Chinese box turtle, Cistoclemmys flavomarginata.
Photograph by Michael J. Connor.
Introduction
This article discusses the natural history and the captive care, breeding and rearing of the Chinese box turtle, Cistoclemmys flavomarginata. This wonderful animal was formerly imported to the U.S. from Taiwan in large numbers for the bulk pet trade. Although direct exports from Taiwan have diminished considerably, quantities continue to enter the international pet trade via Hong Kong. In addition to collection for the pet trade, the species is under pressure from economic development which has spurred both habitat loss and harvesting for China's burgeoning food and medicinal products market. While it still survives in some numbers, like many of Asia's turtles the Chinese box turtle faces an uncertain future.
Description
Cistoclemmys flavomarginata has been given a variety of common names including Chinese box turtle, yellow-margined box turtle, golden-headed turtle and snake-eating turtle. Its generic status has been fluid. In his original 1863 description, John Edward Gray assigned the species to Cistoclemmys. Later workers moved it to Cyclemys in the early 20th century, and then on into the genus Cuora in the 1930's. More recently, Roger Bour (1980) and Ren Hirayama (1983) presented extensive morphological evidence demonstrating that flavomarginata and other turtles in the Cistoclemmys clade are generically distinct from the rest of Cuora. Although criticized (McCord and Iverson, 1991), this hypothesis has never been formally disproved and the revived name Cistoclemmys flavomarginata has slowly gained in acceptance over the years (e.g. Iverson, 1985; Gaffney and Meylan, 1988).
The species occurs in southern China and various offshore islands. It has been divided into 3 poorly defined subspecies (McCord and Iverson, 1991): the nominate taxon Cistoclemmys flavomarginata flavomarginata from Taiwan; C. f. sinensis, a weakly distinguished taxon from southern mainland China; and C. f. evelynae from the Ryukyu Islands that has also been proposed as a separate species (as Cuora evelynae). All the animals discussed in this article are indistinguishable from C. f. flavomarginata as are most specimens seen in the U.S.
Cistoclemmys flavomarginata is a small, highly domed turtle. In adults, the carapace and plastron are a rich, dark brown except for the distinct creamy-yellow stripe down the vertebral keel, and the lightly pigmented lower edges of the marginal scutes and adjacent plastral scutes that effectively form a creamy-yellow rim around the edge of the plastron. In addition to the prominent vertebral keel, two broken lateral keels (one on each side) may be evident along the pleural scutes. The carapace is joined to the plastron by ligaments and not the bony bridge found in most other turtles. Because the plastron has a hinge between the pectoral and abdominal scutes the flexibility endowed by the ligaments allows these turtles to close up very tightly. The skin of the limbs is brown. The top of the head is a pale green marked on each side by a striking bright yellow line that goes from behind the eye to the back of the head. The skin of the chin and neck is colored a delicate apricot to pink or yellow. There are five claws on the forefeet and four on the rear. Sexing these turtles is not easy. Mature males have broader and larger tails than do females; the tails may be so broad in males that they appear to be triangular in shape.
Natural habitat
In his Turtles of Taiwan, Mao gives a secondhand account of one locality in southern Taiwan as: "a forested hill, on the side of which was a shaded stream with extremely luxurious high-stemmed vegetation. Under the vegetation of the damp bank, many turtles of this kind were concealed...about a hundred specimens were collected." He also cites Gray's claim that C. flavomarginata are frequently seen in ponds adjacent to rice fields.
The island of Taiwan is dominated by a central mountain chain that rises to 4450 meters. Lowland (coastal) Taiwan has a sub-tropical climate with cool, wet winters and hot wet summers. Higher elevations may stay cold year round. We obtained climate data for 3 known C. flavomarginata localities on Taiwan from the National Weather Bureau (ROC). I-Lan, in northeast Taiwan, has average minimum and maximum temperatures for January of 13.0° C (55.4° F) and 19.2° C (66.6° F) respectively; and for July of 24.7° C (76.5° F) and 32.1° C (89.8° F). Annual rainfall is 2726 mm (107.3 inches). Hengchun, in the extreme south, averages minimum and maximum temperatures of 17.6° C (63.7° F) and 24.2° C (75.6° F) in January, and 25.1° C (77.2° F) and 31.4° C (88.5° F) in July. Annual rainfall averages 2159 mm (85.0 inches). Taichung, on the drier west side of the island, averages minimum and maximum temperatures of 11.7° C (53.1° F) and 21.9° C (71.4° F) in January, and 24.4° C (75.9° F) and 32.8° C (91.0° F) in July. Annual rainfall averages 1710 mm (67.3 inches).
