Terrapene carolina

(Linnaeus, 1758)
Common box turtle

Terrapene carolina (to 20 cm) has a keeled, high-domed, elongated carapace highest posterior to the plastral hinge. It is rounded dorsally and not serrated posteriorly; a prominent medial keel is usually present on the 2nd to 4th vertebral scutes. Vertebral 1 is elevated at a steep angle (50° or more), and the 1st marginal is usually rectangular. All vertebrals are broader than long. The carapace is brown, usually with an extremely variable pattern of yellow or orange radiating lines, spots, bars, or irregular blotches on each scute. The plastron is often as long as or longer than the carapace, and its lateral rim may be indented at the seam between the femoral and anal scutes. Frequently an axillary scute is present at the 4th marginal. The plastral formula is: an > abd > gul > pect > hum >< fem; there is no posterior notch on the hindlobe. In color the plastron is tan to dark brown; it may be patternless, show dark blotches or smudges, or have a dark central area with branches along the seams. The head is small to moderate in size with a nonprotruding snout and a medially hooked upper jaw lacking a notch.
The diploid chromosome number is 50 (26 macrochromosomes and 24 microchromosomes): 20 metacentric or submetacentric, 10 subtelocentric, and 20 acrocentric or telocentric chromosomes (Stock, 1972; Killebrew, 1977a).
In most adult males the iris is red; in females it is yellowish brown. The posterior lobe of the plastron is concave in males, flat or slightly convex in females. The claws of the hind foot are, in males, short, stocky, and considerably curved; those of females are longer, more slender, and straighter. Males have longer and thicker tails than do the females.

Terrapene carolina ranges from southern Maine south to the Florida Keys and west to Michigan, Illinois, eastern Kansas, Oklahoma, and Texas. It has been reported from isolated localities in New York and western Kansas. In Mexico it occurs in the states of Campeche, Quintana Roo, San Luis Potosí, Tamaulipas, Veracruz, and Yucatán.

Geographic Variation
There are six extant subspecies, four in the United States and two in Mexico. Terrapene carolina carolina (Linnaeus, 1758), the eastern box turtle, ranges from southern Maine south to Georgia and west to Michigan, Illinois, and Tennessee. It has a short, broad, brightly marked carapace with the marginals nearly vertical or only slightly flared, and four toes on each hind foot. T. c. major (Agassiz, 1857), the Gulf Coast box turtle, ranges along the Gulf Coastal Plain from the Florida Panhandle to eastern Texas. This, the largest four-toed box turtle, sometimes exceeds 20 cm in carapace length. It has an elongated carapace on which the markings often are absent or are obscured by black or tan pigment; the rear margin flares strongly outward. The three-toed box turtle T. c. triunguis (Agassiz, 1857) ranges from Missouri south to Alabama and Texas. It usually has only three toes on the hind foot. The carapace typically is tan or olive with an obscure pattern. Orange or yellow spots usually are conspicuous on both the head and the forelimbs, but in males the head is often totally red. The Florida box turtle T. c. bauri Taylor, 1895 is restricted to peninsular Florida and the Keys. It, too, usually has only three toes on the hind foot, but the carapace has a bright pattern of light radiating lines, and there are two characteristic stripes on each side of the head. T. c. yucatana (Boulenger, 1895), the Yucatán box turtle, is restricted to the Yucatán Peninsula in the Mexican states of Campeche, Quintana Roo, and Yucatán. This four-toed subspecies has a long, high-domed carapace with the 3rd vertebral elevated into a small hump, and little flaring of the posterior marginals. The carapace is tan or straw-colored with dark radiating dashes or black scute borders. The Mexican box turtle T. c. mexicana (Gray, 1849) occurs only in a small area in Mexico, including southwestern Tamaulipas, northeastern San Luis Potosí, and northern Veracruz. It is a three-toed turtle with an elongated, high-domed carapace having the 3rd vertebral elevated into a small hump, and only moderate flaring of the posterior marginals. It is often patterned like T. c. triunguis, but may also be pale yellow with dark seams.
Studies of the phalangeal formulae of the subspecies of T. carolina by Minx (1992) showed that bauri and major share a common forefoot pattern, that of carolina is slightly different and intermediate between the pattern of the former two subspecies and that of triunguis, which is the most divergent of the four. Similarly, the hind-foot formulae of bauri, carolina and major are similar, while that of triunguis is divergent. Both the forefoot and hind-foot formulae of triunguis are most similar to that of the Mexican mexicana.

