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Skin surface temperature of broiler chickens is correlated to body core temperature and is indicative of their thermoregulatory status1 M. Giloh, D. Shinder, and S. Yahav2 Agricultural Research Organization, the Volcani Center, Institute of Animal Science, Poultry and Aquaculture Department, PO Box 6, Bet Dagan 50250, Israel ABSTRACT Extreme thermal conditions may dramatically affect the performance of broilers and other domestic animals, thereby impairing animal welfare and causing economic losses. Although body core temperature is the parameter that best reflects a bird’s thermal status, practical and physiological obstacles make it irrelevant as a source of information on the thermal status of commercial flocks. Advances in the technology of infrared thermal imaging have enabled highly accurate, noncontact, and noninvasive measurements of skin surface temperature. Providing that skin surface temperature correlates with body temperature, this technology could enable acquisition of reliable information on the thermal status of animals, thereby improving diagnoses of environmental stress in a flock. This study of broiler chickens found a strong positive correlation between body core temperature and facial surface temperature, as recorded by infrared thermal imaging. The correlation was equally strong at all ages from 8 to 36 d during exposure to acute heat stress with or without proper ventilation and after acclimation to chronic heat exposure. A similar correlation was found by measurements in commercial flocks of broilers. Measurements of blood plasma concentrations of corticosterone, thyroid hormones, and arginine vasotocin confirmed that metabolic activity was low after acclimation to chronic exposure to heat, whereas ventilation was at least as efficient as acclimation in reducing thermal stress but did not impair metabolism. In light of these novel results, commercial benefits of infrared thermal imaging technology are suggested, especially in climate control for commercial poultry flocks. The application of this technique to other domestic animals should be investigated in future experiments. Key words: infrared, broiler, facial surface temperature, body temperature, hot condition 2012 Poultry Science 91:175–188 doi:10.3382/ps.2011-01497 INTRODUCTION and affect Tb within a few minutes (Cabanac and Aizawa, 2000; Cabanac and Guillemette, 2001); however, during the past 10 to 12 yr, adoption of thermal-imaging radiometry technology in biological sciences has enabled noninvasive, noncontact measurement of surface temperature. However, use of infrared thermographic measurement by infrared thermal imaging (IRTI) of skin surface temperature in monitoring the thermal status of chickens in a commercial flock necessitates the selection of a specific surface site and the determination of the exact correlation of its temperature with Tb under various environmental conditions. The present study aimed to (a) elucidate the correlation between Tb and facial surface temperature (Tfs) in broiler chickens of various ages under exposure to acute or chronic elevation of Ta; and (b) to correlate the responses of Tb and Tfs with changes in blood plasma concentrations of corticosterone, thyroid hormones, and arginine vasotocin (AVT), given that these hormones reflect acute stress and changes in the age-dependent metabolic rate. Three main climatic factors affect the performance and productivity of poultry: ambient temperature (Ta), RH, and ventilation or air velocity (AV). Out of the 3 parameters, Ta plays a crucial and major role in the ability to maintain body temperature (Tb) within the normothermic ranges for mammals (Horowitz, 1998) and domestic fowl (Yahav et al., 2009). Nevertheless, the ventilation rate also has a direct effect on the performance of broilers (Dozier et al., 2005; Yahav et al., 2005) and turkeys (Yahav et al., 2008). The commonly used ways to record Tb are invasive and time consuming and, therefore, may be traumatic ©2012 Poultry Science Association Inc. Received March 22, 2011. Accepted September 24, 2011. 1 Contribution from the Agricultural Research Organization, the Volcani Center, Bet Dagan, Israel No. 575/10. 2 Corresponding author: [email protected] 175 176 Giloh et al. Table 1. Ambient temperature and ventilation during the experimental measurements1 Co Day 8 15 22 29 36 H Hve Acc Tco2 (°C) Tmin3 (°C) Tmax4 (°C) Tmin3 (°C) Tmax4 (°C) Vent.5 (m/s) Taccl.6 (°C) 30.6 26.1 24.2 23.4 21.6 29.0 25.4 23.4 21.8 22.1 38.0 36.2 34.8 34.1 33.8 28.6 26.4 23.8 22.5 23.0 38.0 37.0 34.5 34.2 33.8 0.9 1.1 1.5 1.5 1.5 38.1 37.6 34.4 35.1 35.2 1Co = control; H = exposure to heat only; Hve = exposure to heat and ventilation; and Acc = acclimation to heat. ambient temperature in the control group during the measurements. 3Ambient temperature under regular conditions in the chambers where heat exposure took place on the same day. 4Maximum ambient temperature recorded during heat exposure. 5Air velocity during heat exposure in treatment Hve. 6Mean ambient temperature in the acclimated group during the measurements; ambient temperature fluctuated by ±1.5°C. 2Mean MATERIALS AND METHODS Experimental Design All procedures in this study were carried out in accordance with the accepted ethical and welfare standards of the Israeli Ethics Committee (IL-047/06). In total, 700 one-day-old commercial male broiler chickens (Cobb) were obtained from a commercial hatchery. The birds were housed in cages measuring 0.40 × 0.28 × 0.45 m in length, width, and height, covered with 0.02-m wire mesh. There were 3 birds per cage from 1 to 21 d of age, and 1 bird per cage from 21 d of age onwards. Cages were kept in 4 identically designed computer-controlled environmental chambers that maintained the temperature at ± 1.0°C, RH at ± 2.5%, and AV at ± 0.25 m/s under continuous fluorescent illumination. The AV was recorded with an Electronic Air-Flow Sensor AVS200 (Kele and Associates, Memphis, TN). Water and food in mash form were supplied ad libitum in a diet designed according to the US NRC (1994). At the age of 4 d, 108 birds were randomly chosen and 27 birds were allotted to each of 4 treatments. Treatment 1 (control) was maintained under regular conditions in chamber 1. The 3 other treatments started in chamber 1, from which they were transferred to 3 different chambers in which conditions were initially identical to those in chamber 1. The treatments in these chambers were as follows. Treatment 2 (H) was housed in chamber 2 where the chickens were exposed to regular conditions during the first 72 h and thereafter to acutely elevated Ta. Treatment 3 (Hve) was housed in chamber 3 where the chickens were exposed to regular conditions during the first 72 h and thereafter to acutely elevated Ta combined with increased AV. Treatment 4 (Acc) was housed in chamber 4 where Ta was gradually elevated, starting about 2 h after the transfer of the chickens from chamber 1 to reach the designated Ta after a period of 48 h; it was then maintained for another 24 h until measurements began. On d 8, 72 h after the chicks were transferred from chamber 1; that is, 24 h after reaching the designated Ta in treatment Acc, the Ta was abruptly elevated in treatments H and Hve. Then, the Tb was recorded in all treatments, blood samples were taken as described below, and all 108 birds were removed from the experiment. The same procedure was repeated 4 times, with measurements taken at ages 15, 22, 29, and 36 d, with the birds always being transferred to the experimental chambers 72 h before the measurements. Table 1 summarizes the treatments, ages, and Ta values. In the acute treatments (H and Hve) Tb and