Journal of Thermal Biology 90 (2020) 102606

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Journal of Thermal Biology

journal homepage: http://www.elsevier.com/locate/jtherbio

Core and peripheral site measurement of body temperature in short

wool sheep
Tellisa R. Kearton a, b, *, Amanda K. Doughty a, b, Christine L. Morton a, Geoff N. Hinch a, b,
Ian R. Godwin a, Frances C. Cowley a
a
University of New England, Armidale, New South Wales, 2351, Australia
b
CRC for Sheep Industry Innovation, Armidale, NSW, 2350, Australia

A R T I C L E I N F O A B S T R A C T

Keywords: Understanding circadian rhythms of body temperature is important for the interpretation of single body tem­
Body temperature perature measurements and the assessment of the physiological state of an animal. The ability to measure body
Diurnal rhythm temperature at peripheral locations may also be important in the development of minimally invasive tools for
Sheep
remote temperature measurement in livestock. This study aimed to investigate how well body temperature
Remote sensor
measured at peripheral sites reflected a commonly used core measurement (vaginal temperature) and the
Microchip
iButton circadian rhythmicity of the body temperature of sheep with a view to practical application in extensive sheep
production systems. Eleven crossbred ewes were implanted with peripheral temperature sensing microchips
(LifeChip®) which were positioned transversely in the sternocleidomastoid (neck) muscle and subcutaneously
under the tail. iButton® temperature loggers were placed intravaginally to record core body temperature
measurements (Tv). The body temperature measurements observed at the peripheral sites in the neck (Tn) and
tail (Tt) differed significantly to those measured at the core site, Tv (P < 0.05), with Tn lower than Tv and Tt
lower than both Tv and Tn. Similarities in circadian rhythm patterns were observed across the day between Tv,
Tn and Tt in repeated measures analysis, with a short period of difference between Tv and Tn (from 1400 to 1600
h) and a long period of difference between Tv and Tt (from 1000 to 2100 h) (P < 0.05).
These results suggest that neck muscle temperature measurements may have utility in detecting circadian
rhythm patterns in core temperature in sheep, but may not accurately reflect absolute core temperatures. Pe­
ripheral measures may require adjustment or correction to more accurately reflect absolute core temperature
with respect to determining accurate clinical thresholds relative to the expected normal temperature for the time
of day observed. Further investigation into the utility and application of peripheral measurement of body
temperature is warranted.

1. Introduction
Temperature sensing microchips implanted in the body periphery
offer the opportunity for remote, automated and early detection of
abnormal body temperatures and circadian rhythms in livestock. Before
such systems can be implemented, the ability for peripheral measures to
accurately identify changes in core temperature needs to be determined.
Abnormality in body temperature is identified when it falls outside the
range of temperatures covered by the normal circadian rhythm. Core
body temperature for sheep ranges from 38.5 � C to 39.5 � C (Piccione
et al., 2002b, 2005; Riek et al., 1950; Saini et al., 2013). When deter­
mining the normal temperature for an animal, it is important to consider
both the normal core body temperature range, as well as the circadian
pattern of oscillation which may occur around and within this normal
range. While there is no true measure of core body temperature, rectal
and vaginal measures are generally agreed to provide a sufficient
approximation for the purpose of body temperature measurement
(George et al., 2014; Smaill and Barrell, 2006).
Circadian rhythmicity of body temperature is a well-known physio­
logical phenomenon describing the daily oscillation of body tempera­
ture, elevating during the daylight hours and lowering during darkness.
Daily rhythmicity is described by several parameters: the absolute value
of peak and trough; the mesor, which is a circadian rhythm-adjusted
mean; the amplitude, which is the difference between the peak and

* Corresponding author. W49 Animal Science, University of New England, Armidale, NSW, 2351, Australia.
E-mail address: tkearto2@une.edu.au (T.R. Kearton).

