PII: SO306-4565(96)00039-3
WING
J. therm. Biol. Vol. 22, No. 2. pp. 109-I 16, 1997
0 1997 Elsevier Science Ltd
All nghts reserved. Printed in Great Britain
0306-4565/97 $17.00 + 0.00
TEMPERATURE
IN FLYING
BATS
INFRARED
THERMOGRAPHY
WINSTON
C. LANCASTER,*
Department
of Zoology,
(Receioed
SUSAN
University
15 June
C. THOMSON
of Aberdeen,
1996; accepted
and
Aberdeen
in rtwised.form
MEASURED
JOHN
BY
R. SPEAKMAN
AB24 2TZ, Scotland
7 December
1996)
Abstract-l.
We collected data on the wing temperature
of flying bats using infrared thermal imaging
to assess the thermoregulatory
function of wing membranes.
2. Thermographic
images of two Egyptian Fruit Bats, Rouse/tus aeg.vptiacus were captured as they flew
along a 12 m length of corridor.
3. Body temperature
was measured before the first flight and immediately after flight sequences using
a rectal thermister probe.
4. Temperatures
across the wing ranged from 34X near the forearm muscle mass, to less than 24’C
at the trailing edge (mean ambient temperature
23°C). The majority of the wing was I-2°C above ambient
temperature.
5. We found small, but significant changes in body temperature
during flight. These changes did not
correlate with changes in wing temperature.
0 1997 Elsevier Science Ltd
Kqv
Word Index:
Bat, Jight,
thermoregulation,
irzfrared
INTRODUCTION
thermograph)
studies assessed
heat
Endothermic
animals
temperatures
that
thermal
this
tolerance.
approach
phenomenon
include
reactions,
in the speed of muscular
Conversely,
basal metabolic
animals
hazard
strenuous
dissipated
ture, wing temperature
of
membranes.
of bio-
increase in efficiency of digestion,
metabolic
it also
of
upper
the acceleration
increase
high sustainable
limit
of the advantages
the
contraction
rate (Garland
carries
with high body
of hyperthermia
1991).
et al.,
disadvantages.
rate increases
and a
A high
food requirements
and
temperatures
incur
if heat generated
the
by
physical
activity
cannot
be efficiently
(Reeder and Cowles, 1951; Cossins and
Bowler, 1987).
Flight is one of the most metabolically
activities
in which vertebrates
Butler et
al.,
circumstances,
1977; Rothe
the
engage (Tucker,
et al.,
dissipaiion
elevations
may
or vascular
They correlated
in ambient
to
artificially
body temperachanges
vascular
in wing
changes
and body temperature.
with
These
experiments,
however,
the absence
accompanies
of convective
cooling that normally
flight, monitoring
of temperature
from
an inappropriate
may have been confounded
area
stressful experimental
limited technically
of wing
protocol.
and
by
a potentially
Previous
by the difficulty
surface temperature
studies were
of recording
the
of the wings of a bat in flight. We
sought to correlate changes in body temperature and
wing surface temperature
in a more natural situation
in flight
membranes
1966;
to test
the
for thermoregulation.
the first data
1987) and in certain
of heat
bats
heat stress while monitoring
of a bat
demanding
of the wing to dissipate
restrained
imposed
operate
chemical
the capacity
subjecting
at body
commonly
Explanations
by
on changes
flying bat as measured
function
of wing
Here, we present
in wing temperature
by infrared
in a
thermography.
limit
endurance
Speakman
(Carpenter,
1986; Thomas et al., 1991;
et al., 1994). Previous investigations
have
suggested
that the wings of bats are well suited for the
MATERIALS AND METHODS
We
collected
thermoraphic
images
of flying bats
dissipation
of body heat on account of their large
surface area and vascularity (Cowles, 1947; Reeder
using an infrared
imaging system (Thermovision
and Cowles,
Agema
system
Systems, Danderyd,
Sweden). The
of an infrared-sensitive
scanner
1951; Kluger
*To whom correspondence
nhi596waberdeen.ac.uk:
272396.
and Heath,
1970). These
Infrared
consists
operated
by
electromagnetic
was monitored
should be addressed.
e-mail:
Tel. 01224 272879; Fax: 01224
109
a
880,
dedicated
control
system.
