Thermoregulation in the Brown Water Snake, Natrix taxispilota,
with Discussion of the Ecological Significance of
Thermal Preferenda in the Order Squamata
DONALD EUGENE GOODMAN
A DISSERTATION PRESENTED TO THE GRADUATE COUNCIL OF
THE UNIVERSITY OF FLORIDA IN PARTIAL
FULFILLMENT OF '[liE REQUIREMENTS FOR THE DEG'E-E OF
DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA
This work is dedicated to my parents, Arvil E. Goodman and
Clara Metcalf Goodman, who encouraged my pursuit of biology in
general and snakes in particular.
I gratefully acknowledge the help of the many individuals who
contributed to this study. I especially thank Drs. Archie F. Carr,
Brian K. McNab, Frank G. Nordlie, and E. S. Ford for their assistance
in procurement of equipment, and invaluable comments on the manuscript.
I thank Dr. Paul Byvoet and Mr. Ralph Carroll for their technical aid.
I am indebted to Ms. Debbie Bee, Ms. Marion Edwards, Ms. Martha
Johnston and Mr. Craig Parenteau for aid in data collection and to
Mr. Porter Reed for helping me reclaim my experimental pen from the
depths of Lake Alice after heavy rains.
I also thank Ms. Jill Jordan for proofreading the manuscript,
assistance in drawing figures, collection of data, and mind-boggling
assessments of my data. I profited from the useful counsel of Ms. Peg
Estey in the preparation of illustrative material.
Finally, my thanks to Ms. Donna Gillis for typing this manuscript
and for removing many of the bureaucratic barricades to completion of
TABLE OF CONTENTS
LIST OF TABLI
LIST OF FIGUI
RESULTS AND D
SNTS . .
ES . . .
RES . . .
) METHODS ............
.on and Maintenance of Specimens
ilemetry ... .. .. ..
intal Apparatus .
.sm .. . .
re Efficiency .
)ISCUSSION . .
:d Body Temperature .
*al Thermoregulation .
ling Emergence . .
Effect of air and water temperatures
Effect of acclimation
Effect of physiological state
Effect of light
Temporal changes in emergence response
Maintenance of Preferred Body Temperature
Evening Submergence . .
Factors Affecting Preferred Body Temperature ...... 52
Digestion ................ 53
Other Factors .. . 59
Ecological Significance of Reptilian PBT ...... 62
SUMMARY ... ........ ............... 78
LIST OF REFERENCES .................. 80
BIOGRAPHICAL SKETCH ........... ...... .. ... 85
LIST OF TABLES
1 The preferred ranges of body temperature of freshly
caught Natrix taxispilota . .
2 Effect of digestion on normal range of preferred
body temperatures . ..
3 Data for points plotted in Figure 19 for primary
heliothermic lizards . .
4 Data for points plotted in Figure 21 for nocturnal
reptiles . . .
5 Data for points plotted in.Figure 21 for diurnal
snakes and forest lizards . .
LIST OF FIGURES
I X-ray photograph of a Natrix taxispilota with an
ingestible radio transmitter in its stomach 6
2 Experimental pen at Lake Alice ........ 9
3 Experimental chamber used to determine the responses
of water snakes to various combinations of air and
water temperature . ...... 12
4 Effect of acclimation temperature on the range of body
temperatures selected by Natrix taxispilota in a
gradient ... ..... ...... ... 19
5 Natrix taxispilota body temperatures and associated
air temperatures at Newnan's Lake during December
and January. .... ............. 21
6 Natrix taxispilota body temperatures and associated
air temperatures at Newnan's Lake during March 22
7 Body temperature of Natrix taxispilota collected at
Newnan's Lake between 1130 and 1600 hours from March
through October ...... 25
8 Metabolic rate of Natrix taxispilota as a function of
acclimation temperature and body weight 29
9 Behavioral responses of a 554 g Natrix taxispilota to
combinations of air and water temperature from 5C
through 350C . ......... 31
10 Body temperatures of Natrix taxispilota and associated
air temperatures at time of capture at Newnan's
Lake . . 35
11 Average body-air temperature differentials of Natrix
taxispilota at Newnan's Lake as a function of air
temperature .............. .. 37
12 Number of Natrix taxispilota basking on various days
throughout the year .... 40
13 Number of Natrix taxispilota basking at various
times on April 9, 1970 ... ...... .. 43
14 The relationship between body size and body-air
temperature differentials of Natrix taxispilota 49
15 Changes in body temperature of a Natrix taxispilota
thermoregulating under natural climatic
conditions ...... ............ 51
16 Four-day body temperature record of a Natrix
taxispilota digesting a fish ........ 55
17 The effect of temperature on digestive extraction
efficiency of Natrix taxispilota .. .... 57
18 The relationship between preferred body temperature
and critical thermal maximum in reptiles 65
19 Relationship between preferred body temperature of
primary heliotherms and the highest air temperature
recorded in their collection area . 68
20 Effect of temperature on the metabolic rate of a 509 g
Natrix taxispilota ...... ...... 72
21 Relationship between reptilian preferred body temperature
and highest air temperature recorded in their collection
area . . 74
Abstract of Dissertation Presented to the Graduate Council
of the University of Florida in Partial Fulfillment of
the Requirements for the Degree of Doctor of Philosophy
THERMOREGULATION IN THE BROWN WATER SNAKE, NATRIX TAXISPILOTA,
WITH DISCUSSION OF THE ECOLOGICAL SIGNIFICANCE OF
THERMAL PREFERENDA IN THE ORDER SQUAMATA
Donald Eugene Goodman
Chairman: Dr. A. F. Carr, Jr.
Co-Chairman: Dr. B. K. McNab
Major Department: Zoology
Thermoregulatory behavior of the brown water snake, Natrix taxispilota,
was studied under natural and laboratory conditions. During daylight hours,snak
move among shade, sun, and water to maintain their preferred body tempera-
ture. In the evening they submerge regardless of air-water temperature
differential and spend the night in the water. There are minimal thermal
thresholds for morning emergence and these levels are affected by thermal
acclimation and physiological state of the animal.
The preferred range of body temperatures of this species decreases
with increasing acclimation temperature. When digesting food, snakes
thermoregulate within a sub-range of the normal preferred range and
digestive extraction efficiency is greatest at this level -- about 300C.
It is suggested that high thermal extremes are selective forces which
directly fix the critical thermal maximum of reptiles and indirectly fix
the preferred body temperature. The relatively low thermal preferenda of
snakes may be a function of their lack of limbs which precludes thermo-
regulation with the degree of independence of conductive heat exchange with
the substrate characteristic of lizards.
Many species of reptiles utilize solar radiation to attain body
temperatures greatly in excess of ambient temperatures. Some species
have an extensive behavioral repertoire which enables them to regulate
their body temperature within fairly narrow limits. Since these initial
discoveries were reported (Cowles and Bogert, 1944), scores of papers
have appeared documenting such behavior for other reptilian species,
and it now seems obvious that thermoregulation is a general feature of
reptilian behavior. While some reptiles possess physiological mechanisms
that contribute to thermal homeostasis (Lueth, 1941; Cole, 1943; Cowles,
1958; Ruibal, 1961; Bartholomew and Tucker, 1963; Heath, 1965;
Hutchison et al., 1966; Kour and Hutchison, 1970; Weathers, 1970),
it is behavioral utilization, directly or indirectly, of solar
radiation that permits the attainment of high preferred thermal levels.
The contribution of metabolic heat to maintenance of thermal homeostasis
is negligible (Lueth, 1941; Cole, 1943; Mackay, 1964; Schmidt-Nielsen
and Dawson, 1964; Brattstrom, 1965) even in large reptiles.
With few exceptions, these studies have dealt with lizards, and
very little information exists for other reptilian groups. The few
studies of thermoregulation involving snakes (Cowles and Bogert, 1944;
Carpenter, 1956; Fitch, 1956, 1965; Brattstrom, 1965; Stewart, 1965;
Myres and Eells, 1968; Kitchell, 1.969; McGinnis and Moore, 1969;
Osgood, 1970) indicate that snakes differ from lizards in their thermal
behavior. They seem to have lower thermal preferenda and to regulate
less precisely. Some workers (Cowles and Bogert, 1944; Schmidt-Nielsen
and Dawson, 1964) believe these differences are correlated with differences
in the ecology of the two groups. Most snakes, for instance, are nocturnal
or crepuscular and many are fossorial; lizards are mostly diurnally active
and terrestrial. Even among nocturnal and fossorial reptiles, however,
basking in the sun has been either regularly or occasionally reported
(Cowles and Bogert, 1944; Bailey, 1949; Brattstrom, 1952). The signi-
ficance of diurnal thermoregulation in such forms has never been explored.
