261
Insights into animal temperature adaptations revealed
through thermal imaging
Published by Maney Publishing (c) Royal Photographic Society
G J Tattersall* and V Cadena
Department of Biological Sciences, Brock University, St Catharines, Ont. L2S 3A1, Canada
Abstract: Infrared thermal technology allows for the real-time visualisation of fixed or
transient changes in the long-wave radiative energy emanating from an object, in essence,
allowing for the estimation of surface temperature. Animal surface temperatures are, therefore,
readily detected using this technology, allowing for the assessment of physiological responses
associated with the regulation of body temperature. In this paper, we will introduce some recent
advances made possible or enhanced through the use of thermal imaging. In particular, this
imaging technology has shed light on the regulation of peripheral blood flow in endothermic
animals, on the dynamics of animal heat transfer in complex thermal environments, on the
production of heat associated with metabolism and on the importance of evaporative heat loss
to respiratory function and its potential contribution to preventing overheating of the brain.
More than a simple imager for temperature, this technology has the potential to contribute a
greater understanding of animal thermal adaptations, not only since it provides live information
on surface temperatures, but more importantly because its non-invasive nature which allows
measurements to be obtained with minimal disturbance.
Keywords:
thermoregulation, peripheral heat loss, infrared thermal imaging, mammal, bird, reptile
This paper is part of a special issue on infrared
1
INTRODUCTION
Animals achieve thermal balance through a combination of physiological, behavioural and physical processes. As their environmental temperature
changes, they may elect to redistribute internal body
heat or alter their exposure to different microhabitats
in order to achieve their optimum temperature. Some
animals, namely, endotherms (e.g. birds and mammals), produce their own heat, and as such, must have
mechanisms for conserving this heat, whereas most
other animals (e.g. fish, amphibians, reptiles and
invertebrates) are ectothermic, and derive their body
heat from their environment. In other words, they
utilise behavioural mechanisms to capitalise on
physical processes in the environment (radiative,
The MS was accepted for publication on 29 February 2010.
* Corresponding author: Glenn J. Tattersall, Department of
Biological Sciences, Brock University, St Catharines, Ont. L2S
3A1, Canada; email: [email protected]
IMAG IR1 # RPS 2010
DOI: 10.1179/136821910X12695060594165
convective, conductive or evaporative heat exchange).
Understanding these processes has involved, over the
past decades, techniques from a variety of disciplines: neurophysiology, metabolic biochemistry,
neuroethology and ecology. Infrared thermal imaging
and other non-invasive thermal diagnostic tools,
however, have more recently begun to allow us to
visualise and understand some of these thermoregulatory processes in greater detail,1–3 while allowing for
non-invasive measurements on conscious, non-instrumented animals exhibiting spontaneous, normal
behaviours. Thus, not only does infrared thermal
imaging provide access to thermal information on a
rapid time scale, but it also affords an ethically valid
approach to the study of heat exchange in animals,
and as such, is a valuable technique in the physiologist’s or ecologist’s toolkit. In this paper, we will
briefly highlight a number of compelling thermoregulatory examples that have been visualised and
quantified using thermal imaging technology.
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TATTERSALL AND CADENA
Published by Maney Publishing (c) Royal Photographic Society
2 VISUALIZING VASCULAR THERMAL
WINDOWS
Endothermic animals primarily produce the heat
required for maintaining an elevated body temperature through an augmented internal metabolism. In
order, however, for an endotherm to maintain its
temperature throughout the body, the internally
generated body heat must be distributed from the
core to the periphery. Upon the onset of when body
temperature is regulated at a reduced level (e.g.
during sleep, anaesthesia and hibernation) perfusion
to the peripheral tissues must initially be maintained
or increased, thereby delivering core heat to the
periphery and thus more rapidly facilitate conductive,
convective and radiative heat transfer to the environment. At other times, when the internal regulated
level for core body temperature is on the rise,
peripheral blood flow will be reduced, allowing
endogenous heat to be retained within the body.
