Journal of Thermal Biology 26 (2001) 85–93
Can non-shivering thermogenesis in brown adipose tissue
following NA injection be quantified by changes in overlying
surface temperatures using infrared thermography?
D.M. Jacksona,*, C. Hamblya, P. Trayhurnb, J.R. Speakmana
a
Department of Zoology, Aberdeen Centre for Energy Regulation and Obesity (ACERO) University of Aberdeen,
AB24 2TZ, Scotland, UK
b
Division of Medical Science, Rowett Research Institute, Bucksburn, Aberdeen, AB21 9SB, Scotland, UK
Received 23 October 1999; received in revised form 29 January 2000; accepted 3 June 2000
Abstract
We aimed to investigate whether infra red thermography (IRT) can be used to measure and quantify non-shivering
thermogenesis (NST) in the short-tailed field vole Microtus agrestis, by directly comparing it with a standard method,
i.e. metabolic response following Noradrenaline injection (NA). Mean skin surface temperature overlying Brown
adipose tissue (BAT) depot was 0.828C higher than mean surface temperature that did not overly BAT. The difference
in temperature increased by 1.268C after NA was administered. Mean skin surface temperature overlying BAT
increased by 0.328C after NA was administered; however, surface temperature decreased by 1.328C after saline was
administered. Mean skin surface temperature overlying BAT did not change significantly between warm and cold
acclimated voles; in contrast metabolic peak following NA injection significantly increased in cold acclimated voles.
There was no significant correlation between change in surface temperature after NA injection and metabolic peak
following NA injection. The results of this study suggest that IRT is not a sensitive enough method to measure changes
in NST capacity in BAT following NA injection, or to detect changes in NST capacity induced by cold acclimation.
However, IRT can distinguish between skin surfaces overlying BAT and skin surfaces that do not. # 2001 Elsevier
Science Ltd. All rights reserved.
Keywords: Brown adipose tissue (BAT); Non-shivering thermogenesis (NST); Infrared thermography (IRT); Microtus agrestis
1. Introduction
In temperate and arctic regions small mammals
encounter problems with hypothermia, due to their
large surface to volume ratio. In response they have
evolved a number of anatomical, behavioural, and
physiological adaptations to enable them to conserve
heat. For example, increased insulation from fur
(Walsberg, 1991), decreased heat loss from huddling
*Corresponding author. Current address: Human Nutrition
Unit, Rowett Research Institute, Greenburn Rd, Bucksburn,
Aberdeen, AB21 9SB. Tel.: +44-1224-712-751; fax: +44-1224715-349.
E-mail address: [email protected] (D.M. Jackson).
(Bazin and MacArthur, 1992; Hayes et al., 1992;
Conteras, 1984) and increased the capacity for heat
production by non-shivering thermogenesis (NST)
(Jansky, 1973).
NST is heat production in the body that does not
involve muscular contraction (Jansky, 1973). It occurs in
a number of organs in the body; however, the main site
is in the brown adipose tissue BAT (Nicholls et al.,
1984). There are two standard ways to measure the heat
generating capacity of BAT. The most common way is
to measure the metabolic response of the animal to a
mass specific dose of Noradrenaline, which is the
primary mediator of NST (Mory et al., 1984) in the
BAT. The second way to measure NST is to measure
0306-4565/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved.
PII: S 0 3 0 6 - 4 5 6 5 ( 0 0 ) 0 0 0 2 3 - 1
86
D.M. Jackson et al. / Journal of Thermal Biology 26 (2001) 85–93
biochemical correlates of NST in the BAT such as
UCP 1, GDP binding and cytochrome c oxidase activity
(Trayhurn and Milner, 1989).
Intrascapular brown fat can be readily seen using IR
thermography in young rats during cold exposure
(Blumberg et al., 1999), in bats during arousal from
torpor (Bickel and Radermacher, 1994), in human
infants (Oya et al., 1997) and in human adults (Rothwell
and Stock, 1979). Surface temperature of animals is
most easily measured using Infra red thermography
(IRT) (Speakman and Ward, 1999). The main advantage of the IRT method is that it is unobtrusive, unlike
other methods of measuring surface temperature e.g.
using thermocouples (Krattenmacher and Rubsamen,
1987). All objects emit electromagnetic radiation if their
temperature is above absolute zero (273 K). The
intensity of the radiation is dependent on the surface
temperature and the emissivity of the object. Hence, if
the emmisivity is known the surface temperature can be
measured from the intensity of emitted radiation.