This study was undertaken to determine the significance of thermo-
regulation in a species of snake which is both semi-aquatic and
nocturnally active. Natrix taxispilota, the brown water snake,spends
nights in the water of large open lakes or rivers and springs. During
the daylight hours of the warmer months, the species commonly lies on
limbs overhanging the water, either in the sun or in the shade. Except
for reproductive behavior in the early spring, little activity occurs
during the day. This snake almost never occurs away from the water's
edge, and the aerial phase of its existence is limited to basking on
vegetation, rather than shore. While lying above the water, the snake
is surrounded by a thermal medium that is virtually homogeneous, and
heat exchange is largely radiative. Convective heat exchange there
is minimal because snakes remain in the water on windy days. Heat
exchange during the aquatic stage of the activity cycle, however,is
almost completely conductive. Because the species' activity is
partitioned almost completely between these two phases -- nocturnal
aquatic activity and diurnal arboreal basking -- it seems an ideal
snake for a study of the mechanisms and significance of thermo-
MATERIALS AND METHODS
Collection and Maintenance of Specimens
Almost all the snakes used for this study were collected at
Newnan's Lake, 8.7 km east of Gainesville, Alachua County, Florida.
This 2390 hectare lake has a mean depth of two m and is bordered by
trees, particularly pond cypress Taxodium ascendensand water ash
Fraxinus caroliniana, both of which extend from the shoreline out for
as much as 20 m into the lake. It is at the interface of the lake
and the outermost trees that most of the Natrix taxispilota were found
basking. Animals used in laboratory studies were collected by hand
from a motorboat. Cloacal temperature was recorded at this time with
either a Schultheis thermometer or the the.mister probe of a YSI
six-channel tele-thermometer. Air temperature was taken in the shade
at the time of capture and water temperature was recorded at the surface
and at a depth of 2/3 m. A black-bulb temperature was recorded in direct
sunlight with a mercury thermometer, the bulb of which had been coated
with flat black paint.
A 1.12 km section of shoreline was used as a census area and, at
irregular intervals, the number of snakes basking in the trees of this
area was recorded. These surveys were always conducted between 1300 and
1500 hours EST. On a few days, censuses for this and other areas were
taken at hourly intervals between 0700 and 1830 hours EST to determine
the extent of temporal variation in the number of basking individuals.
Associated air, water, and black-bulb temperatures were recorded during
censusing, and general weather conditions were noted.
Snakes used for thermal gradient, digestive efficiency, and metabolic
experiments were acclimated prior to use. Each animal was housed in a
plastic storage container with holes in the removable lid. These containers
were placed in a Jewett environmental cabinet, a Forma model 13 incubator,
or a Lab Line controlled environmental room where the temperature was main-
tained within .5 C. All snakes received 12 hours of light daily (0900-
2100 hours EST) and had water continuously available in dishes which were
too small to permit submergence of snakes weighing more than 100 g.
Ingestible blocking oscillator radio transmitters were used to
obtain snake body temperatures under experimental conditions. The
broadcast frequency used was low enough (500-1000 kc) to permit the re-
ception of both aerial and underwater signals generated within 2 m of
the receiver, an AM-FM portable radio. Antennal loops were always
necessary tu relay the signal to the receiver.
Each cylindrical (radius = 7.5 mm, length = 57 mm) transmitter was
powered by a replaceable 1.5 volt silver oxide hearing aid battery and
was waterproofed with a thin coat of 1:1 mixture of beeswax and
paraffin. The transmitter was lubricated, forced into the throat of
the snake and massaged by hand to the stomach (Fig. 1). The transmitter
was regurgitated in four or more days depending on temperature. Trans-
mitters were calibrated immediately before and after use.
To study the fluctuations of body temperatures with changing
environmental temperatures, an experimental pen was built at another
nearby location, Lake Alice. This 24-hectare lake is located on the
University of Florida campus. The pen consisted of a circular galvanized
steel cattle watering trough 2.44 m in diameter and 61 cm high. Concrete
X-ray photograph of a Natrix taxispilota with
an ingestible radio transmit-er in its stomach.
blocks were stacked in the center of the trough to a level of about 50 cm
and a wooden cable spool 76 cm in diameter was placed on its side atop
the blocks. An antennal loop system was installed so that radio trans-
mitter signals could be monitored at a distance from the pen. This
consisted of a 25-m section of insulated copper cable ringing the
pen in three perpendicular planes. Two loops, therefore, passed under
and over the spool and their components extending above the rim of the
pen were supported by arched sections of screen moulding (Fig. 2); the
third loop was situated along the inside periphery at the rim. The
ends of this antennal loop were connected to a 20-m section of insulated
copper wire which was connected by insulated tip plugs to the antenna
of a portable AM-FIl radio. Signals generated anywhere inside the loop
could thus be monitored many meters away. A 1/4-inch mesh hardware
cloth retaining fence was attached to the top edge of the trough and
directed inward toward the center of the pen to prevent the escape of
snakes. This apparatus was floated into the lake and filled with water
to the level of the bottom of the wooden spool. The free-floating pen
was then anchored and the wire connecting the antennal loop to the
radio was sunk to the bottom between the pen and the shore. Snakes
used in this phase of research were introduced into the pen and allowed
several days to adjust to their environment. They were then force-fed
an ingestible transmitter. On sunny days, the snake had both sunny
and shaded basking sites available on the wooden spool, or it could
remain underwater in the cavities of the concrete blocks. Air, water,
and black-bulb temperatures were monitored with either a YSI tele-
thermometer located on shore or with mercury bulb thermometers. In
trial determinations, the water temperature inside and outside the pen
never differed by more than 1.5C. The water inside was sometimes
I Fi* O
slightly cooler, presumably because of the shade provided by the vertical
sides of the pen. Observations were made from the shore either with the
naked eye or through 30 X binoculars, depending upon the distance
separating the observer and the pen.
A laboratory apparatus was used to study thermoregulatory behavior
under more controlled conditions. A 230 liter aquarium was made by
sealing a refrigerator liner, cutting a large window in one side and
.sealing in a section of reinforced glass. Water temperature was con-
trolled by circulating water between the aquarium and a Forma constant
temperature water bath. A bottomless wood-frame 1/4-inch mesh cage
(90 cm X 70 cm X 40 cm) with sliding glass panels in front. was placed
above the aquarium, and Sambucus limbs were wired into positions both
underwater and above water to provide the snakes with numerous resting
and basking sites. A 250 watt infrared heat lamp was placed directly
above the right side of the cage about 20 cm above the highest basking
site. A wooden partition was hung from the top of the cage; this did
not restrict movement but rather shaded the left side of the cage from
"sunlight" (Fig. 3). Caged animals could thus either remain submerged
or bask aerially in the "sun" or shade. This aquarium-cage-water bath
combination was placed inside a Lab Line controlled environmental room
which maintains temperatures between -20 and 700C within .50C. Water,
air and black-bulb temperatures were monitored with a YSI tele-thermometer
placed outside the room. The probes were placed inside the aquarium pen
in the water, shaded air and approximately 20 cm directly below the
sunlamp respectively. The black-bulb probe was coated with flat black
paint. Ingestible transmitters were used to monitor body temperatures.
A three-plane antennal loop was placed in the aquarium cage and leads
were extended outside the room to the antenna of an AM-FM radio. All
Experimental chamber used to determine the
responses of water snakes to various combinations
of air and water temperature.
observations were made through two 10 cm X 6 cm holes in a sheet of
brownm paper which covered the glass door of the environmental room.
