Thermoregulation in the brown water snake, Natrix taxispilota, with discussion of the ecological significance of therman...


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Thermoregulation in the brown water snake, Natrix taxispilota, with discussion of the ecological significance of therman preferenda in the order Squamata
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ix, 85 leaves. : illus. ; 28 cm.
Goodman, Donald Eugene, 1944-
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Water-snakes   ( lcsh )
Animal heat   ( lcsh )
Body temperature -- Regulation   ( lcsh )
Zoology thesis Ph. D   ( lcsh )
Dissertations, Academic -- Zoology -- UF   ( lcsh )
bibliography   ( marcgt )
non-fiction   ( marcgt )


Thesis - University of Florida.
Bibliography: leaves 80-84.
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Thermoregulation in the Brown Water Snake, Natrix taxispilota,
with Discussion of the Ecological Significance of
Thermal Preferenda in the Order Squamata





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

my degree.










Radio Tc









SNTS . .

ES . . .

RES . . .

) METHODS ............

.on and Maintenance of Specimens

ilemetry ... .. .. ..

intal Apparatus .

Gradient .............

.sm .. . .

re Efficiency .


: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




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


* 58



snakes and forest lizards . .



Figure Page

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



Donald Eugene Goodman

June, 1971

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-



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.

Radio Telemetry

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.

Experimental Apparatus

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.

Figure 1.








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





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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.

Figure 3.

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.

Thermal Gradient

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.

Digestive Efficiency

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


here as:
Cf Cm
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.


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.

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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

Natrix taxispilota body temperatures and
associated air temperatures at Newnan's
Lake during (A) late December and early
January and (B) late January.

Figure 5.


d 26

w 22



Natrix taxispilota body temperatures and
associated air temperatures at Ncwnan's
Lpke during March.

Figure 6.

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

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Table 1. The preferred ranges of body temperature of
freshly caught Natrix taxispilota.


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
body weight.

A. acclimated to 200C, B. 250C, C. 300C,
D. 35C, E. varying temperatures (200C
night, 300C day).

Figure 8.



G6- A


1.5 0o 2:5 3.0 35

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.

Behavioral Thermoregulation

Morning Emergence

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



30 2./


--- 26-:/
S- ---

10 12 1 16 18 20 22 24 26 28 3 Z 4


cx 16

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;

Regal, 1966).

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

Figure 13.

The number of Natrix taxispilota basking at
Newnan's Lake at various times on April 9,
1970, and the associated air, water, and black
bulb temperatures.

........ AIR



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-

ferred temperatures.

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).

Evening Submergence

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.

XI r 0 O rC
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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


Figure 17.

The effect of temperature on digestive extraction
efficiency of Natrix taxispilo ta. Horizontal line,
mean; vertical bar, standard deviation; vertical
line, range.


>- 90-


25 30


~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

heliothemnic species.

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

when shedding.

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 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
1 2
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).

Figure 18.

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+.

40- e





30 -

0 28


20 li 14 i6 4'8 50
0 5



76 8

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.

Q) -j
'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

a)4J a
ts U) u a)

P '0 -4 r)
0k r4 e
s-I .4

0 41 r4
l)4J x C4W
sa'v ~ a

V~t4 C44-
>0 41 ,- m

., .-4 ) --4
4 ) .CU (-r4a-
cV).Z UC
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)
vl C

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~

naom~:~-Sa~ll~-r-l-I-~~L~(~PI ;~-~-(I~ICPY--llll~~CIi

Table 3. Data for points plotted in Figure 19 for
primary heliothermic lizards.

FIG. 19

















Anolis allisoni

Anolis homolechis

Anolis sagrei

Crotaphytus collaris

Dipsosaurus dorsalis

Sauromalus obesus

Sceloporus graciosus

Sceloporus occidentalis

Sceloporus orcutti

Urosaurus ornatus

Cnemidophorus sexlineatus

Sceloporus woodi

Cnemidophorus tesselatus

Amphibolorus barbatus

Aniphibolorus inermis



















EQUATION FOR LINE Y = .492X + 14.46 ----



















Ruibal, 1961

Ruibal, 1961

Ruibal, 1961

Fitch, 1956

DeWitt, 1967b

Cowles and Bogert, 1944

Mueller, 1969

Larson, 1961

Mayhew, 1963

Brattstrom, 1965

Fitch, 1956

Bogert, 1949

Bogert, 1949

Lee and Badham, 1963

Pianka, 1971

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)

Cd 41
p ca
c) .,-I

. c u

U 0

S4-L- tr

4 -i

0 0-

0 *to T.

4- r Cd s*


u 0



(jt/Z0~) wslloevlw




\ 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

terrestrial species.

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







,Lu 0

136 3'48 42 4 4 6 48 56

Figure 21.

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
(line. B).


Table 4. Data for points plotted in Figure 21 for
nocturnal reptiles (line A).

;. 21
































Bogert and del Campo, 1956

Fitch, 1956

Carpenter, 1956

Kitchell, 1969

Fitch, 1965

Stewart, 1965

Stewart, 1965

Carpenter, 1956

Carpenter, 1956

Kitchell, 1969

Present paper

Fitch, 1956, 1960

Cowles and Bogert, 1944



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).


Anolis allogus

Anolis lucius

Eumeces fasciatus

Eumeces obsoletus

Coluber constrictor

Coluber constrictor

Heterodon platyrhinos


















Ruibal, 1961

Ruibal, 1961

Fitch, 1954, 1956

Fitch, 1955

Fitch, 1956

Kitchell, 1969

Kitchell, 1969



EQUATION FOR LINE Y = 0.344X + 40.27

FIG. 21










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

determined calorimetrically.

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

Natrix taxispilota.

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.

G. Nordliee
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.

June, 1971

Dean, Collgt of Atsld/Sciences

Dean, Graduate School


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