Salamandrella keyserlingii Dybowski, 1870
There are no major threats to this species, which is listed as of least concern by IUCN (2010). Salamandrella keyserlingii is a widespread and common species in northeastern China and Russia. It is also distributed in the northern Hokkaido island of Japan, Mongolia, and northern Korea. In Kazakhstan it is a rare species deserving conservation.
Brown salamander with flattened tail; usually 13 to 15 costal grooves; four toes; a light dorsal band and darker sides (Dunn, 1923). Labial fold absent. A large longitudinal fontanelle present between frontals and parietals (Fei et al., 2006).
2n=62. The mitochondrial genome has been sequenced by Zhang et al. (2006).
It is hard to distinguish this species from Salamandrella tridactyla on the basis of external characters. Salamandrella keyserlingii may have more costal grooves than S. tridactyla (usually 13–15 vs. usually 11–12).
Moderately sized, inconspicuous brown salamander. 10 to 14, exceptionally 15 costal grooves. One fold between digits when limbs are laid against the body. Head oval; paratoid glands well developed; gular fold present. Skin smooth. Limbs well developed; four fingers and (usually) four toes. Tail sometimes longer, equal to or shorter than snout-vent length. Flattened laterally and a dorsal keel throughout, ventral keel in distal two-thirds. Vent formed by three slits converging with apex forwards, median longest. Vomerine teeth beginning behind inner edge of nares, in V-shaped series. Lungs present (Dunn, 1923; Borkin, 1999; Kuzmin & Maslova, 2003; Litvinchuk & Borkin, 2003). Males have relatively longer and higher tails, a larger cloaca (both in length and width), relatively longer forelegs than females. These differences are more pronounced during the reproductive period (Kuzmin, 1999). Color dull grayish brown, lighter below; a broad gold-colored band runs from snout to tip of tail. Inside this band, a thin dark stripe runs from neck to tail base. The golden band becomes dark and indistinct in males in the breeding season (Goris & Maeda, 2004). Total length 12 to 16 cm (Kuzmin, 1999).
Based on the mitogenomic phylogeny, Salamandrella is the sister clade to the group of Liua, Pseudohynobius and Batrachuperus (Peng et al., 2010).
Salamandrella keyserlingii has the widest distribution of all recent amphibian species. It is found in Russia, Kazakhstan, Mongolia, China, North Korea and Japan. Its range extends across the Ural Mountains, well into the European part of Russia; the eastern limit is formed by the Chukotski Mountains near the Bering Strait. The northern limits are the Chaunski Lowlands along the East Siberian Sea in Chukotski and the Kolyma River-Kolyuchinskaya tundra zone. The southern limits are northern Kazakhstan, the Altay and Tuva areas of southern Russia, the Hangayn Mountains in northern Mongolia, Inner Mongolia and Heilongjiang provinces in north-eastern China. The Changbai Mountains in northern North Korea may be home to S. tridactyla. Salamandrella keyserlingii further occurs on Sakhalin Island, and some of the Kuril Islands: Paramushir, Kunashir and Shikotan Islands, as well as in the Kushiro wetlands in Hokkaido, Japan (Kang et al., 1975; Sato, 1993; Borkin, 1999; Fei et al., 1999, 2006; Kuzmin & Maslova, 2003; Song, 2007).
The species is characterized by a high morphological uniformity without distinct geographical variation. Recent molecular work has resulted in the discovery of a cryptic species, now named Salamandrella tridactyla, occurring in the basin of Ussuri River in Primorye, including Lazovsky, Vladivostok and many other localities, southern Khabarovsk territory (Berman et al., 2005; Poyarkov & Kuzmin, 2008; Matsui et al., 2008), as well as in neighbouring Chinese provinces of Jilin and Heilongjiang (Poyarkov, unpubl. data) and North Korea.