https://doi.org/10.1016/j.jtherbio.2020.102606
Received 31 March 2019; Received in revised form 7 April 2020; Accepted 22 April 2020
Available online 28 April 2020
0306-4565/© 2020 Elsevier Ltd. All rights reserved.
T.R. Kearton et al.
the mean value of a wave; acrophase, the time at which the peak of a
rhythm occurs; and the range of oscillation, the difference between the
peak and the trough.
There are several factors which can impact on daily rhythmicity of
normal body temperature of sheep, including environmental tempera­
ture, activity, and physiological status. Additionally, abnormal rhyth­
micity may indicate specific health issues; for example, the presence of
fever has been found to eliminate the observable circadian pattern of
rectal temperature in sheep suffering from foot rot (D’Alterio et al.,
2012). As a result, the ability to observe and analyze circadian rhythms
in body temperature and identify abnormal rhythm may give insight
into a variety of changes in the physiological state of the animal.
The range and rhythmicity of core temperature is likely to differ from
temperature measured at peripheral locations, and may also vary be­
tween peripheral locations. Thermoregulatory processes influencing
heat exchange at the skin surface are likely to cause deviations in pe­
ripheral temperatures not reflected by core body temperature changes
(Hales et al., 1978a). An understanding of how accurately peripheral
temperature measurements reflect core temperature measurements is
therefore necessary if they are to be used to detect change in core
temperature.
Most studies testing the usefulness of peripheral measures of body
temperature in animals have used an approach of measuring the linear
relationship between measured peripheral and core body temperatures
to determine (or correct by modelling) the ability of peripheral measures
to predict core temperature. However, the correlations between raw
values of rectal temperature, as an approximation of core temperature
(Mansel et al., 2008), and peripheral temperatures are not strong. For
example, r-values of 0.53, 0.24 and 0.74 for subcutaneous microchips in
sheep, horses and goats, respectively (Goodwin, 1998); between 0.16
and 0.21 for various subcutaneous microchip locations in cattle (Reid
et al., 2012); and 0.67 for skin temperature detected with non-contact
infra-red thermometer in horses (Ramey et al., 2011). The variation in
physiological controls and responses associated with change in core and
peripheral temperature means that a single linear mathematical rela­
tionship is unlikely to be sufficient to identify an ‘abnormal’ core tem­
perature. Such an approach does not account for the fact that peripheral
and core body temperatures display different circadian rhythms, and
thus will have a different relationship at different time points (Smo­
lander et al., 1993).
Continuous or frequent logging by microchips offers an opportunity
to use circadian rhythm pattern analysis to identify changes in body
temperature, which may be more effective than a one-off measure. The
identification of abnormal body temperature rhythmicity may be useful
in the development and application of remote animal monitoring sys­
tems. In the case of changes within the body temperature pattern which
are not accompanied by an increase in temperature that is clinically
significant (i.e. outside the normal body temperature range for that
species or individual), then comparing the pattern with the animal’s
normal rate of change over the day may provide valuable information
about its physiological state. However, there is first a need to understand
how accurately normal core body temperature circadian rhythm is re­
flected at peripheral and core locations, in order to determine the use­
fulness of peripheral sites for detection of circadian body temperature
abnormality.
While it may be reasonably expected that peripheral body temper­
ature measurements would differ in absolute values from core body
temperature, as has been observed in previous work, it was hypothesized
that peripherally implanted microchips would reflect circadian body
temperature rhythm sufficiently to determine the presence of a circadian
rhythm. It was also hypothesized that the pattern of change seen in
peripheral body temperature measures may be reflective of that seen in
normal core body temperature rhythms. This may provide an indication
of the usefulness of these measures in field situations for the detection of
clinically significant changes in body temperature rhythms.
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Journal of Thermal Biology 90 (2020) 102606
2. Materials and methods
2.1. Animals and housing
Eleven crossbred ewes (approximately 23–26 months of age, tail
docked as lambs with a short tail remaining) were introduced into the
animal house 16 days prior to the commencement of measurements
(acclimation period) and were habituated to handling once a day. The
sheep were housed throughout the acclimation period in groups of five
or six, and were then introduced into individual pens two days prior to
commencement of the experimental period. The sheep were shorn
immediately prior to entering the animal house, had been treated for
internal and external parasites, were in good health and condition, and
free of disease. Mean live weight of the sheep was 61 � 6.5 kg (mean � s.
d.).
All procedures were approved by the University of New England
Animal Ethics Committee, authority number AEC15-096. The care and