Relative changes in blood flow to the surface can be
visualised using infra-red thermal imaging technology,4,5 since the delivery of relatively warm blood to
the surface will produce temporal changes in surface
temperature. The surface temperature of an animal,
however, also depends on the interactions between
ambient temperature, metabolic heat production and
insulation, in addition to underlying blood flow.6,7
Although fur and feathers form insulative barriers to
heat flux, changes in blood flow through the subcutaneous shunt vessels and the capillary beds are still
instrumental in regulating body temperature and heat
loss, particularly within the zone of thermally neutral
ambient temperatures.8 The body surfaces that play
important roles in regulating heat loss in endotherms
are sometimes covered in relatively short fur,9 but
often entirely devoid of insulation. These ‘thermal
windows’ typically experience a much greater range
of cutaneous blood flow.8 Known examples of these
‘thermal windows’ include the ears, feet, and nose of
mammals,4,9 and the bills, feet and facial skin (comb
and wattles) of birds.5,10–15 Recently, we have
demonstrated that birds, especially toucans, make
extensive use of the bill to radiate body heat when
heat stressed, or likewise to vasoconstrict blood
vessels under the keratinised surface when exposed
to cold (Fig. 1).5 In this extreme case, we calculate
that the bill can, in theory, be responsible for losing
up to 500% of basal metabolic heat production,
suggesting that rather rapid changes in body
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1
The bill of the Toco toucan (Ramphastos toco) acts
as a thermal radiator. In the above infrared thermal
images, relative to the awake state (A), entry into
sleep (B) is associated with a transient increase in
heat loss from the bill as superficial blood vessels
receive increased blood flow. Once sleep occurs, the
bill cools down towards air temperature (C), being
virtually indistinguishable from the background temperature. Toucans are capable of modulating blood
flow to the bill surface to conserve or release heat as
necessary
temperature can be accomplished through this
thermal window.
Numerous endotherms, however, lack an external
insulative layer of fur or feathers (e.g. Fig. 2). Some,
like seals and hippopotamuses, exhibit an extensive
sub-cutaneous fat layer that provides the necessary
insulation (Fig. 3). One of the challenges with
internal insulation, however, is how to cope with
excessive heat production at elevated air temperatures. Seals, for example, when they haul out onto
land exhibit regional ‘hot spots’ on their skin.16 These
regions of high blood flow to the external environment are thought to facilitate localised heat loss,
particularly when the skin is wet and evaporative
cooling can effectively transfer heat away. Whether
this occurs in all large, furless mammals is not, to our
knowledge, known; however, we would expect similar
strategies to exist in these other animals. For
example, when observed through an infrared imaging
camera, the skin of hippopotamuses appears to
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THERMAL IMAGING IN ANIMALS
Published by Maney Publishing (c) Royal Photographic Society
2
263
Nine-banded Armadillo (Dasypus novemcinctus) are
mammals that possess little to no fur, but instead a
heavily keratinised skin. In spite of that thick skin,
these tropical mammals still exhibit very high skin
surface temperatures, indicative of a high heat loss,
but a relative intolerance of low air temperatures.
Nevertheless, they retain the capacity to restrict
blood flow to their ‘thermal windows’, as evidenced
by the much cooler tail and ears
exhibit similar hot-spots (Fig. 3), which may serve as
regions of controlled blood flow to aid in heat loss.
Differential skin temperatures between adult and
juvenile hippopotamuses is also evident from thermal
imaging, suggesting that the development of fatty
insulation and subsequent thermal independence
takes time to occur (Fig. 3), leaving the young at
greater risk of cooling than adults.
