AMER. ZOOL..19:239-247 (1979).
Behavioral and Physiological Thermoregulation of Crocodilians
E. NORBERT SMITH
Northeastern Oklahoma State University, Tahlequah, Oklahoma 74464
SYNOPSIS. Crocodilians, like other reptiles, regulate their body temperatures by a combination of behavioral and physiological mechanisms. Behaviorally, they seek warm surface
water or bask when cool and avoid overheating by the evaporation of water from their
dorsum, evaporation of water by gaping or by retreating to deep, cool water. Physiologically, crocodilians increase cutaneous thermal conductance by increasing blood flow to the
skin (and subdermal musculature) during warming. This hastens the warming process.
Cutaneous blood flow is reduced during general cooling and locally if the body temperature exceeds skin temperature. This enables crocodilians to increase body temperature
significantly while basking in cool shallow water. Large crocodilians appear to be able to
alter their rates of heat exchange to a larger extent than small ones and they can do so with
less cardiovascular involvement. Large crocodilians, with their lower surface/volume
ratio, are capable of producing sufficient metabolic heat to elevate their body temperature
above water temperature.
INTRODUCTION
It is often advantageous for animals to
have a high and stable body temperature.
Biochemical reactions are hastened by
high temperatures, resulting in rapid digestion and assimilation of food, faster
conduction of neural impulses, better
coordination, and more rapid growth and
healing. Disadvantages include rapid depletion of stored energy due to the high
rate of metabolism and a reduced safety
margin between body temperature and
upper lethal temperature. Animals can
achieve a high and stable body temperature by either endothermy or ectothermy.
Endothermic birds and mammals increase thermal insulation and produce
Much of the original research was supported by the
National Geographic Society, Welder Wildlife Foundation and Caesar Kleberg Foundation. Recent support has been from N1H (MBS) Grant No. 5 S06
RR08123 and NIH National Institute of General
Medical Science MARC Grant No. 5 T32 GM07694.
This research would not have been possible without
the analysis, critical review and encouragement of
Stanley Robertson, Physicist, Northeastern Oklahoma
State University. W. W. Reynolds and Larry Crawshaw critically reviewed an early version of the paper
and offered several helpful suggestions. I respectfully
acknowledge my sincere appreciation to William W.
Reynolds, The Pennsylvania State University, for organizing and for the invitation to participate in this
symposium. Page charges were paid by N.S.F. Grant
PCM 78-05691 to W. W. Reynolds.
significant heat endogenously. This effectively uncouples their body temperature
from the thermal environment, but depletes large amounts of stored energy
during exposure to severe cold. Ectotherms obtain body heat from the environment but little stored energy is required under low temperature conditions.
Neither approach is unequivocally advantageous. Intergrades benefiting from both
approaches are numerous. Facultative or
partial endotherms include hibernating
mammals, birds and mammals exhibiting
torpor, incubating pythons, many insects
and certain large marine fish.
Most extant reptiles are fully ectothermic, relying on heat from outside the body.
Only in active reptiles exceeding about 5
Kg is a significant amount of endogenous
heat produced. Early studies of reptilian
thermoregulation dealt with behavioral
thermoregulation of lizards (Mazek-Fialla,
1941; Strel'nikov, 1944; Bogert, 1949;
Pearson, 1954). During the 1950's and
1960's, preferred and lethal temperatures
of numerous reptiles were described
(Brattstrom, 1965). In the 1960s, emphasis
in reptilian thermoregulation studies
began shifting from behavior to physiology. Bartholomew and his students at
UCLA demonstrated that several species
of lizards are able to alter their rates of
heat exchange physiologically (Bar-
239
240
E. NORBERT SMITH
tholomevv and Tucker, 1963; 1964; Bartholomew and Lasiewski, 1965; Bartholomew et al., 1965). More recently,
similar phenomena have been observed in
fishes (Reynolds, 1977; Reynolds and
Casterlin, 1978).
