The foregoing remarks on basking indicate the approximate, normal,
thermal tolerances of ornate box turtles. Many additional records of
body temperature were taken from turtles that were found under cover.
Turtles under cover in daylight were usually seeking protection from
either below-optimum or above-optimum temperatures. In avoiding low
temperatures, turtles usually chose more complete and permanent cover
than in avoiding high temperatures.
Body temperatures of 64 box turtles that were seeking cover or that
were under cover because of high temperatures ranged from 28.9 to 35.8
degrees (mean, 31.9 A+- 1.55[sigma]). Fifty-nine of these temperatures
(92 per cent) were 30 degrees or higher. Figure 22 shows this range to
overlap broadly with the temperature range of active turtles and the
means of the two groups are close to each other. Body temperatures
below 30 degrees (5) were all recorded late in the morning on hot
summer days when the air temperature was well above 30 degrees; they
are somewhat misleading because they are from turtles that were under
cover long enough to lower body temperature to the range of activity
although the turtles remained under cover because of hazardous
environmental temperatures.
The commonest retreats used by box turtles to escape heat were burrows
of other animals and small dens under thick limestone rocks, where the
air remained cool, even in late afternoon. Most of the burrows and
dens on the Damm Farm were known to me and could be checked each day.
Turtles seeking temporary refuge from high temperatures
characteristically rested just inside the opening of a den or burrow.
Less frequently, turtles burrowed into ravine banks or just under the
sod on level ground. A number of individuals with above-optimum body
temperatures were found in the shade of trees or high weeds in early
afternoon on hot days. Mulberry trees provided ample shade for such
activity and, in June and July, when ripe mulberries were abundant on
the ground, turtles frequently fed on them at times of the day when
temperatures were more hazardous in other areas.
Several turtles were found buried in mud or immersed in water at the
edges of ponds in the hottest part of the day; they were discovered at
first by accident and, on subsequent field trips by systematic
probing. Ordinarily the turtles were covered with mud or muddy water
and remained motionless, except for periodically raising the head to
the surface to breath. There was little vegetation near the edges of
ponds and by late morning on hot days the temperature of the
shallowest water was as high as the air temperature or higher.
Correspondingly, turtles found resting in mud and water had body
temperatures much higher than turtles in dens, burrows, or forms at
the same time of day. Box turtles that retreat to mud or shallow water
cool themselves less efficiently than they would in drier, better
protected microhabitats. I found no evidence that turtles went into
deeper water to cool themselves.
The length of time spent under cover varied; most turtles had two
daily periods of activity, the second beginning in late afternoon.
Some turtles moved from shelter to shelter in the time between periods
of activity. Several turtles were known to remain quiescent
continuously for several days in the hottest part of the summer.
The maximum temperature that a reptile can tolerate physiologically is
ordinarily higher than the maximum temperature tolerated voluntarily
(Cowles and Bogert, 1944:277); but, the two maxima may be separated by
only a few degrees. Most poikilothormous vertebrates neither tolerate
nor long survive body temperatures exceeding 40 degrees (Cowles and
Bogert, _op. cit._:269).
It is evident (Fig. 22) that ornate box turtles do not often tolerate
body temperatures above 33 degrees and that temperatures in excess of
35 degrees are probably never tolerated under natural conditions. At
9:15 A. M. on July 5, 1955, an adult female emerged from mud where she
had spent the night (body temperature 28.4A deg., mud 28.4A deg., air 30A deg.).
After foraging for 40 minutes in bright sunlight on a grassy hillside
she had moved approximately 100 feet and her temperature had reached
34.6 degrees (air 33.0A deg.). At 9:56 A. M. she moved rapidly and directly
to a den under a rock nearby; 15 minutes later her body temperature
had not changed but after 65 minutes it had dropped to 33.4 degrees.
The temperature of air in the den was 31 degrees. This female began
her activities at nearly optimum body temperature relatively late in
the morning and, by foraging intensively for less than one hour,
probably was able nearly to satisfy her daily food requirements; by
foraging near suitable cover she could remain active until her body
temperature reached a critical threshold, and she thereby saved time
otherwise required for finding cover or making a form.
