Eurasian pond and river turtles, and Neotropical wood turtles

(Geoemydidae)

Class Reptilia

Order Testudines

Suborder Cryptodira

Family Geoemydidae

Thumbnail description
A diverse family of hard-shelled turtles with a single articulation between the fifth and sixth cervical vertebrae, webbing between the toes, and posterior marginal scutes that extend up on to the suprapygal bone

Size
Up to 32 in (80 cm) carapace length and 110 lb (50 kg)

Number of genera, species
27 genera; 62 species

Habitat
Freshwater to coastal marine systems to primary and secondary forests

Conservation status
Extinct: 1 species; Critically Endangered: 13 species; Endangered: 18 species; Vulnerable: 11 species

Distribution
Eurasia and North Africa and the tropical Americas

Evolution and systematics

Formerly known as the Bataguridae, this family is most closely related to the tortoises of the family Testudinidae. Together these two families are next most closely related to the pond turtles of the family Emydidae. Fossils are known from as long ago as the Eocene. Geoemydid turtles previously were divided into two subfamilies based on the upper jaw width (i.e., wide alveolar crushing surfaces versus narrow ones). However, molecular studies have demonstrated that similarities in jaw width do not precisely reflect phylogenetic relationships. Hence, no subfamilies currently are recognized.

Physical characteristics

The well-developed shell includes 24 marginal and 12 plastral scutes. The pectoral and abdominal scutes contact the marginal scutes. In addition, the posterior marginal scutes extend up on to the suprapygal bone. A single articulation is found between the fifth and sixth cervical vertebrae. Most included species have at least some webbing between the toes and some species have a hinged plastron. Sexual dimorphism is extraordinary in some species; for example, males of the Indian tent turtle (Kachuga tentoria) are usually less than 4 in (10 cm) in shell length, whereas females approach 12 in (30 cm).

Distribution

Europe and North Africa to southern China and the East Indies; the Americas from northern Mexico to Brazil and Ecuador.

Habitat

From almost any freshwater ecosystem to coastal marine systems to fully terrestrial in primary and secondary forests; mainly tropical and subtropical.

Behavior

These turtles are fully aquatic to terrestrial. Some species are active year-round, while others are seasonally inactive (dry season or winter). The adult males are aggressive breeders, often intimidating unresponsive females by bumping or biting during courtship.

Feeding ecology and diet

This family includes species that are strictly herbivorous to those that are strictly carnivorous, with many omnivorous species as well. Some species have diverse, generalized diets and others have highly specialized diets.

Reproductive biology

The reproductive biology of most included species is very poorly known. Several species exhibit seasonal changes in the color of the head and soft parts that are apparently related to breeding. The production of multiple clutches per year is typical (at least five in some cases). In general, clutch size is positively related to body size. Many smaller species lay only one or two large eggs per clutch, but some of the larger species may lay up to 35 eggs in a clutch. Incubation times are highly variable, ranging from 60 to 272 days. Those with the longer times experience embryonic diapause,

in which development arrests for various lengths of time early during incubation. Two species are known to have dimorphic sex chromosomes, and therefore genetically determined sex. However, five species also are known to have temperature-dependent sex determination, with warm temperatures producing females and cooler temperatures resulting in males. In one of these five species, still cooler temperatures again produce females. These turtles hybridize readily in captivity, even between distant genera, and wild populations of hybrids may exist.

Conservation status

On the IUCN Red List, 11 species are listed as Vulnerable, 18 as Endangered, 13 as Critically Endangered, and one as Extinct. These turtles are in precipitous decline in Asia, where they are ruthlessly exploited for food, traditional medicines, and the pet trade. Habitat loss further compounds this crisis situation. Beyond the species presumed to be extinct, several species have not recently been seen in the wild. The extinction in nature of perhaps one-third of the included species is virtually a certainty unless this exploitation and the forces behind it can be curbed. Captive breeding programs for many of these threatened species are underway and may be the only hope for their long-term existence.

Significance to humans

Most species are collected by local humans for food or medicine whenever they are encountered.