These laboratory and physiological approaches
that show differential regulation of skin and other
body surface temperatures could also be taken into
the field. For example, many endotherms must cope
with high or low thermal challenges in their environment. A recent study in musk-oxen used infrared
thermal imaging to estimate heat loss rates from
juvenile and adult animals, and concluded that
contrary to expectations, the juveniles are not at a
relatively greater risk of expending excessive amounts
of energy maintaining thermal balance compared to
adults at extreme cold temperatures (down to
250uC), despite being much smaller and having
higher surface area/mass ratios.17 At the other
extreme, we have witnessed interesting physiological
thermal adaptations in nesting birds, captured with
infrared thermal imaging. During a field trip to
Queimada Grande Island, Brasil (24u29900S,
46u41900W), we were able to obtain infrared thermal
images from numerous incubating Brown Boobies
(Sula leucogaster). These birds were exposed to
relatively warm air temperatures (about 28–30uC),
in addition to the intense solar radiation of the
tropics. Under these conditions, rather than incubate
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3
The hippopotamus (Hippopotamus amphibius), a hairless mammal, has relatively cool skin surfaces
throughout the body (A, adult only), except for the
inner surfaces of the ears. In contrast, a neonatal
hippopotamus (B, with adult), with undeveloped fatty
insulation, demonstrates higher skin surface temperatures at the same air temperature, demonstrating
their higher relative rates of heat loss
their eggs, these birds will shade the eggs in an effort
to prevent overheating.18 One of the interesting
results from our observations using thermal imaging,
however, is that regardless of whether the birds are in
the shade or in full sun, the peripheral ‘thermal
windows’ (e.g. the bills) are at, or very near to body
temperature (Fig. 4). This is in contrast to the
feathered areas of the body exposed to the sun,
which warm to extreme temperatures (.50uC),
emphasizing that vasodilation of blood vessels is
occurring at the thermal windows. This is consistent
with what we have observed in other birds in the
laboratory,5,19 but emphasises the fact that the
surface temperatures of regions of the body with an
underlying vasculature are being determined by the
flow of blood beneath them. This also supports the
notion that endotherms make use of their ‘thermal
windows’ under natural conditions, in order to
modify their heat loads. In the future, this approach
could be used to ascertain whether a bird or a
mammal is relatively heat stressed or not, by
comparing the temperature of the vascularised region
of the body to non-vascularised regions. Vascularised
skin areas should approach body temperature if an
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TATTERSALL AND CADENA
5 Thermal preference and behavioural thermoregulation
in reptiles can be assessed in the laboratory using a
simple, linear gradient of temperatures (e.g. 15–45uC)
that allow animals to freely select a ‘preferred’ temperature. In this example, a cold bearded dragon
(Pogona vitticeps) was placed into a thermal gradient,
and within minutes, it had oriented to a floor temperature of about 34–35uC. Given its body mass
(y300 g), thermal equilibration is slow, and thus the
infrared image above depicts a cool animal relative
to its background selected temperature
4
Brown boobies (Sula leucogaster) often chose nest
sites in exposed locations, with little insulation. The
above images, taken at Queimada Grande Island,
Brazil, demonstrate that boobies in shaded conditions
(A, air temperature 28uC) will incubate their eggs,
whereas boobies in locations exposed to the full summer sun will stand over their eggs (B), thereby shading them. Interestingly, in both instances, the bill
temperature remains between 38 and 40uC (equal to
body temperature), despite the fact that in the
exposed state, the non-vascularised regions of the
bird can achieve temperatures of up to 55–60uC. The
net result is the preservation of egg temperature, but
presumably, with considerable thermoregulatory cost
to the adult
animal is heat stressed, as they attempt to utilise their
non-insulated regions to facilitate heat transfer to the
environment; likewise, these vascularised regions will
approach ambient temperature if the animal is
preserving its body heat by constricting or reducing
blood flow to the underlying vessels.
