific gravity and selected blood parameters of laying hens fed various levels of nonphytate phosphorus (NPP) with chronic exposure to different temperatures (experiment 3)1 Temperature (°C)
NPP level (%)
Feeding program
0.10 0.45 0.10 0.45 0.10 0.45
Ad libitum
25
35
Limit3 Ad libitum
pH
4 4 4 4 8 8
7.37 7.37 7.35 7.39 7.39 7.37 0.06
48.1 47.8 57.3 48.7 46.1 47.7 8.5
0.92 0.78 0.76 0.92 0.37
0.37 0.78 0.24 0.80 0.33
HCO3− (mmol/L)
29.3 27.5 31.0 29.5 27.4 27.0 2.4 Probability 0.17 0.20 0.09 0.46 0.91
Specific gravity (g/cm3) 1.072 1.073 1.072 1.077 1.071 1.071 0.003 0.13 0.22 0.32 0.84 0.72
1 Data for blood parameters are means of blood samples taken from the laying hens 14 d after starting the 14-d experimental period. Data for egg specific gravity are means for eggs collected on d 10 to 14 of the experimental period. 2 Partial pressure CO2. 3 Birds were pair-fed to maintain equal feed intake with hens exposed to the 35°C treatment and fed the same NPP diet.
to the hens being able to maintain feed intake during the 5 h of light in which there was no increased environmental temperature. In experiment 2, feed intake was lower during the experimental period than the adjustment period, suggesting a more severe HS than in experiment 1 (Table 3). As in experiment 1, decreased dietary NPP reduced feed intake and egg production (P ≤ 0.01). The HS had no effect on egg production and no interaction between dietary NPP and temperature was observed. There were no differences in mortality (P > 0.05; data not shown) among treatments. The finding that cyclic HS with maximum temperatures of 35°C in experiments 1 and 2 did not increase mortality in laying hens fed a low-P diet agrees with the previous study by Usayran et al. (2001). The lower NPP diet did produce a decrease in tibia ash (P ≤ 0.01). This decrease in tibia ash seen with a low-P diet agrees with Boling et al. (2000a) where hens fed 0.10 and 0.15% available P diets showed decreased tibia bone ash in comparison to hens fed 0.45% available P diets. The increased temperature did not affect tibia ash in the current study. In a previous report, de Andrade et al. (1977) showed no significant decreases in TABLE 7. Severe heat distress (SHD) of laying hens fed various levels of nonphytate phosphorus (NPP) and exposed to acute heat stress (38°C) for 8 h (experiment 4) NPP level (%) 0.10 0.45 Pooled SEM
SHD (%) 16a 0b 4
a,b Means without a common superscript letter are significantly different (P ≤ 0.05). 1 Means of eight groups of four 71-wk-old Hy-Line W-98 laying hens per treatment. Hens were fed experimental diets for 4 wk prior to heat stress. Mean egg production for the week prior to initiation of heat stress was 48 and 82% for the hens fed 0.10 and 0.45% NPP, respectively.
