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Real-time variations in body temperature of laying hens with increasing ambient temperature at different relative humidity levels
Real-time variations in body temperature of laying hens with increasing ambient temperature at different relative humidity levels Y. Chang,∗,2 X. J. Wang,∗,2 J. H. Feng,∗,1 M. H. Zhang,∗ H. J. Diao,† S. S. Zhang,∗ Q. Q. Peng,‡ Y. Zhou,∗ M. Li,† and X. Li‡ ∗
State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China; † School of Animal Science and Technology Northeast Agricultural University, Harbin 150030, China; and ‡ College of Agriculture, HeBei University of Engineering, Handan 056021, China that the upper critical temperature of the thermoneutral zone of hens may be a specific temperature between 23.89◦ C and 25.46◦ C. The IPTs of the laying hens were 24.11 and 25.20◦ C based on ST and CT at RH 35%, respectively, and 21.93 and 24.45◦ C at RH 85%. The RH significantly affected the IPT of ST (P < 0.001). The IPTs were higher at 35 and 50% RH than that at 85% RH (P < 0.05). The coefficients of variation for the IPTs between individual hens were 2.96 to 4.51, and coefficients of variation for the IPTs for the same bird measured on 3 d were 0.69 to 1.59, thereby indicating that this method for estimating the IPTs of hens is stable and repeatable, although more samples are needed. In conclusion, our results indicate that analyzing the real-time variation in body temperature with increasing AT is a reliable method for estimating the IPT to provide an important reference for regulating the temperature in poultry houses.
ABSTRACT In order to measure the real-time variations in body temperature with increasing ambient temperature (AT) at different relative humidity (RH) levels, 60 Jinghong laying hens (35-wk-old) were raised in 3 controlled climate chambers (10 cages with 2 birds per chamber). The RH was fixed at one of 3 levels comprising 35, 50, or 85%, and the AT was increased gradually by 1 degree per 0.5 h from 18 to 35◦ C in the 3 chambers. The core temperature (CT) and surface temperature (ST) of the hens, as well as the AT in the 3 chambers were recorded at 3 min intervals using mini temperature data loggers. The data were analyzed with a broken-line model to determine the inflection point temperature (IPT, the certain AT above which the body temperature of the hens started to change). The experiment was repeated 3 times on 3 d. The IPTs of the laying hens were 23.89 and 25.46◦ C based on ST and CT at 50% RH, respectively, which indicated
Key words: core temperature, increasing ambient temperature, laying hen, relative humidity, surface temperature 2018 Poultry Science 0:1–7 http://dx.doi.org/10.3382/ps/pey184
INTRODUCTION
an important reference when adjusting the temperature of poultry houses. However, the TNZ of poultry is related to their body weight (BW) or age (Meltzer, 1983), as well as depending on the temperature to which the poultry are adapted. Arieli et al. (1980) found that a 10◦ C change in the mean daily temperature during the experimental period caused a 3◦ C change in the upper critical temperature (UCT) and an 8.5◦ C change in the lower critical temperature. Therefore, it is necessary to develop a convenient and rapid method for estimating the TNZ of poultry for various strains, ages, and BWs at different experimental ATs. Pereira and N¨ aa¨s (2008) estimated the TNZ for broiler breeders using real-time recordings of the field temperature as well as the frequency of drinking and movement by electronic monitoring, and they demonstrated that it was an effective tool in decision support systems for controlling the poultry housing environment. In the present study, we quantified the real-time responses of the body temperature of hens to increases in AT
Heat stress has detrimental effects on poultry growth and health (Smith, 1993; Niu et al., 2009; Sohail et al., 2012; Mack et al., 2013). The temperature in poultry houses can be adjusted using cooling equipment (i.e., fans and cooling pads) in the hot summer season. In the 1970s, several studies estimated the thermoneutral zone (TNZ) for laying hens (Van Es et al., 1973; Arieli et al., 1980; Meltzer et al., 1982) and broilers (Van Kampen et al., 1979; Meltzer, 1983). The TNZ describes the specific range of ambient temperatures (ATs) within which the energy requirement of poultry is minimal and constant (Mount, 1974), and thus it is
C 2018 Poultry Science Association Inc. Received February 20, 2018. Accepted May 3, 2018. 1 Corresponding author: [email protected] 2 These authors contributed equally to this study.
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CHANG ET AL.
Figure 1. Ambient temperature and relative humidity measured in 3 controlled climate chambers in first day. Relative humidity levels were respectively set at 35% (a), 50% (b), and 85% (c).
and we estimated the UCT for laying hens using these real-time data.
MATERIALS AND METHODS Birds and Treatments Jinghong laying hens (32 wk old), obtained from a commercial company, were raised in an environmentally controlled room (20◦ C and 50%) for 2 wk to eliminate transportation stress. The laying hens were fed a standard commercial diet (2700 kcal of ME/kg and 16.50% crude protein) and kept under a lighting regime of 16 h light (from 6:30 am to 22:30 pm) and 8 h dark. Two birds were kept in each 1-deck cage (35 × 29 cm). At 34 wk of age, 60 laying hens (1920 ± 66 g BW) were transferred into 3 controlled climate chambers (10 cages with 2 birds per chamber) and adapted to the new environment for 5 d. The temperature (±0.5◦ C) and humidity (±7%) in the controlled climate chambers can be independently controlled by a computer according to our demand. During the adaptation period, the AT and relative humidity (RH) were fixed at 20◦ C and 50% in all 3 chambers. At 10:30 am on the sixth day, the RH levels in the 3 chambers were adjusted to an RH of either 35%, 50%, or 85% within 0.5 h, and kept at this level until 20:30 pm, before gradually adjusting the level to 50% in 4 h. In the 3 chambers, AT was gradually adjusted to 18◦ C in 0.5 h, and then increased by 1 degree per 0.5 h from 18◦ C at 11:00 am to 35◦ C at
20:00 pm, and 0.5 h later, the AT was gradually decreased to 20◦ C in 4 h. The AT and RH values measured in the 3 chambers are shown in Figure 1. The experiment was repeated 3 times on 3 d. The birds were reared in compliance with the Guidelines for Experimental Animals established by the Ministry of Science and Technology (Beijing, China).