One final, inventive application of infra-red thermal imaging in mammal ecology research is the use of
remote sensing of difficult to access animal populations for disease related mortality monitoring20 or
population assessments.21 This technique works
particularly well in large mammals due to the large
thermal signature they provide. Since these large
animals emanate a significant heat signal, sensing and
censuses can take place from an aircraft, and the
images acquired are analysed offline. Infrared imaging technology, however, has also been proven
The Imaging Science Journal Vol 58
fruitful in population monitoring of small nocturnal
mammals, such as bats,22 which can be difficult to
count when emerging from their caves at night. Were
it not for the fact that these animals were producing
and losing heat, however, it would prove difficult to
detect them from such large distances or in the
darkness.
3 ASSESSING FIELD TEMPERATURES AND
THERMAL PREFERENCES
Since temperature is inextricably linked to animal
energy requirements, accurate measurements of body
temperature are crucial in many fields of biology.
Many ecological studies attempt to assess these
energetic costs and thermal adaptations by measuring
core temperatures in wild animals and relating these
to their optimal physiological temperatures.23
Infrared thermal imaging can be used, in the simplest
manner, to estimate body temperature in the field
without requiring physical handling or contact. For
small ectotherms of very low thermal inertia (,20–
50 g), thermal imaging provides a reasonable approximation to internal body temperature.24,25 Thermal
preferences in animals can also be estimated in the
laboratory by providing animals with a choice of
temperatures.26,27 Although thermal imaging is not
essential to ascertaining these behavioural responses,
it can be instrumental in elucidating compromises or
interactions between physiological and behavioural
thermoregulation (Fig. 5). Use of thermal imaging
for larger ectotherms, however, which exhibit extensive basking behaviour, can prove to be more
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THERMAL IMAGING IN ANIMALS
Published by Maney Publishing (c) Royal Photographic Society
6
A basking caiman crocodile (Caiman latirostris)
shown half in shade (left, cool) and half in full sun
(right, warm)
problematic, due to the fact that regional heating by
solar radiation can lead to major differences in the
surface temperature throughout the body, without
necessarily a similar change in core body temperature
(Fig. 6). Indeed, it might be that many ectotherms
regulate head or brain temperature rather than body
temperature, as has been so often speculated
(Fig. 7).28 Future use of thermal imaging, which
provides simultaneous measurements of surface
temperatures all over the body, along with core
temperature measurements, should make it possible
to better ascertain the relationship between core and
brain temperature regulation and how peripheral
vasomotor changes contribute to these processes.
4
265
VISUALIZING HEAT PRODUCTION
Ectotherms are generally considered to produce
negligible heat, since their body temperatures normally
track ambient temperature in the absence of radiative
and evaporative heat exchange. However, following
feeding in many ectotherms, particularly snakes and in
those lizards that consume large meals, a significant rise
in metabolism occurs.29,30 This post-prandial metabolic response is often accompanied by behaviours that
allow these animals to capitalise on natural heat
sources in their environment (i.e. augment their body
temperature behaviourally).31 However, the possibility
of using the heat by-product from elevated metabolism
to increase body temperature has only recently been
appreciated. For example, in South American rattlesnakes, a 1–2uC rise in surface temperature occurs
(Fig. 8A), which is sustained for nearly 2 days following a meal.32 Furthermore, the amount of heat
produced is proportional to the size of the meal
consumed as well as the change in metabolism.33,34
IMAG IR1 # RPS 2010
7
A red-footed tortoise (Geochelone carbonaria) shown
in the sun (A) and at a later point in time after the
sun has set and air temperatures have fallen (B),
demonstrating prolonged retention of heat acquired
from solar heating, particularly in the head which
will be shielded from thermal changes when it is kept
withdrawn under the shell
Whether these small changes in temperature assist in
the digestive or assimilative process, however, remain a
subject of study. In addition to total body heating from
post-prandial metabolism, rattlesnakes also exhibit
localised heat production in their tail shaker muscles.
These muscles drive the rattle response, and can
contract up to 90 times a second,35 producing little
work, but releasing most of the chemical energy as
heat. The heat signature can be 1–2uC above the rest of
the body, and is readily detected through thermal
imaging (Fig. 8B). This heat production is not known
to serve any purpose; however, its visualisation with
thermal imaging could be used as a non-invasive way of
assessing muscle recruitment in the context of animal
defence adaptations.