Southern China has a sub-tropical to temperate climate. Of the few mainland voucher specimens, the most northerly is from Ganyu (Jiangsu), China. How much further north the range extends is unknown, but Ganyu has hot, humid summers and cold, harsh winters. We obtained climate data for Ganyu from the U.S. National Climatic Data Center. Average minimum and maximum temperatures for January are -4.58° C (24° F) and 4.18° C (39.5° F) respectively; and for July are 23.4° C (74.0° F) and 29.9° C (84.4° F). Annual rainfall is 909 mm (35.8 inches).
Captive housing
VW keeps her C. flavomarginata in a mixed group with other species of box and water turtle at liberty in her specially modified back yard. The yard is divided into three main areas. A sunny, open area planted with shrubs, rocks and driftwood has an above ground pond that the turtles can access by climbing up plastic rain gutters. Adjacent to this area is a 26-foot by 13-foot wind-protected concrete patio that is used for basking on cooler days and where a 3-foot by 3-foot roofed turtle house is located that is heated to 24° C (75° F) in winter with a thermostatically-controlled, dog kennel heating pad. A second, similarly heated turtle house is located in an adjacent 14-foot by 18-foot section that is roofed over with clear fiberglass and enclosed with lattice. This shady area is extensively planted and has a waterfall with a catch basin, many water dishes and misters that are used on hot, dry days. This is the preferred haunt of her C. flavomarginata. Off this section through a hole cut in the lattice is a drier 6-foot by 9-foot area surrounded by a 3-foot high brick wall. This is also well stocked with plants and grasses, and is the second preferred area for her C. flavomarginata.
For the first three years the C. flavomarginata were moved indoors each winter. Now, they are left out year-round, unless there is a very heavy winter storm when they are moved indoors because their favorite brumation site tends to flood. Occasionally a C. flavomarginata will be found in one of the heated houses in winter. Normally, however, they spend most of the winter dug down in the soil. They have bred successfully both when allowed to hibernate and when kept warm during the winter.
MJC houses his C. flavomarginata in 2 separate groups. A breeding pair is housed in a 9-foot by 13-foot enclosure that they share with breeding pairs of Emys orbicularis and Terrapene carolina carolina. They have lived in this enclosure since 1988 and have passed through every winter (including the recent El Niño bruiser) burrowed down into compost. A densely foliated lemon tree permanently shades half the enclosure. Water is always available from a small (3-foot by 4-foot) pond. The enclosure includes compost piles (mainly decomposing leaves and lawn clippings), a large tuft of deergrass (Muhlenbergia rigens) and rotting logs that are used as refuges. The other 1.2 young adults are housed in a 6-foot by 18-foot pen that they share with 2.2 Terrapene carolina major and an immature pair of Pseudemys concinna gorzugi. A banana plant and small shrubs provide shade all day, and the entire enclosure is shaded from the afternoon sun by an adjacent building. It is furnished in similar manner to that housing the breeding pair. The C. flavomarginata have been housed in this pen for 2 to 6 years. Both pens are watered daily from a sprinkler during the summer.
Diet
C. flavomarginata are highly omnivorous. VW's adults favor earthworms, frozen pinkies (defrosted), snails, slugs, and mealworms. They also eat dry trout chow and moistened Whiskas dry cat food, canned cat food; fruits including strawberries, bananas, cantaloupe, and papaya; and vegetables including grated carrots, corn on the cob, and squash. Leafy greens are ignored. Cuttlebone and parrot mineral blocks provide a source of calcium. Mineral blocks are preferred and eaten by females and young regularly. MJC offers as much Purina trout chow as they will consume 3 times a week, dry cat food once a month, and seasonal fruits from his garden (loquot, apple, fig, nectarine, and strawberry guava) daily. Grapevine leaves and other sweet, green leafy vegetables and weeds are offered once a week. The carefully tended compost piles in the pens are a ready source of invertebrates that the turtles hunt for, with June bug larvae and slugs being principal prey. Occasionally they enter the pond and consume food (trout chow) meant for the pond turtles but usually they eat on land.