Measurements Ten laying hens per chamber were monitored with mini temperature data loggers (DS1922L, Maxim Integrated Products, Sunnyvale, CA, USA) to obtain measurements of their surface temperature (ST) and core temperature (CT). On the first day of the adaptation period, the feathers were cut from the backs of the birds, and data loggers were attached to the surface of the skin by wrapping self-adhesive medical-grade bandaging tape around the bird’s body in order to acquire ST measurements. Other data loggers were placed inside the gizzard to record the CT according the method of Strawford et al. (2011). Briefly, the logger was placed behind the tongue so that the bird could swallow it with ease, then gently massaged the crop, push the logger down the alimentary tract into the gizzard. The logger was remained in the gizzard for the duration of the adaptation (5 d) and experiment (3 d), which had no significant effects on feeding and drinking behaviors of hens. The data loggers were set to record the temperature once every 3 min, and they were retrieved
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REAL-TIME VARIATIONS OF HENS’ TEMPERATURE
Figure 2. Variations in the surface temperature (ST) of one of the laying hens reared at a relative humidity (RH) of 35% with increasing ambient temperature (a), and the average inflection point temperature estimated based on the variations in ST for all birds reared at RH levels of 35% (b), 50% (c), and 85% (d).
after the birds were euthanized at the end of the trial. The AT and RH were also recorded in the chambers at 3-min intervals using mini temperature data loggers and humidity recorders (174H, Testo SE & Co. KGaA, Lenzkirch, Germany). All of the data loggers were calibrated using a stable-temperature water bath and a thermometer certified by the Haidian metrological verification station before the trial.
Statistical Analysis To calculate the inflection point temperature (IPT, the specific AT above which the variables started to change in the hens), the ST or CT of each bird and the corresponding AT (measured at the same time) in each chamber were subjected to broken-line analysis using nonlinear regression procedures with SPSS software. The parameter used in the broken-line model of each bird was the average based on 3 trials. The parameter used in the broken-line model at each RH level was the average based on all of the hens reared in the same chamber. The broken-line model was defined by Huynh et al. (2005) as follows: when AT ≥ IPT, Y = C + Z × (AT − IPT) ; when AT < IPT, Y = C,
where Y is the response variable (ST and CT), C is a constant, Z is a linear regression coefficient, AT is the chamber temperature (18◦ C to 35◦ C), and IPT is the inflection point temperature. In order to determine the effects of the RH, the parameters in the broken-line model based on ST and CT were analyzed by 1-way ANOVA using a general linear model procedure with SPSS software. All of the data were represented as the mean ± standard deviation and statistically significant differences were accepted at P < 0.05.
RESULTS Inflection Point Temperatures Estimated Based on the Variations in ST The trend in the ST of laying hens as AT increased was fitted to the broken-line model (Figure 2a). The average broken-line model for all birds reared under different RH levels is as follows. At 35% RH: when AT ≥ 24.11◦ C, ST 0.18 × (AT – 24.11); when AT < 24.11◦ C, (Table 1; Figure 2b). At 50% RH: when AT ≥ 23.89◦ C, ST 0.14 × (AT – 23.89); when AT < 23.89◦ C, (Table 1; Figure 2c).
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= 39.03 + ST = 39.03 = 39.26 + ST = 39.26
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CHANG ET AL. Table 1. Nonlinear regression analysis of different dependent variables with temperature using the brokenline model. Humidity, % Dependent variables ◦
ST/ C
CT/◦ C
Nonlinear regression model components
35
50 ∗
85
P value < 0.001 0.438 0.064
Number IPTc /◦ C Constant/◦ C Zc
n = 10 24.11 ± 1.07a 39.03 ± 0.70 0.18 ± 0.04
n=9 23.89 ± 1.96a 39.26 ± 0.18 0.14 ± 0.02
n = 10 21.93 ± 0.81b 38.98 ± 0.43 0.16 ± 0.03
Number IPT/◦ C Constant/◦ C Z
n = 9∗ 25.20 ± 0.14 41.31 ± 0.14 0.10 ± 0.03
n = 7∗ 25.46 ± 0.73 41.30 ± 0.33 0.10 ± 0.04
n = 9∗ 24.45 ± 0.97 41.39 ± 0.15 0.11 ± 0.02
0.098 0.613 0.487
Different letter superscripts indicate values within same row that are significantly different (P < 0.05). IPT = inflection point temperature; Z = linear regression coefficient. ∗ Some temperature data loggers were damaged. a,b c
At 85% RH: when AT ≥ 21.93◦ C, ST = 38.98 + 0.16 × (AT – 21.93); when AT < 21.93◦ C, ST = 38.98 (Table 1; Figure 2d). The average IPT of all birds reared at 35% RH was 24.11◦ C. The ST of laying hens remained constant at an average of 39.03◦ C when AT was lower than IPT. When AT was higher than IPT, ST increased in a linear manner by an average of 0.18◦ C per degree Celsius increase in AT. The average IPT of all birds was 23.89◦ C when reared at 50% RH and 21.93◦ C when reared at 85% RH. Relative humidity had no significant influence on the constant (P = 0.438) and linear regression coefficient (P = 0.064), but it significantly affected the IPT (P < 0.001). The IPT of laying hens reared at RH 85% was lower than that of those reared at RH 35% and 50% (Table 1).
