Asiatic salamanders

(Hynobiidae)

Class Amphibia

Order Caudata

Suborder Cryptobranchoidea

Family Hynobiidae

Thumbnail description
Medium-size to small salamanders, usually dark brown to olive in color

Size
Body length 4–10 in (100–250 mm)

Number of genera, species
8 genera; 43 species

Habitat
Marshes, mountain streams, and ponds

Conservation status
Endangered: 5 species; Vulnerable: 4 species; Data Deficient: 1 species

Distribution
Central and eastern Asia

Evolution and systematics

In 1995 the first fossil record of hynobiid, which resembles the extant species Ranodon sibiricus, was discovered from the Upper Pliocene in Kazakhstan. Later, two other fossil species were described from late Miocene and Lower Pleistocene deposits in Europe. The oldest fossil hynobiid is perhaps Liaoxitriton zhongjiani, which was discovered from the early Cretaceous of western Liaoning, China. In morphological features, it most closely resembles hynobiids of the genus Batrachuperus. It may represent an extinct branch of extant hynobiid salamanders or an early branch of ancestral hynobiids.

The current understanding about the origin of hynobiids is based on comparisons among extant salamander groups using a phylogenetic approach. Recent morphological and molecular studies have suggested that hynobiid salamanders are related most closely to the family Cryptobranchidae, which includes the hellbender (Cryptobranchus alleganiensis) and the Chinese giant salamander (Andrias davidianus). They may share a recent common ancestor and may represent one of the oldest salamander lineages. Together with the family Sirenidae, the three families usually are considered the most "primitive" salamanders.

At present, there are eight recognized genera. Most genera are well established, but the validity of Pseudohynobius and Liua is still in dispute. In addition, the genus Batrachuperus may not be a natural group. It may consist of two distantly related groups. About half of the described species belong to the genus Hynobius, most of which occur only in Japan. The Japanese species are the best studied of the hynobiids. Several other genera may be as diverse as Hynobius. The small numbers of described species in these genera may be attributed more to lack of knowledge than to lack of diversity.

The species Protohynobius puxiongensis is morphologically very different and has been placed into its own subfamily. All other hynobiids are placed into another subfamily and sorted into two groups based on morphological characters. One group includes Hynobius and Salamandrella, and the other includes Onychodactylus, Ranodon, Pseudohynobius, Batrachuperus, and Liua. The former genera share several characters, such as large number of eggs and a one-year duration of larval development. The latter group has a much smaller number of eggs and two to three years of larval development. The genus Onychodactylus once was considered an "advanced" group, because it possesses several unique characteristics: lack of lungs, a round and slender tail, a short egg sac, and distinctive male secondary sexual characters. Data from molecular studies, however, have shown a different pattern, in which Onychodactylus may represent the oldest lineage of hynobiids, instead of an "advanced" group. Two subfamilies are recognized.

Subfamily Hynobiinae

This subfamily lacks an internasal bone and includes all the other hynobiids. Their distribution covers a large area of central and eastern Asia. At present there are about 42 species, which are grouped into seven genera.

Subfamily Protohynobiinae

This subfamily is characterized by the presence of an internasal bone. Currently, only one species (Protohynobius puxiongensis) is assigned to the Protohynobiinae. Its distribution is limited to western China.

Physical characteristics

Hynobiids are small to medium-size salamanders. The body length typically is between 4 and 10 in (100 and 250 mm), although some species may grow as long as 11.8 in (300 mm). Metamorphosis is complete in all species, and adults have eyelids and lack larval teeth and gill slits. Larvae have four pairs of gill slits. The coloration of most species is dull and varies from sandy brown to dark olive, although a few species, such as Pseudohynobius flavomaculatus, have colorful spots on their backs.

Some mountain stream dwellers have keratinized structures on their appendages. Onychodactylus species have claw-like structures on the fingers and toes; Liua shihi and a few Batrachuperus species have horny covers on their hands and feet. Such structures presumably aid in the grasp of the substrate by increasing friction. Other morphological variations include reduced lungs in Ranodon, Liua, and Batrachuperus and

a complete lack of lungs in Onychodactylus. Such reduction of the lung may be associated with the aquatic lifestyle. All Batrachuperus, Salamandrella keyserlingii, and some Hynobius have four instead of five toes. The arrangement of vomerine teeth, which are located on the roof of the mouth cavity, is an important character for identifying genera and species. Overall, the external appearance is similar and rather uniform in hynobiid salamanders.