The
radiation from the surface of objects
to generate false-color depictions of
110
W. C. Lancaster (‘I trl.
(accurate to 0.1C) based on an
of 0.95. For the surfaces of
surface temperature
assumed emissivity
animals,
emissivity
of “infrared
almost
always
between
Gates,
1969). Flight
thermal
0.95 and
sequences
filmed with a video camera
radiation
1.00” (Porter
is
and
were simultaneously
(Sony
Hi-8) to record
were used in these experiments.
bred from a stock originally
maintained
in captivity
membrane
Bats were captive
captured
in Israel, and
on a diet of fruit and vitamin
to generate
temperature.
from the camera,
pixel counts
percentage
distance
body
value,
length
was
forearm
muscle
560 mm and their masses were 153 g
sharply
to
and
130 g. The
naked.
although
forearm
wing
membranes
muscular
were sparsely
were housed
of
portions
covered
in an indoor
both
bats
were
virtually
of the arm and
with hair.
flight
2.7 m x 3.7 m x 3.0 m.
A
I2 h
established
temperature
arena
Animals
measuring
photoperiod
was
the
inflection
temperature
at
30%
(Fig. I ). From this point, values of the pixels declined
gradually
toward
the majority
the temperature
of the wing
small temperature
characteristic
membrane.
difference
Second,
of
the
between the trailing edge
of the wing and the background
12 m by I.5 m by 2 m
screen, 150 cm in height. situated
flight path left an opening
of
which
bats
flew. The
ther-
establish
the second
the restricted
made determination
Data were analyzed
ANOVA.
to changes
temperature
past. Over a period of one week prior to recording,
interpolated
bats were given at least three
flight in the corridor.
Flights
comparisons
evening, approximately
training sessions of
commenced
in the
3 h after the beginning
daily dark phase. Bats landed occasionally
between
hereafter
Because
were
and
both with respect to
body temperature
not
recorded
body temperature
records
and wing
simultaneously,
values were used for
on the assumption
successive
analysis
changes in body temperature
in wing temperature,
camera manually
an image as the bat flew
called
using regression
We compared
time in flight.
to capture
measurement,
mean wing temperature.
mograph was positioned
adjacent to this opening.
where an observer was stationed who triggered the
of linear
change
of body temperature.
of the
and were
RESULTS
to rest after 2-3 min of flight, thus dividing
recording
sessions
into
several
Recording sessions were terminated
reluctant to fly.
Ambient
throughout
and body
temperature
flight
sequences.
if the bat became
We analyzed
sequences
94 images of two bats from 37 flight
recorded
on eight nights.
images were captured
were monitored
flight sessions with an electronic
ter and Type K thermocouple.
thermis-
Body temperature
was
per recording
temperature
ranged
Through
significant
change in the proportion
were
flight
each flight sequence.
During
flights the thermister displayed ambient temperature
in the corridor;
this typically remained
constant
(mean & sd. 23.8 C + 0.28 C, N = 43) through
sessions.
Images were analyzed using software provided by
the manufacturer.
We selected images that depicted
the surface of one entire wing. The temperature
of
each pixel was recorded along a profile defined by the
video scanning line from the peak temperature at the
elbow to the trailing edge of the wing membrane.
Variations in the bat’s orientation
could place this
profile at any alignment across a triangular area of
82
in
from 22224-C.
Data from a third bat were eliminated
from the
analysis due to its erratic flight and limited images.
immediately
following
On average,
session, of which
I3 were usable. A typical usable image is depicted
Fig. 2. Ambient
measured
by inserting the thermocouple
approximately I cm into the rectum before the first flight and
recording
decreased
approximately
caudal to the elbow and 10% of the distal values to
50 x 150 cm through
allowed
be
bats flew in a section of corridor
approximately
high. An opaque
midway
in the
mean
could
of the precise position of the edge ambiguous.