Recently, IRT has been used in a number of thermoregulation studies, e.g. in the study of heat loss during
flight in the starling Sturnus vulgaris (Ward et al., 1999),
in the study of wing surface temperature changes in the
Egyptian fruit bat Rousettus aegyptiacus (Lancaster
et al., 1997) and heat loss in the barn owl (McCafferty
et al., 1998).
Only one study to date has attempted to use IR
thermography to measure or quantify NST in the BAT
(Oya et al., 1997). This study measured NST in human
new-borns to investigate how quickly NST was initiated
after birth; however, NST capacity was not quantified or
compared with other methods of measuring NST.
Earlier work (Rothwell and Stock, 1979) described
changes in skin temperature following adrenaline injection in adult humans using IR thermography; however,
NST was not quantified. Several other studies have
indicated that increases in skin temperature may follow
catecolamine stimulation using IR thermography but
results have been confused (Astrup et al., 1986;
Contaldo et al., 1981). To an extent this confusion
may arise because of the differences in the IR thermography equipment utilised in different studies. Over the
past 20 years since these studies, significant advances
have been made in the ability to capture images digitally
and analyse them using computers. In the light of these
advances it is appropriate to ask whether modern thermal
imaging provides a method for quantification of NST.
In this study, we investigated whether capacity for
NST in the BAT can be quantified using IR thermography in the short-tailed field vole Microtus agrestis by
directly comparing it to the standard method for
measuring NST, i.e. metabolic response to NA injection.
We also investigated whether IR thermography can detect
differences in capacity for NST in skin areas known to
overly BAT and in warm and cold acclimated voles.
2. Methods
2.1. Study species
Twenty-nine short-tailed field voles (Microtus agrestis) were taken from a colony maintained at the Zoology
Department, Aberdeen University. Approximately, half
of the voles (14) were transferred to a cold room,
average ambient temperature 9.68C 1.0 and half
(15) placed in a warm room of average ambient
temperature 21.88C 0.9. Both experimental groups
were fed ad libitum with rodent chow (SDS diets,
BP Nutrition Ltd., UK) and supplemented with barley
Hordeum vulgare and carrot Daucus carota. Both
groups were kept at a photoperiod of 16 : 8 light : dark,
and allowed for 10 days to acclimate, (this time
period has been shown to be long enough for any
physiological changes to occur (McDevitt and Speakman, 1996)).
2.2. Metabolic measurements
Once the 10 day acclimation period was over,
metabolism was measured by placing the animal in a
respirometry chamber housed in a temperature-controlled incubator (Gallencamp UK) set at 308C (thermoneutral zone, McDevitt and Speakman, 1996). Airflow
was controlled by a pump (Charles Austin pumps Ltd.)
and set to around 550 ml/min (Alexander Wright
flowmeter DM3A). The air was dried (silica gel), and
oxygen consumption measured via an oxygen analyser
(Servomex 1100, Crowborough, Sussex, UK). Oxygen
consumption was measured every 30 s using an Acer PC
personal computer and corrected for STPD. Carbon
dioxide production was not absorbed prior to the
measurement of oxygen content, since this configuration
produces the most accurate estimates of energy expenditure (Koteja, 1996).
Energy expenditure was calculated using the Weir
equation (Weir, 1949). Instantaneous corrections were
made to the estimate of O2 consumption (Bartholemew
et al., 1981). Behaviour was monitored throughout the
injection period and was corrected for, using the
protocol as described by Jackson et al. (submitted).
The voles were placed in the chamber for 2 h to
measure resting metabolic rate (RMR), this time period
having been shown previously to be sufficient to measure
RMR in this species (Hayes et al., 1992). RMR was
estimated as mean of the lowest ten 30 s measurements
during the 2 h period. After 2 h the voles were taken
out of the chamber and injected with 1.2 mg/kg of
Noradrenaline (NA) (bitartrate salt, Sigma chemicals,
Dorset, UK) in 0.9% saline. This dose has been
calculated to be sufficient to stimulate the maximum
thermogenic response in this species (Jackson et al.,
submitted). Eight of the voles were injected with 0.9%
D.M. Jackson et al. / Journal of Thermal Biology 26 (2001) 85–93
87
saline and these acted as controls. NST was taken as the
peak metabolism reached after the injection, accounting
for activity and instantaneous corrections.