bone ash for laying hens subjected to 12 wk of cyclic HS. No interaction between NPP and temperature was observed for tibia ash values in the current study. Dietary NPP, temperature, and feeding program all affected feed intake (P ≤ 0.01) in experiment 3 (Table 4). Feed intake was markedly reduced by the constant HS treatment. There was a dietary NPP by temperature interaction (P < 0.01) for feed intake as the constant HS reduced feed intake more severely for the ad libitum 0.45% NPP treatment than for the ad libitum 0.10% NPP treatment. Consequently, the NPP by feeding program interaction (P ≤ 0.01) at 25°C resulted because limit or pair feeding caused a greater decrease in feed intake at 0.45% NPP than for hens fed 0.10% NPP. Egg production of hens fed 0.10% NPP was numerically, but not significantly, reduced (P = 0.11). Constant HS reduced egg production (P ≤ 0.01). No significant interaction was observed between dietary NPP and temperature. No differences in mortality (P > 0.05; data not shown) were noted even with a constant 35°C HS for the 14-d period. As mentioned earlier, these mortality data are consistent with reports from Usayran et al. (2001) that showed no interaction between dietary NPP level and environmental temperature when hens were exposed to a 35°C HS. Tibia ash was reduced (P ≤ 0.03) by the 0.10% NPP diet, but no other treatment main effects or interactions were significant in experiment 3. Tables 5 and 6 show selected blood parameters for hens fed various levels of NPP and exposed to HS for 6 h or 14 d, respectively, in experiment 3. During the acute response to HS (6 h), hens at 35°C had increased blood pH (P ≤ 0.01) compared to hens at 25°C. An increase in blood pH and a decrease in pCO2 during acute HS have been previously reported (Bottje and Harrison, 1985; Koelkebeck and Odom, 1994). Dietary NPP level had no significant effect on blood pH, pCO2 or HCO3−. Because P or P-containing compounds are important as buffers and in regulating
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Pooled SD ANOVA NPP Temperature Program NPP × temperature NPP × program
n
pCO22 (mm of Hg)
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ACKNOWLEDGMENTS This study was funded by a grant from the Illinois Council for Food and Agricultural Research (C-FAR). The authors also express their appreciation to J. L. Snow, A. C.
Martinez, K. A. Rafacz, A. M. Schafer, and K. L. Formas for their contributions during blood sampling and analysis.
REFERENCES Ait-Boulahsen, A., J. D. Garlich and F. W. Edens. 1993. Calcium deficiency and food deprivation improve the response of chickens to acute heat stress. J. Nutr. 123:98–105. Arima, Y., F. B. Mather, and M. M. Ahmad. 1976. Response of egg production and shell quality to increases in environmental temperature in two age groups of hens. Poult. Sci. 55:818–820. Belay, T., and R. G. Teeter. 1996. Effects of ambient temperature on broiler mineral balance partitioned into urinary and faecal loss. Br. Poult. Sci. 37:423–433. Belay, T., C. J. Wiernusz, and R. G. Teeter. 1992. Mineral balance and urinary and fecal mineral excretion profile of broilers housed in thermoneutral and heat-distressed environments. Poult. Sci. 71:1043–1047. Boling, S. D., M. W. Douglas, M. L. Johnson, X. Wang, C. M. Parsons, K. W. Koelkebeck, and R. A. Zimmerman. 2000a. The effects of dietary available phosphorus levels and phytase on performance of young and older laying hens. Poult. Sci. 79:224–230. Boling, S. D., M. W. Douglas, R. B. Shirley, C. M. Parsons, and K. W. Koelkebeck. 2000b. The effects of various dietary levels of phytase and available phosphorus on performance of laying hens. Poult. Sci. 79:535–538. Bonnet, S., P. A. Geraert, M. Lessire, B. Carre, and S. Guillaumin. 1997. Effect of high ambient temperature on feed digestibility in broilers. Poult. Sci. 76:857–863. Bottje, W. G., and P. C. Harrison. 1985. The effect of tap water, carbonated water, sodium bicarbonate, and calcium chloride on blood acid-base balance in cockerels subjected to heat stress. Poult. Sci. 64:107–113. de Andrade, A. N., J. C. Rogler, W. R. Featherston, and C. W. Alliston. 1977. Interrelationships between diet and elevated temperatures (cyclic and constant) on egg production and shell quality. Poult. Sci. 56:1178–1188. Garlich, J. D., F. W. Edens, and C. R. Parkhurst. 1978. The phosphorus requirement of laying hens with special reference to high environmental temperature. Proc. 16th World’s Poult. Congress IV-EF:598–609. Harrison, P. C., and H. V. Biellier. 