With this apparatus, air and water temperatures could be monitored and
varied independently, the snake's behavioral adjustments could be
observed and its body temperature recorded without disturbing the
Responses of the animals were recorded for all combinations of
air and water temperatures from 50 through 350C. A timer was attached to
the environmental room and a 12-hour light cycle (0900-2100 hours EST)
was used throughout. Because of the nature of the transmitter used,
it was difficult to separate two signals; consequently one animal,
a 554 g female, was used for all determinations. Numerous individuals
were later run at selected temperature combinations to verify the
generality of responses of this individual. The female used in this
experiment was not acclimated to any particular temperature because
reacclimation after each run would have prolonged the experiment by
many months. Also, the temperature combination changes were never
drastic. Usually the water temperature remained constant while all
air temperatures from 5C through 350C were run. Each combination was
run for two hours and then the air temperature was elevated 20C. Since
these temperature changes were gradual, there is no reason to believe
that the snakes used in this experiment were acclimated to temperatures
to which they would not ordinarily be acclimated under the same thermal
conditions in the wild.
A thermal gradient was used to determine preferred body temperature
levels in this species. The gradient consisted of a rectangular open-
top wooden box 3.35 mm long, 30 cm wide and 30 cm high with a nickle-steel
alloy floor. The front of the box was marked at 5 cm intervals from the
hot to the cool end. At the cool end, a bottomless one-gallon aluminum can
was cemented to the floor of the gradient and filled 2/3 full of water.
Cold water was then circulated through a coiled section of copper tubing
in the can. Heat was provided at the other end by an electric iron that
was placed flat on the metal floor. A 500 ml beaker of water was placed
beside the iron to maintain a high humidity inside the gradient. Panes
of glass were placed on top of the gradient to prevent escape of snakes
and to permit observation. A gradient with an average aT of 10C per
30 cm between 200 and 340C could be maintained indefinitely after an
initial eight hour warm-up period. Acclimated snakes were force-fed
ingestible transmitters at about 2100 hours, placed in the gradient,
and left overnight for adjustment. Body temperature and location in
the gradient were recorded at approximately 1-1/2 hour intervals between
0900 and 2400 hours of the following day. Snakes in the gradient re-
ceived the same 12 hour photoperiod from overhead lighting as in their
acclimation quarters. A red light was used when readings were taken
during hours of darkness.
Metabolic rates were measured with a Beckman G-2 oxygen analyzer.
Metabolic chambers consisted of 21.5 cm diameter glass battery jars
30.5 cm high, with holes drilled at low and high levels on the sides
to let air in and out. A plexiglass lid with a 9.0 cm diameter hole
for a size 15 rubber stopper was cemented to the top of the chamber.
Acclimated snakes were introduced into the chamber which was then
submerged in a controlled-temperature water-bath that maintained water
temperature within .5 C. Air was pumped through a coil of copper
tubing that was submerged in the water bath before entering the chamber.
Oxygen consumption readings were taken at half-hour intervals until
stable values were obtained.
The effect of temperature upon digestive efficiency was measured
calorimetrically. A lirge number of gizzard shad, Dorosoma cepedianum,
were collected by rotenone poisoning at Newnan's Lake, and immediately
frozen. In feeding experiments, fish were weighed, ground whole in a
Waring blender and freeze-dried in a Virtis freeze-drying apparatus.
The resulting mixture was ground again and filtered through 1/4-inch
mesh screening to remove scales and large scale fragments. The re-
sulting powder was thoroughly mixed and a .5 to 1.0 g sample removed
for calorimetric determination in a Parr adiabatic oxygen bomb calori-
meter. The remaining powder was rehydrated to the original wet weight
calorimetric value and immediately fed to preweighed acclimated snakes
at a level of .1 g per g of body weight. The food was massaged by
hand to the snake's stomach and animals were then replaced in acclimation
quarters and permitted to digest the meal at the temperature to which
they were acclimated.
Cages were checked daily for defecation and the feces were rinsed
out of the cages, collected in individual beakers and refrigerated.
After digestion was completed (the cessation of defecation) the
accumulated feces were either freeze-dried or vacuum dessicated and
the dry feces weighed and bombed. At the temperatures of 200C and
above, snakes passed musk from the musk glands, the amount increasing
with temperature. The quantity of musk per g of body weight was
determined at the acclimation temperatures used and samples were
bombed to determine calorimetric value. A correction for this factor
was introduced into the calculations. Digestive efficiency is defined
E = 1 Ci
where E = digestive efficiency; Cf = caloric value of feces; Ci =
caloric value of ingested food; and Cm = caloric value of musk. Dried
samples of fish, feces, and musk were weighed to tha nearest .0001
gram on a Mettler H15 balance.
RESULTS AND DISCUSSION
Preferred Body Temperature
Throughout this discussion, the term preferred body temperature
(abbreviated PBT) will be used in accordance with Peters (1964) who
defined it as "that temperature at or about which all members of a
reptilian species will maintain themselves given the opportunity to
select proper substrate, exposure to sunlight, or other thermal factors."
The PBT can thus refer to a thermal range, as initially defined (Cowles
and Bogert, 1944) or to the mean of that range, the latter being more
useful for comparisons of interspecific preferences.
The level of body temperature selected by Natrix taxispilota in a
thermal gradient is inversely proportional to the temperature at which
the snakes were acclimated (Fig. 4). This is consistent with the find-
ings of Wilhoft and Anderson (1960) for Sceloporus occidentalis. The
ecological significance of such interdependence is not immediately clear.
It might be expected that PBT would be independent of acclimation as
Licht (1968) found in Anolis, and serve as an immutable focal point for
thermoregulatory behavior. In other vertebrate poikilotherms, similarly
disparate results have been obtained. Rana pipiens tadpoles (Lucas and
Reynolds, 1967) and many fish (Norris, 1963; Fry, 1964) show changes in
PBT with acclimation, but the preferred thermal level of the newt
Taricha rivularis cannot be shifted by acclimation (Licht and Brown,
1967). Thus, it is impossible to generalize about the capacity of
vertebrate poikilotherms for adjustment of their thermal preferenda.
(1) 4.1 .
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Especially puzzling is the fact that the relationship in Natrix
taxispilota is inverse, because the critical thermal maximum is directly
correlated with the acclimation temperature (Lowe and Vance, 1955; Larson,
1961; Bradshaw, 1965; Kour and Hutchison, 1970) and PBT, at least in
interspecific comparisons, is directly proportional to critical thermal
maximum (Brattstrom, 1965; see Fig. 18). These inconsistencies warrant
an examination of the ecological significance of the physiological capacity
for thermal acclimation in these snakes.
There is some evidence that seasonal acclimation of PBT does occur
in temperate zone reptiles. Mueller (1969) found that both PBT (measured
in a gradient) and critical thermal maximum were higher in Sceloporus
graciosus collected in the summer than in those collected in the spring.
Similar increases in the level of field body temperatures from spring to
summer have been found in two garter snakes, Thamnophis sirtalis and T.
butler (Carpenter, 1956), and in two lizards, Cnemidophorus sexlineatus
and Sceloporus woodi (Bogert, 1949). A similar seasonal variation was
found in body temperatures of Natrix taxispilota, but the differences
were not consistent with the laboratory evidence for the relationship
between acclimation temperature and PBT. The level of body temperature
in December and early January ranged between 14 and 200C and most values
were below air temperatures (Fig. 5). By late January, higher air
temperatures resulted in body temperatures of 22.5 to 260C with values
approximating air temperature. In March, most body temperatures ranged
between 26 and 300C (Fig. 6) and exceeded air temperature. These
observations were made on sunny and relatively windless days when black-
bulb temperatures exceeded air temperatures by 4 to 100C. The occurrence
of snake body temperatures below air temperature can be explained only
as resulting from recent emergence from cooler water and initial evaporative
18 20 22 24 26
AIR TEMPERATURE (C)
Natrix taxispilota body temperatures and
associated air temperatures at Newnan's
Lake during (A) late December and early
January and (B) late January.
AIR TEMPERATURE (C)
Natrix taxispilota body temperatures and
associated air temperatures at Ncwnan's
Lpke during March.
cooling. Throughout the warmer months, body temperatures remained
approximately within the range found in March (Fig. 7), but by mid-
October, lower air temperatures again caused a decrease in the field
body temperatures. Thus, field data provided no evidence of the inverse
relationship that might be expected between seasonal temperature (and
presumably thermal acclimation of PBT) and level of body temperature.
However, these field values for winter represent, at best, levels
of temperature attainable and not necessarily those preferred. Snakes
collected in January selected warmer temperatures in a gradient than those
collected in April or July (Table 1), suggesting that acclimation of
PBT does occur in nature. The body temperatures selected by snakes
collected in April and July did not differ significantly, indicating
that these snakes were acclimated to a common thermal level, their PBT.