water is an important avenue of heat exchange. Heat may be lost by the evaporation of water. Although its thermoregulatory significance in crocodilians was denied
by Neill (1971), basking is generally recognized as occuring when air temperature
exceeds water temperature. How does a
wet crocodilian determine when the dry
Crocodilian thermoregulation
bulb air temperature exceeds the water
Thermoregulation of crocodilians was temperatuere? Recent studies with allipoorly studied until the present decade. gators showed that alligators pause parallel
Mcllhenny (1935) reported much of the to the shore with the dorsum exposed to
natural history of alligators and mentioned the air in a "pre-basking" posture. After
that they "sunned" or "basked" when air the dorsum was dry, alligators either crawled
temperature exceeded water temperature. out to bask or retreated to deeper water
Colbert et al., (1946) established preferred (Smith, 1975«) depending on skin or core
and lethal temperatures for alligators, and temperature. This behavior along with
Cott (1961) reported thermoregulatory the response to local heating and cooling
behavior in the Nile crocodile, Crocodilus (Smith et al., 1978) suggests crocodilians
niloticus. Coulson and Hernandez (1964) possess cutaneous thermal receptors.
reported effects of temperature on bioCrocodilians bask in part to increase
chemical reactions in alligators.
body temperature (Cott, 1961; Smith,
Of the crocodilians, alligators have re- 1975a; Grigg and Alchin, 1976; Drane et
ceived the most attention (review by Lang, al., 1977; Johnson et al., 1978). They may
1976). Alligators range far from the also derive other benefits from basking, as
tropics and survive in temperate winters. has been suggested for turtles (Cagle,
Throughout much of their range they are 1950). Forced prolonged basking is lethal
the largest ectotherm. Animals living at (Colbert and Cowles, 1946) when excessive
latitudinal or thermal extremes often show core temperatures are reached. Semi-aquahighly refined anatomical, physiological tic basking is accomplished in alligators by
and behavioral adaptations that make them maintaining a high floating posture (Smith,
well suited for study. Spotila (1973) re- 1975a).
ported behavioral thermoregulation of alMy research with the American alligator,
ligators, using telemetry to monitor body Alligator mississippiensis, over the past ten
temperatures. He stressed the importance years, provides insight into crocodilian
of water to minimize extreme fluctuations thermoregulation in general. Unlike many
in body temperatue and developed a "heat crocodilians, the American alligator ranges
energy budget" (Spotila et al., 1972), and well into temperate climates. Throughout
extrapolated dinosaurs (Spotila, 1973). much of its range in North America, it is
Unfortunately, insufficient data regarding the largest ectotherm. In contrast to their
physiological variables (Smith, 19766), and present endangered status, alligators were
various conceptual errors, severely limit once abundant and ecologically importhe utility of their mathematical model.
tant reptiles (Mcllhenny, 1935; Giles and
Childs, 1949; Craighead, 1968). Field
studies were conducted in southern Texas
Behavioral thermoregulation
at the Welder Wildlife Refuge (San PatriCrocodilians, like most other reptiles, cio County) and in central Texas at the
rely on a combination of behavioral and Waco Zoo. Multichannel radio telemetry
physiological mechanisms to regulate their (Smith, 1974) was used to monitor subbody temperature. Crocodilians gain heat dermal ventral and dorsal temperatures,
by radiation, conduction, and metabolism. deep body temperature and heart rate. At
Metabolic heat is significant in large croco- the zoo and in the field, non-telemetered
dilians. Thermal conduction from air or and telemetered alligators showed the
241
CROCODILIAN THERMOREGULATION
same thermoregulatory behavior.
Figure 1, showing the relation between
various environmental and telemetrically
measured temperatures, clearly demonstrates that basking may be triggered when
air temperatue exceeds water temperature. On three separate occasions, basking
commenced when air temperature exceeded water temperature. A drop in air
temperature (by intermittent cloud cover)
resulted in retreat into the warmer water.
Alligators were observed leaving the water
at night and on heavily overcast days when
the air was cooler than the water, indicating behavioral drives other than thermoregulation play a role in terrestrial activity.