Distribution

Hynobiids are exclusively Asian. They range from Japan, Taiwan, and the mainland of China westward to Afghanistan, Iran, and Kazakhstan in central Asia. To the north, the salamanders occur from the Kamchatka peninsula, the island of Sakhalin, Siberia, and Mongolia westward to the west of the Ural Mountains. The Siberian salamander (Salamandrella keyserlingii) is the only member of the family that ranges into European Russia and is the only salamander found north of the Arctic Circle. Some hynobiids, such as Hynobius nebulosus, are lowland species, whereas others, such as species of Batrachuperus, are strictly montane. The latter are particularly common at elevations of 6,500–13,000 ft (2,000–4,000 m). The highest record is for B. tibetanus, which occurs at an elevation of 13,940 ft (4,250 m) in western China.

Habitat

Species of the genera Batrachuperus and Liua are aquatic year-round. They occur primarily in mountain streams with cool, often fast-flowing water. During daylight hours, they frequently are found under rocks in the water. Occasionally, they are under large rocks on shore but are never far from water. Adults of other hynobiid species are terrestrial, but in the breeding season (February to June) they migrate to and congregate at breeding sites, either mountain streams with running water or ponds. Most species breed in only one of the types of water. For example, Hynobius leechii breeds exclusively in ponds. Nevertheless, other species, such as Hynobius chinensis, breed in both ponds and streams. Little is known about the activities of most of the terrestrial species out of the breeding season. They have been found under rocks or grasses or in burrows, and Pseudohynobius flavomaculatus and some species of Hynobius have been dug out of soil.

Behavior

Little is known about the behavior of this group aside from feeding and reproductive behavior.

Feeding ecology and diet

Hynobiids actively forage at night. They are carnivorous, and both larvae and adults feed on various insects and on aquatic and terrestrial invertebrates. Some species (Hynobius retardatus and Batrachuperus londongensis) practice cannibalism. Batrachuperus mustersi has the most bizarre diet of all hynobiids. This species is a cave dweller and often shares caves with bats; baby bats have been found in the stomachs of these salamanders. Apparently, the baby bats fall into the water, where they are eaten.

Reproductive biology

Fertilization in hynobiids is external. Males of most hynobiids release sperm into the water while the females are depositing eggs. The only exception is Ranodon sibiricus; the males of this species produce a spermatophore-like structure, but the eggs are fertilized externally. Eggs are deposited in two groups, representing the eggs from each oviduct, respectively; each group is contained in a gelatinous sac. The egg sacs generally are attached to rocks or vegetation in ponds, streams, or marshes. Egg sacs that fail to attach to an object are often not fertilized. The number of eggs in each sac varies within as well as across species, ranging from three in Onychodactylus japonicus to 105 in Salamandrella keyserlingii.

In most species, males actively participate in the spawning process. The female chooses an object, which she grasps firmly and to which the egg sacs adhere. After she releases part of the egg sac, she lets go of the object and floats backward. The males, waiting nearby, immediately move onto the egg sac. The males often push and kick the female with their limbs and press the egg sacs with the cloacal area to fertilize the eggs. The male's activity may help and accelerate the egg-deposition process.

Most eggs hatch in three to five weeks, although their development is temperature-dependent. Larvae of some species, such as most Hynobius, hatch at an early developmental stage and have balancers, which are temporary appendages and provide stability for the larvae. Larvae of most stream breeders, such as Batrachuperus, hatch at a more advanced stage and do not have balancers. The duration of the larval stage varies from one to three years. Water temperature plays an important role in determining duration.

The breeding season varies from late winter to early summer. Most Hynobius breed in late winter and early spring. The eggs develop in ice-cold water mixed with ice and snow. On the other hand, Batrachuperus breed in early summer. The breeding season may be as late as July for some western Chinese species. Little is known about parental care in hynobiid salamanders. It is known that males of Hynobius nebulosus guard and vigorously defend the egg sacs.