Inflection Point Temperatures Estimated Based on the Variations in CT The trend in the CT of laying hens as AT increased was fitted to the broken-line model (Figure 3a). The average broken-line model for all birds reared at different RH levels is as follows. At 35% RH: when AT ≥ 25.20◦ C, CT = 41.31 + 0.10 × (AT – 25.20); when AT < 25.20◦ C, ST = 41.31 (Table 1; Figure 3b). At 50% RH: when AT ≥ 25.46◦ C, CT = 41.30 + 0.10 × (AT – 25.46); when AT < 25.46◦ C, ST = 41.30 (Table 1; Figure 3c). At 85% RH: when AT ≥ 24.45◦ C, CT = 41.39 + 0.11 × (AT – 24.45); when AT < 24.45◦ C, ST = 41.39 (Table 1; Figure 3d). The average IPT of all birds reared at 35% RH was 25.20◦ C. The ST of laying hens remained constant at an average of 41.31◦ C when AT was lower than IPT. When AT was higher than IPT, ST increased in a linear manner by an average of 0.10◦ C per degree Celsius increase in AT. The average IPT of all birds was 25.46◦ C when reared at 50% RH and 24.45◦ C when reared at 85% RH.
Relative humidity had no significant influence on the constant (P = 0.613), linear regression coefficient (P = 0.487), and IPT (P = 0.098, Table 1).
Variation in IPT Between Individual Hens or Repeated Trials The variations in the IPT values were high between individual hens. Based on ST, the coefficients of variation for the IPT values between all individual hens reared at RH levels of 35%, 50%, and 85% were 4.51, 4.34, and 3.83, respectively (Figure 4). Based on CT, the coefficients of variation for the IPT values between all individual hens reared at RH levels of 35%, 50%, and 85% were 4.15, 2.96, and 4.04, respectively (Figure 5). These results indicate that more samples are needed. However, the variation in the IPT value for the same hen measured on 3 d was low. Based on ST, the coefficients of variation for the IPT value for a single hen measured on 3 d were 0.79, 1.59, and 1.08 at RH levels of 35%, 50%, and 85%, respectively (Figure 4). Based on CT, the coefficients of variation for the IPT value for a single hen measured on 3 d were 0.69, 0.72, and 0.76 at RH levels of 35%, 50%, and 85%, respectively (Figure 5). These results indicate that this method for estimating the IPT in hens is stable and repeatable.
DISCUSSION Exposure to elevated AT increases the blood flow to the skin due to vasodilatation and heat is transported from the viscera to the periphery (Wolfenson et al., 1981; Wolfenson, 1986), thereby increasing the ST in poultry (Yahav et al., 1998, 2008; De Souza et al., 2013). Malheiros et al. (2000) found that the ST of broilers increased in a linear manner as AT increased from 20◦ C to 35◦ C. Nascimento et al. (2011) also found that the ST of broilers increased in a linear manner as AT increased from 18◦ C to 32◦ C. The body CT is a parameter that best reflects a bird’s thermal status. Many
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REAL-TIME VARIATIONS OF HENS’ TEMPERATURE
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Figure 3. Variations in the core temperature (CT) of one of the laying hens reared at a relative humidity (RH) of 35% as the ambient temperature increased (a), and the average inflection point temperature estimated based on the variations in CT for all birds reared at RH levels of 35% (b), 50% (c), and 85% (d).
Figure 4. Inflection point temperatures (IPTs) for each of all the laying hens reared at relative humidity levels of 35% (a), 50% (b), and 85% (c) on 3 d, where the IPTs were estimated based on the surface temperatures of the birds. The numbers listed in X axis are the experimental number of birds. ∗ Coefficient of variation for the IPT value in the same bird measured on 3 d (mean value of all laying hens reared at different relative humidity levels). # Coefficient of variation for the IPT values in all individual hens reared at different relative humidity levels (mean value on 3 d). Downloaded from https://academic.oup.com/ps/advance-article-abstract/doi/10.3382/ps/pey184/4996662 by university of winnipeg user on 16 May 2018
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CHANG ET AL.