Small- to medium-size alligators (up to
50— 100 kg) are essentially ectothermic poikilotherms. That is, in an environmental
chamber or water bath where radiant
heating and evaporative losses are minimal, body temperature will approximate
environmental temperature. Similar results have been observed for a wide variety
of reptiles and fish.
In their natural environment where animals are free to select optimal microhabitats from the available temperature mosaic,
40-1 ENVIRONMENTAL
a high degree of regulation of body temperature has been found. Similar results
have been observed for alligators. Figure 2
illustrates the relation between body temperature at the end of basking and water
temperature. Solid circles are daily mean
body temperatures. The solid line represents no regulation or complete equilibrium (T b =T w ). The dashed line is the least
squares best fit for the data points. A true
homeotherm would exhibit a line parallel
to the lower axis indicating complete independence of body temperature from water
temperature. The slope of alligator body
temperatures indicates that the alligator,
by a combination of behavioral and physiological thermoregulation, is able to reduce changes in body temperature to
1/13th the amount that the water temperature changes. This indicates a high degree of thermoregulation indeed.
Seasonal variation of alligator thermoregulatory behavior is profound. Alligators in southern Texas rarely bask in
the summer. Basking sites are often used
in spring and fall. Basking occurs occasionally on warm days during winter. Daily
activity changes from nocturnal in summer
to diurnal at other seasons. Crocodilians
often crawl out to bask on warm mud
banks, where conductive heat exchange
occurs. An alligator moved to a new warm
spot each time the telemetrically measured
ventral subdermal temperature began to
•
35
UJ
a.
TELEMETRIC
a.
LJ
a.
g33i
32-
29
9
II
13
TIME
OF
15
17
30
WATER
31
32
33
34
TEMPERATURE 'C
DJT
FIG. I. Environmental and telemetric measurements of a mature male alligator. (Redrawn from
Smith. 1975c/)
FIG. 2. Relation between body temperature after
basking and water temperature of a mature male alligator. The dashed line represents the least squares
fit and the solid line indicates TB = T w .
242
E. NORBERT SMITH
drop. Each relocation resulted in a temporary increase of subdermal temperature, as
heat was absorbed and conducted to the
interior of the alligator (Smith, 1975a).
Water is important in the thermoregulation of crocodilians. Thermal gradients
in natural water are often steep. Shallow
surface water can be used to gain heat,
while deep water provides a retreat from
high temperatures. Alligators dig a hole in
response to high temperatures. Alligators
can take thermally significant postures
with respect to water surface as shown in
Figure 3. An efficient method of evaporative cooling (Smith, 1975a) was periodic
submergence enabling a high floating
posture to lower body temperature by
evaporation of water.
Alligators construct elaborate hibernating dens, often shared by several individuals. Dens provide protection from freezing
temperatures. Nothing has been written
about crocodilian body temperature during hibernation.
the thermal response of live animals to differ from dead animals. It includes passive
and active elements. Passive elements include physical processes over which the
animal may have no control such as the
effects of temperature on blood viscosity,
pacemaker activity and metabolism.
Physiological thermoregulation also includes active elements over which the animal exerts control. Important active mechanisms of physiological thermoregulation
include changes in amount and distribution of blood flow, endogenous heat production, and evaporation of body water.
Each of these are important to crocodilians
and will be discussed in turn.
Amount of blood jlow
In crocodilians, as in other reptiles, physiological thermoregulation often enhances
or extends the effects of behavioral thermoregulation. Physiological thermoregulation can be defined as changes that cause
Although the stroke volume (ml/heartbeat) varies slightly as heart rate changes,
general trends in cardiac output (ml/min)
can be established by measurement of
heart rate (Reynolds, 1977; Reynolds and
Casterlin, 1978) for fish, reptiles and mammals. Bartholomew and Lasiewski (1965)
observed a marked hysteresis when body
temperature, during warming and cooling,
was plotted against heart rate. Similar results were observed in several lizards (Bartholomew and Tucker, 1963, 1964), and
fish (Reynolds, 1977; Reynolds and Cas-
FIG. 3. Thermoregulatory postures of alligators
with respect to water surface. A —high float, B —
common float, C — submerged breathing, Dcomplete submergence.