use of the animals was in accordance with the Australian Code for the
Care and Use of Animals for Scientific Purposes (National Health and
Medical Research Council, 2013).
2.2. Feeding and husbandry
During the experimental period, the sheep were individually penned
(2 � 2 m) indoors in an animal house and were always in visual and
auditory contact with each other. The animal house was well ventilated
with wooden slatted floors, automatic waterers were available to the
animals at all times, and the pens were cleaned daily.
Animals were fed once each day at approximately 0730 h during the
acclimation period, and any feed refusals were removed and weighed
immediately prior to the next ration being given. The ration was a blend
of oaten, lucerne and wheaten chaff offered at maintenance levels at a
fixed weight calculated per individual sheep weight (9–12 MJ ME/
sheep/day).
2.3. Temperature monitoring devices
A blank (progesterone-free) controlled intravaginal drug release
device (CIDR®, Zoetis, Parsippany, NJ, USA) was used to secure an
iButton® temperature logging device (Model number DS1921H–F5#,
accuracy � 1 � C, resolution 0.125 � C, Maxim International, San Jose,
CA, USA (Wolaver and Sharp Jr (2007)). iButton calibration is per­
formed at manufacturing, additional verification was performed prior to
beginning the experiment to ensure that the devices were operational
within the specified calibrated range. The iButton sensors were config­
ured to record vaginal temperature at intervals of 10 min throughout the
experimental period. The iButton® sensors were secured to the CIDR
using shrink-wrap. The vaginal measurement site was chosen as an
equivalent substitute for rectal temperature as demonstrated in previous
work (Suthar et al., 2013), and as an approximation of core body tem­
perature (Mansel et al., 2008). This site allowed for multiple automated
measures to be taken without additional handling stress associated with
rectal temperature measurement.
Temperature sensing LifeChip® microchips (Destron Fearing, Dal­
las/Fort Worth, TX, USA) consisted of a BIO-THERMO® temperature
sensor (accuracy ~ � 0.5 � C, resolution ~ � 0.1 � C.) coated with a
BioBond® Anti-Migration Cap, which is a porous polypropylene poly­
mer sheath that encourages the accumulation of tissue to hold the
microchip in place and prevent migration. One microchip was implanted
transversely in the sternocleidomastoid muscle (neck) at a depth which
would ensure the microchip was fully embedded in the muscle, and a
second was implanted subcutaneously on the underside of the docked
tail. The peripheral measurement sites were chosen with consideration
given to limiting carcass downgrade if the implants were to be removed.
Calibration of these measurement devices is performed at
manufacturing, additional verification was not possible prior to
T.R. Kearton et al.
beginning the experiment as the devices are packaged together with the
applicator under sterile conditions. Topical administration of lignocaine
and disinfecting solutions were applied to the skin prior to implantation
of the microchips, which was performed 3–5 days prior to the
commencement of the experiment in order to allow localized inflam­
mation to subside. No detectable inflammatory response to the implants
was noted. An Allflex® RS420 wand reader was used to read the mi­
crochips at a distance of 10–20 cm from the chip site for a few seconds.
The animals became habituated to the reading procedure during the
initial acclimation period.
Ambient temperatures were recorded from iButton® loggers (Model
number DS1921G-F5#, accuracy � 1 � C, measures in 0.5 � C increments)
positioned at points at the northern, southern, western, eastern and
central points of the sheep pens inside the animal house, which would
give a representative ambient temperature for the sheep pens. These
loggers recorded temperature measurements at intervals of 5 min
throughout the trial period. Outside temperatures during the trial period
ranged from 7.6 to 29.5 � C, with relative humidity for the region ranging
from 61 to 95% (Australian Bureau of Meteorology, 2015). Hourly
ambient temperature was determined to be the average of the 4 loca­
tions. Unfortunately, relative humidity data for inside the animal house
was unable to be recorded, although the facility maintained good
ventilation throughout the study with slatted floors and open windows.
2.4. Experimental design
Core (vaginal) and peripheral (neck and tail) body temperatures
were recorded individually for the sheep simultaneously over a total 48
h period, with measures for n ¼ 5 or 6 sheep recorded on different days
than the measures for the remaining sheep, all completed within 4 days
of each other. Vaginal temperature (Tv) was measured using iButton®
temperature logging devices placed intravaginally, automatically log­
ging at 10 min intervals. Vaginal temperatures have been shown to
correlate highly with rectal temperatures in previous studies in sheep
(George et al., 2014) and cattle (Suthar et al., 2013), and were therefore
considered indicative of core body temperatures (Mansel et al., 2008)
for the purposes of this experiment. Peripheral body temperature mea­
surements from the neck (Tn) and tail (Tt) temperature-sensing micro­
chips were recorded with a wand reader at hourly intervals between
0700 and 2400 h, and at two-hourly intervals between 2400 and 0600 h.
Tv for each of these time intervals was extracted from the 10-min
iButton® dataset at the point closest to the Tn and Tt measurement time.