Tfs—in the following, referred to as physiological temperatures, as distinct from the nonphysiological ambient temperature Ta—were recorded in 9 individuals before the elevation of Ta at the start of the experiment. Immediately afterward, the heaters were activated and, in the Hve treatment, the ventilation was activated at a predetermined air velocity (Table 1). The designated Ta was reached within less than 30 min, and after a further 30 and 90 min, Tb and Tfs of the same chickens were recorded again. After the last measurement, the climate control systems in treatments H and Hve were reset to regular conditions. Approximately 2 h after restoration of regular conditions, Tb and Tfs of the same chickens were recorded again. In the control and Acc treatments, while the measurements in treatments H and Hve were proceeding, Tb and Tfs of 9 birds were recorded twice: once while chambers 2 and 3 were heating up, and once during the measurements in the acute treatments. In treatments H and Hve, blood samples were drawn 30 and 90 min after attainment of the designated Ta. The blood was drawn from the hearts of 7 to 9 birds, which were removed from the experiment immediately afterward. In the Acc and control treatments, blood samples were drawn in the same way only once while heat exposure in the acute treatments H and Hve was proceeding. IRTI Radiometry The infrared thermal imager (model PM545; FLIR Systems, Danderyd, Sweden) that was used in this study includes an uncooled thermal-imaging camera equipped with a high-resolution (320 × 240)-pixel focal SURFACE AND BODY TEMPERATURE CORRELATIONS 177 plane array microbolometer that is sensitive to longwave radiation in the 7.5- to 13-μm range and has a temperature precision of ± 0.1°C. The temperature of the hottest spot on the face of the chickens was recorded by analyzing the thermographs with the Thermacam program (FLIR Systems). In each thermograph, a blackbody reference point was included for calibration. The blackbody was composed of a closed hollow cylinder with a small hole in the lid and a thermocouple in the bottom for measuring the temperature of the cavity. The temperature reading of the camera was adjusted manually according to the difference between the actual blackbody temperature, as recorded by the thermocouple, and the camera reading of the temperature of the hole. Temperature data for each pixel in the thermograph were stored digitally and retrieved by the computer software. in concentrations of 256, 128, 64, 32, 16, and 8 pg/ mL in RIA buffer. Plasma AVT concentrations were recorded with an [Arg8]-Vasopressin commercial kit (RIK 8103, [Arg8]-Vasopressin, Rabbit Antiserum, Peninsula Laboratories Inc., Belmont, CA). The kit antibody has cross-reactivity levels: [Arg8]-vasotocin, 100%; adrenocorticotropic hormone, 0%; and oxytocin, 0%. The sensitivity of the method is 10 pg/mL to IC80; 50 pg/mL to IC50; and 190 pg/mL to IC20. Intraassay variation, estimated according to the extraction and assay of 6 control plasma samples, averaged 6.6%, and interassay variation, estimated in triplicate over 3 assays, averaged 8.7%. Recovery was 91%, as determined by comparing the extraction of 6 control samples with samples spiked with equal amounts of the 32 and 64 pg/mL standards. Temperature Measurements The measurements of Tb and Tfs were applied to the same individual birds before and during activation of the H and Hve treatments. This enabled analysis of changes in individual Tb and Tfs levels in the H and Hve treatments. For the Acc treatment, the control chickens were used for the baseline measurements of Tb and Tfs; therefore, only the mean and SE were analyzed in this treatment. In each treatment, a different set of chickens was used as a control for the measurements of Tb and Tfs; therefore, intertreatment comparison of absolute values of physiological temperatures would not be statistically valid. However, mean values of differential temperature changes (ΔTb/ΔTa and ΔTfs/ΔTa) in the 2 respective acute treatments are similar, because changes in temperatures were related to each individual bird, and the only differences between the identical chambers were in Ta and AV. A comparison between the values of these differential parameters in the acute treatments with those in the Acc treatment, in which the baseline values of Tb and Tfs were those recorded in the control birds, is presented merely as a general reference, without statistical verification (Tables 2 and 3). For the hormone-concentration measurements, the baseline concentrations in all of the treatments were those recorded in individual birds in the control treatment. Therefore, each bird was regarded as one replicate in the comparison of individual hormone concentrations with the mean of the controls, using n = 9. During analysis of the data, it became clear that some results were repeated for all or almost all of the age groups, although they were not statistically significant for any particular age group. In such cases, the ratio between individual hormone concentration and the mean among the controls on the same day was regarded as a parameter that could be compared between treatments and averaged over all of the experiment, with age differences disregarded. Linear regressions were calculated with Microsoft Excel software (Microsoft, Redmond, WA). Statistical significance was estimated by means of the Tukey- For each IRTI thermographic measurement, the bird was taken out of the cage and placed on a small platform, one of which was identically located in each of the chambers. The thermographic measurement was generally taken within less than 10 s after the bird was handled, and immediately it was followed by the measurement of Tb with a medical thermometer that was inserted approximately 30 mm into the cloaca. The thermometer had been previously calibrated against a manufacturer-calibrated standard alcohol thermometer and found to be accurate within ± 0.1°C. The whole measurement procedure took less than 1 min for each chicken. Because it takes several minutes for Tb to rise during handling (Mitchell, 1981), it was assumed that the effect of the procedure on Tb could be neglected. Plasma Hormone Analysis Radioimmunoassays (RIA) of total thyroxine (T4) and total triiodothyronine (T3) in plasma samples were performed with commercial RIA kits Coat-A-Count Canine T4 (Diagnostic Products Corp., Los Angeles, CA) and RIA-gnost T3 (CIS Bio International, Gif-surYvette, France). The intraassay and interassay CV of the T4 assay were 5.0 and 7.5%, and those of the T3 assay were 7.8 and 8.2%, respectively. Plasma corticosterone concentrations were recorded with the radioimmunoassay kit with ImmuChem double antibody (ICN Biomedical, Diagnostics Division, Orangeburg, NY), which yielded intraassay (within run) and interassay (between runs) CV of 4.7 and 6.5%, respectively. Plasma samples for the assay of the antidiuretic hormone AVT were extracted according to Arnason et al. (1986). Extracts were reconstituted in 0.15 mL of RIA buffer immediately before the assay. One milligram of synthetic AVT acetate salt was dissolved in 0.1 N acetic acid to prepare assay standards that were prepared Data Analysis 178 Giloh et al. Table 2. Mean ambient (Ta), body (Tb), and facial surface temperature (Tfs) of the acclimated (Acc) and the control (Co) groups, during the measurements1 Acc (°C) Co (°C) Day Ta Tb Tfs Ta Tb Tfs 8 37.5 38.1 38.2 35.0 34.3 34.5 35.0 35.2 34.9 35.5 1.5 43.2 43.4 43.9 43.8 43.0 42.8 43.1 43.0 43.3 43.3 0.17 41.1 42.0 42.5 42.6 41.3 41.1 41.6 41.5 41.8 41.5 0.22 30.7 30.5 25.7 26.2 26.4 24.4 24.5 23.5 23.4 23.4 21.3 22.0 1.5 41.3 41.2 41.5 41.6 41.3 41.6 41.7 41.6 41.3 41.2 41.4 41.4 0.21 39.2 39.5 38.2 40.2 38.8 39.4 39.4 39.8 39.4 39.5 39.1 38.5 0.23 152 222 29 36 Maximum SE3 1n = 9, except for T , which was recorded 3 times in every chamber for each series of measurements. Temperaa tures were generally recorded twice in the Acc and Co groups. 