Effect of ambient temperature and light intensity on physiological

0 downloads 19 Views 715KB Size Report
that vary from the thermoneutral zone to determine ... der of the grow-out period. ... many studies have been conducted to evaluate the ef- .... We have previously used ... Influence of temperature and light intensity on plasma pH and HCO3 .... (Hb) and hematocrit (Hct) of heavy broiler chickens. Item. Hb (g/dL). Hct (%). 21 d.

Effect of ambient temperature and light intensity on physiological reactions of heavy broiler chickens1 H. A. Olanrewaju,2 J. L. Purswell, S. D. Collier, and S. L. Branton USDA, Agricultural Research Service, Poultry Research Unit, PO Box 5367, Mississippi State, MS 39762-5367 ABSTRACT The effects of ambient temperature, light intensity, and their interaction on blood acid-base balance, metabolites, and electrolytes in broiler chickens under environmentally controlled conditions were examined in 2 trials. The experiment consisted of a factorial arrangement of treatments in a randomized complete block design. The 9 treatments consisted of 3 levels of temperatures (low = 15.6°C; moderate = 21.1°C; high = 26.7°C) from 21 to 56 d of age and 3 levels of light intensities (0.5, 3.0, 20 lx) from 8 to 56 d of age at 50% RH. A total of 540 Ross 708 chicks were randomly distributed into 9 environmentally controlled chambers (30 male and 30 female chicks/chamber) at 1 d of age. Feed and water were provided ad libitum. Venous blood samples were collected on d 21 (baseline), 28, 42, and 56. High ambient temperature significantly (P ≤ 0.05) reduced BW, partial pressure of CO2, bicar-

bonate, hematocrit, hemoglobin, K+, and Na+ along with significantly (P ≤ 0.05) elevated pH level, Cl−, glucose, osmolality, and anion gap concentrations. Partial pressure of O2 was slightly increased in response to increased ambient temperature. There was no effect of light intensity on most of the blood variables examined. Acid-base regulation during high ambient temperature and light intensity exposure did not deteriorate despite a lower partial pressure of CO2, which consequently increased blood pH because of a compensatory decrease in HCO3− concentration. Plasma corticosterone was not affected by temperature, light intensity, or their interaction. These results indicate that continuous exposure of broiler chickens to varying light intensities had a minor effect on physiological blood variables, whereas high ambient temperature markedly affected various blood variables without inducing stress in broilers.

Key words: temperature, light intensity, acid-base balance, broiler, well-being 2010 Poultry Science 89:2668–2677 doi:10.3382/ps.2010-00806

INTRODUCTION International animal welfare concerns have included the effects of temperature and lighting programs on broilers (Food Marketing Institute and National Council of Chain Restaurants, 2003; National Chicken Council, 2005). Research development in poultry production has been displayed through the genetic selection of breeds for high productivity. However, this genetic potential will not be fully realized until microenvironmental constraints (temperature, humidity, light intensity, air velocity, etc.) have been fully addressed. It has been reported that during heat stress, behavioral, physiological, hormonal, and molecular adjustments can occur (Etches et al., 1995; Nalini et al., 2008). Exposure of poultry to ambient temperatures outside the thermoneutral zone during the course of production may adversely ©2010 Poultry Science Association Inc. Received March 26, 2010. Accepted September 19, 2010. 1 Mention of trade names or commercial products in this publication is solely for providing specific information and does not imply recommendation or endorsement by the USDA. 2 Corresponding author: [email protected]

affect production [BW, BW gain (BWG), and feed conversion ratio (FCR)] efficiency, meat yield, immune response, and mortality (Washburn, 1985; Howlinder and Rose, 1989). Heavy broilers (>2.5 kg) may need to be grown under lower ambient temperature than previously reported because of their higher BW and metabolic rates. The body temperature of an adult chicken is 40.6 to 41.7°C, and the thermoneutral zone that allows chickens to maintain their body temperature is 18 to 24°C. However, under high ambient temperature, fast-growing broilers of heavy BW are particularly susceptible to heat stress because of their high level of production. The highest and lowest temperatures that are critical for optimal performance are dependent on bird age, BW, housing system, feeding level, RH, air velocity, and overall health. In the southern United States and in many countries of the world, especially those in tropical regions that are characteristically hot and humid, broiler chickens are often maintained at ambient temperatures above the thermoneutral zone. In these areas where high ambient temperatures are prevalent for most of the year, further studies are required to elucidate the responses of modern broilers to temperatures that vary from the thermoneutral zone to determine

2668

TEMPERATURE, LIGHT INTENSITY, AND ACID-BASE BALANCE

temperature levels and light intensities that may limit production. Chickens raised where ambient temperature is high have higher energy needs than those that are in thermoneutral environments. Major losses result from a less efficient conversion of feed to meat, which detrimentally affects poultry health and productivity. It is estimated that a 1% improvement in feed conversion would save US poultry producers more than $50 million/yr. Light management is also an important factor affecting broiler production. Most modern lighting programs begin with a high light intensity (approximately 20 lx) that is decreased to approximately 5 lx by 14 to 21 d, and is then maintained at 5 lx or less for the remainder of the grow-out period. However, a wide variety of lighting programs currently exist that take into account light wavelength, intensity, duration, and the various devices for their regulation that are available to poultry producers. Each program possesses its own characteristics and applicability to rearing poultry. Although we have a good understanding of how photoperiod affects poultry production, our knowledge of how light intensity affects poultry production is shallow by comparison. These deficiencies, as well as the associated financial losses, have led to an increased interest in developing management techniques that will maximize broiler productivity while minimizing other associated problems. As such, poultry house ambient conditions along with adequate management strategies affect productivity and livability of poultry. The potential for changing temperature and light intensity to influence broiler productivity and health is under considerable investigation. Therefore, it is important to determine the levels of the various ambient factors in poultry houses that can influence the genetic growth potential in poultry (Xin et al., 1994; Gates et al., 1998). An evaluation of blood pH, electrolytes, blood gases, and metabolites could elucidate acid-base disturbances and differentiate between metabolic and respiratory disorders in broilers exposed to fluctuations in factors controlling ambient environmental conditions (Lin et al., 2000). Although many studies have been conducted to evaluate the effect of the thermal environment in birds (Borges et al., 2004, Rahimi, 2005), still more studies are necessary to examine the interrelationship of temperature and light intensity in affecting the mechanisms that control the physiology of the bird (acid-base balance, electrolytes, metabolites, endocrine system). Determination of these factors is essential so that therapeutic or nutritional strategies can be applied to reduce these negative effects and thereby optimize the environment in broiler houses to maximize the genetic potential of birds while reducing production costs. The objective of the present study was to evaluate the specific effects of ambient temperature, light intensity, and their interaction on various key physiological parameters in heavy broiler chickens.