2.3. Calculation of surface temperature
Images of each animal’s dorsal surface were taken
using an infrared camera (Agema Thermovision 880).
The camera was connected to a dedicated thermal
imaging computer running the Cats E 1.00 software
which allowed the calculation of surface temperature
( 0.18C), assuming a surface emissivity of 0.95 (Cossins
and Bowler, 1987). One day prior to the measurement of
surface temperature, each vole had an area of its back
shaved (Wahl UK No. 1 guard) to allow measurements
of skin surface temperature.
Each vole was held 0.5 m away from the camera, with
its dorsal surface towards the camera to allow images of
the back to be stored. Average ambient temperature
during the measurements was 21.8 2.1. Images from
the camera were stored every 2 min for a 20 min period
prior to NA injection. After 20 min the vole was injected
with 1.2 mg/kg NA (bitartrate salt, Sigma chemicals,
Dorset) and further images of the dorsal surface were
stored every 2 min for 20 min after the injection. This
time period was chosen because the peak thermogenic
capacity of this species is normally reached between 10
and 15 min after the NA injection (Jackson et al.,
submitted). The mean surface temperature was calculated as the average over 10–16 min after collection of
thermal images started, before and after injection, to
ensure thermogenic capacity had been reached. Body
temperature (rectal) was recorded every 4 min
(Digitron 0.38C) during the measurement period.
Mean body temperature was calculated as an average,
10–20 min after collection of thermal images started, to
ensure that peak body temperature was reached.
Ambient temperature was measured using a thermocouple linked to a digital thermometer (Digitron
0.38C).
Two regions of the dorsal surface were chosen for
subsequent analysis of mean surface temperature (Plate
1). The upper dorsal interscapular region was chosen to
allow surface temperature of the skin overlying the
Brown adipose tissue (BAT) to be measured. The
lower dorsal surface was chosen to allow surface
temperature to be calculated with out BAT. Two areas
were used for the analysis of surface temperature 195
pixels and 81 pixels, since the size of the BAT depot can
vary between animals. A lower dorsal area was
chosen for comparison to the upper dorsal surface
temperature above the BAT region. As with the BAT
region, two areas of the lower dorsum (195 pixels and 81
pixels) were used for subsequent analysis of surface
temperature.
Plate 1. Dorsal thermal image of vole showing the upper and
lower regions used in the analysis of surface temperature. Two
areas were used for analysis, 195 pixels (Large box) and 81
pixels (small box).
2.4. Statistical analysis
Analysis of variance (ANOVA), linear regression and
t-tests were performed using Minitab statistical software
(Ryan et al., 1985). Statistical significance is denoted on
graphs by (*p50.05, **p5 0.005, ***p50.001). Four
voles died between measurement of NA-induced metabolism and measurement of surface temperature; therefore, 17 voles were used in the statistical analysis of
surface temperature in response to NA.
3. Results
3.1. Body mass
Resting metabolic rate did not correlate significantly
with body mass (Linear regression, F=0.82, r2=0.0109,
p=0.380); however, instantaneous peak metabolism did
significantly correlate with body mass following NA
injection (Fig. 1, F=8.4, p=0.009). Peak metabolism
including RMR also correlated with body mass (Fig. 2,
F=9.6, p=0.006). Average body temperature of the
voles did not correlate with body mass of the voles
(linear regression, F=3.17, p=0.094). Average surface
temperature using 195 pixels or 81 did not correlate
significantly with body mass (linear regression 195
pixels, F=3.05, p=0.101; linear regression 81 pixels,
F=1.14, p=0.303).
88
D.M. Jackson et al. / Journal of Thermal Biology 26 (2001) 85–93
injection
F=0.03,
p=0.07.
F=2.18,
(before injection, 195 pixels, linear regression,
p=0.874, 81 pixels, linear regression, F=4.85,
After injection, 195 pixels, linear regression,
p=0.191).
3.3. Upper dorsal skin surface temperature
Upper dorsal surface temperature significantly
increased by an average of 0.2398C after NA was
Fig. 1. Relationship between instantaneous peak metabolism
not including RMR following NA injection and body mass of
short-tailed field voles (linear regression, y=0.415+0.0043x,
F=8.4, r2=0.307, p=0.009).