2On d 15 and 22 the temperatures in the Co group were recorded 3 times. 3The empirically found random fluctuation range is specified as SE for T . a Kramer algorithm with JMP software (SAS Institute Inc., Cary, NC). In all, graphs error bars represent SE, unless stated otherwise. Field Observations A commercial farm in Kibbutz Lavi, Israel, was chosen for the field observations. The farm contains 5 buildings, 3 of which are closed and equipped with computerized climate control systems that include tunnel ventilation combined with ceiling ventilation and an evaporative cooling pad. Two older buildings are open and equipped only with thermostat-controlled internal fans and with thermostat-controlled internal sprinklers that are pulse-activated to lower Ta during high-Ta periods. Two different flocks were chosen for the observation: (1) a group of approximately 3,000 male chickens that were reared in a climate-controlled building, separated by a fence from 15,000 female chickens in the same building; and (2) approximately 6,000 male chickens of the same age and from the same source, that were reared in a small open building. The mea- Table 3. Mean elevations of physiological temperatures [body temperature (Tb) and facial surface temperature (Tfs)] per degree of elevation of ambient temperature (Ta) as ΔTb/ΔTa and ΔTfs/ΔTa during each measuring day and averaged over all measuring days, regardless of age1 Item2 Age (d) Treatment3 A 8 H Hve Acc H Hve Acc H Hve Acc H Hve Acc H Hve Acc H Hve Acc 15 22 29 36 B Maximum SE Mean overall ages ΔTb/ΔTa ΔTfs/ΔTa 0.25 0.17* 0.29 0.13 0.07* 0.24 0.16 0.02* 0.12 0.13 0.08 0.15 0.25 0.13* 0.14 0.18c 0.09d 0.19c 0.02 0.37a 0.34a 0.30 0.25a 0.28a 0.30a 0.27a 0.17*a 0.16a 0.19a 0.12*a 0.18a 0.28 0.19* 0.21a 0.27a 0.22bc 0.23b 0.03 a–dDifferent superscript letters indicate a significant (P ≤ 0.05) difference between T and T within treatment b fs on the same day; *significant differences between the 2 acute treatments H and Hve on the same day. 1Data for the Acc treatment on each day cannot be compared with those for other treatments in a statistically valid manner because the control for the Acc group was in another chamber; they are presented only for comparison between ΔTb/ΔTa and ΔTfs/ΔTa, which relate to the same control group. 2In the upper part of the table (A), average of individual data for each treatment and each of the ages are presented. In the bottom part (B), means of individual data irrespective of age are presented. 3H = exposure to heat only; Hve = exposure to heat and ventilation; and Acc = acclimation to heat. SURFACE AND BODY TEMPERATURE CORRELATIONS surements were performed at midday on d 30, during the following night, and at midday on d 31. The night measurements were performed with illumination. In each measurement session, a portable, foldable low fence (2 × 1.5 m) was used to segregate about 30 to 60 chickens in a randomly chosen measurement site, where 10 to 20 of them were then caught 1 by 1 and their Tb and Tfs were recorded simultaneously. The number of birds recorded each time was determined by the general behavior of the segregated birds: when behavioral stress became evident, the measurement was terminated in the specific site. After each bird was recorded, it was placed outside the fence to prevent its being recorded twice. The blackbody temperature was recorded for each thermogram as described above and, in addition, Ta was recorded 4 or 5 times in each site with a calibrated alcohol thermometer, and the mean value in each station was used in analyzing the responses to Ta. After completion of the measurements, the fence was folded to be taken to the next site in the building, and the remaining chickens were released. Generally, 3 to 5 measurement sites were designated for each session in the controlled building and 5 to 8 in the open building. RESULTS Dependency Among Tb, Tfs, and Ta As expected, acute elevation of Ta caused increases in Tb to levels that were stabilized in almost all cases 30 min after maximum Ta was reached (data not shown). This was also true for Tfs, which had a baseline value approximately 2°C below Tb under standard conditions (Figure 1). Chickens that were exposed to high Ta exhibited values of Tb ranging from 42 through 44°C, and Tfs ranging from 40 through 42°C. As indicated by the weakly inclined and statistically nonsignificant least-squares-fit regression lines inserted into Figure 1, although Ta in both the control and heat exposure treatments was reduced as chicken age increased (Table 1), Tb and Tfs were almost similar for all control measurements. During exposure to heat, within the range of Ta that was used to induce heat stress and that was lowered from 38.5 to 33.7°C as chicken age increased, the responses of Tb and Tfs to Ta change remained relatively constant throughout the experiment. A plot of mean Tb and Tfs in all treatments, and irrespective of ages (Figure 2), shows that Tb was similar in all treatments before the acute heat exposure, whereas the Tfs baseline level differed slightly between treatments. During exposure to heat, Tb values in the Acc treatment and the H treatment were similar, at approximately 1.9°C above the control; and the Hve treatment had a mean Tb approximately 1.2°C above the control. As evident from Figures 1 and 2, the differences between Tb and Tfs were smaller when chickens were exposed to heat compared with the differences under control conditions. This is confirmed by a quantitative comparison of the rates of Tb and Tfs elevation per degree 179 Figure 1. Laboratory dependence of body (Tb) and facial surface temperature (Tfs) on ambient temperature (Ta). The graph presents data from individual measurements in all treatments and at all ages. The solid marks indicate the control and the acute treatments before elevation of Ta. The hollow symbols indicate chickens exposed to heat (Acc = acclimated to heat; H = exposure to heat only; and Hve = exposure to heat and ventilation). Grey symbols indicate Tfs and black marks indicate Tb. The solid lines are least-square linear regressions calculated separately for heat-exposed and unexposed chickens and for Tb and Tfs, specified as follows: bC = body temperature of control; fsC = face surface temperature of control; bE = body temperature of heat-exposed chickens; and fsE = face surface temperature of heatexposed chickens. of increase in Ta (ΔTb/ΔTa and ΔTfs/ΔTa; Table 3), which shows that Tfs rose faster than Tb in response to Ta elevation in all treatments and at all ages and that the difference was significant (P ≤ 0.05) in 12 out of 15 cases. To compare the responses of Tb and Tfs to Ta elevation with and without increased ventilation (treatments Hve and H), the data from the Acc treatment were ignored, and the significance of the differences between Hve and H birds was calculated for ΔTb/ΔTa and ΔTfs/ΔTa separately. When ventilation was applied, both ΔTb/ΔTa and ΔTfs/ΔTa were significantly lower (although not for all ages) in treatment Hve compared with those in treatment H. Section B of Table 3 shows the mean over individual birds of all ages. The sharpest rise in physiological temperatures was in Tfs in treatment H (without ventilation). In treatment Acc, the response of Tb was similar to that in treatment H, whereas that of Tfs was similar to that in HVe; ΔTb/ ΔTa was 50% lower and ΔTfs/ΔTa was 20% lower in Hve than in H (P ≤ 0.05). Hormone Concentration Because the control chickens