2669

MATERIALS AND METHODS Bird Husbandry In each of 2 trials, with each lasting 8 wk, a total of 540 one-day-old Ross 708 (Aviagen Inc., Huntsville, AL) chicks were purchased from a commercial hatchery, and on arrival, the chicks were sexed and then group weighed. Chicks were randomly distributed into 9 environmentally controlled chambers (30 males and 30 females chicks/chamber). Each environmentally controlled chamber had a floor area of 6 m2 (2.3 m width × 2.6 m depth) with a chamber volume of 15.3 m3 (2.5 m height). Chicks were vaccinated for Marek’s, Newcastle, and infectious bronchitis diseases at the hatchery. At 12 d of age, birds received a Gumboro vaccination via water administration. Each chamber contained fresh pine shavings at a depth of 7.62, tube feeders, and a 7-nipple watering system. Birds were provided a 4-phase feeding program (starter: 1 to 14 d; grower: 15 to 28 d; finisher: 29 to 42 d; withdrawal: 43 to 56). Diets were formulated to meet or exceed NRC (1994) nutrient recommendations. Starter feed was provided as crumbles, and subsequent feeds were provided as whole pellets. Feed and water were offered ad libitum. Ambient temperature was maintained at 33°C at the beginning of experimentation and was reduced as the birds progressed in age until d 22, when temperature treatments started.

Experimental Treatments The experiment consisted of a factorial arrangement of treatments in a randomized complete block design. The treatments consisted of 3 levels of temperature (low = 15.6°C; moderate = 21.1°C; high = 26.7°C) from d 21 to 56 d of age and 3 levels of light intensity (0.5, 3.0, 20 lx) from 8 to 56 d of age at 50% RH. There were 3 different chambers for each temperature treatment along with 3 different chambers for each light intensity treatment, for a total of 9 chambers. Each of the 3 temperature level treatments was paired with 1 of the 3 light intensity treatments so that each chamber represented a particular temperature:light intensity level combination. The ambient temperatures in each temperature treatment were stepped down so that they decreased linearly every day from 33°C at 1 d of age to reach their targeted temperatures of 26.7, 21.1, and 15.6°C, respectively, by d 21, and were continued through 56 d of age (Figure 1). The light intensity from d 1 to 7 was 20 lx in each chamber. Each chamber was equipped with incandescent lighting, typical of that used in commercial housing. Light intensity settings were verified at the bird level (30 cm) by using a photometric sensor with National Institute of Standards and Technology-traceable calibration (403125, Extech Instruments, Waltham, MA) for each intensity adjustment. The light fittings and tubes were dusted weekly to minimize dust buildup, which would otherwise reduce the intensity.

2670

Olanrewaju et al.

Blood Collections and Chemical Analyses On d 21 (day before initiation of the treatments), 28, 42, and 56, blood samples were collected between 0800 and 0900 h on sampling day from a brachial vein of 6 (3 male and 3 female chicks/chamber) randomly selected birds from each chamber, and the birds were then returned to the appropriate chambers by using our standard handling procedure (Olanrewaju et al., 2008). In addition, unnecessary discomfort to the birds was avoided by using proper housing and handling techniques, as described by the NRC (1996). Blood samples (3 mL) were collected directly into heparinized (50 IU/ mL) monovette syringes. All bleedings were completed within 45 s after birds were caught. Blood samples were drawn directly from the syringes into a blood gas electrolyte analyzer (ABL-80 Flex, Radiometer America, Westlake, OH) for immediate analysis of partial pressure of CO2 (pCO2), partial pressure of O2 (pO2), pH, hematocrit (Hct), hemoglobin (Hb), and electrolytes (Na+, K+, Ca2+, HCO3−, and Cl−). In addition, immediate glucose (GLU), osmolality (mOsm), and anion gap were analyzed. The pH, pCO2, pO2, and HCO3− values were corrected to reflect a body temperature of 41.5°C (Burnett and Noonan, 1974). The mean corpuscular Hb concentration was calculated using the standard formula [(Hb × 100)/Hct]. The needle mounted on each monovette syringe was then removed, a cap was placed over the needle port, and the syringes containing the blood samples were plunged into ice. After

all birds were bled, the iced samples were transferred to the laboratory and centrifuged at 4,000 × g for 20 min at 4°C, and the packed blood cells were expelled from the syringes. The plunger on each monovette was broken off and the syringe served as a storage vial for the remaining plasma. This procedure ensured that the plasma samples were never exposed to ambient air. Plasma samples were stored at −20°C for later chemical analysis. Plasma samples were removed from the freezer, thawed, and analyzed for corticosterone (CS) using a universal microplate spectrophotometer (BioTek Instruments Inc., Winooski, VT) with ELISA reagent assay test kits from Assay Designs (EIA-CS Kit, Assay Designs Inc., Ann Arbor, MI), according to the manufacturer’s instructions. We have previously used this methodology of the kit as it relates to the manufacturer’s instructions in broilers (Olanrewaju et al., 2006, 2008).

Heart and Blood Collections for Analysis On d 56 at the end of each trial, 10 (5 males and 5 females) birds were randomly selected from each chamber. The birds were weighed individually, and rectal temperatures (RT) were measured using a thermocouple digital thermometer (accuracy of ±0.1°C; VWRTraceable, Friendswood, TX). After inserting the thermometer, the temperature was allowed to stabilize for 30 s before the reading was obtained. Immediately after temperature measurement, blood samples (3 mL) were

Figure 1. Ambient temperature treatments stepped down to decrease linearly every day from 33°C at 1 d of age to reach the targeted temperatures of 26.7, 21.1, and 15.6°C, respectively, on d 21 through 56 d of age.

2671

TEMPERATURE, LIGHT INTENSITY, AND ACID-BASE BALANCE −

Table 1. Influence of temperature and light intensity on plasma pH and HCO3 of heavy broiler chickens HCO3− (mm of Hg)

pH Item

21 d

28 d

42 d

56 d

Temperature treatment (°C)   Low (15.6)    Moderate (21.1)    High (26.7)  Intensity treatment    0.5 lx     3.0 lx     20 lx   SEM1       Temperature-light intensity treatment   Low-0.5 lx    Low-3.0 lx    Low-20 lx    Moderate-0.5 lx    Moderate-3.0 lx    Moderate-20 lx    High-0.5 lx    High-3.0 lx    High-20 lx  SEM2    

  7.35 7.37 7.37   7.36 7.38 7.36 0.016     7.33 7.38 7.34 7.35 7.39 7.37 7.39 7.35 7.37 0.022  

  7.37 7.39 7.38   7.38 7.39 7.38 0.015     7.36 7.41 7.35 7.38 7.40 7.38 7.38 7.36 7.40 0.020  