To
avoid these biases, we eliminated 30% of the pixels
I8 C and 23’C.
During recording,
overall
however,
First, due to the heat of the
mass,
an
wing
of pixel
ranged between
and ambient
that measured
(henceforth,
into
using
Mean
as the average
This mean,
skewed by two factors.
The
were converted
as a reference.
less the ambient
wing temperature).
approximately
of pixels
of the bat
along the wing membrane
were expressed
We
of wing
Since the number
based on the distance
supplements.
wingspan
measurements
per profile varied.
temperatures
(Rousrtrus
aeg~pptiucvx)
Fruit bats
with the apex at the elbow.
used these data
the bat’s
flight times and verbal notes.
Two Egyptian
the plagiopaagium
the periods of flight sequences,
in
(ANOVA,
there was no
of time that bats
F = 0.96,
P > 0.05).
Dividing total elapsed times into 100 set periods, bats
were in flight an average (mean _t sd) 49 + 27.1 set
per 100 sec.
On average.
the body
temperature
was
38.o’C
( + 0.77) prior to flight. For each night of data, the
relationship
between
body temperature
and elapsed
time in flight followed a curvilinear relationship that
in some cases was well described by a second order
polynomial regression (Fig. 3a). In other instances,
the second order polynomial
explained less of the
variability (Fig. 3b). For the eight nights of data, r2
Wing temperature in bats
values of these regressions ranged from 0.231 to
0.973. The pooled data for all eight nights are
presented in Fig. 4. This curve reached a maximum
of 385°C after approximately 950 set of flight. From
that peak, the curve returned to 38°C at approximately 1890 sec.
Wing membrane surface temperatures were about
15°C below body temperature and on average, only
slightly above ambient. The overall mean wing
temperature
( _t sd) was 1.8”C ( + 0.5) above
ambient, with a range of 0.7”C to 3.3”C (N = 92).
The restricted mean wing temperature was 0.8”C
( + 0.2) above ambient, ranging from 0.3 to 2.1%.
During flight, there was no significant relationship
between wing temperatures
and elapsed time,
regardless of the measure of wing temperature used
(Fig. 5). Wing temperature (based on the restricted
data set), showed a nearly significant, positive
correlation
with actual and interpolated
body
temperature (F = 3.3, P = 0.073).
DISCUSSION
Through most of the recordings, the majority of
the wing membrane surface was less than 1°C warmer
than ambient. Although we detected small changes
during flight, they did not appear to relate to elapsed
time in flight and were only weakly correlated to
changes in body temperature.
111
The role of the wings in thermoregulation has been
the subject of several studies. Cowles (1947) Reeder
and Cowles (1951) and Bartholomew et al. (1964)
reported vasodilation in the wings and uropatagium
of stationary
bats (both Megachiroptera
and
Microchiroptera) in response to elevated ambient
temperature. Some species of flying fox (Pferopus sp.)
envelop the body with the wings when at rest to
conserve heat. Bartholomew et al. (1964) found that
the external surface of the wing membrane of a
roosting Pteropus poliocephalus closely tracked a
falling ambient temperature (1 to 2°C above), while
the body temperature remained constant.
Our data on wing temperatures contrast with those
of Kluger and Heath (1970). They reported elevations
in excess of 5°C in correlation with elevated body
temperatures. The greatest increase we measured in
the reduced data set was about 2°C. In part, we
attribute the discrepancy to differences in methodology. Data reported by Kluger and Heath (1970) as
wing temperature were recorded from a subcutaneous
thermocouple on the foreann. In our thermographic
were consistently
images, forearm temperatures
higher than the webbing of the wing (Figs 1 and 2).