Figure 5. The inflection point temperature (IPT) of each laying hens reared at 35% (a), 50% (b), and 85% (c) relative humidity, the IPTs were estimated basing on core temperature of birds. The numbers listed in X axis are the experimental number of birds. ∗ Coefficient of variation for the IPT value in the same bird measured on 3 d (mean value of all laying hens reared at different relative humidity levels). # Coefficient of variation for the IPT value in all individual hens reared at different relative humidity levels (mean value on 3 d).
studies have shown that the CT of poultry reared at 32–37◦ C was significantly higher than that of those reared at 20–22◦ C, but the CT of poultry reared at 25– 27◦ C was not significantly different compared with that of those reared at 20–22◦ C (Richards, 1971; Donkoh, 1989; Tzschentke et al., 1996; Yahav et al., 1997; Yahav 1999). These previous studies generally tested less than 4 temperature treatments, so the IPT was not estimated exactly. In present the study, we tested 18 temperature treatments from 18 to 35◦ C and measured CT, ST, and AT over 3-min intervals during 9 h of experiments using mini temperature data loggers. The scatter plots showed clearly that the variations in ST and CT as AT increased could be fitted by broken-line model analysis. The coefficients of variation for the IPTs in the same bird estimated on 3 d were 0.69 to 1.59, which indicates that our method for estimating the IPT in hens is stable and repeatable. TNZ was defined by the Thermal Commission of International Union of Physiological Sciences (1987) as the range of ATs within which body temperature regulation is achieved only by the control of sensible heat loss, i.e., without regulatory changes in metabolic heat production or evaporative heat loss. Regulation of sensible heat loss refers to heat loss by conduction, convection, or radiation. Thus, thermoregulation in the TNZ only occurs via vasomotor control (Savage and Brengelmann, 1996; Brengelmann and Savage 1997; Mekjavic and Eiken, 2006). Therefore, the TNZ can be divided into 2 distinct parts based on vasomotor control in poultry: the comfort zone, which covers the range
from the LCT of the TNZ to the point where poultry activate their vasomotor control; and the zone from the upper border of the comfort zone to the UCT of the TNZ. In the present study, the IPT of ST for laying hens was 23.89◦ C at an RH of 50%, above which the ST of hens started increasing, thereby indicating that the upper border of the thermal comfort zone for hens may be 23.89◦ C. The IPT of CT for laying hens was 25.46◦ C at an RH of 50%, above which the CT of laying hens started increasing, thereby indicating that the hens suffered from heat stress. Thus, we suggest that the UCT of the TNZ in hens may be a specific temperature between 23.89◦ C and 25.46◦ C, above which the respiratory frequency, feed intake, or heat production may start to change in hens. The IPT of CT and ST cannot be used to accurately the estimate UCT of TNZ of hens, but it is still an important reference for regulating the temperature in poultry houses. The main pathway for heat dissipation by birds in a hot environment is respiratory evaporation (Hillman et al., 1985). The amount of evaporative heat loss depends on the humidity in the air and it is suppressed as the humidity rises (Chwalibog and Eggum, 1989; Nichelmann et al., 1991). Lin et al. (2005) found that the CT and ST were higher in broilers at an RH of 85% than that those at RH levels of 35% and 50% in a hot environment (30 or 35◦ C). In the present study, the IPTs of ST were higher at 35% and 50% RH than those at 85% RH, which indicates that even in a mild hot environment (21 to 23◦ C), a high level of humidity in the air may still suppress evaporative heat loss
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REAL-TIME VARIATIONS OF HENS’ TEMPERATURE
via the normal respiratory route and skin by birds. As a compensatory behavior, birds raised their ST at a relatively lower AT to improve the sensible heat loss dissipation. In conclusion, our results indicate that analyzing the real-time variations in body temperature as AT increases is a reliable method for estimating the IPT in laying hens to provide an important reference for regulating the temperature in poultry houses.
ACKNOWLEDGMENTS This study was supported by the National Key Research and Development Program of China (2016YFD0500509). This research was also supported by the Science and Technology Innovation Project of the Chinese Academy of Agricultural Sciences (ASTIP-IAS07).
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Meltzer, A. 1983. Thermoneutral zone and resting metabolic rate of broilers. Br. Poult. Sci. 24:471–476. Meltzer, A., G. Goodman, and J. Fistul. 1982. Thermoneutral zone and resting metabolic rate of growing White Leghorn type chicks. Br. Poult. Sci. 23:383–391. Mount, L. E. 1974. The concept of thermal neutrality. In Heat Loss from Animals and Man. Assessment and Control. J. L. Mount, and L. E. Mount eds. London, England, Butterworths, 425–439. Nascimento, G. R., I. A. N¨ aa¨s, D. F. Pereira, M. S. Baracho, and R. Garcia. 2011. Assessment of broiler surface temperature variation when exposed to different air temperatures. Rev. Bras. Cienc. Avic. 13:259–263. Nichelmann, M., B. Tzschentke, and A. Burmeister. 1991. Evaporative warmeabgabe des geflugels bei hoher relativer luftfeuchtigkeit. Arch. Geflu¨ gelkd. 55:110–115. Niu, Z. Y., F. Z. Liu, Q. L. Yan, and W. C. Li. 2009. Effects of different levels of vitamin E on growth performance and immune responses of broilers under heat stress. Poult. Sci. 88:2101–2107. Pereira, D. F., and I. A. N¨ aa¨s. 2008. Estimating the thermoneutral zone for broiler breeders using behavioral analysis. Comput. Electron. Agric. 62:2–7. Richards, S. 1971. The significance of changes in the temperature of the skin and body core of the chicken in the regulation of heat loss. J. Physiol. 216:1–10. Savage, M. V., and G. L. Brengelmann. 1996. Control of skin blood flow in the neutral zone of human body temperature regulation. J. Appl. Physiol. 80:1249–1257. Smith, M. O. 1993. Parts yield of broilers reared under cycling high temperatures. Poult. Sci. 72:1146–1150. Sohail, M. U., M. E. Hume, J. A. Byrd, D. J. Nisbet, A. Ljaz, A. Sohail, M. Z. Shabbir, and H. Rehman. 