were housed in a separate chamber (chamber 1), comparison between mean hormone concentrations in the various treatments with those in the control on any particular day would not have been valid. Therefore, the ratios between individual hormone concentrations and the means in the 180 Giloh et al. treatments H and Acc. In treatment H, the corticosterone concentration continued to rise to more than 4 times that of the controls, whereas in treatments Hve and Acc, it was similar to that of the controls. Plasma AVT concentrations in treatment Acc were lower than those in the controls, whereas in the other treatments, they were similar to those in the controls. Correlation Among Physiological Parameters Figure 2. Mean body temperature and facial surface temperature for heat-exposed and unexposed chickens, irrespective of age differences. The black bars indicate body temperature. The grey bars indicate facial surface temperature. Co = control (including control group and the acute treatments before elevation of ambient temperature); H = before exposure to heat only; Hve = before exposure to heat and ventilation; and Acc = acclimated to heat. Exp: during exposure to heat. Capital letters indicate statistically significant (P < 0.05) differences in body temperature; lowercase letters indicate statistically significant differences in facial surface temperature (P < 0.05). control birds on the same day were calculated for each chicken, and means for each group on all measurement days were then computed, irrespective of ages. Thirty minutes after attainment of a designated Ta, significant increases in the plasma corticosterone and T4 concentrations, relative to the controls were observed in treatment H, whereas T3 and AVT concentrations remained close to those of the controls. In treatment Hve, 30 min after attainment of the designated Ta, the plasma concentrations of all the hormones were close to those of the controls (Table 4). Ninety minutes after attainment of the designated Ta (Figure 3), the plasma T4 concentration rose the furthest above the controls in treatment H and to a level between those in the H and the controls in the Hve treatment. The T3 concentrations decreased significantly compared with the controls in In all treatments and for all ages, a strong correlation was found between Tb and Tfs (Figure 4). The shape of the cluster in Figure 4 indicates a sigmoid pattern of correlation, but least-square fits of various sigmoid regression curves did not yield higher R2 values than the linear regression line shown in Figure 4. Linear regressions for individual birds for each separate day had R2 values of 0.75 to 0.89 (not shown). Mean hormone concentrations for each treatment and each age were plotted against corresponding mean values of Ta, Tb, and Tfs, and correlations between mean hormone concentrations and temperatures were calculated at first with a linear least-square fit (Figure 5). Although no (or only weak) regression was found for the data yielded by combining the acute and the acclimated treatments (not shown), the acute and the acclimated treatments were analyzed separately, and the results for treatment Acc are presented graphically in Figure 5. Corticosterone concentrations did not correlate with any of the Ta, Tb, or Tfs, as indicated by R2 values close to zero. However, the T4 concentration showed significant negative linear correlations with all 3 temperature parameters; that with Ta (R2 = 0.49) was somewhat weaker than those with Tb and Tfs (R2 = 0.62 and 0.60, respectively). The T3 concentrations also displayed significant negative correlations with Ta, Tb, and Tfs; that with Ta had the lowest R2 value (0.47) and those for Tb and Tfs were higher (0.65 and 0.79, respectively). In this treatment, AVT displayed a negative correlation with Tfs (R2 = 0.51) and weaker correlations with Tb (R2 = 0.36) and Ta (R2 = 0.16). Table 4. Mean relative hormone concentrations1 in the acute treatments 30 min after reaching targeted ambient temperature (Ta) Hormone2 Treatment H Hve Co a,bDifferent Value T4 Mean SE Mean SE Mean SE 1.46a 0.15 1.01b 0.08 1.00b 0.07 T3 Cort AVT 1.06 0.04 1.11 0.05 1.00 0.03 1.76a 1.13 0.07 1.08 0.07 1.00 0.04 0.22 0.90b 0.10 1.00b 0.08 letter superscripts indicate values within a column that are significantly different (P ≤ 0.05). individual ratios of absolute hormone concentrations to the mean of the control concentrations on the same day were averaged over the whole experimental period, ignoring age differences. Control is the mean ratio of individual hormone concentrations in the control group to the mean concentration of the same control group on the same day. 2T = thyroxine; T = triiodotyronine; Cort = corticosterone; and AVT = arginine vasotocin. 4 3 1The SURFACE AND BODY TEMPERATURE CORRELATIONS 181 (Figures 5 and 6). In treatment Acc, T4 had a positive correlation with Tb and Tfs (P = 0.02) and a lower significance with respect to correlation with Ta (P = 0.06); and T3 and AVT had significant negative correlations with all 3 parameters (P ≤ 0.05). In the acute treatments, concentrations of corticosterone and T3 showed positive and negative correlations with both Tb and Tfs, (P ≤ 0.05); no significant correlations with Ta were found for corticosterone (P = 0.21) or T3 (P ≤ 0.13). In the acute treatments, T4 and AVT displayed no correlation with temperatures. Field Observations Figure 3. Ratios of individual hormone concentrations to mean control concentration on the same day, 90 min after reaching target ambient temperature, averaged over the whole experiment and irrespective of age differences. A: thyroxine (T4); B: triiodothyronine (T3); C: corticosterone; D: arginine vasotocin (AVT). Different letters indicate significantly different relative concentrations (P < 0.05). In all plots, control represents the mean ratio between individual hormone concentrations in the control group and the overall mean concentration in the control on the same day. Co = control; H = exposure to heat only; Hv = exposure to heat and ventilation; and Ac = acclimated to heat. To analyze the acute treatments in a similar way, data obtained during 30-min heat exposures were ignored because, as indicated above, 30 min after attainment of the designated Ta the trends were the same as or weaker than those seen after 90 min. The data for the acute treatments (H and Hve) and the control after 90 min of heat exposure are shown in Figure 6. For corticosterone, positive correlations with Ta, Tb, and Tfs were found; although R2 was low for all 3 regression lines, it was higher for Tb and Tfs (0.33 and 0.29, respectively) than for Ta (0.12). Similar correlations were found for T3, although in this case the slopes of the regression lines were negative. The negative correlation of T3 with temperature was strongest with Tfs (R2 = 0.40), weaker with Tb (R2 = 0.34), and weakest or practically nonexistent with Ta (R2 = 0.17). In the acute treatments, no correlations were found between T4 or AVT and any of the 3 temperatures, with R2 being lower than 0.1 in all 3 cases. In the acute treatments, and also in the Acc treatment and the control, data for individual chickens 90 min after the attainment of the designated Ta were analyzed with the Jump software for statistical analysis. Table 5 columns A and B summarize the results of the analysis of the data from treatments Acc, H, and Hve together with the R2 values computed by Excel To compare the strong correlation that was found between Tb and Tfs in climate-controlled chambers with the situation in a commercial flock, observations were made in a poultry farm on a summer day, when solar radiation was high and midday shade temperatures reached 37°C; conditions