  7.35 7.37 7.37   7.36 7.37 7.37 0.015     7.34 7.37 7.35 7.37 7.38 7.36 7.35 7.35 7.40 0.026  

  7.36b 7.38ab 7.40a   7.38 7.39 7.37 0.008     7.35 7.37 7.37 7.38 7.38 7.37 7.41 7.41 7.38 0.038  

Source of variation   Temperature    Light intensity    Temperature × light intensity

0.412 0.608 0.276

0.712 0.566 0.231

0.729 0.845 0.587

0.047 0.915 0.967

                                            P-value      

21 d

28 d

42 d

56 d

  25.86 26.17 26.47   25.98 26.67 25.85 0.424     24.96 26.94 25.68 25.70 26.63 26.18 27.28 26.44 25.40 0.734  

  26.30 26.01 25.84   26.05 26.62 25.47 0.382     25.32 27.30 26.27 26.63 26.59 24.82 26.21 25.97 25.33 0.662  

  26.18a 25.80a 24.04b   25.44 25.65 24.93 0.401     25.99 26.92 25.62 26.32 25.71 25.37 24.00 24.33 23.79 0.695  

  26.42a 26.08ab 23.85b   25.64 25.43 25.28 0.709     26.36 26.74 26.15 26.63 26.31 25.31 23.93 29.23 24.39 1.227  

0.609 0.381 0.384

0.701 0.161 0.295

0.010 0.453 0.838

0.051 0.938 0.891

a,bMeans

within a column and effect that lack common superscripts differ significantly (P ≤ 0.05). SEM for main effects (n = 6). 2Pooled SEM for interaction effect (n = 2). 1Pooled

collected directly into heparinized (50 IU/mL) monovette syringes, as stated above for plasma analysis of cholesterol (CHOL), triglycerides (TRIG), total protein (TP), and high-density lipoprotein (HDL) using an autoanalyzer (Vitro DT 6011, Ortho-Clinical Diagnostic, Rochester, NY). This analyzer uses the enzymatic procedures described by Elliott (1984). Subsequently, birds were euthanatized by cervical dislocation according to the Animal Care and Ethics Committeeapproved blood sampling and organ collection procedures. The chest was opened and the heart was removed and the atria, great vessels, and epicardial fat were trimmed off. The weight of the total heart was determined and calculation of the BW:total heart ratio was determined.

Statistical Analysis A 3 × 3 factorial data analysis arranged in a randomized complete block design was used in this study. Data were replicated over time, with trial being the blocking factor. Chamber was considered the experimental unit. The 9 treatments consisted of 3 levels of temperature × 3 levels of light intensity. The main effects of temperature and light intensity and the interaction of these 2 factors on physiological variables were tested using the MIXED procedure of SAS software (SAS Institute, 2004). Means comparisons on d 21, 28, 42, and 56 were

assessed by least significant differences, and statements of significance were based on P ≤ 0.05.

RESULTS Table 1 shows the effect of ambient temperature exposure, light intensity, and their interaction on plasma pH and HCO3−. In comparison with low ambient temperature, high ambient temperature significantly increased pH on d 56 (P ≤ 0.0465). The main effect of light intensity on pH was not observed on any of the sampling days. Furthermore, high ambient temperature significantly reduced HCO3− on d 42 (P ≤ 0.0097) and d 56 (P ≤ 0.0510). However, there was no main effect of light intensity on HCO3− on any of the sampling days. No significant temperature × light intensity interaction for pH or HCO3− was found on any of the sampling days. High ambient temperature caused a significant decrease in pCO2 on d 28 (P ≤ 0.0030), d 42 (P ≤ 0.0526), and d 56 (P ≤ 0.0021) in comparison with low and moderate ambient temperatures (Table 2). No effects of temperature or light intensity on pO2 were found on any of the sampling days. No significant temperature × light intensity interaction for either pCO2 or pO2 was found on any of the sampling days. As shown in Table 3, high ambient temperature significantly decreased Hb (P ≤ 0.0098, P ≤ 0.0541) and Hct (P ≤ 0.0086, P ≤ 0.0408) on d 42 and 56, respec-

2672

Olanrewaju et al.

tively. No effect of light intensity on Hb and Hct was found on any of the sampling days. Table 4 shows the influence of temperature and light intensity on plasma Na+ and Cl−. High ambient temperature significantly reduced plasma Na+ levels from d 21 (P ≤ 0.0002) through d 56 (P ≤ 0.0001). In addition, high ambient temperature significantly increased Cl− on d 56 (P ≤ 0.0146). No effect of light intensity on plasma Na+ and Cl− was found on any of the sampling days. No temperature × light intensity interaction for either plasma Na+ or Cl− was found on any of the sampling days. No main effects on Ca2+ or interactions were due to temperature or light intensity on any of the sampling days (data not shown). Table 5 shows the influence of temperature and light intensity on plasma K+ and mOsm. High ambient temperature caused a significant decrease in plasma K+ on d 42 (P ≤ 0.0024) and d 56 (P ≤ 0.0015) compared with low and moderate ambient temperatures. High ambient temperature also significantly increased plasma mOsm levels from d 21 (P ≤ 0.0005) through d 56 (P ≤ 0.0027). No significant temperature × light intensity interaction for plasma K+ or plasma mOsm was found on any of the sampling days. The effects of temperature and light intensity on plasma GLU and CS are presented in Table 6. High ambient temperature caused a significant increase in plasma GLU concentration on d 42 (P ≤ 0.0002) and on d 56 (P ≤ 0.0009) compared with low and moderate

ambient temperatures. The high (20 lx) light intensity significantly increased plasma GLU concentration on d 56 (P ≤ 0.0369). Corticosterone concentrations were not significantly affected by the temperature and light treatments or their interaction on any of the sampling days in the present study. As shown in Table 7, there was a main effect of temperature on BW, RT, CHOL, TRIG, HDL, and plasma TP on d 56 of age. At d 56, high ambient temperature significantly reduced BW (P ≤ 0.0001), HDL (P ≤ 0.0001), and TP (P ≤ 0.0002), whereas it increased RT (P ≤ 0.0001), CHOL (P ≤ 0.0001), and TRIG (P ≤ 0.0004) compared with low and medium ambient temperatures. Furthermore, on d 56, there was a significant main effect of light intensity on TRIG (P ≤ 0.0010) and HDL (P ≤ 0.0078). Temperature and light intensity also had an interaction effect on BW (P ≤ 0.0158), RT (P ≤ 0.0497), TRIG (P ≤ 0.0216), HDL (P ≤ 0.0001), and TRIG:HDL (P ≤ 0.0001) on d 56.