During the colder weather of January, however, thermoregulatory behavior
ceased and the snakes became acclimated to the colder thermal regime of
the water in which they remained torpid. Their PBT at this time re-
flected this acclimation.
Metabolic data also suggest this relationship. Figure 8 gives
the metabolic rate of snakes as a function of size and acclimation
temperature. Ihe level of metabolism at a given temperature is in-
versely correlated with acclimation temperature. This relationship has
been reported for fish, amphibians, reptiles and many invertebrates (for
extensive reviews, see Berg, 1953; Bullock, 1955; Fry, 1958) and appears
to be a nearly universal characteristic of poikilotherms. When snakes
were maintained at varying thermal regimes (300C from 0901 hours
through 2100 hours, 200C from 2101 hours through 0900 hours), however,
their metabolism became acclimated to the higher of the two temperatures
(Fig. 8). Acclimation to the highest of varying temperatures has been
4-J i C
SMJNODEB AO AdJUWflN 3
Table 1. The preferred ranges of body temperature of
freshly caught Natrix taxispilota.
JANUARY APRIL JULY
PBT RANGE (C) 29.4-33.5 25.3-30.9 25.2-31.1
MEAN 31.6* 27.9 28.2
N (OBS.) 3 (37) 3 (38) 4 (47)
"Differences between means for April and July are not
statistically significant but the mean for January
differs significantly (p= 0.05) from the other means.
reported for Rana pipiens (Hutchison and Ferrance, 1970) and for several
species of fish in both the field (Brett, 1944) and under controlled
conditions (Fry et al., 1946; Heath, 1963). These data suggest that a
poikilothermal animal can acclimate the level of its metabolism by
thermoregulatory behavior. Only when the environmental temperature
becomes too cold to permit thermoregulation at the preferred level
would there occur acclimation of body functiorsto a non-PBT level.
There is, then, a seasonal variation in PBT of Natrix taxispilota.
It appears that the level at which body temperature is maintained sets
the acclimation temperature, and the level of thermal acclimation in
turn affects the PBT. The range of body temperatures found in Natrix
taxispilota during March through October (23-320C) correlates almost
exactly with those preferred (23.9-33.1C) by snakes acclimated to
250C and 300C -- a close agreement between field and laboratory data.
Thermoregulacion at the preferred level apparently fixes the level
of thermal acclimation throughout those parts of the year.when adequate
thermal opportunities exist. During the colder months, when this is
not possible (Fig. 5), the level of body temperature, and presumably
thermal acclimation, varies with water temperature.
The inverse relationship between acclimation temperature and
PBT probably represents an overcompensation mechanism which is of
value during periods of thermal extremes. It is unlikely that cold-
acclimated snakes in nature could ever attain the body temperatures
selected by cold-acclimated individuals in a gradient. But by be-
haviorally thermoregulating in such a manner as to attain these high
levels, snakes may significantly elevate their body temperatures.
The lower levels preferred by warm-acclimated snakes probably reflect
a mechanism that is of importance only in an evolutionary sense. The
Metabolic rate of Natrix taxispilota as a
function of acclimation temperature and
A. acclimated to 200C, B. 250C, C. 300C,
D. 35C, E. varying temperatures (200C
night, 300C day).
1.5 0o 2:5 3.0 35
LOG BODY WEIGHT (g)
highest air temperature recorded in Gainesville in a 40 year period
(Kincer, 1941) is 39.40C which is several degrees below the probable
critical thermal maximum for Natrix taxispilota (Brattstrom, 1965).
Only when drastic climatic warming occurs would snakes become acclimated
to temperatures significantly above their preferred range and there
would be a clear selective pressure favoring individuals who behavior-
ally sought cool body temperatures even if the lowest attainable body
temperature was above the preferred level.
Brownwater snakes almost invariably spend the night in the water.
The time of emergence depends upon several climatic factors and upon
some endogenous responses of the snake.
The effect of air and water temperatures on emergence
Figure 9 shows the response of a 554 g female water snake main-
tained in the environmental chamber to all combinations of air and water
temperatures between 5 and 350C. lTh1is includes all the thermal regimes
which the species ever encounters in nature and several artificial situ-
ations. The responses of several other animals to a number of these
thermal combinations never differed appreciably from those of the
554 g female so the pattern shown in Figure 9 may therefore be con-
sidered representative. It should be remembered throughout the
discussion that animals used in this laboratory experiment were adapted
to the approximate thermal combinations to which their responses were
recorded (see Materials and Methods).
The lowest air temperature that elicited emergence was 160C and
then only if the water temperature was 210C or above. This latter
combination is an artificial situation at one extreme of a general
10 12 1 16 18 20 22 24 26 28 3 Z 4
WATER TEMPERATURE (C)
Figure 9. Behavioral responses of a 554 g Natrix taxispilota
to comnbinations of air and water temperature from
50C through 350C.
snake in water
E/ sn.?ke in sun
EL snake in shade
pattern; the colder the water temperature, the warmer the air
temperature needed to elicit emergence. The lowest water temperature
at which snakes emerged was 10C and then only if air temperature
was at least 25 C (again an artificial situation). There are,
therefore, lower limits for air and water temperatures that
elicit emergence in Natrix taxispilota and above these extremes,
these minimal values are inversely related. This inverse relation-
ship is not isothermal -- i.e. the slope of this air-water temperature
interface is not -1.0.
At a water temperature of 180C, snakes will emerge for a minimal
air temperature of 180C, but at water temperatures below this level
air temperatures must exceed water temperature to evoke emergence
(Fig. 9). The lower the water temperature, the greater the air-water
temperature differential required for emergence. Values for this
differential at or near the water temperature asymptote of 100C are,
as mentioned, not ecologically significant because such differentials
do not occur in nature.
At water temperatures above the air-water isothermal emergence
point (180C), the minimal water temperatures that evoked emergence
were in excess of air temperature. The higher the water temperature.
from which a snake emerges, the higher its body temperature at
emergence and the less time it takes a basking individual to reach
the preferred thermal level. This may explain why snakes emerge
from warm water into cooler air at water temperature above 180C.
Although the water is relatively warm, it is still below the preferred
level. Basking permits attainment of PBT, or at least a closer
approximation than is represented by the water temperature. Thus,
snakes apparently will not emerge when their body temperatures are
below 18 0C unless the aerial phase insures rapid attainment of this
Figure 10 summarizes the field relationship between air and
body temperature. It is significant that only 5 percent of the body
temperature records are below 180C, a close agreement with laboratory
results. The decrease in number of records for snake body temperature
at air temperatures below 18 C is precipitous and not a gradual attenu-
ation. The body-air differentials maintained by snakes at air
temperatures from 18 C through 30 C are inversely correlated with
air temperature (Fig. 11). This is clearly a reflection of differential
utilization of sunlight as a function of environmental temperatures.
It is ecologically significant that there exists a lower thermal
threshold for thermophilic responses as evidenced by the refusal of
snakes to emerge at water (and therefore body) temperatures below
10 C even when air temperature was warmer. Below the body temperature
required for coordinated locomotion, emergent snakes would be very
vulnerable to predation by homoiotherms. Also, at temperatures below
the threshholds for feeding and digestion, thermophilic responses
would increase the metabolic maintenance cost without providing
additional energy sources. This would deplete the reptile's energy
stores needed for periods of torpor and (at higher latitudes) hiber-
When the water temperature approached the lower limit of the
preferred range (25 C), a common occurrence between April and October,
the minimal air temperature required to evoke emergence increased
sharply from 17 C at 24 C water temperature to 23 C at 25 C water
temperature (Fig. 9). At water temperatures above 250 C, the minimal
air temperatures necessary for emergence were inversely proportional
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to water temperatures. This sharp increase in the minimal air temper-
atures necessary to elicit emergence suggests that water is of con-
siderable importance for thermoregulation between April and October
when such thermal conditions are common. When water temperatures
exceeded the PBT, emergence into lower air temperatures permitted
cooling to the preferred level. These water-air temperature differen-
tials probably never obtain in nature, and ordinarily, water tempera-
.turcs appreciably above air temperature would occur in the evening
well after the emergence period.