2.5. Circadian cosinor analysis
CircWave software (v 1.4, 2007 R. Hut) uses Fourier transformation
to recognise wave forms and adds harmonics in a step-wise regression
using cosinor analysis and F-testing (Huisman et al., 2015; van der Spek
et al., 2018) and was used to generate a 24-h periodogram for temper­
ature measured at each location, for each sheep, using the 48 h datasets
Tn, Tt and Tv. This analysis used harmonic regression, producing
‘goodness of fit’ coefficients for each curve. The coefficient of determi­
nation for the CircWave periodogram transformation for each sheep
ranged between 0.424 and 0.995 for Tv, between 0.465 and 0.967 for
Tn, and between 0.503 and 0.954 for Tt. The circadian rhythm param­
eters were then characterized for each periodogram. Several commonly
used circadian parameters were derived from the transformed data for
analysis, these were: trough, peak, acrophase (the time at which peak
occurs), range of oscillation, mesor (mean value of a wave), standard
deviation and amplitude (the difference between the peak and the
mesor) of the Fourier curve (D’Alterio et al., 2012).
2.6. Statistical analysis
Once the raw data was transformed through CircWave and the
circadian parameters characterized, the statistical software R (v 3.3.1, R
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Journal of Thermal Biology 90 (2020) 102606
Core team, 2016) was used for the remainder of the statistical analyses.
Temperature data for predicted fitted values from the CircWave function
were log transformed to meet normality assumptions and Q-Q and re­
sidual plots were checked for normality. The difference in means of the
rhythm parameters of the Fourier curve between core temperature (Tv)
and the peripheral measurement sites (Tn and Tt) was compared using a
two-sided paired t-test, where the individual sheep was the experimental
unit.
A repeated measures linear mixed effect interaction model (lme)
(Pinheiro et al., 2011) was used to compare the slope (defined for the
purpose of this study as the rate of change from one hourly measurement
point to the next) of the Tv circadian curve with the slope of the circa­
dian curve of each of the peripheral measurement sites. In the lme
models, individual sheep was entered as a random effect to avoid
pseudoreplication and the model included an interaction term to assess
difference in slope over each hourly interval for each measurement site.
Time and site were included in the model as fixed effects. Mean tem­
perature was plotted as an interaction plot at hourly time points to show
the range of temperature fluctuation across the 24 h period for each
measurement site. For one animal (ID43) Tt measurements were not
available as the tail microchip was expelled by the animal at the
beginning of the experiment and thus this animal was excluded from all
Tt measurement analysis.
To test the association of hourly ambient temperature with sheep
body temperature, for each of the different body temperature methods,
and each sheep group, the hourly body temperature (median of n ¼ 5–6
sheep/group) was tested against hourly ambient temperature. The
hourly ambient temperature was calculated to be the mean of Day 1 and
Day 2 ambient temperature. Variability of hourly body temperature
explained by ambient temperature was evaluated by R-squared esti­
mates. Correlations between hourly body temperature measures and
ambient temperature were evaluated using Pearson correlation
coefficients.
3. Results
Pairwise analysis of the differences between measurement sites for
the fitted circadian curve parameters revealed that there were signifi­
cant differences (P < 0.05) between Tv and both peripheral sites for all
circadian parameters, with the exception of acrophase for Tn (Table 1).
The peripheral sites both measured lower fitted temperatures than Tv;
Tn by an average of 0.846 � C (95% CI -3.088 - 1.395), and Tt by an
average of 1.715 � C (95% CI -3.873 - 0.444), when compared to mean
Tv.
While these results demonstrated that fitted temperature curve pa­
rameters from the Fourier transform procedure differed between Tv, Tn
and Tt, pattern similarities were observed at time points across the
measurement day; with Tv, Tn and Tt exhibiting similar rhythmicity
across the measurement day. This pattern was reflected in the repeated
measures interaction analyses, in which site and time interactions were
analyzed. The model analyzed these interactions for the fitted data at
each time point across a 24-h circadian cycle, with results showing a
short 2 h period of slope dissimilarity (where slope refers to degree/
direction of change between one hourly timepoint and the next) be­
tween Tv and Tn from 14 to 16 h (P < 0.05), and a much longer 11 h
period of dissimilarity between Tv and Tt from 10 to 21 h (P < 0.05) as
shown in Fig. 1. The standard error for the measurement periods for Tv,
Tn and Tt were 0.006, 0.008 and 0.009 respectively. Fig. 2 shows the
between sheep variation for each measurement site, Tv showed little
variation, variation increased at Tn and was greatest in Tt across the
same 24-h measurement cycle (see Fig. 3).
Correlations between hourly ambient temperature and body device
measurement were higher for the tail (r ¼ 0.97) and neck (r ¼ 0.96)
microchip measures, compared to vaginal temperature (r ¼ 0.76). Tail
temperature variability was also better explained by ambient tempera­
ture (R2 ¼ 0.90) compared to vaginal temperature (R2 ¼ 0.50).
T.R. Kearton et al. Journal of Thermal Biology 90 (2020) 102606