Fig. 3. Relationship between body temperature and upper
dorsal surface temperature using 81 pixels before NA injection
(linear regression, y=33.9+0.0144x, r2=0.052, F=0.82,
p=0.38).
Fig. 2. Relationship between peak metabolism including RMR
following NA injection and body mass of the short-tailed field
voles (linear regression, y=0.453+0.00539x, F=9.6, r2=0.336,
p=0.006).
3.2. Body temperature
Mean body temperature of the voles did not correlate
with average surface temperature before NA injection
was administered using 81 pixels (Fig. 3, F=1.82,
p=0.380); however, there was a significant correlation
after NA injection (Fig. 4, F=14.48, p=0.002). The
body temperature of voles injected with saline only did
not correlate with surface temperature before or after
Fig. 4. Relationship between body temperature and upper
dorsal surface temperature using 81 pixels following NA
injection (linear regression, y=23.5+0.0452x, F=14.48,
r2=0.491, p=0.002).
89
D.M. Jackson et al. / Journal of Thermal Biology 26 (2001) 85–93
Table 1
Comparison of upper dorsal surface temperature, before and after injection with saline or Noradrenaline
Saline
Pre-injection
Paired t-test
Post-injection
Mean
SD
N
34.423
1.652
8
Difference=ÿ0.429
T=1.66
p=0.142
33.994
1.752
8
Two sample t-test
T=0.9
p=0.39
(a) 195 pixels upper dorsal surface
Noradrenaline
Mean
SD
N
T=1.86
p=0.1
34.98
0.83
17
Difference=0.239
T=2.22
p=0.041*
35.219
0.927
17
Mean
SD
N
34.83
1.738
8
Difference=ÿ1.329
T=2.26
p=0.058
33.44
1.564
8
Two sample t-test
T=0.79
P=0.45
(b) 81 pixels upper dorsal surface
Noradrenaline
Mean
SD
N
35.336
0.71
17
T=1.76
p=0.12
Difference=0.324
T=2.57
p=0.02*
35.66
0.916
17
Table 2
Comparison of lower dorsal surface temperature before and after injection with saline or Noradrenaline
Saline
Pre-injection
Paired t-test
Post-injection
Mean
SD
N
33.513
0.613
8
Difference=ÿ0.433
T=0.65
p=0.539
33.08
1.582
8
Two sample t-test
T=2.69
p=0.016*
(a) 195 pixels lower dorsal surface
Noradrenaline
Mean
SD
N
T=1.87
p=0.094
34.272
0.743
17
Difference=ÿ0.067
T=0.61
p=0.553
34.205
0.906
17
Mean
SD
N
33.257
1.083
8
Difference=ÿ0.183
T=0.48
p=0.64
33.44
1.564
8
Two sample t-test
T=2.88
p=0.015*
(b) 81 pixels lower dorsal surface
Noradrenaline
Mean
SD
N
34.515
0.87
17
T=1.61
p=0.14
Difference=ÿ0.113
T=0.89
p=0.388
34.402
0.948
17
90
D.M. Jackson et al. / Journal of Thermal Biology 26 (2001) 85–93
administered using 195 pixels for analysis. This difference increased to 0.3248C when 81 pixels was used for
the analysis (Table 1a and b). An increase in temperature was not shown when animals were injected with
saline. In contrast, the upper dorsal surface temperature
decreased by an average of 0.4298C using 195 pixels for
analysis, and 1.3298C using 81 pixels for analysis.
However, this decrease was not significant (Table 1a
and b).
3.4. Lower dorsal surface temperature
Lower dorsal surface temperature was lower post
injection for animals injected with saline and NA;
however, none of the changes were significantly different
(Table 2a and b).
3.5. Comparison of upper and lower surface temperatures
Lower dorsal skin surface temperature was significantly lower than the upper dorsal surface skin
temperature when analysed using 81 pixels and 195
pixels (Table 3a and b); however, the difference in
temperature was greater after NA injection was administered. (Table 3a and b). The pattern of surface
temperature change seen in the experimental voles was
not seen in the control group, which were injected with
saline. A significant difference was only shown between
the upper and lower dorsal surface temperature when
using 81 pixels for analysis and before injection with
saline (Table 3b). There was no significant difference
between upper and lower dorsal surface temperature
when using 195 pixels before or after injection with saline
(Table 3a) in contrast to the group injected with NA.