that apparently often lead to thermal stress in the flock. The tests encompassed chickens in 2 buildings, one of which was climate controlled and the other open. The details of the setting are described in Materials and Methods. Altogether approximately 370 individual measurements were performed and the general correlations between Tb and Tfs for individual chickens are shown in Figure 7. For the linear regression curve, R2 values were 0.54 and 0.44 for the open and the climate-controlled building. The mean Tfs for each measurement site and each measurement session (10–20 chickens in each site) displayed a positive linear correlation with the mean Tb, with R2 values of 0.86 and 0.91 for the open and the climate- Figure 4. Correlation of individual facial surface temperature (Tfs) with body temperature (Tb). The data represented in the graph are for all measurements of individual chickens in all treatments and all ages. 182 Giloh et al. Figure 5. Correlations of mean plasma hormone concentrations with body (Tb), facial surface (Tfs), and ambient temperature (Ta) for the control and the acclimated treatments. Each data point represents the mean concentration of corticosterone (Cort), thyroxine (T4), triiodothyronine (T3), or arginine vasotocin (AVT) in a certain treatment on a certain day and time vs. Tb, Tfs, or Ta (n = 9). The graphs represent results from the whole experiment period, irrespective of age differences, and do not distinguish between the different treatments because each point is regarded as one replicate of the same experiment. All error bars represent ± SE, except for the horizontal error bars for Ta that represent ±1.5°C, the typical fluctuation range of ambient temperature, as recorded in the climate-controlled chambers. controlled building, respectively (Figure 8). In both figures, the inclination of the regression line for the correlation between Tb and Tfs was higher for the open than for the climate-controlled building. Mean physiological temperatures in each site correlated well with Ta, with R2 being 0.77 for Tb and 0.83 for Tfs (Figure 9). The responses of mean Tb and Tfs to Ta revealed no statistically significant difference between the 2 buildings (not shown), in both of which Tfs rose more sharply than Tb in response to elevation of Ta, as indicated by the consistent regressions in Figure 9. DISCUSSION Responses of Tb and Tfs to Elevation of Ta During recent decades, significant progress has taken place in the genetic selection of fast-growing meat-type SURFACE AND BODY TEMPERATURE CORRELATIONS 183 Figure 6. Correlation of mean plasma hormone concentrations with body (Tb), facial surface (Tfs), and ambient temperature (Ta) for the control and the acutely exposed treatments. Each data point represents the mean concentration of corticosterone (Cort), thyroxine (T4), triiodothyronine (T3), or arginine vasotocin (AVT) in a certain treatment on a certain day and time vs. Tb, Tfs, or Ta (n = 9). broiler chickens; their growth rate, feed conversion, and livability have all been improved (Havenstein et al., 2003a). However, this improvement was accompanied by a significant increase in heat production that caused difficulties in coping with extreme environmental conditions because development of visceral systems, such as the cardiovascular and respiratory, did not match that of muscle tissue (Havenstein et al., 2003b). Several studies found decreased performance in chickens that were exposed to higher than optimal Ta (Donkoh, 1989; Yahav et al., 1995; Geraert et al., 1996; Bonnet et al., 1997; Cooper and Washburn, 1998; Yahav and Plavnik, 1999). In most cases, persistent exposure to high Ta resulted in a significant reduction in performance, as reflected in reduced BW at marketing age, coupled with reduction of feed intake, and, to some extent, in feed utilization. One of the immediate responses to extreme elevated Ta is the development of hyperthermia (Hillman et al., 1985; Etches and John, 1995; reviewed by Yahav et al., 2009). Exposure to elevated Ta increases blood flow to the skin, especially to the nonfeathered areas, as a result of vasodilatation (Wolfenson et al., 1981; Wolfenson, 1986; Yahav et al., 1998, 2004), as well as to the 184 Giloh et al. Figure 7. Correlation of individual face surface temperature with body temperature in 2 buildings in a commercial poultry farm. Solid diamonds and thin regression line indicate the open building; hollow squares and thick regression line indicate the climate-controlled (Cl. Cont.) building. The equations and R2 values of the regression lines are inserted at the bottom of the graph. Figure 8. Correlation of mean face surface temperature with mean body temperature for each measurement station (n = 10–20) in 2 commercial flocks. Solid diamonds and thin regression line indicate the open building; hollow squares and thick regression line indicate the climate-controlled building (Cl. Cont.). The equations and R2 values of the regression lines are inserted at the bottom of the graph. upper respiratory passageways (Wolfenson et al., 1981) to transport heat from the viscera to the periphery. This redistribution of the blood flow leads to increased heat dissipation from the body via radiation, convection, and conduction. Heat production of a chicken is regulated by several hormones, especially the thyroid hormones T4 and T3 (Kühn et al., 1984; Iqbal et al., 1990; McNabb and King, 1993; Gabarrou et al., 1997; reviewed in Silva, 2006), and the hydrodynamic balance is regulated by the main fowl antidiuretic hormone AVT (Stallone and Braun, 1985). Exposure to high Ta induces a reduction in heat production, which is re- flected in a drop in plasma T3 concentration (Yahav, 2000). During acute exposure to high Ta, this reduction is achieved by reducing the rate of peripheral deiodinization of T4 to T3, with a consequent increase in the concentration of T4. This response is part of a general acute stress response, reflected in a rise in plasma corticosterone concentrations during acute exposure to heat (Iqbal et al., 1990; Darras et al., 1996). Persistent exposure to heat caused a general decrease in thyroid gland activity, leading to low plasma concentrations of both T3 and T4 and to a permanently low metabolic rate, all to adapt to high Ta (Geraert et al., 1996; Bon- Table 5. The R2 values, correlation coefficient, and P-value for the dependence of mean hormone concentrations on body (Tb), facial surface (Tfs), and ambient temperature (Ta) of chickens1 Acc compared to Co3 Hormone2 Calculation Cort R2 T4 T3 AVT 1R2 Corr. coeff. P-value R2 Corr. coeff. P-value R2 Corr. coeff. P-value R2 Corr. coeff. P-value H and Hve compared to Co3 Tb Tfs Ta Tb Tfs Ta 0.01 0.10 0.79 0.62 −0.71 0.02 0.65 −0.81 0.00 0.36 −0.60 0.06 0.00 −0.01 0.97 0.60 −0.70 0.02 0.79 −0.89 0.00 0.51 −0.72 0.02 0.07 0.25 0.49 0.49 −0.61 0.06 0.47 −0.69 0.03 0.16 −0.40 0.03 0.33 0.56 0.03 0.05 0.26 0.34 0.34 −0.59 0.02 0.01 −0.10 0.72 0.29 0.54 0.04 0.05 0.26 0.35 0.40 −0.64 0.01 0.05 −0.22 0.43 0.12 0.35 0.21 0.07 0.31 0.26 0.17 −0.41 0.13 0.02 0.13 0.65 values >0.5, correlations >0.7, and significance probabilities <0.05 are shown in boldface. = corticosterone; T4 = thyroxine; T3 = triiodothyronine; and AVT = arginine vasotocin. 