Natural History of the Ornate Box Turtle, Terrapene ornata ornata Agassiz Part 8

Burrows, dens beneath rocks, and forms, were used as shelter from high and low temperatures as well as from predators. Determining whether a turtle was truly active (moving about freely, feeding, or copulating), was basking, or was seeking shelter was difficult because the turtle sometimes reacted to the observer; for instance, basking turtles, whose body temperatures were still suboptimum, might take cover when surprised, and truly active turtles might remain motionless and appear to be basking. By scanning open areas from a distance with binoculars, an observer frequently could determine what turtles were doing without disturbing them. In the final a.n.a.lysis of data, temperature records accompanied by data insufficient to determine correctly the state of activity of the turtle, were discarded, as were temperature records of injured turtles and turtles in livetraps.

Cowles and Bogert (1944:275-276) and Woodbury and Hardy (1948:177) emphasized the influence of soil temperatures on body temperatures. It is thought that air temperatures played a more important role than soil temperatures in influencing body temperatures of _T. ornata_.

Soil temperatures were taken in the present study only when the turtle was in a form, hibernaculum, or den.

Optimum Temperature

Cowles and Bogert (1944:277) determined optimum levels of body temperature of desert reptiles by averaging body temperatures falling within the range of normal activity; they defined this range as, "...

extending from the resumption of ordinary routine [activity] ... to ... a point just below the level at which high temperatures drive the animal to shelter." Fitch (1956b:439) considered optimum body temperature in the several species that he studied to be near the temperature recorded most frequently for "active" individuals; he found (_loc. cit._) that of body temperatures of 55 active _T.

ornata_, 66 per cent were between 24 and 30 degrees, and that the temperatures 27 and 28 occurred most frequently. Fitch concluded (_op.

cit._:473) that the probable optimum body temperature of _T. ornata_ was 28 degrees and that temperatures from 24 to 30 degrees were preferred. Although Fitch treated all non-torpid individuals that were abroad in daytime as "active" and did not consider the phenomenon of basking, his observations on optimum body temperature agree closely with my own.

Body temperatures of 153 box turtles that were known definitely to be active, ranged from 15.3 to 35.3 degrees. The mean body temperature for active turtles was 28.8 degrees ( 3.78[sigma]) (Fig. 22).

Ninety-two per cent of the temperatures were between 24 and 30 degrees and 50 per cent were between 28 and 32; temperatures of 29 and 30 degrees occurred most frequently (22 and 21 times, respectively). The ten body temperatures below 24 degrees all were recorded before 9 A.

M. on overcast days when the air was cool and humid. It is noteworthy that two of these low temperatures (18.8 and 19.0) were from a copulating pair of turtles; two others (21.8 and 22.0) were from individuals that were eating. The highest temperature (35.3) was from a large female that was feeding at mid-morning in a partly shaded area.

The mean body temperature for active individuals (Fig. 22) is probably somewhat below the ecological optimum, because a few temperatures were abnormally low. The large number of body temperatures in the range of 29 to 31 degrees indicates an optimum closer to 30 degrees. Optimum body temperatures may vary somewhat with the size, s.e.x, or individual preference of the turtle concerned.

Basking

Although basking is common in terrestrial turtles, only a few authors have mentioned it. Woodbury and Hardy (1948:177-178) did not use the term in their account of thermal relations.h.i.+ps in _Gopherus aga.s.sizi_; their discussion indicates, however, that the tortoises move alternately from sunny to shady areas to regulate body temperature.

Desert tortoises removed from hibernacula and placed in the sun warmed to approximately 29.5 degrees before they became active, although a few did so at temperatures as low as 15 degrees. According to Cagle (1950:45), Sergeev (1939) studied body temperature and activity in the Asiatic tortoise, _Testudo horsefieldi_, and found that individuals basked for as much as two hours in the morning before beginning the first activity of the day (feeding), but that tortoises did not bask after a period of quiescense from late morning to late afternoon, during which body temperatures were seemingly maintained nearer the optimum than they were during nocturnal rest; body temperatures rose to approximately 30 degrees before the tortoises became active. Since body temperatures of 23 to 24 degrees were maintained at night, the basking range of _Testudo horsefieldi_ may be considered to be approximately 23 to 32 degrees.

Ornate box turtles basked chiefly between sunrise and 10 or 11 A. M.

Body temperatures of 60 basking turtles ranged from 17.3 to 31.4 degrees (mean, 25.5 3.08[sigma]). More than two-thirds (42) of these body temperatures were higher than the air temperature near the turtle, indicating probably that body temperature rises rapidly once basking is begun. In the instances where body temperature was below air temperature, the turtles had recently begun to bask (many were known to have just emerged from forms or other cover where they had spent the night) or were warming up more slowly because of reduced sunlight. On cloudy days basking began later than on clear days and body temperatures usually remained at a suboptimum level. Turtles that basked on days that were cloudy and windy, or cold and windy, did so in sheltered places, usually on the leeward sides of windbreaks such as limestone rocks, rock fences, or ravine banks. It was evident in these instances that the turtles either sought such shelter from the wind or remained ensconced in the more complete shelter of a form or burrow, not emerging at all.

Open areas of various kinds were used as basking sites. Level ground--such as on roads, cattle pathways, and bare areas surrounding farm ponds--having un.o.bstructed morning sunlight, nearby dense vegetation, and choice opportunities for feeding (cow dung, mulberry trees) was preferred. Basking was frequently combined with feeding; in several instances box turtles were noted early in the morning at suboptimum body temperatures eating gra.s.shoppers, berries, or dung insects. The predilection of box turtles for open areas is probably important in permitting extended activity at suboptimum temperatures.

_T. ornata_ probably carries on more nearly normal activity on cool days than do reptilian species with more sharply delimited thermal tolerances. Collared lizards (_Crotaphytus collaris_), for example, are chiefly inactive on days when the sky is overcast, although a few individuals having suboptimum body temperatures can be found in open situations (Fitch, 1956a:229 and 1956b:442).

[Ill.u.s.tration: FIG. 22. The relations.h.i.+p of body temperature (Centigrade) and kind of activity in _T. o. ornata_, compiled from 355 field observations. Vertical and horizontal lines represent, respectively, the range and mean. Open and solid rectangles represent one standard deviation and two standard errors of the mean, respectively.]

Toleration of Thermal Maxima and Minima

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 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 28.4, mud 28.4, air 30).

After foraging for 40 minutes in bright sunlight on a gra.s.sy hillside she had moved approximately 100 feet and her temperature had reached 34.6 degrees (air 33.0). 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 33.4). The turtle's response to steadily rising body temperature over a period of 31 minutes is ill.u.s.trated 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 sh.e.l.l 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 sh.o.r.e.

11:37 38.8 Turtle thrown into center of pond where it remains motionless and drifts with wind to opposite sh.o.r.e; 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 (15.3 and 16.3) were taken from individuals crossing roads on overcast days in early May.