The following observations, extracted from field notes, indicate that
body temperatures near 40 degrees are the approximate lethal maximum
and are well above those temperatures voluntarily tolerated by _T.
ornata_. On July 4, 1955, a subadult female was in the water at the
edge of a pond. The temperatures of the air, water, and turtle were
32.0, 30.6, and 30.2 degrees, respectively. At 11 A. M. the turtle was
tethered in direct sunlight on the hard-baked clay of the pond
embankment (temperature of air 33.4A deg.). The turtle's response to
steadily rising body temperature over a period of 31 minutes is
illustrated by the following notes.
Body
Time (A. M.) temperature Remarks
11:00 33.0 Tethered on slope.
11:05 34.6 Strains at tether in several directions.
11:09 36.5 Tries frantically to get away; draws in limbs and
head rapidly and momentarily at any movement on
my part, and hisses loudly.
11:13 37.5 Mouth held open slightly; turtle overturns in effort
to escape; frantic scrambling resumed a few seconds
after I right turtle.
11:17 38.2 Mouth now held open most of the time; white
froth begins to appear around mouth.
11:20 38.6 Stops activities every 10 seconds or so, rests chin
on ground and gapes widely; will still pull into
shell when prodded with stick.
11:23 39.2 Still wildly active; continues to gape widely every
few seconds.
11:27 39.4 Frothing at mouth profusely.
11:30 39.6 Attempts to escape are now in short feeble bursts.
11:31 Turtle released; crawls toward me and immediately
seeks shade of my body; when I move off, turtle
seeks shade of small isolated weed on pond embankment;
turtle removed to damp earth at edge
of pond.
11:35 39.5 Attempts to burrow into mud at edge of pond.
11:36 Enters shallow water and moves slowly back to
shore.
11:37 38.8 Turtle thrown into center of pond where it remains
motionless and drifts with wind to opposite
shore; remains inactive in mud and shallow water
at edge of pond; temperature of water near turtle
35.5.
11:57 35.0 Moves 50 ft. up slope to shade of low vegetation.
01:55 P. M. 32.5 Turtle has not moved.
The overheating may have incapacitated the turtle since it moved only
50 feet in the next two days; its body temperatures on the two days
subsequent to the experiment were 26.8 and 20.6, respectively.
The mentioned gaping, as in higher vertebrates generally, cools the
animal by evaporation from the moist surfaces of the mouth and
pharynx. By keeping the mouth open for more than a few minutes at a
time in hot dry weather, a turtle would surely lose body water in
amounts that could not always be easily replaced. Ornate box turtles
seem to utilize evaporation for cooling only in emergencies and rely
for the most part on radiation and conduction to lower body
temperature after reaching a relatively cool, dark retreat.
Box turtles were never active at body temperatures below 15 degrees
and were seldom active at temperatures below 24 degrees. The two
lowest temperatures (15.3A deg. and 16.3A deg.) were taken from individuals
crossing roads on overcast days in early May.
In 78 box turtles that were under cover because their environmental
temperatures were low, the body temperatures ranged from 2.7 to 30.6
degrees (mean 19.8 A+- 6.38[sigma]). The range of body temperatures in
this group is greater than in the other groups shown in Figure 22
because low body temperatures were studied over a wide range of
conditions, including hibernation.
Box turtles actually seek cover because of low temperatures only in
fall and spring and on occasional unseasonable days in summer when
temperatures drop rapidly. Retreat to cover, in the normal cycle of
daily activity, is governed usually by high temperatures at mid-day or
by darkness at the end of the day. Turtles in dens, burrows, and grass
forms, tended to burrow if temperatures remained low for more than a
few hours.
Box turtles under cover where they cannot bask have little control
over the lower range of body temperatures. The freezing temperatures
of winter can be escaped by burrowing deeper into the ground.
Temperatures approaching the lethal minimum, however, seldom occur
during the season of normal activity. By remaining hidden in a burrow
or den therefore, box turtles are fairly well protected from predators
but are at a thermal disadvantage.
A number of turtles that had wet mud on their shells were found
basking in early morning near ditches, ponds, and marshy areas;
several others were partly buried in mud, shortly after daybreak, and
another was at the edge of a pond after dark.
Eight adults, located just as they emerged from cover in early morning
on sunny days, had body temperatures of 19.7, 21.9, 24.2, 24.5, 25.8,
26.6, 28.7, and 29.5 degrees. In five emerging from earth forms, body
temperatures were at least a degree or two below the temperature of
the air; the other three came from mud or shallow water and had body
temperatures higher than the air temperature.