3Co = control; H = exposure to heat only; Hve = exposure to heat and ventilation; and Acc = acclimation to heat. 2Cort SURFACE AND BODY TEMPERATURE CORRELATIONS Figure 9. Correlation of mean body and facial surface temperatures with ambient temperature in commercial flocks. The data are from measurements in both the open and the climate-controlled (Cl. Cont.) building. Solid diamonds and solid regression line indicate body temperature; open squares and dashed regression line indicate facial surface temperature. The y-axis error lines represent ±SE. The x-axis error lines represent ±SE of the ambient temperature in each measurement site during the measurements. The equations and R2 values of the regression lines are inserted in the bottom of the graph. net et al., 1997; Garriga et al., 2006; Tao et al., 2006; Yahav et al., 2009). Several researchers reported that water deprivation resulted in increased plasma AVT concentration (Koike et al., 1977; Tanaka et al., 1984; Arad et al., 1985; Saito and Grossman, 1998. Thermal stress is induced by unfavorable combinations of temperature, RH, and AV in the micro-environment surrounding the chicken, but sensors dispersed throughout the space of the farm provide mean values of these parameters, and thus, might present unrepresentative information about the birds’ actual microenvironment. As a result, feedback mechanisms that control the environmental conditions in a chicken house might not respond to the actual needs of the birds, and decisions regarding climate-control system settings (heating, cooling, and ventilation rates) might not directly relate to optimization of the chickens’ environmental conditions; therefore, it might dramatically affect their performance and consequently reduce the economic benefits. However, during the past 10 to 12 yr, adoption of IRTI radiometry technology in the biological sciences has enabled measurement of animals’ surface temperature in a noninvasive, contact-free manner. This technology has been used in diverse biological contexts (Zontak et al., 1998; Ring and Ammer, 2000; Kastberger and Stachl, 2003; Vianna and Carrive, 2005), including application to poultry, to evaluate the thermal 185 balance between a chicken and its environment (Yahav et al., 2004, 2005). As expected, in the present study, the direct thermodynamic consequence of elevations in Ta was parallel to increases in Tb and Tfs, which facilitated thermodynamic balance with the environment, in which higher physiological temperatures were needed to dissipate excessive metabolic heat. In this series of experiments, Tb were fairly similar for all unexposed chickens; that is, those in the control group and also those in all other groups before the Ta was raised, irrespective of age and baseline Ta. Heat-exposed chickens also had fairly similar Tb levels, irrespective of age and Ta (which was reset according to the age of the exposed chickens); and the same was also true for Tfs (Figure 1). This relative age-independence of Tb and Tfs justified our disregarding age differences in the statistical comparison of differential temperature changes (ΔTb/ΔTa and ΔTfs/ΔTa), and thus allowed averaging over the whole experimental period. The outcome of the analysis confirmed a simple thermodynamic picture of the effects of heat stress and ventilation: when exposure to heat was combined with increased ventilation, as in treatment Hve, Tb rose less than in treatment H (Table 2). This result complies with the standard practice regarding domestic fowl (Yahav et al., 2009) and is consistent with a thermodynamic model in which elevated Tb is the driving force that enables dissipation of excessive metabolic heat in a hot environment. Because ventilation dramatically increases convective heat loss, it enables a lower increase in Tb to establish thermal equilibrium. The increased convective heat loss did not affect the correlation between Tb and Tfs, probably because convection is a form of peripheral heat loss that affects peripheral temperature directly, so that the relationship between Tb and peripheral (Tfs) temperatures remained unchanged. Analysis of the results in terms of ΔTb/ΔTa and ΔTfs/ΔTa showed that Tfs rose more sharply than Tb in response to Ta elevation in all treatments and at all ages. This applied in the commercial flock as well as in the climate-controlled buildings. The stronger response of Tfs than of Tb to environmental changes is attributed to the surface being closer than the body core to the surroundings and also to the effect of vasodilation that, by increasing blood flow to the periphery, reduces the temperature gradient between core and surface. The strong positive correlation that was found between Tb and Tfs, independently of age differences and temperature regimen, is a further example of the simple thermodynamic relationship between these 2 parameters. Among heat-exposed chickens, Tb responded to ventilation more strongly than Tfs, with regard to measurements averaged over the whole experimental period (Table 3). This somewhat surprising result may reflect differences in vasomotor responses between the 2 treatments. Measurements in the commercial flock exhibited wider variability than those in the laboratory when in- 186 Giloh et al. dividual Tfs values were plotted against those of Tb. However, even for means over small subpopulations (n = 10), the correlation between these physiological temperatures was strong, which indicates that the mean Tfs of 10 chickens reliably expressed their thermal status. The tendency of Tfs to rise together with Tb was weaker in the climate-controlled poultry house than in the open building (Figures 7 and 8), possibly because of a difference in environmental parameters, such as humidity and ventilation. However, ventilation rate in the climate-controlled chambers did not affect the correlation between Tb and Tfs (Figure 4); therefore, we suggest that differences in regression between the buildings might be because of differences in humidity. The climate-controlled house had dryer bedding than the open house and the resulting lower RH close to the floor might have enhanced evaporative heat loss. The less-humid surroundings found in the climate-controlled poultry house would enable chickens to maintain a thermodynamic balance with the environment, with evaporative heat loss through panting playing a larger role (compared with radiation and convection) than in the open house. Because Tfs measurement was based on radiation, this could explain why, on the mean, Tfs rose less sharply in the climate-controlled building than in the open one. On the whole, the observations in the commercial farm confirmed the following results that were obtained in the laboratory: (1) face surface temperature rose more sharply than Tb in response to Ta elevation and (2) there was a strong positive correlation between Tb and Tfs, at least at the level of population means. As seen clearly in Figure 1, apart from the crude distinction in the laboratory between regular and high Ta, neither Tb nor Tfs showed a simple correlation with Ta. In the commercial flock, the mean physiological temperatures showed a strong positive correlation with Ta, but there were slight differences between the buildings in the correlations between Tb and Tfs. It should be noted, however, that the Ta used in the plots of the field results was the mean Ta recorded close to the chickens in each measurement site. Further field observations are needed to compare laboratory findings with those from a commercial farm. However, if the laboratory findings should turn out to be representative of the field situation, which is to be expected because they are consistent with a thermodynamic and physiological model of heat stress, it would indicate that Ta should be regarded as a less reliable parameter for retrieving accurate information about changes of the thermal status in a population of chickens than Tb and Tfs. Facial surface temperature, however, showed a strong linear correlation with Tb, irrespective of age and of Ta; therefore, if its dependence on other environmental factors, such as humidity, were clarified, it could apparently serve as