PHYSIOLOGICAL THERMOREGULATION
243
CROCODILIAN THERMOREGULATION
terlin, 1978). Heart rate for any body temperature during warming generally exceeded the heart rate during cooling at the
same body temperature. This was taken as
indicative of increased blood How during
warming. Spray and Belkin (1972) attributed the hysteresis to artifactual thermal
lag of the cloacal temperature of iguanas.
Simultaneous measurement of heart, stomach, and cloacal temperature in alligators
indicated that a significant hysteresis does
exist, suggesting increased warming blood
flow (Smith, 1976a).
i oo
. Alligator
mississippiensis
80
60
ft
i> 4 0
• = 3 0
•(-
20
I 0
8
CHANGING PATTERNS OF BLOOD FLOW
Inanimate objects and dead animals heat
and cool at the same rate (other factors,
such as evaporation, being equal). Live animals heat and cool faster than dead animals largely due to blood flow (Reynolds
and Casterlin, 1978). Crocodilians generally heat faster than they cool, resulting
from a change in thermal conductance altered by blood flow. Ischemic skin (e.g.,
during cooling) conducts heat poorly. During warming, cutaneous vasodilation increases blood flow and heat transport
(Smith, 1976rt). Xenon clearance studies
(Smith et al., 1978; Grigg and Alchin,
1976) and direct heat flow measurements
(Smith, 19766) clearly indicate that patterns of blood flow are altered during
warming and cooling.
The results of heating and cooling experiments can be compared in several
ways. The rate change (°C/min) at the
mid-temperature is useful only if the size
of the temperature step is the same for all
experiments. This is seldom the case. A
thermal time constant (Smith, 1976a; Reynolds and Casterlin, 1978) or half-time (Spigarelli et al., 1977) has more utility because
neither is strongly dependent upon the
size of the temperature step. In the relation between thermal time constant and
body weight for several alligators, certain
trends are apparent: Heat exchange in
water exceeds heat exchange in air (Fig. 4),
due to the higher thermal conductance
and specific heat of water. Large alligators
require longer to heat and cool than small
alligators, due to mass (s/v ratio) and sur-
.6
8
I
Body
2
weight
3
in
4 5 6
8 10
kilograms
FIG. 4. Log-log relation between thermal time constant and body mass. Open circles represent cooling.
Closed circles are warming. Dashed lines indicate
water experiments. Solid lines represent air measurement. (Redrawn from Smith, 197(V;)
face area differences. Interestingly, hatchling alligators heat and cool at the same
rate (Smith and Adams, 1978) while large
alligators heat faster than they cool, indicating that large crocodilians are better
physiological thermoregulators than are
small ones. Indirect evidence indicates a
similar situation for marine iguanas (White,
1973): Large iguanas depend on a combination of behavioral and physiological
thermoregulation, while juveniles depend
predominantly on behavioral thermoregulation. It is adaptive for large crocodilians to heat faster than they cool. A high
body temperature obtained by basking of
a large crocodilian (100 Kg) drops very
slowly upon entrance to cold water—requiring hours. In contrast, even if a 100 g
crocodilian could cool at 10% of the warming rate, a thermal equilibration could be
delayed for only a few minutes.
The cutaneous vascular response of
crocodilians appears to be different from
that of other reptiles. The response appears to be local in all reptiles. Portions of
the skin heated show vasodilation. The
skin of lizards shows increased bloodflowas
body temperature increases (Morgareidge
and White, 1969; Weathers amd Mor-
244
E. NORBERT SMITH
gareidge, 1971; Baker et al., 1972). In
crocodilians, cool portions of the skin show
reduced blood flow even if body temperature increases (Smith et al., 1978; Grigg
and Alchin, 1976). This is presumably
adaptive for crocodilians especially during
aquatic basking. Mechanisms of this response remain to be elucidated.