1969. Physiological response of domestic fowl to abrupt changes of ambient air temperature. Poult. Sci. 48:1034–1045. Koelkebeck, K. W. and T. W. Odom. 1994. Laying hen responses to acute heat stress and carbon dioxide supplementation: I. Blood gas changes and plasma lactate accumulation. Comp. Biochem. Physiol. 107A:603–606. National Research Council. 1994. Nutrient Requirements of Poultry. 9th rev. ed. National Academy Press, Washington, DC. Persia, M. E., and C. M. Parsons. 2003. Interrelationship between environmental temperature and dietary nonphytate phosphorus in chicks. Poult. Sci. 82:1616–1623. SAS Institute. 1985. SAS User’s Guide: Statistics. Version 5 ed. SAS Institute Inc., Cary, NC. Siegel, H. S., L. N. Drury, and W. C. Patterson. 1974. Blood parameters of broilers grown in plastic coops and on litter at two temperatures. Poult. Sci. 53:1016–1024. Steel, R. G. D., and J. H. Torrie. 1980. Principles and Procedures of Statistics. A Biometrical Approach. 2nd ed. McGraw-Hill, New York, NY. Wolfenson, D., D. Sklan, Y. Graber, O. Kedar, I. Bengal, and S. Hurwitz. 1987. Absorption of protein, fatty acids and minerals in young turkeys under heat and cold stress. Br. Poult. Sci. 28:739–742. Usayran, N., M. T. Farran, H. H. O. Awadallah, I. R. Al-Hawi, R. J. Asmar, and V. M. Ashkarian. 2001. Effects of added dietary fat and phosphorus on the performance and egg quality of laying hens subjected to a constant high environmental temperature. Poult. Sci. 80:1695–1701.
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blood acid/base balance, we hypothesized that a dietary NPP deficiency might impair a hen’s ability to regulate blood pH, CO2, and HCO3 during acute HS. No such effect, however, was observed in experiment 3. Egg specific gravity was reduced (P ≤ 0.01) during the first 2 d of heat exposure (Table 5). This response has been demonstrated previously, with decreases in egg breaking strength and specific gravity with onset of HS (Harrison and Biellier, 1969; Arima et al., 1976; de Andrade et al., 1977). After the 14-d exposure to HS no significant differences among treatments were observed in any blood parameters, suggesting that the hens were able to adapt to the HS (Table 6). Egg specific gravity for the eggs collected from d 10 to 14 were not different among treatments, also suggesting adaptation (Table 6). Harrison and Biellier (1969) also reported an adaptive response to HS, where after an initial HS induced decrease, egg specific gravity gradually increased in hens exposed to chronic HS. The incidence of SHD in hens previously fed different levels of dietary NPP and exposed to a severe acute HS is shown in Table 7. Egg production for the week prior to HS initiation was 48 and 82% for the 0.10 and 0.45% NPP treatments, respectively. This difference indicated that the hens fed the 0.10% NPP diets were very deficient in P at the time of HS exposure. Hens fed the diet containing 0.10% NPP showed 16% incidence of SHD, which was higher (P ≤ 0.03) than that for hens fed 0.45% NPP. This increased SHD at 38°C for hens fed the 0.10% NPP diet is in accordance with earlier research by Garlich et al. (1978) that suggested laying hens fed a low-P diet are more adversely affected by temperatures of 38°C and above. In summary, neither cyclic nor constant chronic HS (35°C) affected mortality and did not interact with dietary NPP level. Although NPP level and HS often affected egg production, there were generally no significant interactions between the treatment variables. An acute exposure to a severe HS (38°C) did result in an increased incidence of SHD in hens fed a 0.10% NPP diet. This NPP level is much lower than the levels fed in practical situations. Consequently, it seems that a potential adverse interaction between feeding lower NPP diets and increased environmental temperature is of little concern for commercial laying hens. In contrast, another study from our laboratory (Persia and Parsons, 2003) showed that acute HS (35 to 38°C) caused high mortality and SHD in 22-d-old broiler chicks fed a low-P diet (0.2% NPP). The latter results suggest that broiler chicks are more susceptible to an interaction of dietary NPP and HS than are laying hens. Thus, an interrelationship between dietary P and HS does exist in poultry, and some caution should be exercised when feeding lower NPP diets during periods of elevated environmental temperature.