Download Skin surface temperature of broiler chickens is correlated to body

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.
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