Species accounts

List of Species

Painted terrapin

Callagur borneoensis

taxonomy

Emys borneoensis Schlegel and Müller, 1844, Borneo. No sub-species are recognized.

other common names

English: Painted batagur, saw-jawed turtle, three-stripe batagur, Sungei tuntong.

physical characteristics

This is a large geoemydid turtle (up to 30 in [76 cm] carapace length) with a rigid plastron and bridge (i.e., no plastral hinge); a fourth vertebral scute that is wider than long; crushing surfaces of the upper jaw that are broad along their entire length and bear a single, well-developed medial ridge; five claws on the forefeet; and no neck stripes.

distribution

Southern Thailand, Malay Peninsula, Sumatra, and Borneo.

habitat

Tidal sections of rivers and estuaries.

behavior

The females migrate considerable distances to nest (e.g., 9–31 mi [15–50 km] in the Malay Peninsula).

feeding ecology and diet

This species is primarily herbivorous, feeding on leaves and fruits, but also apparently eating clams and other shellfish on occasion.

reproductive biology

There are color differences between the males and females; those colors intensify incredibly during the breeding season. For example, nonbreeding males have a gray head, whereas during the breeding season the male's head becomes white with a black-edged red stripe between the eyes. Courtship and mating have not been described, but apparently occur in at least January and February on the east coast of the Malay Peninsula. Females migrate great distances to nest, either upstream on river sandbanks above tidal influence or on coastal beaches. Nesting occurs from late May to August, is nocturnal, and apparently peaks during the night at low tides. During the nesting season, one to three clutches of six to 25 (usually 10 to 15) large, elongate, hard-shelled eggs (measuring 2.4–3.1 in × 1.4–1.8 in [61–79 mm × 36–45 mm], and 2–3 oz [56–83 g]) are laid. The female digs no body pit, but rather uses her hind legs to dig a nest chamber to a depth of 9–13 in (24–34 cm). The internesting interval averages 26 days. Incubation requires 85–98 days at 88°F (31°C). The means by which hatchlings produced on sea beaches migrate to freshwater rivers is unknown, as is the effect of incubation temperature on sex.

conservation status

This species is listed as Critically Endangered on the IUCN Red List. A government-sponsored hatching program in the Malay Peninsula seeks to counteract local exploitation in the wild.

significance to humans

The eggs and meat of these turtles are relished by local people. In addition, since it is believed by some that this turtle brings good luck to its owner, a local pet trade has developed.

Yellow-margined box turtle

Cistoclemmys flavomarginata

taxonomy

Cistoclemmys flavomarginata Gray, 1863, Mainland China and Taiwan. Two or three subspecies are recognized.

other common names

Japanese: Hakogame.

physical characteristics

A small turtle (up to 7 in [17 cm] carapace length) with a high-domed carapace, unserrated posteriorly, with a distinct yellow vertebral stripe. The plastron is large and unnotched posteriorly, with a movable hinge between the pectoral and abdominal scutes, and the plastral lobes are capable of closing the shell opening completely. A single lemon-yellow stripe passes posteriorly from the eye onto the neck.

distribution

Southern China, Taiwan, and the Ryukyu Islands.

habitat

This species may occasionally inhabit freshwater ponds and streams, as well as rice paddies, but spends most of its time terrestrially in primary and secondary forests.

behavior

These turtles are often considered to be semiaquatic, but some populations may be almost exclusively terrestrial in their habits. Their ability to close up the plastron like a box is an adaptation for terrestriality, both for predator protection and desiccation resistance. On Taiwan terrestrial home ranges average 1.2 acres (0.5 ha) for females and 8.6 acres (3.5 ha) for males. Adults overwinter terrestrially by burying themselves under leaf litter or fallen logs or in the abandoned burrows of other animals.

feeding ecology and diet

These turtles are apparently omnivorous. They are attracted to traps baited with bananas in the field in Taiwan, but they eat both plant and animal matter in captivity. They are reported to consume worms, insects, snails, and fruit.

reproductive biology

During courtship the male rams the front of the female's shell to subdue her, and then moves to mount her shell from behind for copulation. On Taiwan this species is estimated to mature at 12 or 13 years. Females apparently nest from May through at least July on Taiwan, May to perhaps September on mainland China, and June to perhaps September in the Ryukyu Islands. On Taiwan, females produce one to three clutches per season; however, some females apparently do not reproduce every year. The shallow nests (2–3 in [5–8 cm]) are constructed at well-drained, open sites at the edges of forests. The clutch size ranges from one to four eggs. Eggs are elongate, brittle-shelled, and measure 1.6–2.1 in (40–54 mm) in length, 0.9–1.1 in (23–28 mm) in diameter, and 0.4–1.0 oz (12–27 g) in mass. Incubation apparently takes about two months, but the effect of incubation temperature on sex is unknown. This species apparently hybridizes with Geoemyda japonica.

conservation status

This species is listed as Endangered on the IUCN Red List. It is removed by humans for consumption for food and traditional medicine and for pets, and is also affected by habitat destruction (i.e., forest cutting).

significance to humans

These turtles are eaten by local people and also are exploited for the pet trade.

