SEXUAL DIMORPHISMDifferences between adult males and females ofT. ornatahave been mentioned in several places in the preceding discussion of growth and development. Several sexual characteristics—greaterpreanal length, thickened base of the tail, slightly concave plastron, and smaller bulk—are found also in males of many other kinds of emyid turtles. From females, males ofT. ornataare most easily distinguished by the bright colors of their eyes, heads, and antebrachial scales. An additional, distinctive characteristic of males is the highly modified hind foot. The first toe is greatly thickened and widened; when the foot is extended, the first toe is held in a horizontal plane nearly at right angles to the medial edge of the plantar surface (Fig. 21). The hind foot of females is unmodified in this respect. Males tend to have heavier, more muscular hind legs than females.The bright colors of males are maintained throughout the year and do not become more intense in the breeding season. Males ofT. o. luteolabecome melanistic in old age whereas males of the subspeciesornatado not. In old males ofluteolathe skin becomes dark gray, bluish, or nearly black and much of the bright orange or red of the antebrachial scales and the green of the head is obliterated; the iris may also darken but in most specimens it retains some red. Females ofluteolatend also to darken somewhat in old age but not so much as males; females ofornatado not. Table 4 summarizes the more important secondary sexual characters ofT. ornata.Table 4.—A Summary of Sexual Dimorphism inTerrapene ornataCharacterMalesFemalesHeadSnout truncate in lateral profile, top of head and front of maxilliary beak forming an angle of nearly 90°; head yellowish green to bluish green; markings on head and neck reduced; head never spotted dorsally (Pl. 19, Figs. 7 and 8).Snout relatively round in lateral profile; front of maxillary beak not forming right angle with top of head; head dark brown, distinct pale markings on head and neck; head commonly spotted dorsally (Pl. 25, Figs. 5 and 6).IrisRedYellowish brownHind legsHeavy and muscular; first toe turned in, thickened, and widened (Fig. 21).Not especially heavy or muscular; first toe, if turned in, never thickened or widened (Fig. 21).ForelegsCenters of antebrachial scales bright orange or red.Centers of antebrachial scales yellow, pale orange, or brown.CarapaceRelatively lower, length contained in height (48 specimens) .58 times (± .005σm, range, .50 to .69).Relatively higher, length contained in height (94 specimens) .50 times (± .005σm, range .44 to .60).Plastron (hind lobe)Ordinarily slightly concave.Flat or convex, never concave.TEMPERATURE RELATIONSHIPSTolerances to environmental temperatures, and reactions to thermal stimuli influence the behavior of ectothermal animals to a large extent.Terrapene ornata, like other terrestrial reptiles inhabitating open grassland, is especially subject to the vicissitudes of environmental temperature. Other species of turtles living in the same area are more nearly aquatic and therefore live in a microhabitat that is more stable as regards temperature.Approximately 500 temperature readings in the field and many others in the laboratory were obtained from enough individuals to permit interpretation of reactions involved in basking, in seeking cover, and in emerging from temporary periods of quiescence at various times of the day.Box turtles commonly used open places such as cow paths, ravines, and wallows, for basking as well as for feeding and as routes of travel. 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 analysis 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 ofT. ornata. Soil temperatures were taken in the present study only when the turtle was in a form, hibernaculum, or den.Optimum TemperatureCowles 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 activeT. 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 ofT. ornatawas 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 (± 3.78σ) (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, sex, or individual preference of the turtle concerned.BaskingAlthough 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 relationships inGopherus agassizi; 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 ofTestudo horsefieldimay 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 ± 3.08σ). 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 surroundingfarm ponds—having unobstructed morning sunlight, nearby dense vegetation, and choice opportunities for feeding (cow dung,mulberrytrees) was preferred. Basking was frequently combined with feeding; in several instances box turtles were noted early in the morning at suboptimum body temperatures eating grasshoppers, berries, or dung insects. The predilection of box turtles for open areas is probably important in permitting extended activity at suboptimum temperatures.T. ornataprobably 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).Fig. 22.The relationship of body temperature (Centigrade) and kind of activity inT. 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 MinimaThe 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 usuallyseeking 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 ± 1.55σ). Fifty-nine of these temperatures (92 per cent) were 30 degrees or higher.Figure 22shows 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 retreatto 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 grassy 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 byT. 