Table 1 temperature in sheep were significantly different from those of vaginal

Pairwise comparisons for the mean difference between circadian rhythm pa­ temperature, when changes in the degree and direction of the curves
rameters of vaginal temperature and peripheral temperature at the neck and the were compared on an hour-by-hour basis, then intramuscular neck
tail. Data are shown as mean � s.d., and mean difference (95% confidence in­ temperature pattern showed a close similarity to diurnal vaginal tem­
terval), n ¼ 11 animals. perature cycle.
Site Vagina Neck Tail Vagina - Vagina - Previously, circadian temperature patterns have been observed in
(Tv) (Tn) (Tt) Neck (95% Tail (95% sheep, as measured by both rectal temperature (Mohr and Krzywanek,
CI) CI)
1995; Piccione and Caola, 2003; Piccione et al., 2002b), and vaginal
Mesor (� C) 39.09 � 37.35 35.92 1.75 (1.21, 3.19 (2.63, temperature (Hunsaker et al., 1976). Foot temperature measurement
0.25 � 0.90 � 0.70 2.29)*** 3.75)***
taken with infrared thermography (IRT) suggests a daily rhythm
Peak (� C) 39.57 � 38.08 37.11 1.49 (1.05, 2.49 (2.10,
0.24 � 0.74 � 0.47 1.92)*** 2.87)*** (D’Alterio et al., 2011), which indicates that peripheral temperature
Trough (� C) 38.61 � 36.51 34.52 2.10 (1.35, 4.10 (3.25, measures may be of use in detecting circadian temperature patterns in
0.25 � 1.13 � 1.15 2.86)*** 4.05)*** sheep. However, the results of the present study found significant dif­
Acrophase (h) 11:46 � 13:23 14:07 1:36 2:18 ferences between the core and peripheral (neck and tail) sites for most of
2.17 � 2.29 � 2.50 ( 2.84, ( 3.67,
the common circadian parameters used in rhythm analyses.
0.38)ns 0.89)*
Range of 0.96 � 1.57 � 2.59 � 0.61 1.62 Neck and tail temperatures in this experiment differed from vaginal
oscillation 0.23 0.60 1.15 ( 1.00, ( 2.41, temperature in absolute value, as indicated by the parameters peak,
(� C) 0.23)* 0.83)* trough and mesor, but also in the circadian pattern, as demonstrated by
Standard 0.26 � 0.49 � 0.85 � 0.23 0.58
significant differences in standard deviation, amplitude and range of
deviation 0.06 0.20 0.36 ( 0.37, ( 0.84,
(� C) 0.9) * 0.32)** oscillation, and the time of the acrophase (1 h 36 min difference for neck
Amplitude 0.48 � 0.74 � 1.19 � 0.26 0.71 temperature and 2 h 18 min difference for tail temperature, compared to
(� C) 0.15 0.25 0.52 ( 0.41, ( 1.05, vaginal temperature). Comparison of the rhythmic parameters of rectal
0.12)* 0.36)* temperature and infra-red thermography-detected foot temperature
*P < 0.05; **P < 0.01; ***P < 0.001; ns not significant. previously found similar differences in mesor, amplitude, and acrophase
(D’Alterio et al., 2011). In humans, the circadian temperature parame­
4. Discussion ters of thoracic and axillary skin temperatures showed significant dif­
ferences in mesor, amplitude and acrophase, and were not considered
The results of this research demonstrate that while the parameters of substitutable (Thomas et al., 2004). Therefore, it was expected that
the circadian rhythms of intramuscular neck and subcutaneous tail differences for the circadian parameters would be observed, however
differences observed both between and within individuals may also be

Fig. 1. Comparison of the 24 h circadian rhythms at

vaginal (dotted line), neck (dashed line) and tail
(solid line) sites using hourly time points in n ¼ 11
animals for vaginal and neck site, and n ¼ 10 animals
for tail site. While curves demonstrate hourly means,
the horizontal bars indicate time periods during
which temperature pattern slopes at the peripheral
sites were significantly different from the vaginal site
(P < 0.05) when adjusted for measurements collected
on the same animal. Ambient temperature demon­
strates mean animal house temperature averaged
over the 2 study days.

