Part 21

Ontogenetic change and sexual dimorphism in shape, color, and markings of head and neck. Females retain much of the juvenal pattern of spots and blotches. In males, the top and sides of the head become greenish or bluish and markings are obscured. FIGS. 1 and 3. Lateral and dorsal views of hatchling (A-- 3A1/2); FIGS. 2 and 4. Lateral and dorsal views of juvenile (A-- 2); FIGS. 5 and 6. Adult female (A-- 1); FIGS. 7 and 8. Adult male (A-- 1) showing relatively wider and more truncated snout in this sex.

FIG. 1. A foraging station next to a rock fence at the Damm Farm (June 28, 1958). The box turtle in foreground was in the act of tearing apart a pile of partially dried cow dung to obtain dung insects.

FIG. 2. A depression (A-- A1/2) made by a foraging box turtle in a pile of partially dried cow dung (June 28, 1958). Similar "sign" of box turtles was found in cow dung everywhere on the pasture at the Damm Farm.

FIG. 1. Thread-laying device ("trailer") taped to the carapace of an adult female T. o. ornata. The squares of tape on the sides are to keep the bent-over ends of the wire axle from catching on vegetation (A-- A1/2).

FIG. 2. A dermal pocket ("cyst") removed from an adult T. ornata and cut open to show two larval bot flies (Sarcophaga cistudinis) (A-- 2, May 15, 1956).

FIGS. 1-3. Stages in courtship of T. o. ornata: male pursuing female and biting her shell; male lunging at female in attempt to mount; and, male just after mounting female (A-- A1/4). FIG. 4. T. o. ornata smelling food (A-- 1). FIG. 5. T. o. ornata in attitude of alertness after detecting intruder (A-- 3/8). FIG. 6. Tracks of T. o. ornata in muddy ravine (A-- 1/8) (June 5, 1956).

FIG. 1. A small, nearly-healed, injury on the carapace of an adult T. o. ornata (A-- 2). Note regenerated epidermis at bottom of depression and two pieces of dead bone ("splinter scars") at upper right margin of depression. FIG. 2. Injured area on the carapace of a juvenal T. o. ornata (A-- 3) with dead bone removed and laid to the right, exposing regenerating epidermis in its early stages. FIG. 3. Anterior edge of carapace (held away with forceps) of specimen of T. carolina (KU 51461, Gulf Co., Florida) that had been badly burned (A-- 8/9). Nearly all the scutes of the shell had fallen off and large pieces of dead bone could be pulled away, exposing a gnarled mass of regenerating bone and epidermis. FIG. 4. A fracture that has healed and joined the tibia (upper bone) to the fibula in a specimen of T. o. ornata (KU 1877, A-- 3A1/2).

Top: A shell of T. o. ornata (A-- A1/2) as it was found at the Damm Farm June 1, 1956. A serious injury (probably resulting from burns) had exposed a large area of dead bone on the carapace. Center: Same shell with some of scutes removed. Bottom: Same shell with dead bone removed to expose regenerating epidermis and bone. Note that the injury involved several of the neural bones; the turtle probably died as a result of this injury but not before regeneration was approximately one-half completed.

Terrapene ornata seems to concentrate its breeding season (laying, incubation, and hatching of eggs) more nearly in the middle of the warm season than does T. c. carolina. This concentration probably is an adaptation for breeding in open habitats where, under environmental temperatures less equable than in forest, eggs would develop more rapidly and hatch sooner but would be less able to survive winter temperatures.

Males of T. o. ornata become sexually mature when younger and smaller than females and rarely grow as large as females. Nichols (1939a:20) indicated the reverse to be true of T. c. carolina; Nichols further indicated that growth continued some six to eight years after puberty. Most individuals of T. o. ornata attain maximum size within two to three years after puberty.