Table 3
Comparison of upper dorsal surface temperature and lower dorsal surface temperature before and after injection with saline or
Noradrenaline
Pre injection
Mean
SD
Post injection
Mean
SD
Upper dorsal surface
Lower dorsal surface
34.323
33.513
1.652
0.613
33.994
33.08
1.752
1.583
Paired t-test
Difference 0.81
T=1.63
p=0.148
Saline
(a) 195 pixels
Difference=0.914
T=1.82
p=0.111
Noradrenaline
Upper dorsal surface
Lower dorsal surface
34.98
34.272
Paired t–test
Difference=0.708
T=6.7
p50.001***
0.83
0.743
35.219
34.205
0.927
0.906
Difference=1.014
T=4.43
p50.001***
(b) 81 pixels
Upper dorsal surface
Lower dorsal surface
34.83
33.257
Paired t-test
Difference=1.573
T=3.75
p=50.007**
1.738
1.083
34.457
33.44
1.829
1.564
Difference=1.017
T=1.9
p=0.009
Noradrenaline
Upper dorsal surface
Lower dorsal surface
35.336
34.515
Paired t–test
Difference=0.821
T=4.45
p50.001***
0.71
0.87
35.66
34.402
Difference=1.258
T=8.17
p50.001***
0.916
0.948
91
D.M. Jackson et al. / Journal of Thermal Biology 26 (2001) 85–93
3.6. Warm and cold acclimation
4. Discussion
3.6.1. Surface temperature
Average surface temperature of the upper and lower
dorsal surface was not significantly different between
warm and cold acclimated voles, before or after injection
with NA (Table 4a and b).
In small mammals BAT is found in distinct depots
situated in the neck and dorsal interscapular region
(Davenport, 1992; Cossins and Bowler, 1987). The
results of previous studies have shown that the shorttailed field vole Microtus agrestis also has an interscapular depot of brown fat, (Jackson et al., submitted;
McDevitt and Speakman, 1996). Non-shivering thermogenesis is initiated in the BAT by cold acclimation, or it
can be experimentally induced by injection with NA
(Jansky, 1973; Bockler et al., 1982). In the present study,
upper dorsal surface temperature, overlying the BAT
measured by IRT was 0.8218C greater than lower dorsal
surface temperature, and this was increased to 1.2588C
after NA was administered. This suggests that IRT can
be used to distinguish between skin surface areas
overlying BAT and skin surface areas that do not
possess BAT. This finding agrees with other studies
that have used IRT to show BAT in the rat (Blumberg
et al., 1999), in the bat Nyctalus noctula (Bickel and
Radermacher, 1994) and the new-born infant (Oya et al.,
1997). However, these studies did not directly compare
skin surface temperature overlying BAT depots with
areas that had no BAT.
3.6.2. Metabolism
Resting metabolic rate was not significantly different
between warm and cold acclimated voles (t-test, t=0.76,
p=0.46). However, peak metabolism following NA
injection was significantly higher in cold acclimated
voles (ANCOVA, F=6.26, p=0.022) and was also
significantly higher in cold acclimated voles if RMR
was included in the peak metabolism estimate (ANCOVA, F=6.96, p=0.017).
3.6.3. Comparison between change in surface temperature
following NA injection and peak metabolism reached after
NA injection
Change in upper dorsal surface temperature did not
significantly correlate with residual peak metabolism
(Fig. 5, F=0.67, p=0.425).
Table 4
Comparison of upper and lower dorsal surface temperature between warm and cold acclimated short tailed field voles
Pre injection
Mean
SD
Post injection
Mean
SD
(a) Upper dorsal surface
195 pixels
Cold acclimated
Warm acclimated
Two sample t-test
34.71
35.22
T=1.32, p=0.21
0.676
0.916
35.043
35.376
T=0.73, p=0.48
0.901
0.974
81 pixels
Cold acclimated
Warm acclimated
35.134
35.516
0.666
0.737
35.515
35.79
0.844
1.007
Two sample t-test
T=1.12, p=0.28
T=0.61, p=0.55
(b) Lower dorsal surface
195 pixels
Cold acclimated
Warm acclimated
34.257
34.285
Two sample t-test
T=0.08, p=0.94
81 pixels
Cold acclimated
Warm acclimated
Two sample t-test
34.509
34.52
T=0.03, p=0.98
0.514
0.935
34.201
34.21
0.77
1.059
T=0.02, p=0.98
0.55
1.12
34.431
34.38
T=0.12, p=0.91
0.843
1.08
92
D.M. Jackson et al. / Journal of Thermal Biology 26 (2001) 85–93
5. Conclusion
In summary, the results of this study suggest that IRT
is not an effective method for measuring NST capacity
in the BAT, since changes in upper dorsal surface
temperature did not significantly correlate with peak
metabolism following NA. In addition, changes in upper
dorsal surface temperature did not reflect changes in
peak metabolism following NA injection brought about
by cold acclimation.