4
T.R. Kearton et al.
Fig. 2. Variation in circadian rhythm across n ¼ 11 animals for vaginal and neck site, and n ¼ 10 animals for tail site at 1 hourly time points for vaginal, neck and tail
temperature. Black dots represent median values for each hourly measurement and single hollow circles represent outlier values (1.5 times above or below the
interquartile range).
implicated in variability, such as those which may occur due to differ­
ences in microchip placement and tail length. Therefore, in order to
assess the utility of peripherally implanted microchips in temperature
change detection it was necessary to also evaluate the circadian patterns
of change as they compare between peripheral and core temperature
measures. This method of pattern analysis reveals more information
about the nature of the rhythmicity, not just the presence or absence of
rhythmicity. This method of analysis may provide more information
about how illness and other physiological conditions may impact on the
circadian pattern of body temperature, as well as providing useful
comparisons for different measures of body temperature. As these
regression models represent simple hypothesis tests for the slope (degree
and direction of the curve) between each hourly interval (i.e. time x and
xþ1) rather than the global circadian model (allowing assessment of site
difference for change in temperature from 1 h to the next), a multimodal
inference approach was not necessary. Similar models of varying
complexity for analyzing circadian rhythm have been described by
Wang et al. (2003) and Weissenbock et al. (2012).
While the circadian parameters of both Tn and Tt differed
5
Journal of Thermal Biology 90 (2020) 102606
significantly from Tv, the pattern of change in the circadian rhythm
showed similarities in Tn and Tv. The finding that there was only a 2 h
period where modelling indicated a statistically different direction in
slope between Tv and Tn also suggests that the neck is a better mea­
surement site than the tail. There was a lack of circadian rhythm con­
formity of Tt with Tv over 11 h during the day for the tail site, during a
period when most sheep are active. These results suggest that Tn could
be of use in determining a threshold at which a temperature differs from
normal at any given time point along the daily oscillation, and may be a
useful reflection of patterns of core temperature, for identifying
abnormalities.
The ability of peripheral temperature measurements to reflect core
temperature may be impacted by several factors relating to both ther­
mophysiology and the effectiveness of the measurement device and
placement, particularly with consideration to the skin as a thermoreg­
ulatory organ. Temperature measurements at the tail site varied more
than those from the vagina or the neck. This variation could be the result
of the subcutaneous placement of Tt being closer to the skin surface than
Tn (which was located deeper into the muscle tissue) and therefore
T.R. Kearton et al. Journal of Thermal Biology 90 (2020) 102606

Fig. 3. Hourly temperature data for individual animals at (a) vaginal site, (b) neck and (c) tail sites over a 24 h period. Number of animals n ¼ 11 for vaginal and
neck site, n ¼ 10 for tail site.

subject to greater flux due to the role of the skin in thermoregulatory
processes (Hales et al., 1978b; Kuhnen and Jessen, 1988). Adjustment of
skin temperature is predominantly centered on the extremities as
opposed to the skin on the trunk of the body, and therefore the greatest
variation in skin temperature occurs at the extremities (Yousef, 1986),
since distal regions of the body are rich in arteriovenous anastomoses
which regulate blood flow and play a key role in thermoregulation
(D’Alterio et al., 2011). The greater variation exhibited by Tt may also
have resulted from the skin being more subject to the influence of
ambient temperature, a phenomenon which would also vary depending