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,and30.2 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 illustrated by the following notes.Time(A. M.)BodytemperatureRemarks11:0033.0Tethered on slope.11:0534.6Strains at tether in several directions.11:0936.5Tries frantically to get away; draws in limbs and head rapidly andmomentarilyat any movement on my part, and hisses loudly.11:1337.5Mouth held open slightly; turtle overturns in effort to escape; frantic scrambling resumed a few seconds after I right turtle.11:1738.2Mouth now held open most of the time; white froth begins to appear around mouth.11:2038.6Stops activities every 10 seconds or so, rests chin on ground and gapes widely; will still pull into shell when prodded with stick.11:2339.2Still wildly active; continues to gape widely every few seconds.11:2739.4Frothing at mouth profusely.11:3039.6Attempts to escape are now in short feeble bursts. 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.11:3539.5Attempts to burrow into mud at edge of pond.11:36Enters shallow water and moves slowly back to shore.11:3738.8Turtle 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 35.5.11:5735.0Moves 50 ft. up slope to shade of low vegetation.1:55 P. M.32.5Turtle 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 conductionto 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.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 ± 6.38σ). The range of body temperatures in this group is greater than in the other groups shown inFigure 22because 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 thoroughlya 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, nineT. ornataof 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.AgeclassCarapacelength in mm.Weightin grams1) Hatchling33.18.42) Hatchling[A]29.96.73) Juvenile52.529.34) Juvenile50.226.15) Adult ♂1253766) Adult ♀1184007) Adult ♂1193868) Adult ♀1103259) Adult ♀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 individualtherefore 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).GroupNumberCooling phaseWarming phase (to 25°)Hatchlings2.282.310Juveniles2.264.180Adult ♂2.122.152Adult ♀3.119.130[B]Adult (all)5.120.138[B]None of the females reached a temperature of 25° before the experiment was terminated.Click on image to view larger sized.Fig. 23.Changes in temperature of the body of four juvenal (nos. 1 to 4) and five adult individuals ofT. 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 (2.5° 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, therateof 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 largerspecies 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 ofT. ornatawould 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, andPseudemys 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.HIBERNATIONIn 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 agassizi) 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 ofT. ornataandT. carolina, kept under the same conditions in Illinois. Individuals ofT. ornataburrowed into the ground in October, two weeks before those ofT. carolinadid, and continued to burrow to a maximum depth of 22½ inches. Some individuals ofT. carolinaspent the entire winter in the mud bottom of a puddle and became semiactive on warm winter days. Other individuals ofT. carolinaburrowed nearly as deeply as didT. ornata. Individuals ofT. ornataemerged from hibernation one or two weeks later in the spring than did those ofT. carolina. There are some indications that populations ofT. carolinain eastern Kansas are dormant for a shorter period of time than those ofT. ornatabut comparative studies are needed to verify this. Richard B. Loomis gave me a large female ofT. carolinathat he found active beside a highway in Johnson County, Kansas, on November 23, 1954; on that date most individuals ofT. ornataunder 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 ofrocks or logs; the overhanging edge of an unyielding object acts as a fulcrum on the shell and hastens digging. Ornate box turtles are slow but efficient burrowers.Forms in open grassy 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 pushing 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 grassland.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 grassland. Turtles in the grassland 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 grassland pen descended to depths of eight and one half and 11½ 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 adepthof nine inches were usually slightly lower at the grassland 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 grasses 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.SeveralT. ornatakept 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 juvenalT. ornatahibernating 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 association 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. Grasses 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 24shows 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 oneanother 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 (♂), 12 (juvenile), and seven (♀) 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.