Acknowledgements
Fig. 5. Relationship between change in temperature after NA
injection and residual peak metabolism, (linear regression,
y=1.79+0.36x, f=0.67, r2=0.043, p=0.425).
We are grateful to Peter Anthony for technical
assistance with the thermograph and to the BBSRC
equipment loan pool for the loan of the equipment. This
work was supported by a BBSRC studentship awarded
to DMJ and by the Scottish Office Agriculture,
Environment and Fisheries Department.
References
Capacity for NST in the BAT increases after cold
acclimation (Jansky, 1973; Feist and Rosenmann, 1976;
Rafael et al., 1985). If heat production in the BAT was
increased by cold acclimation, one would expect that
surface temperature overlying the BAT would reflect
this increase in heat production. In the present study,
peak metabolism following NA injection was significantly greater in cold acclimated voles; however, there
was no significant difference shown in the surface
temperature of the upper dorsal surface (overlying the
BAT). There was also no significant correlation found
between change in the surface temperature of the upper
dorsal skin temperature and peak metabolism reached
following NA injection.
Blood flow to the BAT significantly increases following NA injection (Puchalski et al., 1987), a possible
reason for our findings is that the heat produced by the
BAT is shunted away by the increase in blood flow
initiated by the NA injection. Therefore, surface
temperature measurements would not reflect the
capacity for NST in the BAT. Alternatively cold
acclimation could have increased the size of the BAT
depot rather than the capacity for NST. The change in
BAT size would not have been evident from the
IRT results as the areas used for the analysis were
consistent; however, the change would have been
evident using metabolism following NST. Another
possible explanation is that the cold acclimated animals
are constricting the blood flow to the skin surface to
reduce heat loss, therefore, surface temperature
would not be a good indicator of capacity for NST in
the BAT.
Astrup, A., 1986. Thermogenesis in human brown adipose
tissue and skeletal muscle induced by sympathomimetic
stimulation. Acta Endocrinol. 278, 112–132.
Bartholomew, G.A., Vleck, D., Vleck, C.M., 1981. Instantaneous measurements of oxygen consumption during preflight warm-up and post flight cooling in sphingid and
saturniid moths. J. Exp. Biol. 90, 17–32.
Bazin, R., MacArthur, R., 1992. Thermal benefits of huddling
in the muskrat (Ondatra zibethicus). J. Mammal. 73, 559–564.
Bickel, H., Radermacher, H., 1994. Thermographie einer
erwachenden Fledermaus. Biol. unserer Z. 24 (3), 129–130.
Blumberg, M.S., Deaver, K., Kirby, R.F., 1999. Leptin
disinhibits non-shivering thermogenesis in infants after
maternal separation. Am. J. Physiol. 276 (45), R606–R610.
Bockler, H., Steinlechner, S.T., Heldmaier, G., 1982. Complete
cold substitution of noradrenaline-induced thermogenesis in
the Djungarian hamster Phodopus sungorus. Experimentia 38,
261–262.
Contaldo, F., Presta, E., di Biase, G., Scalfi, L., Mancini, M.,
Maddalena, G., de Divitiis, O., Rocco, P., 1981. Preliminary
evidence for brown fat defect in human obesity. The Body
Weight Regulatory System: Normal and Disturbed Mechanisms. Raven Press, New York, pp. 143–146.
Contreras, L.C., 1984. Bioenergetics of huddling- test of a
psycho-physiological hypothesis. J. Mammal. 65 (2), 256–262.
Cossins, A.R., Bowler, K., 1987. Temperature Biology of
Animals. Chapman & Hall, London.