Conservation status

Hynobiid salamanders are highly endemic. Many are restricted to one island or mountain, and most have limited distributions. Local range reduction and fragmentation are well documented in Japan and China. For example, Hynobius chinensis of eastern China has disappeared from many sites. The primary threat to their survival is probably their limited distributions and small population sizes. Human habitat destruction poses another problem. Five species are listed as Endangered: Batrachuperus mustersi, Hynobius abei, Hynobius okiensis, Hynobius takedai and Ranodon sibiricus. In addition, four species are listed as Vulnerable: Batrachuperus gorganensis, Batrachuperus persicus, Hynobius hidamontanus, and Hynobius dunni. One species, Hynobius stejnegeri, is listed as Data Deficient.

Significance to humans

None known.

Species accounts

List of Species

Tibetan stream salamander

Batrachuperus tibetanus

subfamily

Hynobiinae

taxonomy

Batrachuperus tibetanus Schmidt, 1925, Lintao, China.

other common names

None known.

physical characteristics

The body length is 6.7–8.3 in (170–211 mm), and the coloring is dark brown to olive. In some individuals, there are pale spots on the back. The tail is compressed laterally, which is perhaps an adaptation to an aquatic lifestyle. Like other Batrachuperus and differing from most other salamanders, the species has four instead of five toes.

distribution

This species occurs only in western China along the northeastern corner of the Tibetan plateau.

habitat

This salamander is aquatic throughout the year. Preferred habitats include small mountain streams and creeks at elevations of 4,900–14,000 ft (1,500–4,250 m), but mostly the salamanders live at or above 9,800 ft (3,000 m). Typical creeks are 3.3–6.6 ft (1–2 m) wide and 6–12 in (15–30 cm) deep. During the day the salamanders hide under rocks or logs in moving water. Occasionally, they are under large rocks on mountain slopes near water.

behavior

Little is known aside from feeding and reproductive behavior.

feeding ecology and diet

The salamanders actively forage in shallow water at night. Occasionally they also forage on land. The diet includes small

crustaceans (70–90% amphipods) as well as aquatic and terrestrial insects.

reproductive biology

Breeding occurs once annually. The breeding season lasts from April to June in most areas. Paired egg sacs are attached to the undersides of rocks or logs. Each egg sac typically contains 10–15 eggs. The embryos develop in moving water. The duration of larval development is two to three years.

conservation status

Not threatened.

significance to humans

None known.

Japanese marbled salamander

Hynobius naevius

subfamily

Hynobiinae

taxonomy

Salamandra naevia Temminck and Schlegel, 1838, Honshu and Shikoku islands, Japan.

other common names

None known.

physical characteristics

The body length is 2.7–5.6 in (69–142 mm). This species has relatively short and robust limbs and tail and 14 grooves between

the forelimbs and hindlimbs on each side of the trunk. The color is dark blue with pale blue spots.

distribution

This species occurs on three Japanese islands: Honshu, Shikoku, and Kyushu.

habitat

This species is a mountain forest dweller and is particularly common at elevations of 1,600–3,200 ft (500–1,000 m). Adults are terrestrial during the nonbreeding season. They are commonly found under logs, rocks, and leaf litter near streams on mountain slopes. Eggs are deposited in mountain streams with moving water.

behavior

Nothing is known about the behavior of this species.

feeding ecology and diet

Larvae feed primarily on larvae forms of aquatic insects. Adults feed on both aquatic and terrestrial insects and other small invertebrates.

reproductive biology

The breeding season generally starts in late March and lasts until early April. Each egg sac contains 12–18 eggs. Eggs hatch within four to five weeks, and larvae complete metamorphosis in the fall.

conservation status

Not listed by the IUCN.

significance to humans

None known.

Hokkaido salamander

Hynobius retardatus

subfamily

Hynobiinae

taxonomy

Hynobius retardatus Dunn, 1923, Hokkaido Island, Japan.

other common names

None known.

physical characteristics

The body length is 4.3–7.3 in (110–185 mm). There are 11 or 12 costal grooves and a relatively long tail. The limbs and toes are long compared with other species of Hynobius. The dorsum is dark brown with a few indistinct spots. This species has a low diploid chromosome number of 40, compared with 56–78 in other hynobiids. Neotenic form, in which some individuals maintain the larval morphology and grow to adult size, is present in this species.

distribution

This species occurs on Hokkaido, the northernmost of the main Japanese islands.

habitat

The preferred breeding sites are slow-moving streams or ponds below elevations of 6,500 ft (2,000 m). During nonbreeding periods, the salamanders are terrestrial and are commonly found under grasses, rocks, and leaf litter on the forest floor. Differing from other Hynobius species, individuals of this species frequently visit bodies of water during the nonbreeding season.