The effect of acclimation on emergence
Animals used in the environmental room studies were adapted to
the air-water temperature combinations to which their responses are
graphed in Fig. 9. In the wild, this is not always the case. Sudden
climatic changes may result in exposure of snakes to a thermal environ-
ment to which they are not physiologically adapted. For instance,
the same approximate air and water temperature ranges on February 20,
1971 and April 16, 1970 resulted in the emergence of 118 and 25 snakes
respectively (Fig. 12). Both days were relatively humid and windless
so the disparity seems to be a reflection of the difference in climatic
conditions during the week proceeding these dates. April 16 was warm
and typical of the weather of this period, and snakes were physio-
logically acclimated to their PBT. February 20, however, was the
warmest day of a four day warming trend. Night air temperatures had
been at or near freezing until February 18. These snakes, then, were
acclimated to temperatures well below those of February 20 and the
basking response was greatly accentuated. These data and the re-
lationship between acclimation temperature and PBT suggest that the
minimal air and water temperature combinations required to elicit emergence
and basking are lower in cold than in warm-acclimated snakes.
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Effect of physiological state upon emergence
At 0920 on April 1, 1967, a snake was found basking with a body
temperature of 13.8 C. Corresponding air and water temperatures at
the time were 11.90C and 13.8 0C respectively. These were the lowest
body temperature and associated environmental temperatures recorded
during this study (Fig. 10). It is probably significant that this
individual had a prominent bulge from a fish it had recently eaten.
It is possible that the minimum air and water temperatures necessary
to evoke basking may be lower in snakes digesting food than in those
in a postabsorptive state. Presumably, higher body temperatures should
facilitate digestive processes in reptiles (Cowles and Bogert, 1944;
Effect of light on emergence
Combinations of air and water temperatures ideal for basking did
not induce emergence at any hour in the absence of light. When the
sun lamp was turned on during the night, snakes basked if thermal
conditions were proper. Boyer (1965) found that turtles also
would bask in response to light at any time. During cloudy weather,
basking behavior was either diminished (i.e. fewer individuals emerged)
or emergence was delayed. Boyer, (1965) found this also to be true
for turtles. In the semiaquatic reptiles studied, therefore,
basking behavior does not appear to be an endogenous rhythm, but a
response to the proper conditions of light, water temperature, and
air temperature. The physiological state of the animal is an important
factor in determining the level of the environmental temperatures
necessary to induce emergence.
Figure 13 presents the thermal environment at Newnan's Lake on
April 9, 1970 and the emergence response of snakes. Climatic conditions
The number of Natrix taxispilota basking at
Newnan's Lake at various times on April 9,
1970, and the associated air, water, and black
on this day were typical of the preceding. week so these animals were
adapted to this general thermal regime. The water temperature exceeded
air temperature until 1200 hours but a peak in basking activity
occurred earlier. Emergence appeared to be initially triggered by the
onset of lighting, and to be accentuated by the rise in black-bulb
Temporal changes in emergence response following initial onset of light
On many days, the initial air-water temperature combination used
was below the emergence threshold. Every two hours, air temperature
was raised 2 C and responses were recorded. Under such conditions,
there occurred a temporal change in the snakes' propensity for emergence.
Temperature combinations which would elicit emergence before about 1500
hours (EST) could not elicit initial emergence after that time. The
responses recorded in Fig. 9 were all recorded prior to 1500 hours.
The heating rate (4 T = 2 C/hr) and general warming pattern approximate
conditions occurring in the wild during winter. Under laboratory
conditions, 1500 hours occurred halfway through the "sunlight" cycle
(0900-2100 hours). In nature, six hours after sunrise would be
about 1300 hours EST during December and January. An animal initially
emerging after this time in response to threshold emergence temperatures
would begin to thermoregulate at or following the peak air temperature
of the day and would confront decreasing (and therefore sub-threshold)
air temperatures for the remainder of the day. Clearly, then, this
temporal restraint on the thermophilic emergence response is necessary
to restrict thermoregulatory activity to thermally hospitable periods.
Otherwise, extensive basking would occur at low body temperatures re-
sulting in exposure of snakes to predation at suboptimal activity
Maintenance of Preferred Body Temperature
Elaborate behavioral adjustments permit some lizards to thermo-
regulate within very narrow limits. Desert lizards apparently have
the most elaborate behavioral repertoire, including postural adjust-
ments (Bogert, 1949; Norris, 1953; Heath, 1965), retreat to burrows
(Cowles and Bogert, 1944; Norris, 1953; DeWitt, 1967a, 1967b; McGinnis,
1967), panting (Cole, 1943; Cowles and Bogert, 1944; Ruibal, 1961;
Kour and Hutchison, 1970), climbing (Norris, 1953; DeWitt, 1967a)
and burrowing (Cowles and Bogert, 1944; Heath, 1965). Physiological
modifications are known in these reptiles, but are clearly of secondary
importance in thermal homeostasis. Thermoregulation in snakes has been
studied very little and available information suggests that thermal
control is not as precise, and the behavioral repertoire not as
complex, as in the case of heliothermic lizards.
Following emergence, brown water snakes basked under the sunlamp
(or lay in the shade at higher air temperatures) until a body temperature
in the preferred range was reached and thereafter moved from the "sun,"
to shade, to water in order to maintain this level. No consistent
postural or coiling adjustments were noted. Retreat to the shade
or entrance into "sunlight" usually required 5 to 15 minutes. This
slow pace is probably the result of a slow heating and cooling rate
to be expected in an animal of such bulk and the wide range of pre-
At water temperatures below 25 C (and appropriate air temperatures),
snakes emerged and basked in the "sunlight" until their PBT was reached
and then moved into the shade. There is a broad zone of overlap be-
tween air temperature at which animals basked in the "sun" and those
at which they retreated to the shade. This appears to be largely a
reflection of the distance between the snake and the sunlamp; the
ecologic equivalent would be the directness and/or intensity of
sunlight. Similarly, there was overlap between the air temperatures
at which animals lay in the shade and those at which they entered
the water. This probably is a reflection of variation in body
temperature of the snake, from one experimental run to the next,
at the time it retreated from the "sunlight."
The lowest air temperature at which snakes retreated to shade
vwas. inversely proportional to water temperature at water temperatures
from 100C through 180C. Evidently, more time was required at these
low water temperatures (emergence body temperatures) for attainment
of preferred levels. This resulted in the recorded extreme of a
snake basking in the "sun" at an air temperature of 31C following
emergence from 100C water.
In one air-water thermal regime, snakes could be found in either
air, water, or "sun" (Fig. 9). This was between water temperatures of
approximately 230C and 270C and air temperatures of 23C and 280C.
These are evidently the only water temperatures above 100C at which
snakes may not emerge at all. At water temperatures above this
zone, there is a decline in the realm of air temperatures at
which emergent snakes bask in the sun, a marked increase in the
shade realm, and an extinction of the shade-sun overlap zone.
When air and water temperatures exceeded the preferred level,
snakes lay in the shade. These temperature combinations rarely or
never occur in nature and the value of such behavior is not clear.
In nature, extensive movement among the shade, sunlight, and
water usually occurs only in the late fall, winter, and early spring.
Low ambient temperatures at these times necessitate such thermo-
regulatory behavior and the sparseness of foliage permits abundant
access to sunlight. At such times (Fig. 13) the number of individuals
basking usually peaks in late morning and declines thereafter. There
is an individual turnover and during the afternoon, submergence rate
exceeds emergence rate resulting in a decrease in the number of bask-
ing individuals. The first individuals to attain PBT and eventually
reenter the water are probably the smaller animals since they heat
more rapidly. Data taken on March 5 substantiate this (Fig. 14).
Between 1100 and 1300 hours, there was an inverse relationship be-
tween size of basking individuals and the body-air temperature
differential. No such correlation existed between 0900 and 1100 hours,
indicating that time of emergence was independent of body size. Figure
15 shows the changes in body temperature of a Natrix taxispilota, and
the associated environmental temperatures under natural climatic con-
ditions of November 28, 1970, at Lake Alice.
During the warmer months (mid-April through mid-October), such
thermoregulatory behavior is seldom necessary, because air and water
temperatures during the day are usually within the PBT of this species.
Because of the level and wide range in PBT, snakes occasionally were
found to bask in one location from time of emergence until evening
submergence. Water temperatures during these months were often within
the preferred range, and most snakes either remained in the water or
had submerged by census irne (Fig. 12).