It is particularly interesting that heart
rate response follows the thermoregulatory
requirements much more closely than it
follows oxygen requirements. Heart rate
during warming is often twice as high as it
is during cooling at the same body temperature (but cf., Reynolds, 1977). Oxygen
consumption is greater during cooling
than it is during warming. This difference
between oxygen utilization and heart rate
is illustrated by an 8-fold (at 16.5°C) increase in oxygen pulse during cooling
(Smith, 19756). The available evidence
seems to suggest that the cardiovascular
system in crocodilians (and probably other
reptiles) is more important in heat transport than oxygen transport. This is not to
say that oxygen transport is unimportant in
reptiles, but the available evidence indicates
heart rate follows thermal requirements
more closely than oxygen demands. Of
course, this is in contrast to the way we generally interpret the cardiovascular
responses of endothermic birds and mammals. In mammals and birds the cardiovascular response is important in thermoregulation but oxygen demands take precedence.
ENDOGENOUS HEAT PRODUCTION
Crocodilians grow very large —larger in
fact than any other living reptile. Large
size increases thermal inertia, reduces the
surface/volume ratio and enhances retention of endogenous heat. Large crocodilians produce less heat per kilogram of tissue than small crocodilians, but the effect
of s/v ratio predominates.
EVAPORATION OF WATER
Crocodilian integument is not impervious to water. The effect of cutaneous
evaporation is insignificant for thermoregulation. However, several crocodilians
hold their mouths open (gape) when hot.
This was denied by Neill (1971), but recent
studies have documented both. t.h& extent
and the, effect of gaping (Spotila et al.,
1977). Gaping exposes moist mucosa of the
mouth to evaporation. This can reduce
head temperature significantly.
Thermal and physiological characteristics of
theoretical crocodilians
Although much remains to be done,
enough measurements exist to make several generalizations about thermal and
physiological responses of crocodilians. By
comparing time constants and whole body
conductance of alligators (Table 1) several
conclusions may be drawn. Large alligators
heat and cool more slowly, but large animals heat in a small fraction of the time
required to cool, while small alligators heat
and cool at nearly equal rates. High conductance results in reduced thermal time
constant. Conductance and thermal time
constant are reciprocally related, as indicated by comparison (Table 1) of TW/TC and
C c /C w , which implies endogenous heat
production is not important in crocodilian
thermoregulation in the size range for
which we have data. Heating and cooling
time constant ratios may be estimated from
cooling and warming conductance ratios.
Knowledge of area-specific blood flow
(ml/cmVmin) and total body mass permit
calculation of the total cutaneous blood
flow during heating and cooling (Table 2).
Small alligators heat and cool at the same
rate because they are unable to alter
cutaneous blood How in response to heating and cooling. Cardiac output values for
crocodilians of different sizes are unavailable. One can make assumptions about
cardiac output and the way it would scale
with mass. In all probability, cardiac output
(CO.) can be represented alleometrically
as: CO. = aM". Values of a and b differ
during heating and cooling. For mammals,
b usually is near 0.75.
If one assumes alligator cardiac output
is similar to that of iguanas, a model relating cardiac output and percent CO. to the
245
CROCODILIAN THERMOREGULATION
TABLE 1. Relation between thermal time constants, whole body conductance and body mass for crocodiltans.
Thermal time constant (T) in air3
a
b
Body mass
(Kg)
Warming
(min)
Cooling
(min)
T W /T C
0.05
0.10
0.50
1.00
5.00
10.0
50.0
100
500
1000
9.40
11.8
20.0
25.1
42.5
53.3
90.4
113.5
192.4
241.5
9.40
12.7
25.4
34.4
69.0
93.1
186.9
252.3
506.6
683.9
1.00
0.93
0.79
0.73
0.62
0.57
0.48
0.45
0.38
0.35
Ratio
Whole body conductance at
25°C (Cal/cmVmin/DC)b
Ratios
Cooling
Warming
c c /c w
0.143
0.123
0.088
0.076
0.054
0.047
0.033
0.029
0.021
0.018
0.169
0.133
0.077
0.061
0.035
0.028
0.016
0.013
0.007
0.006
1.18
1.08
0.88
0.80
0.65
0.60
0.49
0.45
0.36
0.33
Smith, 1976a.