A bat in flight generates considerably more heat
than when at rest (Tucker, 1966; Butler et al., 1973;
Rothe et al., 1987). The generation of heat in flight
can be estimated from equations relating power
consumption to body mass (e.g., Speakman and
0 29.010
. 44.007
A 67.016
IA
:’
32
0
b
30
A
q
22-i.
0
t
elbow
I.
10
1.
20
‘.‘.‘.‘.
30
40
Percent
50
60
‘-
70
‘-‘-
80
QO
of Profile
100
t
trailing edge
Fig. I. Profile of surface temperatures across the wing of Rouserrus uegyptiacus from three thermographic
images. Symbols refer to the sequence and image number.
W. C. Lancaster
ei al
Fig. 2. False color image of surface temperature
of Rousertus rregyptiacus in flight. The double image
results from movement of the bat during the lapse in time between the two sets of scans that form a
complete video frame. Scale at right indicates temperature
(“C) represented
by colors. The range of
temperatures represented by a color is determined by the full scale; each pixel can be read to O.l”C,
regardless of the full scale range.
11.8 W.
account
for
two
Not all of this power appears as heat within the flying
animal because some is channeled into mechanical
between
the
expected
instance,
if the bat flew at only 3 ms- ‘, mechanical
power
output.
output
for a 130 g bat with a wingspan
power would increase to 1.85 W, resulting
increase
in the time required
to raise
Racey,
1991), which
We evaluated
using the mechanical
Pennycuick
(1989).
minimum
for a 130 g bat yields
the mechanical
power prediction
The mechanical
power speed (6.8 ms
power
of 560 mm
program
power
of
at
‘) was 1.4 W and thus
temperature
of magnitude
and
observed
difference
values.
For
in a
body
by 1°C to 55 sec.
Martineau
significant
orders
and
quantities
Larochelle
(1988)
found
of heat were dissipated
that
through
the metabolic energy appearing as heat within the
animal amounted to about 10.4 W. The elevation of
the legs of flying pigeons (Coloumba livia). Carpenter
(1986) discussed the role of the feet in thermoregula-
temperature
tion in a l-lying bat (Pteropodidae).
by 1°C (using the specific heat of 130 g
He recorded
low
of water) without convective cooling would require
543 J. The bat’s body temperature
could, therefore,
be expected to increase 1°C in 52 sec. The curve in
ambient
Fig. 4 indicates an increase of only 0.04”C in the first
52 set of flight and less than 0.5”C in 950 sec. The
from 5 to 10°C. Carpenter (1986) noted that elevated
foot temperatures
persisted after flight, presumably
bats, therefore,
until body temperature
declined. He suggested that
changes in blood flow, both to the wings and feet
could conserve heat at low ambient temperatures
or
clearly dissipate
significant
quantities
of the extra heat generated in flight. Even if some of
the assumptions
here are inaccurate, they could not
surface temperatures
in the feet at ambient temperatures below 15°C. Above 15”C, the difference between
and foot
temperatures
increased,
ranging
Wing temperature in bats
alternatively,
dissipate
tures. The effectiveness
heat at high body
on the temperature
gradient
That
temperatures
high ambient
dissipation
tempera-
of either strategy is dependent
render
of heat from the wings ineffective
offered as one explanation
ity (Reeder
and
Cowles,
Thomas
et
al.,
1991),
modeling
suggests
for chiropteran
this may only
Mammals
the
has been
nocturnal-
1951; Carpenter,
although
more
in tropical
regions
(Speakman
have limited options
of excess heat. Heat loss through
et al.,
in bats by the coupling
for the dissipation
respiration
of respiratory
1986;
in
and by the danger
of respiratory
et al., 1991). Dissipation
probably
alkalosis
(Thomas
the feet is
small surface
Body Temperature in Flight
1600
q y =
38.660- &4738&x-
600
Elapsed
Fig. 3. Two examples
1600
2000
2.5033e-7xA2 IV2 = 0.531
1000
1200
1400
Time (sec.)
of body temperature
of Rousettus aegyp/iacus as a function
Each plot depicts data from one night.
to
et al., 1995)
of heat through
limited due to their relatively
is limited
frequency
wing beat (Suthers et al., 1972; Lancaster
detailed
be important
bats
1994).
with the environment.
would
larger
113
of elapsed time in flight.