a more accurate indicator of changes in Tb. In birds that were maintained under high Ta (treatment Acc), Tfs responded more sharply than Tb to Ta increases (Table 2). One may assume that the physical processes through which a bird achieves thermal equilibrium with its surroundings are similar for both acute and persistent exposure to heat; in both cases heat dissipation to the surroundings can be increased only by a rise in peripheral temperature, an increase in evaporation through panting, or both. This follows from the first law of thermodynamics, which has served as the basis of several models for analyzing heat balance between homeotherms and their surroundings (e.g., Porter and Gates, 1969; Tracy, 1972; Turnpenny et al., 2000). Under both acute and persistent heat exposure, peripheral temperature or Tfs has to rise until a new thermodynamic balance is achieved, with heat being carried from the core to the surface by circulation and being dissipated into the environment as a result of the increased temperature gradient. Vasodilation enables this to happen without the core temperature rising to the same extent as the surface temperature. In the present study, we assumed that whereas acutely heatexposed birds would exhibit stress in response to the rise in Tb, acclimated birds would have adapted physiologically to the higher Ta through changes in their metabolic state, in addition to maintaining a higher Tb than that of the control birds. This assumption is discussed in the next section. Response of Thyroid Hormones, Corticosterone, and AVT to Elevations in Ta When the ratios of plasma hormone concentrations in individual birds to the mean concentrations in the control birds were analyzed 30 min after the targeted Ta levels were reached in each of the acute treatments and for birds of different ages, few changes were statistically significant. This was probably because the hormonal turnover rates did not respond to changes in Ta fast enough to be measurable within 30 min. However, when results of the same measurements were averaged after 90 min, consistent acute responses to heat stress were obtained (Figure 3): T4 rose after 90 min in the unventilated treatment (H), and to a lesser and statistically nonsignificant degree in treatment Hve. This may be an indication of an acute decrease in the rate of deiodination of T4 to T3, with a consequently lower plasma concentration of T3 than that in the control. Whereas in the acutely heat-exposed birds, the mechanism behind the lowering of the metabolic rate was based on peripheral deiodination, in the Acc birds it was based mainly on thyroid gland activity (Yahav et al., 2009). In the Acc birds, plasma T4 concentration was lower than in the controls, and the concentration of T3 declined even more than in the acute treatments, which is consistent with the reduced metabolism being caused by lower thyroid gland activity (McNabb and King, 1993; Gabarrou et al., 1997). Corticosterone concentrations were raised significantly only in treatment H, which suggests that acute stress did not (or almost not) develop in Hve birds. SURFACE AND BODY TEMPERATURE CORRELATIONS This is consistent with the well-known positive effect of ventilation on the chicken thermal status during exposure to heat-stress conditions. Ventilation during acute heat stress relatively diminishes the deleterious effect of heat exposure, thereby reducing the level of stress in the chickens, as was dramatically demonstrated in birds exposed to acute heat exposure without ventilation. This phenomenon enables ventilated chickens to undergo only slight changes in their metabolic rate during heat exposure. Acclimation, however, changed the threshold of the metabolic rate response by reducing thyroid gland activity. Plasma AVT concentrations were low in the Acc chickens, a novel result that suggests that these birds were diuretically balanced at a different level from that in the control and the acutely heat-exposed chickens (Saito and Grossman, 1995). Taken all together, the results confirm the accepted picture of the effect of exposure to heat, as described and quoted in detail above. At first, the concentration of corticosterone rose and peripheral deiodinization of T4 to T3 decreased, leading to a rise in T4 and a decline in T3 concentrations; no changes in AVT concentrations occurred within 90 min. Acclimation to persistent high Ta led to reduced thyroid gland activity, expressed in low concentrations of T4 and T3. Acclimated birds did not display high concentrations of corticosterone, which highlights their lower stress level. Ventilation reduced the stress in acutely exposed birds, which did not display a parallel reduction of metabolic rate, as estimated by measuring concentrations of T3. Correlation of Hormone Concentrations with Tb, Tfs, and Ta Figure 5 and Table 5 reveal the greater importance of the physiological parameters Tb and Tfs than of Ta as sources of information about stress and the metabolic status of heat-exposed chickens. In the acute treatments, statistical analysis confirmed the validity of the least-square regression lines, which indicate weak correlations of plasma T3 and corticosterone concentrations with physiological temperatures, whereas there was practically no correlation with Ta. In chickens that were maintained in persistent high Ta (treatment Acc), the negative correlation of the thyroid hormones with the physiological temperatures was somewhat stronger than that with the Ta. The AVT concentration showed a similar but somewhat weaker negative correlation with physiological temperatures and no significant correlation with Ta. These results were not surprising, because the responses of Tb and Tfs differed between acute treatments that had similar Ta but differing air velocities. The strong correlation of thyroid hormone and AVT concentrations with Ta in treatment Acc was probably because of the absence of ventilation; it may be hypothesized that use of ventilation would result in a stronger correlation of hormone concentrations with 187 physiological temperatures than with that of Ta, but this needs to be verified. The present results demonstrate that Tb is a better indicator of the metabolic status and stress level of chickens than ambient temperature. Facial surface temperature is strongly correlated with Tb, as shown above, and it correlates equally well (sometimes, surprisingly, even better) with hormone concentrations. Under laboratory conditions, this was seen only when a distinction was made between acute and persistent heat stress, and in a commercial farm, this distinction might be diffuse and difficult to apply. Moreover, the effects of daily repeated acute exposures to high Ta, as commonly occurs in many regions, must be elucidated before practical conclusions can be drawn regarding the correlation of stress and metabolic activity with Tfs. In spite of these reservations, this study demonstrated for the first time the potentially important application of a remotely recorded physiological parameter, Tfs, for determining the thermal status of a chicken flock to support decisions about setting the environmental parameters in a climate-controlled farm. This parameter, as recorded by IRTI radiometry, was shown in the laboratory to be more informative than Ta. In the future, infrared thermography, which has become progressively less expensive during recent decades, may provide a means for improving efficiency of meat production and welfare of farm animals. ACKNOWLEDGMENTS This research was supported by research grant No. 356-0464 from the Chief Scientist of the Israeli Ministry of Agriculture and Rural Development and research grant No. 356-0456 from the Egg and Poultry Board of Israel. The authors thank M. Ruzal, B. Gill, and P. Shudnovskey for technical assistance and B. Lipnick and M. Goldman of the poultry farm of Kibbutz Lavi, Israel, for permission to perform the field observations in the farm. REFERENCES Arad, Z., S. Sighvatur, S. Arnason, A. Chadwick, and E. Skadhauge. 