With the approach of nightfall, few if any snakes remain on basking
sites above the water (Fig. 13). In initial laboratory experiments,
where lights came on at 0900 hours and went off at 2100 hours, snakes
usually emerged within an hour of onset of lighting (given proper
thermal conditions) and submerged within the 30-minute period after
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light was terminated. After several weeks exposure to this photoperiod,
however, snakes often entered the water an hour or more before 2100 hours.
This evening submergence appears to be a temperature-independent
response to decreased light; snakes slide into the water regardless of
the air-water temperature differential. Boyer (1965) noted that most
basking turtles left their basking sites and submerged prior to
30 minutes before sunset, although no mention was made of air and
water temperatures at these times. Since evening submergence is
evidently common in most semiaquatic reptiles, and since it is temperature-
independent (at least in Natrix taxispilota), this response probably
represents a predator avoidance behavior. Clearly much feeding --
almost exclusively on fish -- does occur at this time, when water
temperatures permit; but little feeding behavior probably occurs below
a water temperature (and therefore body temperature) of 15 C (Lueth,
1941). Large fish could ingest small Natrix, but only alligators would
represent a substantial predation threat to brown water snakes during the
aquatic phase of their activity cycle.
In natural situations, the water is usually warmer at night
than:yth air;-. It may be, therefore, that evening submergence evolved
as a thermal response and persists even in the unnatural situations to
which snakes were subjected in the laboratory.
Factors Affectin- Preferred Body Temperature
As previously mentioned, there appears to be a mutually causal
relationship between the level of physiological acclimation and PBT,
resulting in a fixed preferred level of about 25-300C throughout most
of the year. There are other ecologically relevant factors which may
alter the level of preferred temperature, at least temporarily.
Snakes acclimated to 250C were fed fish containing ingestible
transmitters and were found to regulate (in a gradient) at a warmer
end of the normal range (Table 2). The same pattern was found in
animals that were given access to a heat lamp in an isothermal (21.0C)
environment. Two Natrix taxispilota were fed fish containing transmitters
and permitted to thermoregulate in this environmental chamber. The level
of air and water temperatures was low enough to induce basking but high
enough to permit attainment of body temperatures in excess of 300C
by basking under the sunlamp. The first day following feeding, these
snakes spent at least half the day in the water before emergence. This
delayed emergence is probably unrelated to thermoregulatory behavior. It
is a common behavioral trait of captive snakes, including terrestrial
species, to submerge in any available water after consuming a large
meal. The moisture evidently facilitates stretching of the skin, or
at least provides better support for the portion of the body containing
the food. Upon emergence, snakes maintained body temperatures mostly
between 27.50C and 31CC. When they first emerged, the snakes usually
lay with the bolus directly under the sunlamp and moved to a cooler
area after body temperature reached 300C to 320C. A four-day thermal
record for one of these snakes is shown in Fig. 16.
Thermophilic responses to feeding have been reported for other
reptiles (Regal, 1966; Bustard, 1967; Kitchell, 1969) including two
semiaquatic snakes, Natrix sipedon and Thamnophis sirtalis. In all
cases, the preferred thermal range following feeding seems to con-
stitute a sub-range of the postabsorptive PBT. This increase in pre-
cision of thennoregulation has in all cases been interpreted as a
facilitation of digestive processes.
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The effect of temperature on digestive efficiency was determined
for Natrix taxispilota at 20, 25, 30, and 350C. The greatest extraction
efficiency occurred at 300C (Fig. 17) and decreased both above and below
this temperature. This thermal level corresponds to the preferred
level for digestion (Table II). Regurgitation of food was very common
among snakes maintained at 350C, another indication that this was
supraoptimal thermal level for digestion. Below 300C, digestive
efficiency decreased with decreasing temperature but the 82.6 percent
efficient level at 200C is still a substantial figure. It is obvious
that high body temperatures expedited digestion but were not absolutely
necessary, indicating that under natural conditions, digestive processes
would continue at night well after submergence if water temperature was
not excessively cold. This wide range of digestive activity is probably
necessary in such poikilotherms to prevent putrefaction of ingested
food at night and during other periods when body temperature falls well
below 300C. Putrefaction would be a particularly great problem in
snakes since they ingest items whole and the internal tissue of in-
gested items would not be reached by gastric enzymes for many hours
or days if digestion ceased at temperatures slightly below the optimal
The influence of temperature on gastric digestion in the European
grass snake, Natrix natrix, was studied by Skoczylas (1970) who used
x-ray photography to determine the speed of digestion at temperatures
of 5, 15, 25, and 350C. l!e found that digestion was completely
arrested at 5C and proceeded very slowly (or ended in regurgitation)
at 150C. Digestion was complete at both 25 and 35C but was faster
at 250C. Digestive rates in the king snake, Lamnpropeltis getulus,
were found by Root (1961) to he similar to those of N. natrix below
Jr.-F. 1-1 1 I --. 1 -' -- I I I I
The effect of temperature on digestive extraction
efficiency of Natrix taxispilo ta. Horizontal line,
mean; vertical bar, standard deviation; vertical
~A~P-~- ~c ~--cl--s-L- ---- -- -
Table 2. Effect of digestion on the normal range of
preferred body temperatures.
PBT RANGE (C) 25.7 32.6 28.2-32.1
MEAN 29.86 30.28
N (OBS.) 5 (66) 4 (49)
250C, but the maximum digestive rate occurred at the highest temperature
employed, 33 C. Skoczylas attributed the discrepancy in digestive rates
of the two species at 33-350C to intraspecific differences in PBT.
Research on digestive rates of other poikilotherms tendsto substantiate
this generalization. Many freshwater fish are able t-o digest food at
2C to 50C (Wangensteen et al., 1958; Molnar and T61lg, 1962). These
temperatures are below the lower limit of the thermal activity range
of Spenodon punctatus, the lowest known for any reptile (Bogert, 1953a,
1953b). In fish studied over a wide range, digestive rate appears to
be directly correlated with water temperature (Riddle, 1909). However,
the rate of food input may also influence digestive efficiency. Davies
(1964) found that in Carassius auratus, the proper level of food input
could increase extraction efficiency to 92-94 percent at either 21.50C
or 120C. Other workers (Ivlev, 1939; Gerking, 1955) have found extraction
efficiencies of other fish at a given temperature to be independent of
input rate. Amphibians also show wide thermal ranges for digestion
(Pegel, 1939; Joly, 1958; Root, 1961) and are capable of digesting at
temperatures less than 10C, levels at which peristalsis ceases in most
reptiles (Skoczylas, 1970). The processes of gastric digestion and
peristalsis may have different thermal thresholds, as in the painted
turtle, Chrysemys picta, which cannot digest, but maintains peristalsis,
at 50C (Fox and Masacchia, .1959). Nonheliothermic poikilotherms, there-
fore, seem to have lower thermal thresholds for digestive processes than
Other Factors Affecting Preferred Body Temperature
Regal (1967) clearly demonstrated that several species of lizards
placed in a gradient will select night temperatures that are well be-
low their preferred diurnal PET. This was tru2 of Klauberina riversiana,
a nocturnally-active lizard, as well as three heliothermic
diurnally-active forms. No such endogenous variation in the level
of PBT was found in Natrix taxispilota maintained in a gradient.
From April through October, water temperatures at the study site
were generally warmer at night than air temperatures. A voluntary
hypothermic response to darkness would therefore be inconsistent with
their behavior. Evening submergence appeared to be a temperature-
independent response to diminished light.
The data of Kitchell (1969) suggest that snakes undergoing
ecdysis actively select body temperatures below their normal PBT.
The three species he investigated included two semiaquatic species,
Thamnophis sirtalis and Natrix sipedon. The latter, when not shedding,
had a PBT of 28.03 + .28 C (mean + standard deviation) but a preference
of 18.71 + .38 C when undergoing ecdysis. In the present study, there
were not enough data available to detect ouch voluntary hypothermic
response to ecdysis but, in view of the unanimity of Kitchell's data
for three species of snakes -- one congeneric with N. taxispilota --
it seems likely that brown water snakes have lower thermal preferenda
No pregnant females were used in this study but data from several
sources suggest that such individuals have thermal preferences that
differ from those of males and non-pregnant females. Stewart (1965)
found in Thamnophis sirtalis and T. ordinoides "a consistent tendency
for pregnant females of both species to maintain relatively high body
temperatures." Fitch (1960) found that gravid female copperheads,
Ancistrodon contortrix, regulated within more precise limits than males
or non-pregnant females and noted that "most of the copperheads found
basking in sunshine in sumr.er were females."- Osgood (1970) found
pregnant female Natrix taxispilota and N. fasciata to thermoregulate
within a narrower temperature range than males or non-pregnant females,
but his sample for Natrix taxispilota consisted of only four individuals
(three pregnant females, one male). In all of these accounts, the body
temperatures fell within the limits of the normal PBT but constituted
a smaller sub-range within it.