DISCUSSION The principal organ systems used in acid-base homeostasis in birds are the lungs and kidneys, and these are supported by the gastrointestinal tract (Long, 1982). The cardiovascular system also participates in thermoregulatory processes through modulation of heat dissipation on the one hand, and by oxygen transport

Table 2. Influence of temperature and light intensity on plasma partial pressure of CO2 (pCO2) and partial pressure of O2 (pO2) of heavy broiler chickens pCO2 (mm of Hg) Item Temperature treatment (°C)   Low (15.6)    Moderate (21.1)    High (26.7)  Intensity treatment    0.5 lx     3.0 lx     20 lx   SEM1       Temperature-light intensity treatment   Low-0.5 lx    Low-3.0 lx    Low-20 lx    Moderate-0.5 lx    Moderate-3.0 lx    Moderate-20 lx    High-0.5 lx    High-3.0 lx    High-20 lx  SEM2       Source of variation   Temperature    Light intensity    Temperature × light intensity a,bMeans

pO2 (mm of Hg)

21 d

28 d

42 d

56 d

  42.90 40.32 38.25   42.08 40.07 39.32 1.458     42.25 41.45 45.00 43.15 40.10 37.70 40.85 38.65 35.25 4.515  

  46.07a 44.33a 36.93b   42.32 42.05 42.97 1.408     45.65 43.80 48.75 46.30 43.60 43.10 35.00 38.75 37.05 2.439  

  44.63a 42.25a 37.62b   44.23 40.08 40.18 1.823     46.40 43.60 43.90 45.45 39.50 41.80 40.85 37.15 34.85 3.158  

  43.72a 42.25a 31.67b   39.45 38.35 39.83 1.804     44.85 43.00 43.30 42.10 39.40 45.25 31.40 32.65 30.95 3.125  

0.479 0.747 0.863

0.003 0.895 0.449

0.053 0.239 0.940

0.002 0.837 0.779

                                            P-value      

within a column and effect that lack common superscripts differ significantly (P ≤ 0.05). SEM for main effects (n = 6). 2Pooled SEM for interaction effect (n = 2). 1Pooled

21 d

28 d

42 d

56 d

  38.97 42.73 43.82   40.78 42.50 42.23 5.197     42.05 43.00 35.85 39.50 44.45 44.25 44.80 40.05 46.60 9.002  

  35.87 37.32 39.43   37.30 37.83 37.48 4.012     37.65 37.65 32.30 32.85 41.05 38.05 41.40 34.80 42.10 6.956  

  44.92 45.38 38.22   43.00 43.40 42.12 2.531     46.10 45.15 43.50 41.85 48.15 46.15 41.05 36.90 36.70 4.384  

  42.18 38.82 35.43   38.50 39.92 38.02 2.959     42.35 42.95 41.25 39.10 43.35 34.00 34.05 33.45 38.80 5.125  

0.792 0.969 0.940

0.823 0.996 0.776

0.136 0.935 0.779

0.319 0.896 0.711

2673

TEMPERATURE, LIGHT INTENSITY, AND ACID-BASE BALANCE

Table 3. Influence of temperature and light intensity on plasma hemoglobin (Hb) and hematocrit (Hct) of heavy broiler chickens Hb (g/dL)

Hct (%)

Item

21 d

28 d

42 d

56 d

21 d

Temperature treatment (°C)   Low (15.6)    Moderate (21.1)    High (26.7)  Intensity treatment    0.5 lx     3.0 lx     20 lx   SEM1       Temperature-light intensity treatment   Low-0.5 lx    Low-3.0 lx    Low-20 lx    Moderate-0.5 lx    Moderate-3.0 lx    Moderate-20 lx    High-0.5 lx    High-3.0 lx    High-20 lx  SEM2      

  7.46 7.15 7.36   7.46 7.13 7.37 0.173     7.57 7.42 7.39 7.30 6.93 7.21 7.51 7.06 7.50 0.299  

  7.30 7.21 7.17   7.20 7.24 7.24 0.156     6.93 7.38 7.61 7.27 7.29 7.07 7.41 7.05 7.06 0.270  

  8.25a 7.95ab 7.69b   8.00 8.05 7.84 0.099     8.49 8.23 8.02 7.68 8.01 8.17 7.82 7.92 7.33 0.171  

  8.32a 7.94ab 7.66b   7.96 7.98 7.97 0.165     8.10 8.36 8.51 7.99 7.99 7.83 7.80 7.60 7.58 0.285  

                                           

Source of variation   Temperature    Light intensity    Temperature × light intensity

0.460 0.426 0.953

0.834 0.975 0.378

0.010 0.329 0.072

0.054 0.996 0.800

     

  23.28 22.32 22.95   23.25 22.32 22.98 0.520     23.6 23.15 23.10 22.75 21.70 22.50 23.40 22.10 23.35 0.8998   P-value 0.443 0.457 0.963

28 d

42 d

56 d

  22.82 22.53 22.38   22.50 22.60 22.63 0.468     21.70 23.00 23.75 22.70 22.80 22.10 23.10 22.00 22.05 0.811  

  25.63a 24.75ab 23.95b   24.88 25.05 24.40 0.290     26.35 25.60 24.95 23.95 24.90 25.40 24.35 24.65 22.85 0.502  

  25.92a 24.73ab 23.88b   24.80 24.93 24.80 0.473     25.20 26.15 26.40 24.90 24.95 24.35 24.30 23.70 23.65 0.819  

0.806 0.978 0.372

0.009 0.305 0.067

0.041 0.974 0.760

a,bMeans

within a column and effect that lack common superscripts differ significantly (P ≤ 0.05). SEM for main effects (n = 6). 2Pooled SEM for interaction effect (n = 2). 1Pooled

Table 4. Influence of temperature and light intensity on plasma Na+ and Cl− of heavy broiler chickens Na+ (mEq/L) Item Temperature treatment (°C)   Low (15.6)    Moderate (21.1)    High (26.7)  Intensity treatment    0.5 lx     3.0 lx     20 lx   SEM1       Temperature-light intensity treatment   Low-0.5 lx    Low-3.0 lx    Low-20 lx    Moderate-0.5 lx    Moderate-3.0 lx    Moderate-20 lx    High-0.5 lx    High-3.0 lx    High-20 lx  SEM2       Source of variation    Temperature    Light intensity    Temperature × light intensity a,bMeans

21 d

28 d

42 d

  146.3a 146.1a 131.6b   141.2 141.3 141.5 1.691     146.7 145.7 146.4 146.0 145.9 146.4 130.8 132.2 131.9 2.929  

  146.3a 146.7a 131.5b   142.0 141.5 141.1 1.472     141.9 146.0 146.1 147.5 146.7 146.1 131.7 131.7 131.1 2.550  

  149.3a 150.3a 125.7b   141.6 141.4 142.4 1.874     144.1 149.3 154.6 151.8 150.4 148.8 129.0 124.5 123.8 3.245  