Temperature is probably the primary stimulus governing emergence after
temporary periods of quiescence. Turtles in earthen forms are usually
completely covered or are head downward with only the hind quarters
exposed. Obviously, the more thoroughly a turtle protects itself
(beneath the insulating cover of a form, burrow, or den) against
unfavorable temperatures, the longer it will take for favorable
temperatures to bring about normal activity again. Turtles in forms
and deep burrows have a minimum of contact with the outer environment;
but in dens beneath rocks and in shallow burrows light and air can
enter freely. Turtles might be influenced in their activities to some
extent by the intensity of light at the opening of a burrow or den;
they are surely stimulated by changes in the temperature and humidity
of air coming through the opening. Shallow retreats that a turtle can
enter and leave with the least effort therefore seem most efficient
for purposes of thermocontrol, especially when they provide earthen
surfaces into which the turtles can burrow more deeply if more severe
environmental conditions develop.
In October, 1955, nine _T. ornata_ of various sizes, collected in
Douglas County, Kansas, were brought to the laboratory for observation
under conditions of controlled temperature. They were kept at room
temperature for several days and were fed regularly, with the
exception of one hatchling that was fed nothing in this period. On
October 22 the turtles were placed in a room where the temperature was
maintained constantly at zero degrees. One of the nine turtles, an
adult female, was killed with chloroform immediately prior to its
removal to the cold room. A list of the turtles used in this
experiment is given below.
Age Carapace Weight
class length in mm. in grams
1) Hatchling 33.1 8.4
2) Hatchling[A] 29.9 6.7
3) Juvenile 52.5 29.3
4) Juvenile 50.2 26.1
5) Adult [Male] 125 376
6) Adult [Female] 118 400
7) Adult [Male] 119 386
8) Adult [Female] 110 325
9) Adult [Female] 115 ----
[A] Starved.
Turtles were kept in the cold room for periods of 100 minutes
(hatchlings and juveniles) and 200 minutes (adults). The entire
experiment, including the time in which the turtles were allowed to
warm after they were taken from the cold room, covered a period of
nearly six hours (375 minutes) during which the turtles were under
constant observation. Individual body temperatures were taken
continuously in this period (39 for each juvenile and 24 for each
adult) in the order that the turtles were numbered; gaps between
records of the body temperature of a given individual therefore
represent the time required to record temperatures for the rest of the
turtles in the group. The rates of rise and fall of temperature for
each of the nine turtles considered are shown as a graph in Figure 23.
Rate of temperature change was inversely proportional to bulk;
hatchlings, for example, cooled and warmed a little more than twice as
rapidly as did adults. Rate of temperature change was intermediate in
juveniles but was more nearly like that of adults in the warming phase
and closer to that of hatchlings in the cooling phase (Table 5).
Considering that hatchling no. 2 was smaller than no. 1, the rate of
change in its temperature did not seem to be significantly altered by
starvation. The adult males showed a tendency to change temperature
faster than adult females even though both males were larger than any
of the females. The slight difference in rate of temperature change
between the sexes (Fig. 23) may have been fortuitous.
One hatchling (No. 1), when its temperature dropped below one degree,
fully extended all four limbs and the body was elevated and only the
anterior edge of the plastron was in contact with the confining glass
dish. Raising the body from an uncomfortably cold or hot substrate is
a well known phenomenon in many lizards and in crocodilians, but to my
knowledge has not been reported for turtles.
TABLE 5.--Average Rate of Change in Temperature (Expressed in Degrees
per minute) for four Groups of Turtles Subjected to Temperature
of Zero Degrees and then Allowed to Warm at 27 Degrees
(Centigrade).
==================+========+=========+=============
| | Cooling | Warming
GROUP | Number | phase | phase
| | | (to 25A deg.)
------------------+--------+---------+-------------
Hatchlings | 2 | .282 | .310
| | |
Juveniles | 2 | .264 | .180
| | |
Adult [Male] | 2 | .122 | .152
| | |
Adult [Female] | 3 | .119 | .130[B]
| | |
Adult (all) | 5 | .120 | .138
------------------+--------+---------+-------------
[B] None of the females reached a temperature of 25A deg. before
the experiment was terminated.