5
VISUALIZING EVAPORATIVE COOLING
In addition to augmented warming of animal surfaces
from the underlying blood (at least in endotherms),
any amount of evaporative cooling that occurs from
moist surfaces can also be readily detected using
thermal imaging. In particular, every time air is
inhaled during breathing, moisture on the inner lining
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TATTERSALL AND CADENA
9
8
Snakes have numerous remarkable temperature
responses that are readily revealed from thermal imaging. The top trace (A) depicts a snake 24 h after
consuming a large meal, demonstrating a significant
increase in post-prandial metabolism which manifests
in a rise in body temperature. The middle trace (B)
is an infra-red thermal image of a South American
rattlesnake (Crotalus durrisus), demonstrating the elevated heat production from the tail shaker muscles
that drive the rattle response. The bottom trace (C)
shows quite clearly the degree of evaporative cooling
that occurs during the normal act of breathing in
snakes. The increased thermal clarity of the bottom
image compared to A and B was produced by briefly
heating the snake with a radiant source, thereby
warming up the surface scales with lower thermal
inertia, and revealing that the regions of the face that
exhibit the greatest degree of evaporative cooling
include the upper airways and the facial pit organs
of the nasal passages evaporates, and cools the
airways (Fig. 8C). In many animals, particularly
reptiles, this cooling is very profound,28 producing
temperatures often 5uC lower than body or brain
temperature. One consequence of this transient,
periodic cooling is that thermal imaging can provide
a rapid means of assessing breathing frequency.5
Animals do, however, capitalise on this evaporation
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Bearded dragon lizards (Pogona vitticeps) increasingly
exhibit open-mouth gaping as they experience body
temperatures higher than their normal, preferred temperatures. This open-mouth breathing promotes evaporation from the moist inner lining of the mouth,
manifesting as the cooler temperatures observed
along the margin of the mouth (inset thermal image).
This evaporation is thought to prevent overheating of
the head and brain at elevated air temperatures
for thermoregulatory purposes. In its simplest form,
panting or open mouth gaping is used by mammals,
birds and reptiles to prevent overheating (Fig. 9).
Indeed, in reptiles, the evaporative cooling on the
inner surfaces of the mouth can be readily visualised
with thermal imaging.36 The effectiveness of this
simple mode of heat transfer is readily observed in
those reptiles that exhibit panting being able to
maintain lower head and brain temperatures than
animals prevented from panting.36,37 For the most
part, however, thermal imaging has been applied less
to the detection of evaporative cooling than to other
modes of heat transfer, suggesting that this could be a
fruitful avenue in the future.
6
CONCLUSIONS
In this paper, we have introduced a number of
potential uses and discoveries made possible with
modern infrared thermal imaging. Although in the
simplest sense, thermal imaging provides an estimate
of animal surface temperature, used within a proper
experimental framework in combination with behavioural and physiological measurements, transient
changes in surface temperatures reveal more interesting aspects of animal thermal adaptations,
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THERMAL IMAGING IN ANIMALS
demonstrating the various means by which temperature balance is achieved in animals. Discoveries such
as these may be increasingly important, since many of
the animals we study are beset with increasing
thermal pressures from anthropogenic influences,
without necessarily the capacity to adapt rapidly to
thermal changes.38
Published by Maney Publishing (c) Royal Photographic Society
ACKNOWLEDGEMENTS
We would like to thank Denis Andrade and Augusto
Abe for allowing access to many reptile specimens
used for thermal imaging purposes. The equipment
used to produce the images in this review was a
Mikron Mikroscan 7515 Thermal Imaging Camera.
We also acknowledge the Parque Ecológico Municipal de Americana, São Paulo, Brazil, for access to
the hippopotamus. This research is supported by the
Natural Sciences and Engineering Research Council
of Canada.
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