Chinese stripe-necked turtle

Ocadia sinensis

taxonomy

Emys sinensis Gray, 1834, China. No subspecies are recognized.

other common names

None known.

physical characteristics

This is a medium-sized geoemydid turtle (up to 9 in [24 cm] carapace length) with the plastron rigidly attached to the carapace and lacking a hinge; a fourth vertebral scute that is wider than long; the crushing surfaces of the upper jaw are broad along their entire length, with a single, well-developed medial ridge present on each surface; five claws on the forefoot; and numerous dark-bordered, narrow yellow stripes on the head and neck.

distribution

Taiwan, southern China (including Hainan Island), and northern Vietnam.

habitat

This species inhabits slow-moving lowland freshwater habitats, from ponds and rivers to marshes and human-made canals.

behavior

This is an aquatic turtle that often climbs out of the water to bask. Its behavior is in great need of study.

feeding ecology and diet

The only detailed study of this turtle's diet is from Taiwan; this study suggests that significant dietary differences exist between the sexes. Juveniles of both sexes tend to be carnivorous, eating primarily insects along with plant roots, shoots, and leaves. The males remain primarily carnivorous into adulthood, consuming mainly dipteran (mosquito) larvae and other insects, as well as some plant leaves, seeds, and roots. The females become increasingly herbivorous as they mature, feeding primarily on the leaves of terrestrial plants that grow along riverbanks, but also occasionally eating insects (especially dipteran larvae).

reproductive biology

Males apparently mature after three to four years and females after five to eight years. On Taiwan the females apparently nest from April to early June, although they are reported to nest from April to August on mainland China. On Taiwan the relatively deep nests (6–9 in [15–22 cm]) are constructed on open sandbars along the river or in open areas away from the water. The clutch size ranges from seven to 17 eggs on Taiwan, whereas three to 14 eggs per clutch are apparently laid on mainland China. The eggs are elongate, brittle-shelled, and on Taiwan measure 1.2–1.5 in (30–39 mm) in length, 0.7–0.9 in (18–22 mm) in diameter, and 0.2–0.4 oz (6–10 g) in mass. Three eggs laid in captivity by a female from Hainan Island were 1.6 × 1.0 in (40 × 25 mm), suggesting some geographic variation in reproductive parameters. The effect of temperature on sex is unknown. This species apparently hybridizes with at least the Chinese three-striped box turtle (Cuora trifasciata) and the Annam leaf turtle (Mauremys annamensis).

conservation status

This species is listed as Endangered on the IUCN Red List. It is surprisingly tolerant of polluted aquatic systems.

significance to humans

These turtles are frequently consumed by humans and small numbers still enter the pet trade. They may be ranched in impoundments on Taiwan and Hainan Island for commercial purposes. Studies have shown that plastrons of this species are frequently sold fraudulently as "tortoise shell" in medicine shops.

Resources

Books

Liat, Lim Boo, and Indraneil Das. Turtles of Borneo and Peninsular Malaysia. Kota Kinabalu, Malaysia: Natural History Publications (Borneo), 1999.

Zhou, J., and T. Zhou. Chinese Chelonians Illustrated. Nanjing, China: Jiangsu Science and Technology Publishing House, 1992.

Periodicals

Chen, Tien-Hsi, and Kuang-Yang Lue. "Ecology of the Chinese Stripe-Necked Turtle, Ocadia sinensis (Testudines: Emydidae), in the Keelung River, Northern Taiwan." Copeia 1998, no. 4 (1998): 944–952.

——. "Population Characteristics and Egg Production of the Yellow-Margined Box Turtle, Cuora flavomarginata flavomarginata, in Northern Taiwan." Herpetologica 55, no. 4 (1999): 487–498.

Iverson, J. B., W. P. McCord, P. Spinks, and H. B. Shaffer. "A New Genus of Geoemydid Turtle from Asia (Testudines)." Hamadryad 25, no. 2 (2000): 86–90.

Yasukawa, Yuichirou, Ren Hirayama, and Tsutomu Hikida. "Phylogenetic Relationships of Geoemydine Turtles (Reptilia: Bataguridae)." Current Herpetology 20, no. 2 (2001): 105–133.

John B. Iverson, PhD