Terrapene carolina is predominantly a species of open woodlands, but it also occurs in pastures and marshy meadows. In Mexico, it occurs in scrub forests and brushy grasslands. Fires are an important factor in maintaining the proper habitat in some populations (Ernst et al., 1995). Apparently, individuals of T. carolina may occasionally enter caves (Poly and Noggle, 1996), but caves can not be considered normal habitat.

Natural History
Although sexual maturity has been reported in both sexes at 5-10 years of age by Minton (1972), a captive male received by Mertens (1973) when about 2.5 years old did not mate until it was about 18 years old. The sexual cycles of both sexes are well-known (Altland, 1951). In Maryland and Pennsylvania males, spermatogonia divide from May to July. Primary spermatocytes appear in June, peak in July, and decrease in numbers until autumn. Maturation divisions and spermiogenesis occur in July, and both increase greatly in early August. Spermatogenesis is past its peak by mid-September, after which seminal epithelium is greatly reduced in size. Following hibernation the testis is composed chiefly of Sertoli cells, lipid debris, and spermatogonia; the epididymides is filled with spermatozoa throughout the year. Interstitial cells are large and heavily laden with lipids during May, but are small in July and August. In the fall they increase in size, but there is little increase in lipid material. The oogenetic cycle begins in July and August, when the oogonia divide and grow in the germinal ridges located at sites scattered about the periphery of the ovary. New follicles are formed at this time, and usually 2-8 accumulate yolk during the fall. Ovarian weight is greatest in May. In June, after ovulation in late May, the collapsed follicles are transformed into corpora lutea, which atrophy by mid-August (Altland, 1951). Oviducal eggs are present in North Carolina females from May to July (Stuart and Miller, 1987). Mitchell and De Sá (1994) found oviducal eggs in a road-killed Virginia female in early October, but this was probably a case of egg retention past the normal nesting season.
Courtship and mating usually occur in the spring but may extend through the summer into autumn. Data collected by Evans (1953), Ernst (1981g) and Levell (1985) show that courtship is divided into three phases: a circling, biting, and shoving phase; a preliminary mounting phase; and a copulatory phase. In phase 1 the male approaches the female but stops when about 10 cm away, with his legs straightened, his head held high, and often with one leg raised above the ground. The female retracts her head but watches him. He then walks around the female, nipping her shell as he goes, or pushes her shell a few degrees upon its axis, bites it, and then pushes it farther around and bites it again. Up to an hour may elapse during this phase, depending on the readiness of the female to open her plastron. He eventually mounts and almost instantly hooks his toes into the posterior plastral opening, where she holds them tightly. Apparently, titillation of the claws upon the posterolateral edges of the female's carapace is the final stimulus inducing her to open the rear part of her plastron. In phase 2 the male's hind feet follow the edge of the plastron forward and, when near the hinge, the claws hook on and the rear plastron closes upon them. The stimuli that bring about phase 3 are the contact of plastron and carapace; the downward projection of the male's head in front of the female's head as he bites the forward edge of her shell; the touch of his forefeet upon her shell; and the slight motion of his pinioned claws on the plastral edge. For copulation, the male slips backward until his carapace rests on the ground, while the rear ankles of the female press downward and medially upon his feet, which have shifted farther in under her carapace. After several seconds he leans still farther back and then returns to the vertical position, in which intromission occurs (Terrapene carolina carolina 8). Female T. carolina may lay viable eggs for up to 4 years after mating (Ewing, 1943); tubular albumin-secreting glands in the oviduct serve as seminal receptables for sperm storage (Hattan and Gist, 1975).