Although it is difficult to be certain about the adaptive value of color and pattern, it seems that in box turtles, as in many other kinds of animals, patterns and colors most nearly blending with those of the habitat have some selective value in providing concealment from enemies. The pattern of linear radiations in T. o. ornata closely resembles the patterns formed by light passing through grasses and associated vegetation and camouflages the turtle. In a similar manner, partial or complete loss of radial markings in T. o. luteola seems to provide concealment in habitats where vegetation is sparse and where blending with the substrate is of survival value. The patterns of blotches and broken radiations in most of the subspecies of T. carolina likewise provide camouflage by tending to match patterns formed by the light passing through a leafy canopy.

Although ornate box turtles are omnivorous, they probably depend on insects as a dietary staple. In years when preferred kinds of insects were unusually abundant, the turtles grew more than in other years. A large proportion of the insects eaten is obtained by foraging in or near dung. Alteration of the dung community--at least in a physical sense, but presumably also by influencing the successional stages of the dung biota--is one of the few evident effects of box turtles on the environment. Although certain kinosternids (Carr, 1952:93), emyids (Deraniyagala, 1939:257; Loveridge and Williams, 1957:198), and testudinids (Loveridge and Williams, op. cit.:247) eat mammalian feces, T. ornata is seemingly the only chelonian that habitually seeks its staple diet in dung. The habit seems to be yet another specialization for terrestrial existence. The carnivorous habits of T. ornata reverse the general trend toward omnivorous and herbivorous habits in other turtles that have become partly (emyids) or wholly (testudinids) terrestrial.

It seems remarkable that none of the species of true tortoises occurring in the grasslands of the world has developed insectivorous habits or utilized the unique food niche (in regard to dung-foraging) filled by ornate box turtles in the Great Plains; tortoises are, as far as is known, strictly herbivorous. The ranges of Gopherus and Terrapene are now almost mutually exclusive and the two kinds do not compete with each other for food in the few places where they occur together. It is known, however, that box turtles (T. longinsulae, ornata-like, earliest known box turtle) and true tortoises (genera Testudo and Gopherus, see Williams, 1950:25-26, Fig. 2) occurred together in what is now the Great Plains in early Pliocene times and probably for some time before and after this. Assuming that food habits of fossil representatives of these genera were somewhat like the habits of recent representatives, ornate box turtles may have developed insectivorous habits at a time when other food niches were filled by herbivorous tortoises. Box turtles possibly survived subsequent changes in habitat that made it impossible for populations of large tortoises to exist in the Great Plains.

SUMMARY

Box turtles of the genus Terrapene are emyid turtles that are specialized for terrestrial existence. Two of the seven species now recognized--T. ornata and T. carolina--occur in the United States. Terrapene carolina inhabits forested areas in the east whereas T. ornata is characteristic of open grassy areas in the west; the ranges of the two species overlap in the broad belt of prairie-forest ecotone in the central United States. Terrapene ornata is considered to be the most specialized of living box turtles.

The natural history of T. o. ornata Agassiz was studied in the period, 1953 to 1957. Intensive field studies were made in Douglas County, northeastern Kansas, on a small area of prairie and on the University of Kansas Natural History Reservation. Field observations were made also in a number of other places in eastern Kansas. Laboratory studies supplemented field studies.

Habitats occupied are chiefly open areas; they vary in regard to food supply, temperature, moisture, and kind of soil. The grassy prairies of Nebraska, Kansas, Oklahoma, and northern Texas seem to provide optimum habitat for ornate box turtles; in these areas box turtles are active on a majority of days from April to October. The subspecies luteola is adapted to the more rigorous and arid environment of the southwestern United States, where activity may be possible for only a few weeks in the year. The remainder of the year is spent in a state of quiescence. Factors limiting the distribution of T. ornata are: 1) the presence of a substrate too hard to permit digging of nests and forms (altitudinal distribution in southwestern United States and distribution at western edge of the range); 2) temperatures causing the ground to freeze deep enough (approximately 30 inches) to kill turtles in hibernacula (northern edge of range); and, 3) the lack of one or more relatively wet periods in the course of the warm season, preventing at least temporary emergence from quiescence (southwestern part of range). The activities of man probably have affected population density in local areas but limit the geographic range only in the north (Blanchard, 1923:19-20, 24) where intensive cultivation probably has excluded the species.