2012. Effect of supplementation of prebiotic mannan-oligosaccharides and probiotic mixture on growth performance of broilers subjected to chronic heat stress. Poult. Sci. 91:2235–2240. Strawford, M. L., J. M. Watts, T. G. Crowe, H. L. Classen, and P. J. Shand. 2011. The effect of simulated cold weather transport on core body temperature and behavior of broilers. Poult. Sci. 90:2415–2424. Tzschentke, B., M. Nichelmann, and T. Postel. 1996. Effects of ambient temperature, age and wind speed on the thermal balance of layer-strain fowls. Br. Poult. Sci. 7:501–520. Van Es, A. J. H., D. Van Aggelen, H. J. Nijkamp, J. E. Vogt, and C. W. Scheele. 1973. Thermoneutral zone of laying hens kept in batteries. Z. Tierphysiol. Tierernaehr. Futtermittelkd. 32:121– 129. Van Kampen, M., B. W. Mitchell, and H. S. Siegel. 1979. Thermoneutral zone of chickens as determined by measuring heat production, respiration rate, and electromyographic and electroencephalographic activity in light and dark environments and changing ambient temperatures. J. Agric. Sci. 93:219–226. Wolfenson, D. 1986. The effect of acclimatization on blood flow and its distribution in normothermic and hyperthermic domestic fowl. Comp. Biochem. Physiol. A 85:739–742. Wolfenson, D., Y. F. Frei, N. Snapir, and A. Berman. 1981. Heat stress effects on capillary blood flow and its redistribution in the laying hen. Pflugers Arch. 390:86–93. Yahav, S. 1999. The effect of constant and diurnal cyclic temperatures on performance and blood system of young turkeys. J. Therm. Biol. 24:71–78. Yahav, S., D. Luger, A. Cahaner, M. Dotan, M. Rusal, and S. Hurwitz. 1998. Thermoregulation in naked neck chickens subjected to different ambient temperatures. Br. Poult. Sci. 39:133–138. Yahav, S., M. Rusal, and D. Shinder. 2008. The effect of ventilation on performance, body, and surface temperature of young turkeys. Poult. Sci. 87:133–137. Yahav, S., A. Straschnow, I. Plavnik, and S. Hurwitz. 1997. Blood system response of chickens to changes in environmental temperature. Poult. Sci. 76:627–633.
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State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China; † School of Animal Science and Technology Northeast Agricultural University, Harbin 150030, China; and ‡ College of Agriculture, HeBei University of Engineering, Handan 056021, China that the upper critical temperature of the thermoneutral zone of hens may be a specific temperature between 23.89◦ C and 25.46◦ C. The IPTs of the laying hens were 24.11 and 25.20◦ C based on ST and CT at RH 35%, respectively, and 21.93 and 24.45◦ C at RH 85%. The RH significantly affected the IPT of ST (P < 0.001). The IPTs were higher at 35 and 50% RH than that at 85% RH (P < 0.05). The coefficients of variation for the IPTs between individual hens were 2.96 to 4.51, and coefficients of variation for the IPTs for the same bird measured on 3 d were 0.69 to 1.59, thereby indicating that this method for estimating the IPTs of hens is stable and repeatable, although more samples are needed. In conclusion, our results indicate that analyzing the real-time variation in body temperature with increasing AT is a reliable method for estimating the IPT to provide an important reference for regulating the temperature in poultry houses.
ABSTRACT In order to measure the real-time variations in body temperature with increasing ambient temperature (AT) at different relative humidity (RH) levels, 60 Jinghong laying hens (35-wk-old) were raised in 3 controlled climate chambers (10 cages with 2 birds per chamber). The RH was fixed at one of 3 levels comprising 35, 50, or 85%, and the AT was increased gradually by 1 degree per 0.5 h from 18 to 35◦ C in the 3 chambers. The core temperature (CT) and surface temperature (ST) of the hens, as well as the AT in the 3 chambers were recorded at 3 min intervals using mini temperature data loggers. The data were analyzed with a broken-line model to determine the inflection point temperature (IPT, the certain AT above which the body temperature of the hens started to change). The experiment was repeated 3 times on 3 d. The IPTs of the laying hens were 23.89 and 25.46◦ C based on ST and CT at 50% RH, respectively, which indicated
Key words: core temperature, increasing ambient temperature, laying hen, relative humidity, surface temperature 2018 Poultry Science 0:1–7 http://dx.doi.org/10.3382/ps/pey184
INTRODUCTION
an important reference when adjusting the temperature of poultry houses. However, the TNZ of poultry is related to their body weight (BW) or age (Meltzer, 1983), as well as depending on the temperature to which the poultry are adapted. Arieli et al. (1980) found that a 10◦ C change in the mean daily temperature during the experimental period caused a 3◦ C change in the upper critical temperature (UCT) and an 8.5◦ C change in the lower critical temperature. Therefore, it is necessary to develop a convenient and rapid method for estimating the TNZ of poultry for various strains, ages, and BWs at different experimental ATs. Pereira and N¨ aa¨s (2008) estimated the TNZ for broiler breeders using real-time recordings of the field temperature as well as the frequency of drinking and movement by electronic monitoring, and they demonstrated that it was an effective tool in decision support systems for controlling the poultry housing environment. In the present study, we quantified the real-time responses of the body temperature of hens to increases in AT
Heat stress has detrimental effects on poultry growth and health (Smith, 1993; Niu et al., 2009; Sohail et al., 2012; Mack et al., 2013). The temperature in poultry houses can be adjusted using cooling equipment (i.e., fans and cooling pads) in the hot summer season. In the 1970s, several studies estimated the thermoneutral zone (TNZ) for laying hens (Van Es et al., 1973; Arieli et al., 1980; Meltzer et al., 1982) and broilers (Van Kampen et al., 1979; Meltzer, 1983). The TNZ describes the specific range of ambient temperatures (ATs) within which the energy requirement of poultry is minimal and constant (Mount, 1974), and thus it is
C 2018 Poultry Science Association Inc. Received February 20, 2018. Accepted May 3, 2018. 1 Corresponding author: [email protected] 2 These authors contributed equally to this study.