0.000 0.987 0.996

0.000 0.901 0.999

0.000 0.928 0.225

Cl− (mEq/L) 56 d     153.3a   151.1a   120.9b       143.0   141.5   140.8   1.724           153.1   153.5   153.4   151.8   150.9   150.6   124.3   120.1   118.3   2.9853       P-value 0.000 0.652 0.857

     

within a column and effect that lack common superscripts differ significantly (P ≤ 0.05). SEM for main effects (n = 6). 2Pooled SEM for interaction effect (n = 2). 1Pooled

21 d

28 d

42 d

56 d

  103.6 103.9 103.9   103.4 103.6 104.4 0.512     104.1 103.2 103.7 103.1 104.2 104.5 103.2 103.6 105.0 0.887  

  104.1 105.3 104.8   105.2 104.5 104.6 0.405     105.5 103.5 103.4 105.4 105.5 105.1 104.9 104.4 105.2 0.702  

  110.7 108.4 107.7   110.1 107.8 108.9 1.266     113.3 106.7 112.0 109.7 109.3 106.4 107.4 107.4 108.4 2.193  

  111.1ab 109.1b 113.6a   111.5 111.4 110.8 0.861     110.8 111.4 111.1 109.8 108.8 108.7 114.1 114.2 112.7 1.492  

0.919 0.445 0.696

0.177 0.371 0.450

0.281 0.454 0.364

0.015 0.815 0.959

2674

Olanrewaju et al.

Table 5. Influence of temperature and light intensity on plasma Ca2+ and osmolality (mOsm) of heavy broiler chickens K+ (mEq/L)

mOsm (mmol/kg)

Item

21 d

28 d

42 d

56 d

21 d

Temperature treatment (°C)   Low (15.6)    Moderate (21.1)    High (26.7)  Intensity treatment    0.5 lx     3.0 lx     20 lx   SEM1       Temperature-light intensity treatment   Low-0.5 lx    Low-3.0 lx    Low-20 lx    Moderate-0.5 lx    Moderate-3.0 lx    Moderate-20 lx    High-0.5 lx    High-3.0 lx    High-20 lx  SEM2      

  4.23 4.30 3.14   3.78 4.17 3.73 0.430     4.34 4.18 4.18 4.06 4.57 4.28 2.95 3.75 2.73 0.745  

  4.13 4.25 2.98   3.73 3.88 3.75 0.455     4.23 4.14 4.01 4.05 4.46 4.23 2.90 3.04 3.01 0.788  

  4.24a 4.38a 2.50b   3.30 4.02 3.80 0.2948     3.36 4.75 4.62 4.39 4.43 4.33 2.16 2.89 2.44 0.511  

  4.85a 4.85a 2.37b   4.01 4.17 3.89 0.373     4.92 5.05 4.58 4.64 5.13 4.77 2.47 2.34 2.31 0.646  

                                           

Source of variation    Temperature    Light intensity    Temperature × light intensity

0.158 0.743 0.947

0.151 0.968 0.998

0.002 0.262 0.662

0.002 0.863 0.986

     

28 d

42 d

56 d

  306.2b 305.5b 326.5a   312.8 312.6 312.8 2.660     307.7 305.2 305.8 305.6 305.0 306.0 325.1 327.7 326.7 4.608   P-value

  305.8b 306.0b 329.0a   313.8 314.0 313.1 2.123     308.2 304.9 304.2 306.9 306.1 305.1 326.3 330.9 329.9 3.676  

  318.4b 313.8b 325.5a   321.6 314.6 319.4 2.198     321.6 311.7 321.8 316.6 314.7 310.1 324.6 317.6 326.2 3.807  

  320.8b 316.4b 329.3a   322.0 312.3 323.2 1.862     320.1 320.8 321.4 317.4 315.9 316.0 328.5 327.1 332.2 3.225  

0.001 0.999 0.985

0.000 0.953 0.807

0.037 0.126 0.398

0.003 0.770 0.904

a,bMeans

within a column and effect that lack common superscripts differ significantly (P ≤ 0.05). SEM for main effects (n = 6). 2Pooled SEM for interaction effect (n = 2). 1Pooled

Table 6. Influence of temperature and light intensity on plasma glucose (GLU) and corticosterone (CS) of heavy broiler chickens GLU (mg/dL) Item Temperature treatment (°C)   Low (15.6)    Moderate (21.1)    High (26.7)  Intensity treatment    0.5 lx     3.0 lx     20 lx   SEM1       Temperature-light intensity treatment   Low-0.5 lx    Low-3.0 lx    Low-20 lx    Moderate-0.5 lx    Moderate-3.0 lx    Moderate-20 lx    High-0.5 lx    High-3.0 lx    High-20 lx  SEM2       Source of variation   Temperature    Light intensity    Temperature × light intensity a,bMeans

CS (pg/mL)

21 d

28 d

42 d

56 d

  246.8 240.6 246.6   250.3 245.0 238.6 8.134     258.9 248.9 232.6 244.9 237.6 239.5 247.3 248.7 243.8 14.088  

  234.0 226.0 251.3   238.0 241.1 232.2 7.577     251.7 232.2 218.2 214.2 230.2 233.7 248.1 261.1 244.9 13.124  

  236.5b 236.1b 270.9a   246.5 255.0 242.0 4.028     238.2 241.6 229.7 233.3 250.1 224.9 268.0 273.3 271.6 6.977  

  255.3b 257.5b 285.3a   260.8b 260.8b 276.4a 4.086     251.7 249.7 264.5 249.5 253.3 269.7 281.2 279.5 295.1 7.077  

0.835 0.611 0.911

0.105 0.711 0.386

0.000 0.122 0.544

21 d

28 d

42 d

56 d

      2,054   1,424   1,626       2,051   1,539   1,515   439           3,200   1,607   1,355   1,830   1,541   902   1,123   1,469   2,287   760.3     P-value

  1,239 1,074 1,208   1,168 1,242 1,111 194.9     1,376 1,047 1,296 774 1,645 804 1,355 1,033 1,234 337.5  

  1,763 1,585 1,770   1,830 1,498 1,790 308.4     2,129 1,351 1,808 1,463 1,254 2,038 1,899 1,888 1,524 535.1  

  1,655 1,838 2,917   2,207 2,066 1,938 421.6     1,462 1,725 1,477 1,778 1,888 1,848 3,148 2,586 2,489 731.2  

0.001   0.037   0.983  

within a column and effect that lack common superscripts differ significantly (P ≤ 0.05). SEM for main effects (n = 6). 2Pooled SEM for interaction effect (n = 2). 1Pooled