The effect of intraspecific differences in size upon PBT has- been
examined by several workers, inter alia Bogert (1949), Wilhoft (1958),
Hirth (1963), and Brooks (1968). Only in Basiliscus vittatus (Hirth,
1963) were statistically significant differences found and the differences
were so slight (35.3 + 0.05 C in juveniles, 34.7 + 0.07 C in adults) that
ecological significance cannot be ascribed. The most likely candidate
for an ecologically significant change in PBT with size is probably
Varanus kemodoensis, the world's largest lizard. This species is
arboreal as a juvenile and becomes terrestrial upon attaining the
length of 1.5 to 2.0 meters (Walter Auffenberg, private communication).
It would be surprising if a change in PBT did not accompany this change
in habitat preference.
The PBT in a given species of reptile, then, is not an immutable
thermal level. It nay undergo temporal changes and changes reflecting
the thermal optima for various physiological processes. It has long
been known thai snakes undergoing ecdysic processes refuse to feed.
This behavior pattern has been interpreted as a response to avoid
damage to the newly developing epidermal layer which would be severely
stretched or even split by the ingestion of large items. The pre-
ceding; discussion of the thermal requirements of these two processes
ecdysiss and digestion) in reptiles, suggests a thermal incompatibility
and certainly presents at least as strong an argument for their non-
The Ecological Significance of Reptilian Preferred Body Temperature
Many workers (Ruibal, 1961; Brattstrom, 1965; Kitchell, 1969;
Skoczylas, 1970) have commented on the empirical relationship be-
tween the PBT of reptiles and the microclimate of their habitat.
Again, these generalizations deal mostly with lizards. Diurnally-
active desert lizards generally have higher PBTs than lizards from
non-desert areas. Diurnal reptiles generally have higher thermal
preferenda than nocturnal species. Surprisingly, the significance
of this relationship has never been examined from the standpoint of
causality. Existing data on reptilian thermal preferences and tolerances
suggest that climate may be a major factor in evolutionarily setting
the level of PBT.
The thermal extremes between which reptiles must live are the
approximate levels that freeze their tissues and those that denature
their proteins, or in other ways cause physiological heat-death. But
most, if not all, reptiles keep their body temperature from varying
with environmental temperature, by maintaining it at a certain level
within this 50 C span. Evolutionarily, reptiles can choose the ceiling
of their preferred range by behaviorally utilizing solar energy.
Empirical evidence of this is the occupation by several species of
reptiles with different PBTs of a common habitat (Cowles and Bogert,
1944; Bogert, 1959; Soul6,.1963). However, the thermal characteristics
of the environment leave less evolutionary choice in the lower threshold
of the PBT because reptiles lack the cooling mechanisms characteristic
of most mammals and birds (Schmidt-Nielsen and Dawson, 1964) and can
therefore cool only to the level of the coolest segment of their environ-
ment. Summer shade temperatures in North America set this lower utilizable
level at about 20 0C to 230C for diurnally-active terrestrial reptiles.
Thus, the observation that PBT is generally closer to the critical
thermal maximum than to the critical thermal minimum is to be expected,
because the thermal range between critical thermal minimum and 20-23 C
is unavailable. However, many diurnal reptiles operate at thermal
levels only a few degrees below temperatures that cause irreversible
tissue damage. The question, therefore, becomes why do not all
diurnally active reptiles choose PBTs of about 25-35 0C and leave
margins of safety at both ends? The answer is apparently related to
(1) the biological effects of thermal extremes and (2) the correlation
between PBT and the critical thermal maximum.
Hypothermia slows the rates of physiological processes, but rarely
causes irreversible damage above 0 C. However, irreversible tissue
damage is incurred at temperatures above about 44 C. These temperatures
slightly exceed the highest air temperature (though certainly not the
highest black-bulb temperature) to which a diurnal animal could expect
to be exposed in its normal activity and natural habitat. There is a
direct correlation between the preferred level of body temperature and
the level of critical thermal maximum (Schmidt-Nielsen and Dawson, 1964;
Brattstrom, 1965; see Fig. 18). The highest body temperature a reptile
will ever attain must be below the CTMax if that animal is to survive,
and this body temperature should be directly related to the highest air
temperature experienced. These environmental thermal extremes are
l"The thermal point at which locomotory activity becomes dis-
organized and the animal loses its ability to escape from conditions
that will promptly lead to its death" (Cowles and Bogert, 1944).
2"The temperature that causes a cold narcosis and effectually
prevents locomotion" (Cowles and Bogert, 1944).
The relationship between preferred body temperature
and critical thermal maximum in reptiles (r = .59)
Data are from Brattstrom (1965) for species with
sample sizes of 20+.
20 li 14 i6 4'8 50
CRITICAL THERMAL MAXIMUM (
CRTIA THRA AXMM/C
selective factors which set the level of CTMax by eliminating the
individuals with lowest thermal tolerance. Since CTMax bears a re-
lationship to PBT, that is apparently genetically fixed, there should
be a direct correlation between these environmental extremes and PBT.
Furthermore, the PBT of a reptile should be more strongly correlated
with the highest temperature recorded in its habitat than with any
mean high temperature value because the latter are clearly of less
evolutionary significance in fixing the level of CTMax.
Figure 19 shows the high correlation (r = 0.61) between PBT in
several primarily heliothermic species of reptiles and the highest
temperature ever recorded at the weather station nearest the collection
locality (Kincer, 1941). Studies that failed to list collecting
locality, or for which no such weather data could be found, are excluded.
Data from studies in which field body temperatures constituted the
basis for determination were included only if the sample size exceeded
20 and observational correlations were made. When these conditions
are met, PBT and mean body temperature (Peters, 1964) become synonymous
and comparison between these values is valid. The pertinent statistical
data and references are listed in Table 3..
As expected, the correlation with PBT is significantly greater
for maximum temperature than for the mean temperature of the hottest
month (July in the northern hemisphere, January in the southern). This
supports the hypothesis that the level of PBT is indirectly fixed
evolutionarily by its relationship to the level of CTMax, which is
directly fixed by high environmental temperature extremes. This does
A primary heliotherm is here defined as a diurnally-active lizard
inhabiting an open habitat (or habitats) that offer access to sunlight
throughout the day.
'44 P- (V
V h C)
0 :3 4J
41> 0 c3
ZU cc 4) 4
0)~ W 4-1
6 -4 f-l :3
4~J p-. 0
ts U) u a)
P '0 -4 r)
0k r4 e
0 41 r4
l)4J x C4W
sa'v ~ a
>0 41 ,- m
., .-4 ) --4
4 ) .CU (-r4a-
oo 4)-( u:
0 r:,: 04J
0) *il U 0
(~4 5 U U) *'tO
(C m 0J( d )
r-4 r.4 0 CC a)
C) a C) p
I p u) c
a) 6 dv)
h o (-i r c;
d c: v,- o *
(DoJ 3nivJlV3dW31 ,30O8 4oJ9 fJjAd
Is~rrrrr;i~-larslaas~---slr~~,~~, ~ ~I~
Table 3. Data for points plotted in Figure 19 for
primary heliothermic lizards.
MAXIMUM TEMP. MEAN HIGH TEMIP.
CORRELATION COEFFICIENT 0.78 0.54
EQUATION FOR LINE Y = .492X + 14.46 ----
Cowles and Bogert, 1944
Lee and Badham, 1963
not mean, however, that the absolute level of PBT is solely a function
of high air temperature extremes. Any species-specific behavior
(burrowing, panting, etc.) that meliorates the severity of such
extremes will be of selective advantage. It is the interaction of
these behavior patterns and physiological tolerances that, under the
selective pressures of high temperatures, will determine the level of
PBT. Interspecific differences in behavior and physiological tolerance
will result in the utilization by several species with slightly different
PBTs of a common habitat.