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Figure 1. Ambient temperature and relative humidity measured in 3 controlled climate chambers in first day. Relative humidity levels were respectively set at 35% (a), 50% (b), and 85% (c).
and we estimated the UCT for laying hens using these real-time data.
MATERIALS AND METHODS Birds and Treatments Jinghong laying hens (32 wk old), obtained from a commercial company, were raised in an environmentally controlled room (20◦ C and 50%) for 2 wk to eliminate transportation stress. The laying hens were fed a standard commercial diet (2700 kcal of ME/kg and 16.50% crude protein) and kept under a lighting regime of 16 h light (from 6:30 am to 22:30 pm) and 8 h dark. Two birds were kept in each 1-deck cage (35 × 29 cm). At 34 wk of age, 60 laying hens (1920 ± 66 g BW) were transferred into 3 controlled climate chambers (10 cages with 2 birds per chamber) and adapted to the new environment for 5 d. The temperature (±0.5◦ C) and humidity (±7%) in the controlled climate chambers can be independently controlled by a computer according to our demand. During the adaptation period, the AT and relative humidity (RH) were fixed at 20◦ C and 50% in all 3 chambers. At 10:30 am on the sixth day, the RH levels in the 3 chambers were adjusted to an RH of either 35%, 50%, or 85% within 0.5 h, and kept at this level until 20:30 pm, before gradually adjusting the level to 50% in 4 h. In the 3 chambers, AT was gradually adjusted to 18◦ C in 0.5 h, and then increased by 1 degree per 0.5 h from 18◦ C at 11:00 am to 35◦ C at
20:00 pm, and 0.5 h later, the AT was gradually decreased to 20◦ C in 4 h. The AT and RH values measured in the 3 chambers are shown in Figure 1. The experiment was repeated 3 times on 3 d. The birds were reared in compliance with the Guidelines for Experimental Animals established by the Ministry of Science and Technology (Beijing, China).
Measurements Ten laying hens per chamber were monitored with mini temperature data loggers (DS1922L, Maxim Integrated Products, Sunnyvale, CA, USA) to obtain measurements of their surface temperature (ST) and core temperature (CT). On the first day of the adaptation period, the feathers were cut from the backs of the birds, and data loggers were attached to the surface of the skin by wrapping self-adhesive medical-grade bandaging tape around the bird’s body in order to acquire ST measurements. Other data loggers were placed inside the gizzard to record the CT according the method of Strawford et al. (2011). Briefly, the logger was placed behind the tongue so that the bird could swallow it with ease, then gently massaged the crop, push the logger down the alimentary tract into the gizzard. The logger was remained in the gizzard for the duration of the adaptation (5 d) and experiment (3 d), which had no significant effects on feeding and drinking behaviors of hens. The data loggers were set to record the temperature once every 3 min, and they were retrieved
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REAL-TIME VARIATIONS OF HENS’ TEMPERATURE
Figure 2. Variations in the surface temperature (ST) of one of the laying hens reared at a relative humidity (RH) of 35% with increasing ambient temperature (a), and the average inflection point temperature estimated based on the variations in ST for all birds reared at RH levels of 35% (b), 50% (c), and 85% (d).
after the birds were euthanized at the end of the trial. The AT and RH were also recorded in the chambers at 3-min intervals using mini temperature data loggers and humidity recorders (174H, Testo SE & Co. KGaA, Lenzkirch, Germany). All of the data loggers were calibrated using a stable-temperature water bath and a thermometer certified by the Haidian metrological verification station before the trial.
Statistical Analysis To calculate the inflection point temperature (IPT, the specific AT above which the variables started to change in the hens), the ST or CT of each bird and the corresponding AT (measured at the same time) in each chamber were subjected to broken-line analysis using nonlinear regression procedures with SPSS software. The parameter used in the broken-line model of each bird was the average based on 3 trials. The parameter used in the broken-line model at each RH level was the average based on all of the hens reared in the same chamber. The broken-line model was defined by Huynh et al. (2005) as follows: when AT ≥ IPT, Y = C + Z × (AT − IPT) ; when AT < IPT, Y = C,
where Y is the response variable (ST and CT), C is a constant, Z is a linear regression coefficient, AT is the chamber temperature (18◦ C to 35◦ C), and IPT is the inflection point temperature. In order to determine the effects of the RH, the parameters in the broken-line model based on ST and CT were analyzed by 1-way ANOVA using a general linear model procedure with SPSS software. All of the data were represented as the mean ± standard deviation and statistically significant differences were accepted at P < 0.05.
