Natural History of the Ornate Box Turtle, Terrapene ornata ornata Agassiz Part 9

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 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 gra.s.s 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 sh.e.l.ls 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 cla.s.s 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 s.e.xes (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 gla.s.s 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 25) ------------------+--------+---------+------------- 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 25 before the experiment was terminated.

[Ill.u.s.tration: 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 pinp.r.i.c.ks 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 (2.5 for each of four adults; 10.0 and 6.2 for two juveniles) than those at which locomotion was resumed in the warming phase (13 for the adults, 21.7 and 20.1 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 s.e.xual 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.

HIBERNATION

In northeastern Kansas ornate box turtles are dormant from late October to mid-April--approximately five and one half months of the year. Individuals may be intermittently active for short periods at the beginning and end of the season, however. Once a permanent hibernaculum is selected dormancy continues until spring; unseasonably warm weather between mid-November and March does not stimulate temporary emergence. There is little movement during dormancy except for the deepening or horizontal extension of the hibernaculum.

Woodbury and Hardy (1948:171) found desert tortoises (_Gopherus aga.s.sizi_) in dormancy from mid-October to mid-April in southwestern Utah; some tortoises became temporarily active on warm days in winter.

Cahn (1937:102) was able to compare hibernation in several individuals each of _T. ornata_ and _T. carolina_, kept under the same conditions in Illinois. Individuals of _T. ornata_ burrowed into the ground in October, two weeks before those of _T. carolina_ did, and continued to burrow to a maximum depth of 22 inches. Some individuals of _T.

carolina_ spent the entire winter in the mud bottom of a puddle and became semiactive on warm winter days. Other individuals of _T.

carolina_ burrowed nearly as deeply as did _T. ornata_. Individuals of _T. ornata_ emerged from hibernation one or two weeks later in the spring than did those of _T. carolina_. There are some indications that populations of _T. carolina_ in eastern Kansas are dormant for a shorter period of time than those of _T. ornata_ but comparative studies are needed to verify this. Richard B. Loomis gave me a large female of _T. carolina_ that he found active beside a highway in Johnson County, Kansas, on November 23, 1954; on that date most individuals of _T. ornata_ under my observation had already begun permanent hibernation but a few at the Reservation were still semiactive.

Fitch (1956b:438) listed earliest and latest dates on which box turtles were active at the Reservation in the years 1950 to 1954; in the five year period box turtles were active an average of 162 days per year (range, 140-187) or approximately 5.3 months of the year. It is significant that 1954, having the most days of activity was, according to my studies of growth-rings, an exceptionally good year for growth. Fitch's data indicate the approximate season of growth and reproduction but not of total activity, since he did not take into account the sporadic movements of box turtles in late fall and early spring.

Activity in autumn is characterized by movement into ravines and low areas; many turtles move into wooded strips along the edges of fields or small streams. Sites protected from wind, providing places for basking and for burrowing, are sought. Burrows of other animals, along the banks of ravines, were often used for temporary shelter; overhanging sod at the lips of ravine-banks provided cover beneath which turtles could easily burrow. After mid-October progressively fewer box turtles were found in open places and activity was restricted to a few hours in the warmest part of the day.

Low air temperature probably is the primary stimulus for hibernation.

Autumn rains are usually followed by a decrease in general activity.

Rain probably hastens burrowing by softening the ground.

Ornate box turtles more often than not excavate their own hibernacula.

Digging begins with the excavation of a shallow form which is deepened or extended horizontally over a period of days or weeks. Such hibernacula are sometimes begun at the edges of rocks or logs; the overhanging edge of an unyielding object acts as a fulcrum on the sh.e.l.l and hastens digging. Ornate box turtles are slow but efficient burrowers.

Forms in open gra.s.sy areas are begun at an angle of 30 to 40 degrees; an adult box turtle requires approximately one hour to burrow far enough beneath the sod to conceal itself but can dig into soft, bare earth much more rapidly. Once a hibernaculum is begun, all four feet are used for its excavation, the front feet doing most of the digging and the hind feet pus.h.i.+ng loose earth to the rear.

Several turtles were seen entering burrows and dens in late autumn and trailing records showed that some individuals visited several of these shelters in the course of a single day.

By means of systematic probing of known hibernacula it was found that they are deepened gradually in the course of the winter. Depth seems to be governed by the temperature of the soil. Hibernacula in wooded or sheltered areas were ordinarily shallower than hibernacula in open gra.s.sland.