By setting their body chemistry to operate optimally at a given
temperature, reptiles concomitantly- must accept diminished levels
of 'metabolic efficiency' at non-optimal temperatures. At body
temperatures below PBT, metabolism merely slows down as a function of
temperature (Fig. 20), and normal activity, such as food procurement,
ceases. But, at such times, the animal incurs no tissue damage and
the decreased level of metabolism is compatible with decreased digestive
efficiency (and therefore energy availability) and food consumption.
At temperatures above PBT, however, the decreased levels of digestive
efficiency (and metabolic efficiency generally) and food consumption
coincide with an increase in metabolism. In addition, very high
temperatures will cause irreversible tissue damage. So by choosing
relatively high body temperatures, heliothermic reptiles avoid the
problem of overheating and are penalized by having to remain inactive
or suboptiimally active on-cool days. The opposite strategy of choosing
a low PBT to insure more days of activity entails the risk of over-
heating to the point of death. This, as mentioned, is probably the
mechanism that sets the level of reptilian PBT evolutionarily. High
thermal extremes will eliminate the least heat tolerant latestt CTMax)
. c u
0 *to T.
4- r Cd s*
\ O o
\ \ -0. O
individuals and select for a species with a higher CTMax (and PBT).
Theoretically, a reptile's CTMax should be just above the highest
ambient temperature (and body temperature) the species ever encountered
in its normal habitat during its normal period of activity. Therefore,
diurnal terrestrial species should have higher PBTs than nocturnal
Still, the highest daytime air temperature recorded in an area
should be correlated with the highest night temperature. A correlation,
then, does exist between PBT of nocturnal reptiles and highest air
temperature (Fig. 21). The correlation is weaker than with primarily
heliothermic species, as would be expected. Between the lines relating
PBT with highest air temperature in primary heliothermic species and in
nocturnal species, there are a series of points which form a third line
with an intermediate slope. The points are for diurnally-active snakes
and forest lizards. The lizards (Anolis aad Eumeces) bask (in patches
of sunlight reaching the forest floor) but not nearly as extensively
as primary heliothermic species. However, the heliothermic snakes
(Coluber and Heterodon) occur in the same open habitats in which
heliothermic lizards maintain higher PBTs. This suggests that the
differences in thermal preferenda of snakes and lizards may be a
function of differences in the ecology of the two groups. The nocturnal
species used to determine line A (Fig. 21) were, with one exception
(the Gila monster, Heloderma suspectum), all snakes, so it is impossible
to determine from these data whether their lower thermal preferenda
exist because they are nocturnal or because they are snakes, or both.
One consistent characteristic of snakes that separates them from
almost all lizards suggests a basis for a lower PBT. This is the
absence of legs. The thermoregulatory significance of this is that
136 3'48 42 4 4 6 48 56
MAXIMAL TEMPERATURE (C)
Relationship between reptilian preferred body
temperature and the highest air temperature re-
corded in the collection area. A. nocturnal
reptiles (circles). B. diurnal snakes and forest
lizards (squares). C. primary heliothermic lizards
(from Figure 17). Statistical information and sources
for data are listed in Table 4 (line A) and Table 5
Table 4. Data for points plotted in Figure 21 for
nocturnal reptiles (line A).
Bogert and del Campo, 1956
Fitch, 1956, 1960
Cowles and Bogert, 1944
MAXIMAL TEMP. MEAN HIGH TEMP.
CORRELATION COEFFICIENT 0.68 0.65
EQUATION FOR LINE Y = .368X + 12.07 --
1 Heloderma suspectum
2 Elaphe obsoleta
3 Thamnophis sirtalis
4 Thamnophis sirtalis
5 Thamnophis sirtalis
6 Thamnophis sirtalis
7 Thainnophis ordinoides
8 Thamnophis sauritus
9 Thamnophis butler
10 Natrix sipedon
11 Natrix taxispilota
12 Ancistrodon mokeson
13 Crotalus cerastes
Table 5. Data for points plotted in Figure 21 for
diurnal snakes and forest lizards (line B).
Fitch, 1954, 1956
MAXIMFUM TEMP. MEAN HIGH TEMP.
CORRELATION COEFFICIENT 0.81 0.48
EQUATION FOR LINE Y = 0.344X + 40.27
terrestrial snakes are in more intimate physical contact with their
environment and more vulnerable to conductive heat exchange with the
substrate. This, in part, explains why Carpenter (1956), in his
study of thermoregulation in three species of garter snakes, found
cloacal temperatures to be more closely correlated with the temperature
at the ground surface than with air temperature above or soil temperature
below. Desert lizards rely greatly on such conductive heat exchange as
a cooling mechanism. The desert iguana, Dipsosaurus dorsalis, presses
its venter from side to side in the sand exposing cooler layers to
which it loses body heat by conduction (Norris, 1953). At higher
temperatures, lizards retreat to burrows (DeWitt, 1967a, 1967b;
McGinnis, 1967; Norris, 1953) again relying on conductive heat exchange
to reach the preferred thermal level. The high surface temperatures
characteristic of desert regions frequently exceed the preferred body
temperatures of the reptiles occurring there. While a heliothermic
tetrapod can hold its body above this substrate and thermoregulate with
a degree of independence of it, snakes cannot. This undoubtedly at
least partly accounts for the paucity of diurnally active snakes in
desert areas where lizard species are abundant. And a nocturnal
activity pattern preordains a relatively low PBT.
If the absence of legs is of significance in determining the level
of PBT, diurnally-active legless lizards should fall on line B (Fig. 21)
with diurnal snakes. The only data available for such lizards are: for
the species Ophisaurus attenuatus (Fitch, 1956) in Kansas. Field
temperatures of 15 active individuals collected on clear days ranged
between 30.6 C and 33.7C. The mean value of 32.2 C would fall 1.4C
below the diurnal snake-forest lizard line. This is good agreement even
though this point was based on a sample size toosmall to warrant its
inclusion in Fig. 21.
1. Thermoregulatory behavior under natural and laboratory conditions
was studied in the brown water snake Natrix taxispilota.
2. The effect of temperature on digestive extraction efficiency was
3. The effect of acclimation on metabolic rate and preferred body
temperature was determined.
4. There is an inverse relationship between preferred body temperature
and acclimation temperature in brown water snakes. A seasonal change
in preferred body temperature occurs in nature.
5. There is an inverse relationship between thermal level of acclimation
and metabolic rate at a given temperature. Metabolism becomes accli-
mated to the highest of varying temperatures to which the snake is
exposed in a 24-hour period.
6. There are lower air and water threshold temperatures for emergence
in brown water snakes. Factors affecting the levels of these
thresholds include thermal acclimation and physiological state
of the animal.
7. Natrix taxispilota will not emerge at any air and water temperatures
in the absence of light.
8. There are temporal changes in the propensity for emergence after
initial onset of light.
9. Thermoregulatory responses of brown water snakes to various thermal
regimes are described and discussed.
10. There is a temperatutre-independent evening submergence response in
11. Brown water snakes digesting food thermoregulate at a sub-level
within the nonnrmal preferred body temperature range.
12. Digestive efficiency is greatest at about 300C and decreases above
and below this level.
13. It is suggested that high thermal extremes directly fix the critical
thermal maximum of reptiles and indirectly fix the preferred body
temperature. Supportive evidence is presented and discussed.
14. The absence of legs in snakes precludes thermoregulation with the
degree of independence of conductive heat exchange with the substrate
enjoyed by most lizards. It is suggested that this may, in part,
account for the relatively low preferred body temperatures of
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Donald Eugene Goodman was born January 30, 1944, at Kennett,
Missouri. In June, 1966, he received the degree of Bachelor of
Arts with a major in Zoology from the University of Missouri. In
1966, he enrolled in the Graduate School of the University of Florida
and has until the present time pursued his work toward the degree of
Doctor of Philosophy in the Department of Zoology.
Donald Eugene Goodman is a member of the American Society of
Ichthyologists and Herpetologists and the American Association for
the Advancement for Science.
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
A. F. Carr, Jr., Chairman
Graduate Research Professor of Zoology
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
B. K. McNab, Co-Chairman
Associate Professor of Zoology
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
Associate Professor of Zoology
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
E. S. Ford
Professor of Botany
This dissertation was submitted to the Dean of the College of Arts
and Sciences and to the Graduate Council, and was accepted as partial
fulfillment of the requirements fbr the degree of Doctor of Philosophy.
Dean, Collgt of Atsld/Sciences
Dean, Graduate School
UNIVERSITY OF FLORIDA
3 1262 08556 7401