RESULTS Inflection Point Temperatures Estimated Based on the Variations in ST The trend in the ST of laying hens as AT increased was fitted to the broken-line model (Figure 2a). The average broken-line model for all birds reared under different RH levels is as follows. At 35% RH: when AT ≥ 24.11◦ C, ST 0.18 × (AT – 24.11); when AT < 24.11◦ C, (Table 1; Figure 2b). At 50% RH: when AT ≥ 23.89◦ C, ST 0.14 × (AT – 23.89); when AT < 23.89◦ C, (Table 1; Figure 2c).
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= 39.03 + ST = 39.03 = 39.26 + ST = 39.26
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CHANG ET AL. Table 1. Nonlinear regression analysis of different dependent variables with temperature using the brokenline model. Humidity, % Dependent variables ◦
ST/ C
CT/◦ C
Nonlinear regression model components
35
50 ∗
85
P value < 0.001 0.438 0.064
Number IPTc /◦ C Constant/◦ C Zc
n = 10 24.11 ± 1.07a 39.03 ± 0.70 0.18 ± 0.04
n=9 23.89 ± 1.96a 39.26 ± 0.18 0.14 ± 0.02
n = 10 21.93 ± 0.81b 38.98 ± 0.43 0.16 ± 0.03
Number IPT/◦ C Constant/◦ C Z
n = 9∗ 25.20 ± 0.14 41.31 ± 0.14 0.10 ± 0.03
n = 7∗ 25.46 ± 0.73 41.30 ± 0.33 0.10 ± 0.04
n = 9∗ 24.45 ± 0.97 41.39 ± 0.15 0.11 ± 0.02
0.098 0.613 0.487
Different letter superscripts indicate values within same row that are significantly different (P < 0.05). IPT = inflection point temperature; Z = linear regression coefficient. ∗ Some temperature data loggers were damaged. a,b c
At 85% RH: when AT ≥ 21.93◦ C, ST = 38.98 + 0.16 × (AT – 21.93); when AT < 21.93◦ C, ST = 38.98 (Table 1; Figure 2d). The average IPT of all birds reared at 35% RH was 24.11◦ C. The ST of laying hens remained constant at an average of 39.03◦ C when AT was lower than IPT. When AT was higher than IPT, ST increased in a linear manner by an average of 0.18◦ C per degree Celsius increase in AT. The average IPT of all birds was 23.89◦ C when reared at 50% RH and 21.93◦ C when reared at 85% RH. Relative humidity had no significant influence on the constant (P = 0.438) and linear regression coefficient (P = 0.064), but it significantly affected the IPT (P < 0.001). The IPT of laying hens reared at RH 85% was lower than that of those reared at RH 35% and 50% (Table 1).
Inflection Point Temperatures Estimated Based on the Variations in CT The trend in the CT of laying hens as AT increased was fitted to the broken-line model (Figure 3a). The average broken-line model for all birds reared at different RH levels is as follows. At 35% RH: when AT ≥ 25.20◦ C, CT = 41.31 + 0.10 × (AT – 25.20); when AT < 25.20◦ C, ST = 41.31 (Table 1; Figure 3b). At 50% RH: when AT ≥ 25.46◦ C, CT = 41.30 + 0.10 × (AT – 25.46); when AT < 25.46◦ C, ST = 41.30 (Table 1; Figure 3c). At 85% RH: when AT ≥ 24.45◦ C, CT = 41.39 + 0.11 × (AT – 24.45); when AT < 24.45◦ C, ST = 41.39 (Table 1; Figure 3d). The average IPT of all birds reared at 35% RH was 25.20◦ C. The ST of laying hens remained constant at an average of 41.31◦ C when AT was lower than IPT. When AT was higher than IPT, ST increased in a linear manner by an average of 0.10◦ C per degree Celsius increase in AT. The average IPT of all birds was 25.46◦ C when reared at 50% RH and 24.45◦ C when reared at 85% RH.
Relative humidity had no significant influence on the constant (P = 0.613), linear regression coefficient (P = 0.487), and IPT (P = 0.098, Table 1).
Variation in IPT Between Individual Hens or Repeated Trials The variations in the IPT values were high between individual hens. Based on ST, the coefficients of variation for the IPT values between all individual hens reared at RH levels of 35%, 50%, and 85% were 4.51, 4.34, and 3.83, respectively (Figure 4). Based on CT, the coefficients of variation for the IPT values between all individual hens reared at RH levels of 35%, 50%, and 85% were 4.15, 2.96, and 4.04, respectively (Figure 5). These results indicate that more samples are needed. However, the variation in the IPT value for the same hen measured on 3 d was low. Based on ST, the coefficients of variation for the IPT value for a single hen measured on 3 d were 0.79, 1.59, and 1.08 at RH levels of 35%, 50%, and 85%, respectively (Figure 4). Based on CT, the coefficients of variation for the IPT value for a single hen measured on 3 d were 0.69, 0.72, and 0.76 at RH levels of 35%, 50%, and 85%, respectively (Figure 5). These results indicate that this method for estimating the IPT in hens is stable and repeatable.