W. C. Lancaster
114
et ui.
40
0
O0
39%OOo
G
c
e
!?
3
?!
O.
*oo
zE
cpo
o
00
0
0
0
00
O
“0,”
O”
04
0
a0
&
*o”
OO OO
0
0
0
0
z
i-
0”
0
$
0
*OO
0
\
IO
Elapsed
Time
(WC)
Fig. 4. Body temperature of Rouwrm treg~p/irrcus as a function of elapsed time in flight. pooled data from
eight nights. There was a significant curvilinear relationship
described by the least squares fit polynomial
regression equation.
Th = 38.027 + 8.89.10-‘r
- 4.7-10 ‘t:: r’ = 0.1 12; I = 2.4; P = 0.02; F = 2.96.
area.
Bats
(Crowley
facilitate
have
no
sweat
glands
in the
wings
and Hall, 1994) and licking of the body to
evaporative
Bartholomew
cooling,
as
reported
et al. (I 964) and Carpenter
0
500
probably
of Rouseims
routes
to times when animals
are at rest.
of heat loss are respiratory,
and
and
by
through
the body surface, feet, wing membranes
( 1985) is
surfaces
of limbs
loo0
Elapsed
Fig. 5. Wing temperature
limited
The major
within
the wings.
Dissipation
2otM
1500
Time (set)
aegyppriucus in flight as a function
relationship.
of elapsed
time. No significant
2500
of
Wing temperature
in bats
115
Table I Comparison
of relative heat loss from the wings and body of Rouser~us aegyptiacus using a flat plate model.
Head and body surface area measurements
were estimated as the surface area of cones based on measurements
taken
from a carcass; wing area measurements
from Norberg and Rayner (1987). Flight velocity was based on minimum power
speed (Pennycuick,
1989). Wing velocity was based on the sum of the velocity of the mid point of the wing (assumed
to be the chord) at a wingbeat frequency of 7.1 Hz (Jones, 1994) and the flight velocity. Relative heat loss per unit area
was calculated as the product of temperature
and the square root of velocity; total heat dissipation factors surface area
into the equation
Temperature
difference
Area
(cm’)
Wings
Head and body
heat
1090
123
through
the
wings
(“C)
Velocity
(ms - ‘)
1.8
11.0
10.0
6.8
may
be
an
effective
thermoregulatory
mechanism
gradient
the body surface and environment
between
but, the large thermal
(based on our images, e.g. Fig. 2) may dissipate
heat than the relatively
Heat transfer
proportional
difference
more
cool wings.
(per unit area) from a flat plate is
to
the
product
of
with the environment
the
temperature
and the square root
of the velocity of air moving over it (Holman,
Estimated
Table
value
of these
parameters
I. Due to the greater
body dissipates
approximately
1986).
are listed
thermal
gradient,
in
the
five times more heat
per unit area than the wings. But at 1090 cm’ (545 cm’
per surface), a flat plate of the same area as the wings
would
dissipate
almost
twice as much
heat as the
body. This model suggests that due to the great area,
a small thermal
gradient
at dissipating
excess
recorded
in wing membrane
to those
(Kluger
recorded
and Heath,
of differences
at high
The small
changes
temperature,
in heat-stressed
we
compared
stationary
bats
1970) are more likely the result
in experimental
logical response.
flight
in the wings may be effective
heat.
Changes
ambient
protocol
than physio-
in wing temperature
temperatures
remain
during
to be
established.
Acknowledgements-The
thermograph
was provided
by
EPSRC. We appreciate
the assistance of Peter Anthony in
the operation of the equipment and with data handling. We
thank Beverly Campbell, Diane Jackson, Giles Mackey and
Ros Clubb for their assistance with data collection.
This
work was supported
by BBSRC grant GR/J36150.
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