1985. Osmotic and hormonal responses to heat and dehydration in the fowl. J. Comp. Physiol. B 155:227–234. Arnason, S. S., G. E. Rice, A. Chadwick, and E. Skadhauge. 1986. Plasma levels of arginine vasotocin, prolactin, aldosterone, and corticosterone during prolonged dehydration in the domestic fowl: Effect of dietary NaCl. J. Comp. Physiol. B 156:383–397. Bonnet, S., P. A. Geraert, M. Lessire, B. Carrre, and S. Guillaumin. 1997. Effect of high ambient temperature on feed digestibility in broilers. Poult. Sci. 76:857–863. Cabanac, A. J., and M. Guillemette. 2001. Temperature and heart rate as stress indicators of handled common eider. Physiol. Behav. 74:475–479. Cabanac, M., and S. Aizawa. 2000. Fever and tachycardia in a bird (Gallus domesticus) after simple handling. Physiol. Behav. 69:541–545. Cooper, M. A., and K. W. Washburn. 1998. The relationships of body temperature to weight gain, feed consumption, and feed utilization in broilers under heat stress. Poult. Sci. 77:237–242. 188 Giloh et al. Darras, V. M., S. P. Kotanen, K. L. Geris, L. R. Berghman, and E. R. Kühn. 1996. Plasma thyroid hormone concentrations and iodothyronine deiodinase activity following an acute glucocorticoid challenge in embryonic compared with posthatch chickens. Gen. Comp. Endocrinol. 104:203–212. Donkoh, A. 1989. Ambient temperature: A factor affecting performance and physiological response of broiler chickens. Int. J. Biometeorol. 33:259–265. Dozier, W. A., B. D. Lott, and S. Branton. 2005. Growth responses of male broilers subjected to increasing air velocities at high ambient temperatures and a high dew point. Poult. Sci. 84:962–966. Etches, R. J., and T. M. John. 1995. Behavioral, physiological, neuroendocrine, and molecular responses to heat stress. Pages 31–66 in Poultry Production in Hot Climates. N. J. Daghir, ed. CAB International, Cambridge, UK. Gabarrou, J. F., C. Duchamp, J. Williams, and P. A. Géraert. 1997. A role for thyroid hormones in the regulation of diet-induced thermogenesis in birds. Br. J. Nutr. 78:963–973. Garriga, C., R. H. Richard, A. Concepcio, J. M. Planas, M. A. Mitchell, and M. Moreto. 2006. Heat stress increases apical glucose transport in the chicken jejunum. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290:R195–201. Geraert, P. A., J. C. F. Padilha, and S. Guillaumin. 1996. Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: Growth performance, body composition, and energy retention. Br. J. Nutr. 75:195–204. Havenstein, G. B., P. R. Ferket, and M. A. Qureshi. 2003a. Growth, livability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult. Sci. 82:1500–1508. Havenstein, G. B., P. R. Ferket, and M. A. Qureshi. 2003b. Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult. Sci. 82:1509–1518. Hillman, P. E., N. R. Scott, and A. Van Tienhoven. 1985. Physiological responses and adaptations to hot and cold environments. Pages 27–71 in Stress Physiology in Livestock. M. K. Yousef, ed. CRC Press Inc., Boca Raton, FL. Horowitz, M. 1998. Do cellular heat acclimation responses modulate central thermoregulatory activity? News Physiol. Sci. 13:218– 225. Iqbal, A., I. E. Decuypere, A. Abd El Azim, and E. R. Kühn. 1990. Pre- and posthatch high temperature exposure affects the thyroid hormones and corticosterone response to acute heat stress in growing chicken (Gallus domesticus). J. Therm. Biol. 15:149– 153. Kastberger, G., and R. Stachl. 2003. Infrared imaging technology and biological applications. Behav. Res. Methods Instrum. Comput. 35:429–439. Koike, T. I., L. R. Pryor, H. L. Neldon, and R. S. Venable. 1977. Effect of water deprivation on plasma radioimmunoassay of arginine vasotocin in conscious chickens (Gallus domesticus). Gen. Comp. Endocrinol. 33:359–364. Kühn, E. R., E. Decuypere, and P. Rudas. 1984. Hormonal and environmental interactions on thyroid function in the chick embryo and posthatching chickens. J. Exp. Zool. 232:653–658. McNabb, F., and D. B. King. 1993. Thyroid hormone effects on growth development and metabolism. Pages 393–417 in The Endocrinology of Growth Development and Metabolism in Vertebrates. M. P. Schreibman, C. G. Scanes, and P. K. T. Pang, ed. Academic Press, New York, NY. Mitchell, B. W. 1981. Effect of handling and temperature stress on the heart rate, EKG, and body temperature of chickens. ASAE Paper No. 81–4543. ASAE, St. Joseph, MI. NRC (National Research Council). 1994. Nutrient Requirements of Poultry. 9th ed. Nat. Acad. of Sci., Washington, DC. Porter, W. P., and D. M. Gates. 1969. Thermodynamic equilibria of animals with environment. Ecol. Monogr. 39:227–244. Ring, E. F. J., and K. Ammer. 2000. The technique of infrared imaging in medicine. Thermol. Int. 10:7–14. Saito, N., and R. Grossman. 1998. Effect of short-term dehydration on plasma osmolality, levels of arginine vasotocin, and its hypothalamic gene expression in the laying hen. Comp. Biochem. Physiol. 121A:235–239. Silva, J. E. 2006. Thermogeneic mechanisms and their hormonal regulation. Physiological Rev. 86:435–464. Stallone, J. N., and E. J. Braun. 1985. Contributions of glomerular and tubular mechanisms to antidiuresis in conscious domestic fowl. Am. J. Physiol. Renal Physiol. 249:F842–F850. Tanaka, K., K. Goto, T. Yoshioka, T. Terao, and O. Koga. 1984. Changes in the plasma concentrations of immunoreactive arginine vasotocin during oviposition in the domestic fowl. Br. Poult. Sci. 25:589–595. Tao, X., Z. Y. Zhang, H. Dong, H. Zhang, and H. Xin. 2006. Responses of thyroid hormones of market-size broilers to thermoneutral constant and warm cyclic temperatures. Poult. Sci. 85:1520–1528. Tracy, C. R. 1972. Newton’s Law: Its application for expressing heat losses from homeotherms. Bioscience 22:656–659. Turnpenny, J. R., A. J. McArthur, J. A. Clark, and C. M. Wathes. 2000. Thermal balance of livestock. 1. A parsimonious model . Agric. For. Meteorol. 101:5–27. Vianna, D. M. L., and P. Carrive. 2005. Changes in cutaneous and body temperature during and after conditioned fear to context in the rat. Eur. J. Neurosci. 21:2505–2512. 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. 2000. Domestic fowl—Strategies to confront environmental conditions. Avian Poult. Biol. Rev. 11:81–95. Yahav, S., S. Goldfeld, I. Plavnik, and S. Hurwitz. 1995. Physiological responses of chickens and turkeys to relative humidity during exposure to high ambient temperature. J. Therm. Biol. 20:245–253. 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., and I. Plavnik. 1999. Effect of early-age thermal conditioning and food restriction on performance and thermotolerance of male broiler chickens. Br. Poult. Sci. 40:120–126. 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., D. Shinder, M. Ruzal, M. Giloh, and Y. Piestun. 2009. Controlling body temperature—The opportunities for highly productive domestic fowl. Pages 65–98 in Body Temperature Regulation. A. B. Cisneros, and B. L. Gions, ed. Nova Science, Hauppauge, NY. Yahav, S., D. Shinder, J. Tanny, and S. Cohen. 2005. Sensible heat loss: The broiler’s paradox. World’s Poult. Sci. J. 61:419–434. Yahav, S., A. Straschnow, D. Luger, D. Shinder, J. Tanny, and S. Cohen. 2004. Ventilation, sensible heat loss, broiler energy, and water balance under harsh environmental conditions. Poult. Sci. 83:253–258. Zontak, A., S. Sideman, O. Verbitsky, and R. Beyar. 1998. Dynamic thermography: Analysis of hand temperature during exercise. Ann. Biomed. Eng. 26:988–993.