0.602 0.636 0.401

0.820 0.895 0.353

0.894 0.717 0.763

0.087 0.905 0.780

2675

TEMPERATURE, LIGHT INTENSITY, AND ACID-BASE BALANCE

on the other. In the present study, exposure of broilers to high ambient temperature significantly affected the acid-base balance, especially at 56 d of age. Exposure of modern heavy broilers to high ambient temperature with and without increased light intensity significantly increased pH, Cl−, mOsmo, GLU, CHOL, TRIG, Cl−, and RT, but significantly reduced pCO2, HCO3−, Hb, Hct, Na+, K+, TP, HDL, and BW at 56 d of age. However, exposure of modern heavy broilers to high ambient temperature with and without increased light intensity produced no significant effect on pO2, Ca2+, HW, HW:BW, TRIG:HDL, and CS. Disturbances in venous blood acid-base status (pCO2 and pH) reflecting thermal panting-induced hypocapnic alkalosis were observed frequently in the older birds, which may be attributed to relative differences in the body sizes of birds. This would suggest that thermoregulatory efforts (panting, CO2 elimination) might be greater in the older birds. The older broilers exhibited greater resting venous blood pCO2 tensions and were relatively more acidotic (hypercapnic acidosis). This may be due to age-dependent differences in ventilation rate or may reflect the consequences of an increased metabolic demand in the larger birds (Korte et al., 1999). Results suggest an increased respiratory rate in broilers exposed to the higher ambient temperature with or without increased light intensity. Birds exposed to high ambient temperature exhibited higher respira-

tory rates in an effort to dissipate heat by evaporation. Evaporative heat loss through panting is the most important mechanism used to control body temperature under heat stress (Robertshaw, 2006). The increased respiratory rate disrupted their acid-base balance because of excessive CO2 losses (Toyomizu et al., 2005). Decreases in circulating pCO2 cause a decrease in the concentrations of H2CO3 and H+. In response to this, the kidneys increase HCO3− excretion and reduce H+ excretion in an attempt to control the acid-base balance of the bird homeostatically. This change in acidbase balance is known as respiratory alkalosis (Bottje and Harrison 1985). Physiologically, the changes in systemic pH in response to heat stress are complex in that they involve an initial respiratory response phase, which may produce a systemic alkaloidosis and then a compensatory phenomenon involving homeostatic mechanisms that can produce systemic acidosis. This condition can be accentuated in big birds, as observed in this study. Exposure of broiler chickens to the 26.7°C ambient temperature treatment like this rather than the 15.6°C or 21.1°C temperatures resulted in a significant (P < 0.0001) depression in BW. Increased electrolyte excretions through urine and feces along with continuous loss of water through panting have been shown to further disrupt the acid-base balance (Belay et al., 1992). The degree of water loss in intracellular fluids has been associated with losses

Table 7. Influence of temperature and light intensity on BW, heart weight (HW), and hematological variables1 of heavy broiler chickens at 56 d of age Item

BW (kg)

HW (kg)

HW:BW (%)

RT (°C)

CHOL (mg/dL)

TRIG (mg/dL)

HDL (mg/dL)

TRIG: HDL

TP (g/dL)

Temperature treatment (°C)   Low (15.6)    Moderate (21.1)    High (26.7)  Light intensity treatment   0.5 lx     3.0 lx     20 lx   SEM2       Temperature-light intensity treatment   Low-0.5 lx    Low-3.0 lx    Low-20 lx    Moderate-0.5 lx    Moderate-3.0 lx    Moderate-20 lx    High-0.5 lx    High-3.0 lx    High-20 lx  SEM3      

  4.08a 3.92b 3.35c   3.81 3.78 3.76 0.065     4.07ab 3.95ab 4.24a 3.92ab 4.00ab 3.84b 3.44c 3.40c 3.20c 0.113  

  0.017 0.017 0.016   0.018 0.015 0.016 0.003     0.017 0.016 0.019 0.017 0.017 0.016 0.024 0.012 0.013 0.0004  

  0.415 0.427 0.491   0.522 0.388 0.423 0.087     0.410 0.389 0.445 0.443 0.420 0.417 0.713 0.354 0.408 0.151  

  40.9b 41.1b 41.6a   41.1 41.3 41.2 0.092     40.8c 41.1bc 40.9c 41.1bc 41.2abc 41.1abc 41.5ab 41.6a 41.6a 0.159  

  129.1b 126.4b 166.4a   137.0 149.7 135.1 5.508     131.9 131.9 123.4 114.4 141.2 123.5 164.7 176.1 158.4 9.540   P-value

  71.0b 97.9a 100.3a   102.8a 72.9b 93.5ab 7.812     80.2bcd 81.8bcd 56.8d 118.2ab 64.9cd 102.6abc 125.3a 86.5abcd 91.4abcd 13.531  

  137.8a 120.0a 78.7b   114.8ab 99.1b 122.6a 7.453     151.3ab 149.0ab 117.2bc 164.6a 97.6cd 151.0ab 86.1cd 82.4cd 67.6d 12.91  

  0.515 0.816 1.274   0.895 0.736 0.763 0.099     0.530b 0.549b 0.485b 0.718b 0.665b 0.679b 1.455a 1.050a 1.352a 0.171  

  3.59a 3.57a 3.34b   3.50 3.55 3.45 0.062     3.55 3.69 3.56 3.36 3.43 3.53 3.53 3.28 3.32 0.107  

Source of variation   Temperature    Light intensity    Temperature × light intensity

0.000 0.718 0.016

0.969 0.251 0.315

0.643 0.289 0.391

0.000 0.114 0.050

0.000 0.219 0.362

0.124 0.072 0.000

0.000 0.298 0.519

a–dMeans

0.000 0.001 0.022

0.000 0.008 0.000

within a column and effect that lack common superscripts differ significantly (P ≤ 0.05). = rectal temperature; CHOL = cholesterol; TRIG = triglycerides; HDL = high-density lipoprotein; TP = total protein. 2Pooled SEM for main effects (n = 6). 3Pooled SEM for interaction effect (n = 2). 1RT

2676

Olanrewaju et al.