SEXUAL DIMORPHISM
Differences between adult males and females ofT. ornatahave been mentioned in several places in the preceding discussion of growth and development. Several sexual characteristics—greaterpreanal length, thickened base of the tail, slightly concave plastron, and smaller bulk—are found also in males of many other kinds of emyid turtles. From females, males ofT. ornataare most easily distinguished by the bright colors of their eyes, heads, and antebrachial scales. An additional, distinctive characteristic of males is the highly modified hind foot. The first toe is greatly thickened and widened; when the foot is extended, the first toe is held in a horizontal plane nearly at right angles to the medial edge of the plantar surface (Fig. 21). The hind foot of females is unmodified in this respect. Males tend to have heavier, more muscular hind legs than females.
The bright colors of males are maintained throughout the year and do not become more intense in the breeding season. Males ofT. o. luteolabecome melanistic in old age whereas males of the subspeciesornatado not. In old males ofluteolathe skin becomes dark gray, bluish, or nearly black and much of the bright orange or red of the antebrachial scales and the green of the head is obliterated; the iris may also darken but in most specimens it retains some red. Females ofluteolatend also to darken somewhat in old age but not so much as males; females ofornatado not. Table 4 summarizes the more important secondary sexual characters ofT. ornata.
Table 4.—A Summary of Sexual Dimorphism inTerrapene ornataCharacterMalesFemalesHeadSnout truncate in lateral profile, top of head and front of maxilliary beak forming an angle of nearly 90°; head yellowish green to bluish green; markings on head and neck reduced; head never spotted dorsally (Pl. 19, Figs. 7 and 8).Snout relatively round in lateral profile; front of maxillary beak not forming right angle with top of head; head dark brown, distinct pale markings on head and neck; head commonly spotted dorsally (Pl. 25, Figs. 5 and 6).IrisRedYellowish brownHind legsHeavy and muscular; first toe turned in, thickened, and widened (Fig. 21).Not especially heavy or muscular; first toe, if turned in, never thickened or widened (Fig. 21).ForelegsCenters of antebrachial scales bright orange or red.Centers of antebrachial scales yellow, pale orange, or brown.CarapaceRelatively lower, length contained in height (48 specimens) .58 times (± .005σm, range, .50 to .69).Relatively higher, length contained in height (94 specimens) .50 times (± .005σm, range .44 to .60).Plastron (hind lobe)Ordinarily slightly concave.Flat or convex, never concave.
Table 4.—A Summary of Sexual Dimorphism inTerrapene ornata
TEMPERATURE RELATIONSHIPS
Tolerances to environmental temperatures, and reactions to thermal stimuli influence the behavior of ectothermal animals to a large extent.Terrapene ornata, like other terrestrial reptiles inhabitating open grassland, is especially subject to the vicissitudes of environmental temperature. Other species of turtles living in the same area are more nearly aquatic and therefore live in a microhabitat that is more stable as regards temperature.
Approximately 500 temperature readings in the field and many others in the laboratory were obtained from enough individuals to permit interpretation of reactions involved in basking, in seeking cover, and in emerging from temporary periods of quiescence at various times of the day.
Box turtles commonly used open places such as cow paths, ravines, and wallows, for basking as well as for feeding and as routes of travel. 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 analysis 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 ofT. 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 activeT. 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 ofT. ornatawas 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 (± 3.78σ) (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, sex, 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 relationships inGopherus agassizi; 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 ofTestudo horsefieldimay 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 ± 3.08σ). 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 surroundingfarm ponds—having unobstructed morning sunlight, nearby dense vegetation, and choice opportunities for feeding (cow dung,mulberrytrees) was preferred. Basking was frequently combined with feeding; in several instances box turtles were noted early in the morning at suboptimum body temperatures eating grasshoppers, berries, or dung insects. The predilection of box turtles for open areas is probably important in permitting extended activity at suboptimum temperatures.T. ornataprobably 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).
Fig. 22.The relationship of body temperature (Centigrade) and kind of activity inT. 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.