Davenport, J., 1992. Animal Life at Low Temperature.
Chapman & Hall, London.
Feist, D.D., Rosenmann, M., 1976. Norepinephrine thermogenesis in seasonally acclimitized and cold acclimated
red-backed voles in Alaska. Can. J. Physiol. Pharmacol. 54,
146–153.
Hayes, J.P., Speakman, J.R., Racey, P., 1992. The contributions of local heating and reducing exposed surface area to
D.M. Jackson et al. / Journal of Thermal Biology 26 (2001) 85–93
the energetic benefits of huddling by short-tailed field voles
(Microtus agrestis). Physiol. Zool. 65, 742–762.
Jackson, D.M., Trayhurn, P., Speakman, J.R. Comparison of
physiological and molecular approaches for quantification of
non-shivering thermogenic capacity. Submitted for publication.
Jansky, L., 1973. Non-shivering thermogenesis and its thermoregulatory significance. Biol. Rev. 48, 85–132.
Koteja, P., 1996. Measuring energy metabolism with open-flow
respirometric systems? which design to choose? Funct. Ecol.
10 (5), 675–677.
Krattenmacher, R., Rubsamen, K., 1987. Thermoregulatory
significance of non-evaporative heat loss from the tail of the
coypu (Myocastor coypus) and the tammer-wallaby (Macropus eugenii). J. Therm. Biol. (22), 109–116.
Lancaster, W.C., Thomson, S.C., Speakman, J.R., 1997. Wing
temperature in flying bats measured by infrared thermography. J. Therm. Biol. 22, 109–116.
McCafferty, D.J., Moncreiff, J.B., Taylor, I.R., Boddie, G.F.,
1998. The use of IR thermography to measure the radiative
temperature and heat loss of a barn owl (Tyto alba). J.
Therm. Biol. 23 (5), 311–318.
McDevitt, R.M., Speakman, J.R., 1996. Summer acclimatization in the short tailed field vole, Microtus agrestis. J. Comp.
Physiol. B. 166 (4), 286–293.
Mory, G., Bouillaud, F., Combes-George, M., Ricquier, D.,
1984. Noradrenaline controls the concentration of uncoupling
protein in brown adipose tissue. FEBS Lett. 166, 393–396.
Nicholls, D., Locke, R.M., 1984. Thermogenic mechanisms in
brown fat. Physiol. Rev. 64, 1–64.
Oya, A., Asakura, H., Koshino, T., Araki, T., 1997. Thermographic demonstration of non-shivering thermogenesis in
93
human new-borns after birth: its relation to umbilical gases.
J. Perinatal Med. 25 (5), 447–454.
Puchalski, W., Bockler, H., Heldmaier, G., Langefeld, M.,
1987. Organ blood flow and brown adipose tissue oxygen
consumption during Noradrenaline induced non-shivering
thermogenesis in the Djungarian hamster. J. Exp. Zool. 242,
263–271.
Rafael, J., Vsiansky, P., Heldmaier, G., 1985. Increased
contribution of brown adipose tissue to non-shivering
thermogenesis in Djungarian hamster during cold-adaptation. J. Comp. Physiol. B 155, 717–722.
Rothwell, N.J., Stock, M.J., 1979. A role for brown
adipose tissue in diet-induced thermogenesis. Nature 281,
31–35.
Ryan, B.F., Joiner, B.L., Ryan, T.A., 1985. Minitab Handbook. PWS-Kent, Boston.
Speakman, J.R., Ward, S., 1998. Infrared thermography:
principles and applications. Zoology-Anal. Complex Systems
101 (3), 224–232.
Trayhurn, P., Milner, R.E., 1989. A commentary on the
interpretation of in vitro biochemical measures of brown
adipose tissue thermogenesis. Can. J. Physiol. Pharmacol. 67,
811–819.
Walsberg, G.E., 1991. Thermal effects of seasonal coat change
in 3 sub-artic mammals. J. Therm. Biol. 16, 291–296.
Ward, S., Rayner, J.M.V., Moller, U., Jackson, D.M.,
Nachtigall, W., Speakman, J.R., 1999. Heat transfer from
starlings Sturnus vulgaris during flight. J. Exp. Biol. 202 (12),
1589–1602.
Weir, J.B., 1949. New methods for calculating metabolic rate
with special reference to protein metabolism. J. Physiol. 109,
1–9.