behavior

Little is known aside from feeding and reproductive behavior.

feeding ecology and diet

Larvae feed on small aquatic invertebrates. Adults feed mainly on insects, crustaceans, some aquatic worms, and, occasionally, fish. Cannibalism is common among larvae in high-density populations. A wide head presumably is an adaptation against cannibalism; larvae with narrower heads are more vulnerable to cannibalism. The larvae have kin recognition ability; they preferentially consume nonkin and avoid siblings.

reproductive biology

Breeding starts when the snow begins to melt and the water temperature is typically 37–41°F (3–5°C). In most areas, the breeding season is in April, but at higher elevations, it may be delayed until early June. Both males and females migrate to and congregate at the breeding sites. Mating and egg deposition take place at night. Paired egg sacs are attached to twigs and grass. Each egg sac usually contains 30–50 eggs, but there may be as many as 93 eggs. Larvae typically complete metamorphosis in the same year, but low water temperature sometimes delays metamorphosis until the next year or even the third year.

conservation status

Not listed by the IUCN.

significance to humans

None known.

Japanese clawed salamander

Onychodactylus japonicus

subfamily

Hynobiinae

taxonomy

Salamandra japonica Houttuyn, 1782, Honshu Island, Japan.

other common names

English: Japanese lungless salamander.

physical characteristics

The body length is 4.2–7.2 in (106–184 mm). The body is slender, and the tail is relatively long. The dorsum is brown with orange spots on the back of the head and the limbs, and there are longitudinal orange mid-dorsal stripes. The larvae have clawlike structures on the fingers and toes. Adults have the "claws" only during the breeding season. Lungs are absent.

distribution

This species occurs on two Japanese islands, Honshu and Shikoku.

habitat

Usually this species occurs at elevations of more than 3,200 ft (1,000 m). During the nonbreeding season, they are terrestrial but are very close to water. Their favorite places are beneath wet rocks or logs beside a stream. They also are found frequently under logs on the forest floor, in tree holes, and in other places with high humidity.

behavior

Little is known aside from feeding and reproductive behavior.

feeding ecology and diet

Adults feed primarily on insects and their larvae. Other invertebrates, such as spiders, millipedes, snails, tadpoles, and larval fish, also are part of their diet.

reproductive biology

Males are biennial breeders, and females probably are triennial breeders. The breeding season is in May; in some areas it extends into June. The females deposit eggs at night, generally in the headwaters of mountain streams. Each egg sac typically contains three to eight eggs; the total number of eggs produced per female is seven to 15. Larvae take three years to reach metamorphosis.

conservation status

Not listed by IUCN.

significance to humans

None known.

Semirechensk salamander

Ranodon sibiricus

subfamily

Hynobiinae

taxonomy

Ranodon sibiricus Kessler, 1866, Kazakhstan.

other common names

English: Alatau salamander.

physical characteristics

The body length is 5.9–9.8 in (150–250 mm). The tail is as long as the rest of the body and has a dorsal crest. The body is brown, with scattered black spots. The adults have small lungs.

distribution

This species is limited to the Ala Tau mountains and the adjacent Tien Shan mountains of eastern Kazakhstan and western China.

habitat

This species lives in mountain streams and marshes at elevations of 4,920–9,000 ft (1,500–2,750 m).

behavior

Little is known aside from feeding and reproductive behavior.

feeding ecology and diet

This species forages nocturnally. Larvae begin feeding at four to eight days after hatching. Larvae mainly feed on aquatic invertebrate larvae, such as those of ostracods and trichopterans. Feeding continues during metamorphosis. The diet of newly metamorphosed individuals is exclusively aquatic invertebrates, but mature salamanders feed on both aquatic and terrestrial invertebrates.

reproductive biology

The breeding season is from May to July. The duration of larval development is two to three years. Ranodon sibiricus is the only hynobiid salamander that produces spermatophore-like structures that bear sperm. Males attach the spermatophore to the undersides of rocks and plants. Instead of picking up the spermatophore, the females attach their egg sacs to the same objects, and the eggs are fertilized externally. In such cases, it is the male that chooses the spawning site, not the female.

conservation status

The IUCN lists this species as Endangered. It is currently under protection in both Russia and China. Restricted distribution and habitat destruction are the main threats to the survival of the species. The species is doing well in captivity, and some reintroduction programs are in place.

significance to humans

None known.