K+.

of intracellular This loss of extracellular fluid has been linked to a loss in plasma Na+. Plasma Na+, K+, and Cl− levels were affected by heat stress in this study. Plasma K+ and Na+ concentrations are known to decrease as temperature rises (Belay and Teeter, 1993, Borges et al., 2003), whereas Cl− increases (Belay and Teeter, 1993). The increase in Cl− decreases H+ excretion and HCO3− reabsorption by the kidneys. This might contribute to blood acidification, which, in turn, seems to be an appropriate response to alkalosis. The plasma K+ and Na+ concentration results in the current study are consistent with these earlier reports. High ambient temperature also significantly affected plasma mineral balance and mineral concentrations of broilers in this study. It has been reported that Hct values can decrease with increasing rearing temperature (Kubena et al., 1972; Yahav and Hurwitz 1996). Hematological examinations in these studies have also proved that the total amount of Hb in blood can decrease with increased rearing temperature, which can result in lower metabolic rate, as shown by others (Donkoh, 1989; Jamadar and Jalnapurkar 1995). Concentrations of certain plasma hormones, enzymes, and metabolites such as CS have been suggested to be sensitive indicators of stress levels in broiler chickens (Puvadolpirod and Thaxton, 2000; Olanrewaju et al., 2006). Nonsignificant increases in plasma CS observed in the present study indicated that birds were not stressed. This nonsignificant increase in plasma CS was accompanied by increased concentrations of energy nutrients in sera, such as GLU, CHOL, and TRIG. The increase in plasma GLU concentration indicated stimulation of gluconeogenetic processes as a direct response to increased epinephrine, norepinephrine, and glucocorticoid secretion (Borges et al., 2003, 2004). Hyperthermia has been reported to induce hyperglycemia, whereas hypothermia can cause hypoglycemia in domestic fowl (Hazelwood 1976). Increases in GLU and HDL in response to increased light intensity may have stimulated increased physical activity in birds exposed to bright light (20 lx), with a subsequent increase in energy expenditure for activity rather than growth. Decreased levels of total plasma proteins in birds subjected to hot ambient temperature confirmed the role of CS as a proteolytic hormone (Khan et al., 2002; Kataria et al., 2008). Thus, it is suggested that at high ambient temperatures, a high degree of water loss caused by increased panting together with reduced drinking may lead to dehydration and increases in plasma mOsm (Yahav et al., 1995). Vo et al. (1978) have reported reductions in total plasma protein with increasing ambient temperature similar to those observed in this study. Evidence suggests that decreases in total plasma protein may also be indicative of increased heat stress in chickens (Kutlu and Forbes, 1993; Berrong and Washburn, 1998). Elevated body temperature may also occur in response to heat stress. In this study, RT increased similarly with increased ambient temperature. Ambient temperatures have a considerable influence on

the body temperatures of chickens, as shown by others (Huston 1965; Boone and Hughes 1971). Based on our finding, broilers raised under low and medium ambient temperatures performed better, as indicated by increased BW, and were healthier, as reflected in higher plasma HDL and TP and lower CHOL and TRIG, when compared with those raised under high ambient temperatures. In agreement with our findings, there is evidence that serum TRIG may be an independent risk factor for cardiovascular diseases (Hokanson and Austin, 1996; Jia et al., 2006). Elevated TRIG and low HDL are basic characteristics of a metabolic syndrome that is strongly associated with coronary heart disease (McLaughlin et al., 2003). Calculation of the TRIG:HDL ratio has been shown to be a good predictor of coronary heart disease (Barzi et al., 2005; Hadaegh et al., 2009). A low TRIG:HDL ratio is indicative of primarily large, nonatherogenic low-density lipoprotein particles, whereas a high TRIG:HDL ratio indicates a larger population of small, dense proatherogenic lowdensity lipoprotein particles (Dobiášová and Frohlich, 2001; Maruyama et al., 2003). It has been reported that the log concentration of TRIG:HDL can be used as an atherogenic index to indicate a balance between the actual concentrations of plasma TRIG and HDL, which may predetermine the direction of CHOL transport in the intravascular volume pool (Dobiášová and Frohlich, 2001). Studies have been conducted to examine the effect of high temperature on the thermal levels within birds (Borges et al., 2004; Rahimi, 2005). However, the modulations of the physiological mechanisms involved are poorly understood. The results of this study supplement current knowledge of the hematology and biochemistry of plasma in modern chickens with heavy BW during the growth period and provide warning that even relatively small changes in the ambient temperature from the thermoneutral zone (18 to 24°C) can have a negative effect on their metabolism and performance. In addition, the high ambient temperatures and light intensities used in this study apparently did not act together or separately to affect plasma CS, suggesting that these factors may not be stressors to modern heavy broiler chickens.

ACKNOWLEDGMENTS The authors thank Larry N. Halford and M. Robinson (both of the USDA Poultry Research Unit) for their contributions to this study.

REFERENCES Barzi, F., A. Patel, M. Woodward, C. M. Lawes, T. Ohkubo, and D. Gu. 2005. A comparison of lipid variables as predictors of cardiovascular disease in the Asia Pacific region. Ann. Epidemiol. 15:405–413. Belay, T., C. J. Wiernusz, and R. G. Teeter. 1992. Mineral balance and urinary and fecal mineral excretion profile of broilers housed in thermoneutral and heat-distressed environment. Poult. Sci. 71:1043–1047.