Preferred habitat in northeastern Kansas is open rolling grassland grazed by cattle; populations are most dense near natural breaks in the grassy vegetation such as fences, scattered rocks on hillsides, ravines, and stream-beds.

Mating occurs most commonly in spring and autumn; courtship behavior includes pushing and biting on the part of the male. In coitus the hind legs of the male are held tightly by the female; the male falls backward after coitus, still clasped by the female. A few sperm are stored in the oviducts; fertilization without reinsemination can occur. The spermatogenic cycle begins in May and reaches its peak in September, when large numbers of sperm and spermatids are present in the testes; the cycle is completed in October, when sperm pass into the epididymides. The testes are smallest in spring and largest in September. Females are inseminated with sperm produced in the preceding year. The ovarian cycle begins in midsummer, soon after ovulation, and continues up to the time of the next ovulation. Follicular growth is rapid in the period from spring emergence to ovulation. Large follicles remaining after ovulation represent, in many instances, eggs that will be laid later in the same season. Follicular atresia is never great enough to account for the destruction of all large follicles remaining after ovulation. All mature females lay at least one clutch of eggs per year. It is estimated that one-third of the females produces two clutches of eggs in a single season. Second clutches contain fewer eggs than first clutches. An alternation of ovarian activity occurs, whereby one ovary is more active than its partner in one season and less active in the next season. Alternating activity of ovaries accounts in part for the reduced number of eggs in young females, breeding for the first time, and in older, nearly senile females. Extrauterine migration of ova results usually in a more even distribution of eggs in the oviducts. Corpora lutea constitute an accurate record of the number of eggs produced by the ovary as well as the number of eggs laid.

Nesting occurs from May through July but is most common in mid-June; some of the females nesting early in the season lay a second clutch of eggs in July. Nests are dug in the earth by the female using her hind legs. Preferred nesting sites are open, well-drained places with a soft substrate. The nesting site is selected after a period of wandering, in which the female tests the substrate at a number of places; some females search for a nest site for more than a week. Nest digging begins in the evening and is usually completed after dark. Captive females dug a preliminary cavity in which the body rested during the digging of the main nest cavity. The entire clutch of eggs is laid in one nest. The average number of eggs in 23 clutches was 4.7 (range, 2 to 8). The average size of eggs tends to be inversely proportional to the number of eggs in a clutch. Eggs increase in bulk by absorption of water in the course of incubation. Immersion in water for short periods does not harm eggs. The incubation period under favorable environmental conditions is approximately 65 days; cool, damp conditions prolong the incubation period and probably constitute an important factor of prenatal mortality in certain years. Eggs that do not hatch before winter probably do not survive. Emergence of hatchlings from the nest may, however, be delayed until spring if the soil is dry in autumn. Hatchlings can probably escape freezing by burrowing into the walls of the nest. Infertility and prenatal mortality account for at least 40 per cent of the eggs laid, according to laboratory findings. Progeny of a single adult female (considering factors of mortality, multiple layings, and average age of puberty) would number approximately 300 after 20 years. Reproductive processes probably continue throughout life, although possibly at a somewhat reduced rate in later life.

Young box turtles are active soon after hatching but become quiescent if allowed to burrow in soil or if they are covered with damp cotton. Some captive hatchlings take live food in the first days of life but others do not eat until the following spring; initiation of growth is coincident with initiation of regular feeding. The yolk sac retracts mainly during hatching; it sometimes ruptures after hatching. The caruncle remains on the beak for a variable length of time, but never is present in the spring following hatching.