Siberian salamander

Salamandrella keyserlingii

subfamily

Hynobiinae

taxonomy

Salamandrella keyserlingii Dybowski, 1870, vicinity of Lake Baikal, Russia.

other common names

German: Sibirischer Winkelzahnmolch.

physical characteristics

The body length is 3.9–5.0 in (100–127 mm). Costal grooves, usually 13 in number, are distinctive. The tail is much shorter than the body. A mid-dorsal brown stripe extends the length of the body. This probably is a complex of species.

distribution

This species has the widest distribution of all hynobiid salamanders. Its range includes northern Japan, Korea, northeastern China, Mongolia, and Siberia (including Sakhalin and the Kamchatka Peninsula), and it extends westward to European Russia; it is the only species of salamander that occurs north of the Arctic Circle.

habitat

The Siberian salamander is a terrestrial species. During the nonbreeding season marshes are their preferred habitat; they are found in these marshes under grasses and sometimes in burrows. The females usually deposit eggs in large, shallow ponds.

behavior

Little is known aside from feeding and reproductive behavior.

feeding ecology and diet

Siberian salamanders are nocturnal foragers, especially after rains. The diet consists mainly of insects, small snails, earthworms, and, occasionally, small fish.

reproductive biology

Each egg sac contains 28–105 eggs; the total number of eggs deposited by one female is 59–189. The breeding season in most areas begins in early April. Females first grasp a twig or grass with their four limbs and then deposit the egg sacs. One end of the egg sac is attached to a twig or grass. When the egg sacs are released halfway, the female lets go of the twig and floats backward. At this time, several males usually join in. The males and females often grab each other and form a "ball." The males do not simply fertilize the eggs; their activity often also helps the female deposit the egg sacs. Larvae complete metamorphosis in one year.

conservation status

Not listed by the IUCN, but listed as near threatened in Japan by the National Strategy of Japan on Biological Diversity.

significance to humans

None known.

Resources

Books

Duellman, William E., and Linda Trueb. Biology of Amphibians. Baltimore: Johns Hopkins University Press, 1994.

Pough, F. Henry, Robin M. Andrews, John E. Cadle, Mart L. Crump, Alan H. Savitzky, and Kentwood D. Wells. Herpetology. 2nd ed. Upper Saddle River, NJ: Prentice Hall, 2001.

Weisrock, D. W., J. R. Macey, A. Larson, and T. J. Papenfuss. "Phylogenetic Relationships Among Hynobiid Salamanders: Evidence for an Old North Asian Fauna and Clock-like Evolution in the Mitochondrial Genome." In Abstracts of the Joint Meeting of the ASIH/AE/HL/SSAR. State College, PA: Penn State University, 1999.

Zhao, Ermi, Qixiong Hu, Yaoming Jing, and Yuhua Yang. Studies on Chinese Salamanders. Oxford, OH: Society for the Study of Amphibians and Reptiles, 1988.

Periodicals

Averianov, A. O., and L. A. Tjutkova. "Ranodon cf. sibiricus (Amphibia, Caudata) from the Upper Pliocene of Southern Kazakhstan: The First Fossil Record of the Family Hynobiidae." Palaeontologische Zeitschrift 69 (1995): 257–264.

Dong, Z., and Y. Wang. "A New Urodele (Liaoxitriton zhongjiani gen. et. sp. nov.) from the Early Cretaceous of Western Liaoning Province, China." Vertebrata PalAsiatica 36 (1998): 159–172.

Hasumi, M., and F. Kanda. "Breeding Habitats of the Siberian Salamander (Salamandrella keyserlingii) Within a Fen in Kushiro Marsh, Japan." Herpetological Review 29 (1998): 150–153.

Venczel, M. "Land Salamanders of the Family Hynobiidae from the Neocene and Quaternary of Europe." Amphibia-Reptilia 20 (1990): 401–412.

Wakahara, M. "Kin Recognition Among Intact and Blinded, Mixed-Sibling Larvae of a Cannibalistic Salamander Hynobius retardatus." Zoological Science (Tokyo) 14, no. 6 (1997): 893–899.

Jinzhong Fu, PhD