Natural nesting occurs from May through July, but oviposition has been recorded as late as 17 August in captivity (Jackson, 1991a). Most nests are started in the evening and finished after dark; but some females have been found excavating nests in the morning (Carl H. Ernst, pers. obs.). The nest site usually is in an open, elevated patch of sandy or loamy soil; the flask-shaped nests are 75-100 mm deep.
The eggs are elliptical and have thin, white shells; they are 24.5-40.2 mm in length, 17.0-25.1 mm in width. Clutches range from 1-11 (Congello, 1978; Warner, 1982; Jackson, 1991a), but 4-5 eggs are usual; 5-6 clutches may be laid a season (Tucker et al., 1978; Messinger and Patton, 1995), although 2-3 clutches are more normal (Dodd, 1997). The interval between ovipositions is 12-38 days (Messinger and Patton, 1995). Dodd (1997) found 1.7-54.2% of the females in his population of T. c. bauri to be gravid in any month sampled, and that some females skip reproduction in some years. Normally 70-80 days are needed for incubation. Hatching and emergence usually take place from early September into October, but Schwartz (1968) reported a December emergence. Sometimes hatchlings overwinter in the nest (Gibbons and Nelson, 1978; Carl H. Ernst, pers. obs.).
Hatchlings have a flat, brownish gray carapace (28-35 mm) with a yellow spot on each large scute and a medial keel. The plastron is yellow to cream, with a brown central blotch; the hinge is nonfunctional until the turtle grows to about 50 mm. At hatching a caruncle is present between the nostrils; it is lost and the yolk sac is retracted within a week.
T. carolina is omnivorous. When young it is chiefly carnivorous, but it becomes more herbivorous with age. Animals eaten include snails, slugs, earthworms, insects, crayfish, spiders, millipedes, centipedes, isopods, fish, frogs, salamanders, reptile eggs, lizards, snakes, smaller turtles, and small mammals. They often feed on animal carrion. Roots, stems, fruits, and some seeds (T. carolina is a potential seed disperser; Braun and Brooks, 1987) of plants eaten: mushrooms, mosses, blackberries, blueberries, elderberries, mulberries, wild grapes, plums, strawberries, sweet cicely, tomatoes, mayapple, wintergreen, ground cherry, and grasses. Captives do well on canned dog food, newborn mice, chopped fish, hard-boiled eggs, egg shells, earthworms, tomatoes, apples, pears, bananas, shaved carrots, and commercial trout chow.
In the summer, activity of T. carolina is largely restricted to mornings or after rains. Often these turtles avoid the heat of the day by sheltering under rotting logs or masses of decaying leaves, in mammal burrows, or in mud; in the hottest weather they frequently enter shaded shallow pools and puddles and remain there for periods varying from a few hours to a few days. In other words, thermoregulation is accomplished by seeking a more suitable microenvironment. In the northern part of its range T. carolina enters hibernation in late October or November. In the deep south it may remain semiactive throughout the winter. When entering hibernation these turtles burrow into loose soil, sand, vegetable debris, the mud of ponds or stream bottoms, or old stump holes; they may enter mammal burrows. The same site may be used in successive winters. They go deeper as the soil temperature drops.

IUCN Red List Status (1996)
Lower risk: near threatened. Many populations of Terrapene carolina have been reduced or eliminated by destruction of habitat for agricultural or urban development, and box turtles are frequently killed on roads and highways. Mass collection for the pet trade is a serious threat to these long-lived, slow reproducing animals. Many US states now regulate or prohibit the taking of this species. Terrapene carolina is listed on Appendix II of the CITES treaty.