[Illustration: FIG. 23. Changes in temperature of the body of
four juvenal (nos. 1 to 4) and five adult individuals of
_T. o. ornata_ (nos. 5 to 9) exposed to a constant air
temperature of zero degrees Centigrade for periods of 100 and
200 minutes, respectively. The vertical arrows indicate when
the turtles were removed to an air temperature of 27 degrees.
Sizes and weights of the turtles used are given in the text.
Turtle number nine, a female, was killed by means of chloroform
before experiment began. Rate of change in temperature in
specimens was inversely proportional to size. All turtles
survived the experiment.]
Hibernating turtles and those experimentally chilled were usually
comatose but were almost never completely incapacitated even at
temperatures at or near zero degrees. Experimental pinching, probing,
and pulling revealed that muscles operating the neck, the limbs, and
the lobes of the plastron could be controlled by the turtle at low
temperatures; hissing, resulting from rapid expulsion of air through
the mouth and nostrils (when the head and limbs are drawn in
reflexively) occurred at all body temperatures but was sometimes
barely audible in the coldest turtles. Of all living turtles observed,
only two (hatchlings 1 and 2 in coldroom experiment) were completely
immobile at low temperatures, failing to respond even to pinpricks at
body temperatures of 0.8 and 1.7 degrees, respectively, although other
turtles, under the same experimental conditions, consistently gave at
least some response to the same stimulation.
Turtles chilled experimentally continued to move about voluntarily,
albeit sluggishly, at temperatures much lower (2.5A deg. for each of four
adults; 10.0A deg. and 6.2A deg. for two juveniles) than those at which
locomotion was resumed in the warming phase (13A deg. for the adults, 21.7A deg.
and 20.1A deg. for the juveniles). Hatchlings chilled so rapidly that it
was difficult to ascertain accurately the temperature at which
inactivity was induced. Juveniles became active gradually, moving
slowly about when the body temperature reached approximately 20
degrees but not attempting more strenuous activities such as climbing
the walls of enclosures, until body temperatures of 22 to 25 degrees
were attained. Adults, on the other hand, exhibited "normal" activity
as soon as they became voluntarily active.
The ability of ornate box turtles to move about when the body
temperature is near the lethal minimum probably enables those caught
in the open by a sudden drop in environmental temperature to find
cover that keeps them from freezing to death. Prolonged chilling, on
the other hand, seems to create a physiologically different situation;
the temperature at which activity is resumed is higher and subject to
less variation.
Juveniles were more rapidly affected by environmental temperatures,
were subject to different thresholds, and were inactive over a wider
range than were the adults. Indeed, the _rate_ of chilling, rather
than absolute body temperature alone, might in large measure influence
the reactions of turtles to environmental temperatures. If this be so,
smaller turtles, having a narrower thermal range of normal activity,
must lose at least some of the advantages gained by their ability to
warm up more rapidly.
Hatchlings and juveniles at the Damm Farm were always active on days
when at least some adults were also active. Fitch (1956b:466) found
that, in northeastern Kansas, species of small reptiles and amphibians
are active earlier in the season than larger species and that the
young of certain species become active earlier than adults. Fitch
stated, "... small size confers a distinct advantage in permitting
rapid rise in body temperature by contact with warmed soil, rock or
air, until the threshold of activity is attained"; he pointed out also
that young animals, if able to emerge earlier than adults, would
benefit from a longer growing season. Hatchlings and juveniles of _T.
ornata_ would benefit greatly from an extra period of activity of say,
one or two weeks in spring and a similar period in autumn, especially
if food were plentiful. The extra growth realized from such a "bonus"
period of feeding would significantly increase the chance of the
individual turtle to survive in the following season of growth and
activity.
Ornate box turtles are active within a narrower range of temperatures
than are aquatic turtles in nearby ponds and streams of the same
region. Observations by William R. Brecheisen and myself on winter
activity of aquatic turtles indicate that, in Anderson County, Kansas,
the commoner species (_Chelydra serpentina_, _Chrysemys picta_, and
_Pseudemys scripta_) are more or less active throughout the year;
although they usually do not eat in winter, they are able to swim
about slowly and in some instances (_P. scripta_) even to carry on
sexual activity at body temperatures only one or two degrees above
freezing. But, ornate box turtles hibernating in the ground a few
yards away are incapable of purposeful movement at such low body
temperatures.