Major growth-rings on the epidermal laminae are formed regularly, one after each season of growth, in the first 10 to 14 years of life. Minor growth-rings occur between major rings and are shallower. Growth of epidermal laminae results from the formation, in spring, of a new layer of epidermis beneath the existing scute. The peripheral projection of the new layer is distinct in texture and color from the older part of the scute and is separated from it by a major growth-ring. Minor growth-rings form when growth slows or temporarily stops during periods of quiescence; no new layer of epidermis is formed. Growth-rings constitute an accurate record of growth that can be studied at any time in the life of the turtle; they are accurate indicators of age only as long as regular annual growth persists.

Growth in the season of hatching depends on early hatching and early emergence from the nest. Turtles that remain in the nest until spring probably do not grow. Slightly less than half of the free-living individuals studied grew in the season of hatching. Precociousness in early life often results in the attainment of sexual maturity at an earlier than average age.

Growth is rapid at first (increments in plastral length average 68, 29, and 18 per cent, respectively, in the first three years) and then slows gradually until puberty. Attainment of sexual maturity is more closely correlated with size than with age. Males mature when smaller (76 per cent were mature when plastron 100 to 109 mm. long) and younger (average age, eight to nine years) than females (66 per cent were mature when plastron 110 to 119 mm. long, average age at maturity, ten to eleven years) but females grow larger than males. A few individuals of each sex reach puberty three to four years sooner than average.

The average number of growing days per season is approximately 160. Amount of growth in any season depends on climatic factors that influence food supply and foraging conditions. Growth rate is directly correlated with precipitation, being highest when large populations of grasshoppers and long periods of favorable weather occur in the same year. Zones of epidermis formed in years when growth was especially slow or especially fast constituted landmarks that were helpful in interpreting growth-histories. Growth stops two to three years after puberty. The total growing period is estimated to be not more than 15 to 20 years. Longevity is estimated to be approximately 50 years.

A number of changes in structure and appearance occur in the period from hatching to puberty. Fontanelles of the bony shell close at or before puberty. Movable parts of the plastron are not functional until the fourth year. Markings on the carapace change from a series of dots to distinct, straight-sided radiations, and a similar pattern develops on the plastron. Markings on the heads of females resemble those of juveniles but males have greenish heads. Males further differ from females in having a red iris, more brightly colored antebrachial scales, and a turned in first toe.

Analysis of some 500 body temperatures (Centigrade) obtained under natural conditions revealed the following: the optimum temperature for activity is near 30 degrees; box turtles emerge from cover usually when body temperature is 24 degrees or higher, and almost never when the body temperature is below 15 degrees; body temperature is raised to optimum by basking in open areas although activity begins at suboptimum temperatures if basking is impossible; cover of dens, burrows, or forms is sought when the body temperature rises above 30 degrees; and, maximum and minimum body temperatures that would be lethal to box turtles (for prolonged periods) are approximately 40 and zero degrees, respectively. Laboratory experiments showed speed of response to environmental temperature to be inversely proportional to bulk; hatchlings could be chilled or warmed more than twice as fast as adults and were active within a narrower range of temperature. Ornate box turtles in general are subject to a narrower range of thermal activity than are aquatic turtles that occur in the same areas.

Box turtles are dormant approximately five and one-half months of the year--from late October to mid-April. Warm weather in November and late March sometimes stimulates temporary activity but dormancy is uninterrupted from mid-November to early March. Forms, dens, and burrows are used as hibernacula. Depth of hibernacula is dependent on severity of temperatures and amount of vegetational cover; hibernacula in open grassland were seven to 18 inches deep whereas those in wooded areas were six inches or shallower. Box turtles are ordinarily solitary when hibernating. Injuries and deaths due to freezing probably occur in the coldest part of the winter. The lowest body temperature of a turtle that survived a winter was 2.7 degrees; an individual, the temperature of which was nearly zero for several days, subsequently died. Turtles burrow upward at the end of hibernation and remain just below the surface for a week or two before emerging. The primary stimulus for emergence seems to be a period of warm moist weather.