TEMPERATURE, LIGHT INTENSITY, AND ACID-BASE BALANCE Belay, T., and R. G. Teeter. 1993. Broiler water balance and thermobalance during thermoneutral and high ambient temperature exposure. Poult. Sci. 72:116–124. Berrong, S. L., and K. W. Washburn. 1998. Effects of genetic variation on total plasma protein, body weight gains, and body temperature responses to heat stress. Poult. Sci. 77:379–385. Boone, M. A., and B. L. Hughes. 1971. Effect of heat stress on laying and non-laying hens. Poult. Sci. 50:473–477. Borges, S. A., A. V. Fischer da Silva, A. Maiorka, D. M. Hooge, and K. R. Cummings. 2004. Effects of diet and cyclic daily heat stress on electrolyte, nitrogen and water intake, excretion and retention by colostomized male broiler chickens. Int. J. Poult. Sci. 3:313–321. Borges, S. A., A. V. Fischer da Silva, J. Ariki, D. M. Hooge, and K. R. Cummings. 2003. Dietary electrolyte balance for broiler chickens under moderately high ambient temperatures and relative humidities. Poult. Sci. 82:301–308. Bottje, W. G., and P. C. Harrison. 1985. The effect of tap water, carbonated water, sodium bicarbonate and calcium chloride on blood acid-base balance in cockerels subjected to heat stress. Poult. Sci. 64:107–113. Burnett, R. W., and D. C. Noonan. 1974. Calculations and correction factors used in determination of blood pH and blood gases. Clin. Chem. 20:1499–1506. Dobiášová, M., and J. Frohlich. 2001. The plasma parameter log (TG/HDL-C) as an atherogenic index: Correlation with lipoprotein particle size and esterification rate in apoB-lipoprotein-depleted plasma (FERHDL). Clin. Biochem. 34:583–588. Donkoh, A. 1989. Ambient temperature: A factor affecting performance and physiological response of broiler chickens. Int. J. Biometeorol. 33:259–265. Elliott, R. J. 1984. Physicians and computers. Ektachem DT-60 analyzer. Physician’s Lead. 2:6–13. Etches, R., J. M. John, and A. M. V. Gibbins. 1995. Behavioural, physiological, neuroendocrine and molecular responses to heat stress. Pages 31–65 in Poultry Production in Hot Climates. N. J. Daghir, ed. CAB International, Wallingford, UK. Food Marketing Institute and National Council of Chain Restaurants. 2003. FMI-NCCR Animal Welfare Program. Food Marketing Inst., Washington, DC. Gates, R. S., H. Zhang, D. G. Colliver, and D. G. Overhults. 1998. Regional variation in temperature humidity index for poultry housing. Trans. ASAE 38:197–205. Hadaegh, F., D. Khalili, A. Ghasemi, M. Tohidi, F. Sheikholeslami, and F. Azizi. 2009. Triglyceride/HDL-cholesterol ratio is an independent predictor for coronary heart disease in a population of Iranian men. Nutr. Metab. Cardiovasc. Dis. 19:401–408. Hazelwood, R. L. 1976. Carbohydrate metabolism. Pages 220–232 in Avian Physiology. 3rd ed. P. D. Sturkie, ed. Springer, New York, NY. Hokanson, J. E., and M. A. Austin. 1996. Plasma triglyceride level is a risk factor for cardiovascular disease independent of high-density lipoprotein cholesterol level: A meta-analysis of population based prospective studies. J. Cardiovasc. Risk 3:213–219. Howlinder, M. A. R., and S. P. Rose. 1989. Rearing temperature and meat yield of broilers. Br. Poult. Sci. 30:61–67. Huston, T. M. 1965. The influence of different environmental temperatures on immature fowl. Poult. Sci. 44:1032–1036. Jamadar, S. J., and B. V. Jalnapurkar. 1995. Effect of high ambient temperature on iron status of broilers. Indian Vet. J. 72:577– 579. Jia, L., S. Long, M. Fu, B. Yan, Y. Tian, and Y. Xu. 2006. Relationship between total cholesterol/high-density lipoprotein cholesterol ratio, triglyceride/high-density lipoprotein cholesterol ratio, and high-density lipoprotein subclasses. Metabolism 55:1141–1148. Kataria, N., A. K. Kataria, and A. K. Gahlot. 2008. Ambient temperature associated variations in serum hormones and interrelated analytes of broiler chickens in arid tract. Slov. Vet. Res. 45:127–134. Khan, W. A., A. Khan, A. D. Anjuman, and Z. U. Rehman. 2002. Effects of induced heat stress on some biochemical values in broiler chicks. Int. J. Agric. Biol. 4:74–75. Korte, S. M., A. Sgoifo, W. Ruesink, C. Kwakernaak, S. van Voorst, C. W. Scheele, and H. J. Blokhuis. 1999. High carbon dioxide

2677

tension (pCO2) and the incidence of cardiac arrhythmias in rapidly growing broiler chickens. Vet. Rec. 145:40–43. Kubena, L. F., J. D. May, F. N. Reece, and J. W. Deaton. 1972. Hematocrit and hemoglobin levels of broilers as influenced by environmental temperature and dietary iron level. Poult. Sci. 51:759–763. Kutlu, H. R., and J. M. Forbes. 1993. Changes in growth and blood parameters in heat stressed broiler chicks in response to dietary ascorbic acid. Livest. Prod. Sci. 36:335–350. Lin, H., R. Du, X. H. Gu, F. C. Li, and Z. Y. Zhang. 2000. A study on the plasma biochemical indices of heat stressed broilers. Asian-australas. J. Anim. Sci. 1399:1210–1218. Long, S. 1982. Acid-base balance and urinary acidification in birds. Comp. Biochem. Physiol. A 71:519–526. Maruyama, C, K. Imamura, and T. Teramoto.. 2003. Assessment of LDL particle size by triglyceride/HDL-cholesterol ratio in nondiabetic, healthy subjects without prominent hyperlipidemia. J. Atheroscler. Thromb. 10:186–191. McLaughlin, T., F. Abbasi, K. Cheal, J. Chu, C. Lamendola, and G. Reaven. 2003. Use of metabolic markers to identify overweight individuals who are insulin resistant. Ann. Intern. Med. 139:802–809. Nalini, K., A. K. Kataria, and A. K. Gahlot. 2008. Ambient temperature associated variations in serum hormones and interrelated analytes of broiler chickens in arid tract. Slov. Vet. Res. 45:127–134. National Chicken Council. 2005. National Chicken Council Animal Welfare Guidelines and Audit Guidelines. Natl. Chicken Counc., Washington, DC. NRC. 1994. Nutrient Requirements of Poultry. 9th ed. Natl. Acad. Sci., Washington, DC. NRC. 1996. Guide for the Care and Use of Laboratory Animals. Natl. Acad. Press, Washington, DC. Olanrewaju, H. A., J. P. Thaxton, W. A. Dozier III, J. Purswell, S. D. Collier, and S. L. Branton. 2008. Interactive effects of ammonia and light intensity on hematochemical variables in chickens. Poult. Sci. 87:1407–1414. Olanrewaju, H. A., S. Wongpichet, J. P. Thaxton, W. A. Dozier III, and S. L. Branton. 2006. Stress and acid-base balance in chickens. Poult. Sci. 85:1266–1274. Puvadolpirod, S., and J. P. Thaxton. 2000. Model of physiological stress in chickens. 1. Response parameters. Poult. Sci. 79:363– 369. Rahimi, G. 2005. Effect of heat shock at early growth phase on glucose and calcium regulating axis in broiler chickens. Int. J. Poult. Sci. 4:790–794. Robertshaw, D. 2006. Mechanisms for the control of respiratory evaporative heat loss in panting animals. J. Appl. Physiol. 101:664–668. SAS Institute. 2004. SAS User’s Guide. Statistics. Version 9.1 ed. SAS Inst. Inc., Cary, NC. Toyomizu, M., M. Tokuda, M. Ahmad, and Y. Akiba. 2005. Progressive alteration of core temperature, respiration and blood acidbase balance in broiler chickens exposed to acute heat stress. Jpn. Poult. Sci. 42:110–118. Vo, K. V., M. A. Boone, and W. E. Johnston. 1978. Effect of three life ambient temperatures on growth, feed and water consumption and various blood components in male and female Leghorn chickens. Poult. Sci. 57:798–803. Washburn, K. W. 1985. Breeding poultry in hot and cold environments. Pages 111–122 in Stress Physiology in Livestock. Vol. 3. M. K. Yousef, ed. CRC Press, Boca Raton, FL. Xin, H., I. L. Berry, G. T. Tabler, and T. L. Barton. 1994. Temperature and humidity profiles of broiler houses with experimental conventional and tunnel ventilation. Trans. ASAE 10:535–542. 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., and S. Hurwitz. 1996. Induction of thermotolerance in male broiler chickens by temperature conditioning at an early age. Poult. Sci. 75:402–406.

Suggest Documents