In the autumn of 1953-54 two pens were constructed at the Reservation in order to study hibernation; one pen was on a wooded hillside and the other was on open gra.s.sland. Turtles in the gra.s.sland pen were in newly excavated hibernacula, just beneath the sod, on October 25 and did not emerge for the remainder of the winter, whereas turtles in the woodland pen were intermittently active until November 10.

Correspondingly, turtles in the gra.s.sland pen descended to depths of eight and one half and 11 inches, respectively, whereas those in the woodland pen were covered by a scant six inches of loose earth and leaf litter. In 1954 four turtles were traced (by means of trailing threads) to hibernacula on wooded slopes at the Reservation; two entered permanent hibernacula on November 13 and two remained semiactive until sometime after November 20. All four turtles spent the winter in hibernacula that were not more than six inches deep.

Temperatures of the soil at a depth of nine inches were usually slightly lower at the gra.s.sland pen than at the woodland pen on a given date. It is probably significant that individuals with trailing devices and individuals in experimental pens furnish the latest records for autumn activity. The unnatural conditions created by confining the turtles in pens restricted the number of hibernation sites that were available to them; although trailing devices did not affect the normal movements of box turtles on the surface of the ground these devices certainly hampered the turtles somewhat in digging. However, it is noteworthy that box turtles are able to move about after mid-November, whether this is of general occurrence under more natural conditions or not. Depths of hibernacula at the Damm Farm were also influenced by amount of vegetation or other cover. Maximum depth of hibernacula in more or less open situations ranged from seven to 18 inches whereas a female hibernating in a ditch that was covered with a thick mat of dead gra.s.ses was four inches beneath the surface of the soil, and another female was only two and one half inches below the floor of a den.

Several _T. ornata_ kept by William R. Brecheisen in a soil-filled stock tank on his farm in the winter of 1955-56, burrowed to maximum depths of seven to eight inches in the course of the winter. A layer of straw covered the soil. All the turtles were alive the following spring except for one juvenile, found frozen at a depth of one inch on December 30 (the lowest air temperature up to this time was approximately -12). Three adult and 24 juvenal _T. ornata_ hibernating in the earth of an outdoor cage at the University of Kansas in the winter of 1955-56, were all dead on December 3 after air temperatures had reached a low of -12 degrees.

Ornate box turtles are usually solitary when hibernating; in the rare instances in which more than one turtle is found in the same hibernaculum, the a.s.sociation has no social significance and is simply a reflection of the availability and suitability of the hibernaculum.

The only communal hibernaculum--the "Tree Den"--at the Damm Farm was discovered on October 16, 1955, after a turtle was traced to it by means of a trailing thread. The flask-shaped cavity, approximately two and one-half feet deep, in the north-facing bank of a narrow ravine, had an entrance one foot wide and nine inches high, nearly flush with the bottom of the ravine. Gra.s.ses on the bank of the ravine hung over the entrance and nearly concealed it. The steep sides of the ravine protected the entrance from wind.

Seven turtles were in the den when it was discovered, and on each of five subsequent visits from October 20, 1955, to March 6, 1956, fewer turtles were found in the den. Figure 24 shows the approximate length of stay of each known occupant of the den. Only one of the turtles (an adult female) that left the den returned. Turtles found in the den on three visits in October were more or less torpid and were seen easily from the entrance but on November 6 the two remaining individuals had burrowed into the sides and floor of the den.

Three turtles (one female, one male, and one juvenile) were found in separate form-hibernacula within a few inches of one another on November 6, 1955 (Pl. 21, Fig. 2). The common entrance to all three hibernacula was a shallow depression that resulted from an old post-hole. Soil in the depression was loose and moist and ideal for burrowing. The three hibernating turtles were situated, in a vertical plane, at depths of 18 ([Male]), 12 (juvenile), and seven ([Female]) inches. One of the turtles hibernating at this place on November 6 was basking on October 30 in the shelter of some tall weeds a few feet from the hibernaculum.

[Ill.u.s.tration: FIG. 24. The approximate length of stay of each known occupant of a den that was examined six times in the winter of 1955-1956 at the Damm Farm. Most of the occupants used the den as a temporary shelter and sought permanent hibernacula elsewhere. One turtle left the den for approximately two weeks and then returned to it for the rest of the winter. The temperature of the air outside the den (A) and the average body temperature of turtles in the den (B) are given at the bottom of the diagram for each date the den was examined. The symbol "J" represents a juvenal turtle.]