Robertson and Smith, 1979.
skin during warming and cooling can be
made. Implied in results published by
Baker et al. (1972) is a value of a = 70
ml/min during warming and a = 35
ml/min during cooling. A doubling of
cooling C O . during warming is further
supported by heart rate hysteresis (Smith,
1976a)- In the relation of percent cardiac
output to the skin during warming and
cooling as a function of body mass (Fig. 5),
it should be noted that while the actual
value of cardiac output might be in error
by as much as 50%, the weight-specific
trends remain valid; i.e., actual data may
shift the curves up or down but will not
alter the shapes of the curves. Several
trends are evident. Blood flow to the skin is
slight no matter what value of b is used for
small animals. Percent C O . to the skin is
greater during warming than during cooling. This is true for alligators of all sizes,
but diminishes for small and very large
animals if b is 0.75 to 1.0. Finally, for values of b between 0.75 and 1.0, very large
animals require less cardiovascular effort
to thermoregulate than do smaller animals. This is particularly important as b
approaches 1.0.
FURTHER RESEARCH
Crocodilians are relatively easy to maintain and work with and come in a wide
variety of species and sizes. Many are cur-
IABI.K 2. Relation between body mass and cutaneous blood flow in alligators.
a
Body
mass (Kg)
Skin
thickness (cm)"
0.05
0.10
0.50
1.00
5.00
10.0
50.0
100
500
1000
0.026
0.033
0.061
0.080
0.15
0.19
0.35
0.46
0.85
1.10
Cutaneous blood How
Cooling
Cooling
Warming
Warming
(ml/min)c
(ml/cm Vmin)"
0.0006
0.0010
0.0056
0.0085
0.012
0.014
0.015
0.015
0.015
0.015
0.0006
0.0010
0.0029
0.0035
0.0043
0.0044
0.0045
0.0045
0.0045
0.0045
0.082
0.22
3.53
8.50
35.10
65.00
204.0
324.0
947.0
1503
0.082
0.22
1.83
3.50
12.6
20.4
61.2
97.1
284.0
451.0
Skin thickness (s) in cm and Mass(M) in Kg S = 0.080M"1". Data lor alligators 48gto 124 Kg, Smith rial, 1978.
Obtained from Figure 9: Smith et al., 1978.
c
' Obtained by multiplying Area by cutaneous blood (low ml/cmVmin. (A= lO^'M m7\ Benedict, 1932).
b
246
E. NORBERT SMITH
20 .
x
I8
O
I6
a^— b = 1 0
b = 0.75
• #••• b = 0.67
warming
™" ^ ^
cooling
14
I2
3
O
Q
or
<
* ^ ^* ^
10
•
8
•
warming
^ ^ ^
cooling
6
4
2
UJ
o
or
^ ^ " ^ ^
cooling
_
0
0.01
O.I
1.0
BODY
MASS
FIG. 5. Relation between body mass and percent
cardiac output to the skin during warming and cool-
rently in danger of extinction and most are
of economic importance. Only a few have
been studied in depth. Much work is
needed. Parallel studies need to be made
of the other species of crocodilians. The
relative importance of the cardiovascular
system for heat and oxygen transport
needs to be quantified. Very large individuals need to be studied to confirm validity of extrapolation. The mechanism of
the seemingly anomalous reduction of
cutaneous blood flow in an area of cool
skin while body temperature increases
needs to be studied. Data are badly needed
relating cardiac output during heating and
cooling to body mass. In summary, much
has been learned but much more is to be
gained from careful research of these "last
of the ruling reptiles." Better knowledge of
the thermal physiology of crocodilians will
aid in management for their survival, help
us to understand reptilian thermoregulation broadly, and shed additional light on
the physiology of large extinct reptiles.
10
100
1000
IN K I L O G R A M S
ing for different values of b (see text),
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