Fig. 22.The relationship of body temperature (Centigrade) and kind of activity inT. 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 usuallyseeking 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 ± 1.55σ). Fifty-nine of these temperatures (92 per cent) were 30 degrees or higher.Figure 22shows 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 retreatto 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 grassy 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 byT. 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,and30.2 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 illustrated by the following notes.
Time(A. M.)BodytemperatureRemarks11:0033.0Tethered on slope.11:0534.6Strains at tether in several directions.11:0936.5Tries frantically to get away; draws in limbs and head rapidly andmomentarilyat any movement on my part, and hisses loudly.11:1337.5Mouth held open slightly; turtle overturns in effort to escape; frantic scrambling resumed a few seconds after I right turtle.11:1738.2Mouth now held open most of the time; white froth begins to appear around mouth.11:2038.6Stops activities every 10 seconds or so, rests chin on ground and gapes widely; will still pull into shell when prodded with stick.11:2339.2Still wildly active; continues to gape widely every few seconds.11:2739.4Frothing at mouth profusely.11:3039.6Attempts to escape are now in short feeble bursts. 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.11:3539.5Attempts to burrow into mud at edge of pond.11:36Enters shallow water and moves slowly back to shore.11:3738.8Turtle 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 35.5.11:5735.0Moves 50 ft. up slope to shade of low vegetation.1:55 P. M.32.5Turtle 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 conductionto 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.
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 ± 6.38σ). The range of body temperatures in this group is greater than in the other groups shown inFigure 22because 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 thoroughlya 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, nineT. ornataof 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.
AgeclassCarapacelength in mm.Weightin grams1) Hatchling33.18.42) Hatchling[A]29.96.73) Juvenile52.529.34) Juvenile50.226.15) Adult ♂1253766) Adult ♀1184007) Adult ♂1193868) Adult ♀1103259) Adult ♀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 individualtherefore 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).GroupNumberCooling phaseWarming phase (to 25°)Hatchlings2.282.310Juveniles2.264.180Adult ♂2.122.152Adult ♀3.119.130[B]Adult (all)5.120.138[B]None of the females reached a temperature of 25° before the experiment was terminated.
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).
Click on image to view larger sized.Fig. 23.Changes in temperature of the body of four juvenal (nos. 1 to 4) and five adult individuals ofT. 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.
Fig. 23.Changes in temperature of the body of four juvenal (nos. 1 to 4) and five adult individuals ofT. 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 (2.5° 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, therateof 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 largerspecies 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 ofT. ornatawould 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, andPseudemys 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.
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 agassizi) 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 ofT. ornataandT. carolina, kept under the same conditions in Illinois. Individuals ofT. ornataburrowed into the ground in October, two weeks before those ofT. carolinadid, and continued to burrow to a maximum depth of 22½ inches. Some individuals ofT. carolinaspent the entire winter in the mud bottom of a puddle and became semiactive on warm winter days. Other individuals ofT. carolinaburrowed nearly as deeply as didT. ornata. Individuals ofT. ornataemerged from hibernation one or two weeks later in the spring than did those ofT. carolina. There are some indications that populations ofT. carolinain eastern Kansas are dormant for a shorter period of time than those ofT. ornatabut comparative studies are needed to verify this. Richard B. Loomis gave me a large female ofT. carolinathat he found active beside a highway in Johnson County, Kansas, on November 23, 1954; on that date most individuals ofT. ornataunder 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 ofrocks or logs; the overhanging edge of an unyielding object acts as a fulcrum on the shell and hastens digging. Ornate box turtles are slow but efficient burrowers.
Forms in open grassy 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 pushing 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 grassland.
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 grassland. Turtles in the grassland 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 grassland pen descended to depths of eight and one half and 11½ 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 adepthof nine inches were usually slightly lower at the grassland 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 grasses 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.
SeveralT. ornatakept 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 juvenalT. ornatahibernating 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 association 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. Grasses 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 24shows 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 oneanother 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 (♂), 12 (juvenile), and seven (♀) 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.