DISCUSSION Exposure to elevated AT increases the blood flow to the skin due to vasodilatation and heat is transported from the viscera to the periphery (Wolfenson et al., 1981; Wolfenson, 1986), thereby increasing the ST in poultry (Yahav et al., 1998, 2008; De Souza et al., 2013). Malheiros et al. (2000) found that the ST of broilers increased in a linear manner as AT increased from 20◦ C to 35◦ C. Nascimento et al. (2011) also found that the ST of broilers increased in a linear manner as AT increased from 18◦ C to 32◦ C. The body CT is a parameter that best reflects a bird’s thermal status. Many
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REAL-TIME VARIATIONS OF HENS’ TEMPERATURE
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Figure 3. Variations in the core temperature (CT) of one of the laying hens reared at a relative humidity (RH) of 35% as the ambient temperature increased (a), and the average inflection point temperature estimated based on the variations in CT for all birds reared at RH levels of 35% (b), 50% (c), and 85% (d).
Figure 4. Inflection point temperatures (IPTs) for each of all the laying hens reared at relative humidity levels of 35% (a), 50% (b), and 85% (c) on 3 d, where the IPTs were estimated based on the surface temperatures of the birds. The numbers listed in X axis are the experimental number of birds. ∗ Coefficient of variation for the IPT value in the same bird measured on 3 d (mean value of all laying hens reared at different relative humidity levels). # Coefficient of variation for the IPT values in all individual hens reared at different relative humidity levels (mean value on 3 d). Downloaded from https://academic.oup.com/ps/advance-article-abstract/doi/10.3382/ps/pey184/4996662 by university of winnipeg user on 16 May 2018
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Figure 5. The inflection point temperature (IPT) of each laying hens reared at 35% (a), 50% (b), and 85% (c) relative humidity, the IPTs were estimated basing on core temperature of birds. The numbers listed in X axis are the experimental number of birds. ∗ Coefficient of variation for the IPT value in the same bird measured on 3 d (mean value of all laying hens reared at different relative humidity levels). # Coefficient of variation for the IPT value in all individual hens reared at different relative humidity levels (mean value on 3 d).
studies have shown that the CT of poultry reared at 32–37◦ C was significantly higher than that of those reared at 20–22◦ C, but the CT of poultry reared at 25– 27◦ C was not significantly different compared with that of those reared at 20–22◦ C (Richards, 1971; Donkoh, 1989; Tzschentke et al., 1996; Yahav et al., 1997; Yahav 1999). These previous studies generally tested less than 4 temperature treatments, so the IPT was not estimated exactly. In present the study, we tested 18 temperature treatments from 18 to 35◦ C and measured CT, ST, and AT over 3-min intervals during 9 h of experiments using mini temperature data loggers. The scatter plots showed clearly that the variations in ST and CT as AT increased could be fitted by broken-line model analysis. The coefficients of variation for the IPTs in the same bird estimated on 3 d were 0.69 to 1.59, which indicates that our method for estimating the IPT in hens is stable and repeatable. TNZ was defined by the Thermal Commission of International Union of Physiological Sciences (1987) as the range of ATs within which body temperature regulation is achieved only by the control of sensible heat loss, i.e., without regulatory changes in metabolic heat production or evaporative heat loss. Regulation of sensible heat loss refers to heat loss by conduction, convection, or radiation. Thus, thermoregulation in the TNZ only occurs via vasomotor control (Savage and Brengelmann, 1996; Brengelmann and Savage 1997; Mekjavic and Eiken, 2006). Therefore, the TNZ can be divided into 2 distinct parts based on vasomotor control in poultry: the comfort zone, which covers the range
from the LCT of the TNZ to the point where poultry activate their vasomotor control; and the zone from the upper border of the comfort zone to the UCT of the TNZ. In the present study, the IPT of ST for laying hens was 23.89◦ C at an RH of 50%, above which the ST of hens started increasing, thereby indicating that the upper border of the thermal comfort zone for hens may be 23.89◦ C. The IPT of CT for laying hens was 25.46◦ C at an RH of 50%, above which the CT of laying hens started increasing, thereby indicating that the hens suffered from heat stress. Thus, we suggest that the UCT of the TNZ in hens may be a specific temperature between 23.89◦ C and 25.46◦ C, above which the respiratory frequency, feed intake, or heat production may start to change in hens. The IPT of CT and ST cannot be used to accurately the estimate UCT of TNZ of hens, but it is still an important reference for regulating the temperature in poultry houses. The main pathway for heat dissipation by birds in a hot environment is respiratory evaporation (Hillman et al., 1985). The amount of evaporative heat loss depends on the humidity in the air and it is suppressed as the humidity rises (Chwalibog and Eggum, 1989; Nichelmann et al., 1991). Lin et al. (2005) found that the CT and ST were higher in broilers at an RH of 85% than that those at RH levels of 35% and 50% in a hot environment (30 or 35◦ C). In the present study, the IPTs of ST were higher at 35% and 50% RH than those at 85% RH, which indicates that even in a mild hot environment (21 to 23◦ C), a high level of humidity in the air may still suppress evaporative heat loss
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REAL-TIME VARIATIONS OF HENS’ TEMPERATURE
via the normal respiratory route and skin by birds. As a compensatory behavior, birds raised their ST at a relatively lower AT to improve the sensible heat loss dissipation. In conclusion, our results indicate that analyzing the real-time variations in body temperature as AT increases is a reliable method for estimating the IPT in laying hens to provide an important reference for regulating the temperature in poultry houses.
ACKNOWLEDGMENTS This study was supported by the National Key Research and Development Program of China (2016YFD0500509). This research was also supported by the Science and Technology Innovation Project of the Chinese Academy of Agricultural Sciences (ASTIP-IAS07).
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