6
T.R. Kearton et al.
on the presence or absence of wool (Cockrem and Wickham, 1960).
Additionally, the tail as an appendage is subject to greater influence
from ambient temperature variation due to mobility and exposure to
cold air and cold surfaces when the animal is lying down or leaning
against a surface or when the tail is held away from the body. However,
the skin on the underside of the tail is largely bare and is consequently
thicker than the skin at wool-growing regions, such as the neck, and this
skin thickness impacts on heat transfer at the surface of the skin (Lyne
and Hollis, 1968). Wool impacts on the thermoregulatory processes and
heat loss, and skin thickens within days in response to shearing (Roger
Hegarty, pers. comm.) so utilizing sheep which were >2 weeks off shears
in the present study may have influenced the body temperature mea­
sures differently than it would in the case of unshorn (Beatty et al., 2008;
Done-Currie et al., 1984) or freshly shorn sheep.
Both peripheral measurement sites were more closely correlated
with ambient temperature than was Tv, although core circadian tem­
perature rhythm has a very similar pattern to ambient temperature.
Ambient temperature may more strongly affect Tt as a result of the
absence of wool, the movement in the tail area, and its proximity to
surfaces when laying down, and Tn due to the influence of high blood
flow through the muscle and the proximity to large blood vessels, which
play a role in the dissipation of heat to and from the periphery. While
correlation does not imply causation in this relationship, its possible role
in the differences should be considered when interpreting these results.
Relative humidity was unable to be measured inside the animal house,
and while this may have impacted on the temperature-humidity index
values, since the local conditions did not exceed what may be considered
within the sheep’s thermoneutral zone, it is likely that the impact would
have been minimal. Ventilation via slatted floors and open windows
throughout the barn in the barn reduced this influence. As the sheep had
been shorn there was low risk of heat stress and few thermoregulatory
processes would have been engaged.
Differences between Tv, Tn and Tt in within- and between-individual
variability could also be related to the sensitivity of the two different
devices used in this experiment. While iButtons® have been used to
reliably record body temperature measurements in other experiments
(Piccione et al., 2013b; Wallage, 2014), the temperature sensing mi­
crochips are more sensitive (Langer and Fietz, 2014) and this sensitivity
may influence the variability of the measurements from the microchips.
This sensitivity may be particularly apparent with very small changes in
temperature in the surrounding tissue, such as those resulting from
factors influencing skin temperature (e.g. handling (Piccione et al.,
2002a), ambient temperature (Piccione et al., 2013a), and insulation of
the skin (Cockrem and Wickham, 1960). Further investigation into these
possible sources of variation is warranted, and may be of relevance in
determining the applicability of these measures in detection of clinically
significant temperature changes.
5. Conclusions
The results of the present study suggest that measurement of tem­
perature intramuscularly at the neck may have utility in the detection of
core circadian rhythm pattern changes and temperature anomalies in
shorn sheep, and would be a more reliable site from which to develop a
model of normal and abnormal core body temperature rhythms than the
tail. Pattern of temperature change analysis showed that temperature
measured subcutaneously at the tail had long periods of pattern
dissimilarity from vaginal temperature, suggesting that it was likely to
have limited utility as a representation of core temperature rhythms. In
addition, tail temperature was highly variable between animals. The
importance of the careful evaluation of normal circadian rhythms of
body temperature is evident in these findings, as the different mea­
surement methods and locations can result in significant variations from
normal vaginal body temperature, both in absolute temperatures and
circadian rhythmicity. Analysis of patterns of rhythmicity has revealed
more information about the change in body temperature that occurs
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Journal of Thermal Biology 90 (2020) 102606
throughout the day at peripheral locations. This information has value in
future investigations into circadian rhythmicity of body temperature
and improves our understanding of how these patterns may differ ac­
cording to different thermophysiological conditions within an animal.
This has implications for use of peripheral temperature measurements in
practical applications as an alternative to core temperature for diag­
nostic and clinical purposes. There are several external factors influ­
encing body temperature measurements and these need to be accounted
for in order to determine the applicability and practicality of new
technologies for temperature measurement. Further investigation of
these variations and their causes is warranted when utilizing peripheral
temperature measurements, particularly on their ability, or otherwise,
to reflect normal circadian patterns; as well as the exogenous and
endogenous influences on thermoregulation at the periphery, such as
the presence or absence of wool. The method of pattern of change
analysis used here has utility in detecting similarities and differences
between body temperature measurement sites and may provide more
information than comparison of absolute temperatures or circadian
rhythm parameter values at various sites in shorn sheep.
Declaration of competing interest
We wish to confirm that there are no known conflicts of interest
associated with this publication and there has been no significant
financial support for this work that could have influenced its outcome.
Acknowledgements
Funding: This work was supported by the Australian Cooperative
Research Centre for Sheep Industry Innovation (Sheep CRC) and the
University of New England. The authors declare no conflicts of interest.
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