Courtship
Courtship in C. flavomarginata is both elaborate and elegant, and has been a constant source of interest and amusement for both authors. Although it may involve some chasing and biting, by turtle standards courtship is generally a gentle affair that requires the cooperation of both the male and the female. The most striking component is the goose-like extension and swaying of the neck by the male. The male stretches out his neck towards the female's head, placing his chin just above and parallel with the ground. He undulates his neck and in doing so may rub the top of his head on the chin of the female. This may be repeated several times. Sometimes the animals will then tussle: first the male then the female will attempt to pursue and catch and overturn the other. The male may drool and vocalize with a lip-smacking sound or a hiss. At some point this playful interaction becomes serious. The male will start to bite the front edge of the female's carapace and shake her, or gently nip at her forelimbs. Once she is stationary and has closed into her shell at the front he will move to her rear and mount.
Courtship occurs in the late spring, summer and fall. Neither author has witnessed evidence of courtship or copulation in the water. VW has observed that her adult males are aggressive towards other C. flavomarginata adult and juvenile males. She has seen neither interspecific aggression nor courtship, even though her animals are kept with many other species.
Nesting
All of VW's females have nested during daylight and the nests have all been made at the same location. This site receives only morning sun, and the soil is moist and fairly easy to dig. They may dig several holes before finally nesting. The nests are about 10 cm (4 inches) deep. Nesting has occurred from March through August. The largest female (867 g, 1.9 lb) lays multiple clutches of 2-3 eggs; in 1996 and 1997 she nested as follows:
| Date | Number of eggs |
| 05-20-96 | 3 |
| 08-06-96 | 2 |
| 04-10-97 | 3 |
| 05-05-97 | 3 |
| 06-15-97 | 2 |
VW's smaller females may lay a single egg per clutch but most still lay two to three clutches per year at 1 to 2 month intervals during the nesting season.
Nine out of ten nests detected by MJC were constructed in friable soil in heavy shade at the base of the lemon tree in the enclosure. The tenth nest was located 2-feet away under a rotting Mulberry log. Although he has observed nesting directly on only 2 occasions (completed at 6:15 p.m. and 7:20 p.m.) the relatively shallow nests (dug to a maximum depth of 10 cm) are easy to locate by clearing away the leaves and other debris from the nesting area and gently probing the soil with fingers. In two nests, one of the eggs was at ground level. In the 7 nests detected before 1997, the female had deposited one or two eggs per nest. In 1993 she nested, laid a single egg, and then two days later nested again producing a second egg. Only the second egg was fertile. In 1994, 1995 and 1996 only single clutches of 2 eggs were found. In 1997 she laid a single clutch of 3 eggs. So far this year (1998) she has laid 2 clutches of 3 eggs spaced 5 weeks apart.
Our combined experience has been that as a female grows, both the number of clutches and the number of eggs per clutch increases. The maximum clutch size of 3 eggs has been observed 7 times in 18 clutches (39%). Because the eggs are large, clutch mass forms a significant proportion of the female's total mass. Thus, the most recent clutch of 3 eggs (54 g) from MJC's 773 g female amounted to 7% of her body weight. Although this female laid two consecutive one-egg clutches two days apart in 1993, an internesting period of 3 to 5 weeks is the norm.
Eggs
The hard-shelled eggs are cylindrical and relatively large: 38 to 52 mm (1.5 to 2 inches) long by 13 to 25 mm (0.5 to 1.0 inches) wide, and weighing 11 to 18.5 g. Mean values for 8 fertile eggs were 50 ± 2 mm long, 22.5 ± 5 mm wide and 18.0 ± 0.5 g in weight. Fertile eggs usually develop a chalky, white band around the middle of the egg within a few days; rarely the whole egg will chalk. For artificial incubation, VW buries the eggs in moist vermiculite (equal parts vermiculite and water by weight) in a Tupperware® container fitted with a lid punctured with a few holes for ventilation and incubates them at 28.3° C (83° F). At this temperature, incubation takes from 68 to 85 days. For artificial incubation, MJC buries the eggs in moist vermiculite (2 parts vermiculite to 1 part water by weight) in a plastic shoe box with a loosely fitting lid placed in an incubator set at 28° C; but he usually leaves the eggs undisturbed to develop in the nest. Hatchlings have emerged from eggs left to incubate in the ground after 75 and 90 days for two separate clutches with known laying dates.