The species occupies a wide range of different habitats, from tundra in the north to forest steppe in the south. It occurs in lowland habitats such as larch forests in river valleys, mixed forests, maritime tundras, grassy lands, swamps and wetlands. Reproduction takes place in a broad range of waters, from temporary, shallow puddles to permanent lakes. In tundra, reproduction occurs in small lakes and swamps, and in steppe and forest steppe only in large, permanent water bodies located in the flooded parts of river valleys. In taiga, the salamander uses a diverse range of water bodies, including large lakes, permanent and temporary ponds and puddles, and also man-made ditches. In northern and mountain populations, the species uses open, well-warmed ponds where the ice melts early in spring (Kuzmin, 1999).
In general, the species is most numerous in the taiga. It is abundant in the permafrost zone and in steppe because of its high thermal tolerance and its use of relatively uniform environments in river valleys (Kuzmin, 1999). Terrestrial adults eat invertebrates (Lumbricidae, Mollusca, Aranei, Coleoptera and larval Diptera), aquatic animals eat Gastropoda, Daphniidae, Coleoptera and larval Chironomidae. Larvae eat microcrustaceans, small molluscs and insects, in some streams in the Far East larvae eat mainly rheophilous crustaceans (Gammaridae) (Kuzmin, 1999).
Hibernation starts in September-October, in the north in August-early September. Animals hibernate in rotten (birch) trees, in holes, burrows and under logs, in places where fluctuations of temperature are relatively small. Even so, the salamanders tolerate low temperatures in hibernacula, even if they fall to minus 23° C for a few days. In most places hibernation ends in April - May, or in the north-eastern part of the range from end May to early June (Kuzmin, 1999). The Siberian Newt is unique in its freeze-tolerance. Adults are able to survive freezing to minus 35 to 40° C. Sometimes such frozen salamanders, found in the permafrost at a depth of 4 – 14 m can be revived after melting. The age of one such specimen excavated from a depth of 11 m was determined as 90 ± 15 years (Kuzmin, 1999).
The animals enter the water after hibernation, in mid April to May in the temperate zone or end May to mid June in Arctic and Subarctic zones. In the northern part of its range reproduction may take up to one month, in the main part of its range reproduction takes about a week and a half to two weeks. Group breeding is typical, the majority of females depositing their eggs within a few days, with dozens of clutches attached to the same substrate (Kuzmin, 1999).
In the first stage of breeding behavior the male moves near the surface of the water, grasping decaying grasses or branches with its legs and swinging its tail into the water to attract a female. While doing this, it looks out for an egg-bearing female swimming its way. In the second stage, when a female touches the male’s tail, the male attempts to wrap its tail around the female and bring it closer. In the third stage, if the female is ready to lay eggs, it makes no effort to avoid being wrapped up in the male’s tail. In the fourth stage, as the male loosens its grip on the female, the female climbs up decaying grasses or branches just below the water surface. When the female is ready to lay eggs, it arches its back, raises its tail, and presses its vent against decaying vegetation or some other surface. In the fifth stage, this gesture by the female attracts the attention of other males in the area, which rush towards the released egg sacs. In the sixth stage, the males scramble about the egg sacs in an effort to fertilize the eggs, and the female stops moving and sinks to the bottom. Males may actually pull the egg sacs out of the female’s body. Approximately 30 seconds elapse from the time the female touches the male’s tail to the time the female releases the egg sacs (Sato, 1993). One clutch may be fathered by several males (Fang et al., 1984).
The female produces a pair of egg sacs, connected to one another with a short mucous stalk, by which the clutch is attached to twigs and grasses. One sac of the clutch is spiraled clockwise, the other counter-clockwise. Non-spiraled, banana-form egg sacs found in the Primorye and Khabarovskii regions belong to a separate form, recently recognized as a species and now named Salamandrella tridactyla (Berman et al., 2005; Kuzmin & Maslova, 2003; Poyarkov & Kuzmin, 2008; Matsui et al., 2008).
The size of the egg sac varies with age, becoming larger in the course of embryonic development and reaching a length of 28 cm and a thickness of 32 mm. One clutch may contain 27-305 eggs, distributed asymmetrically over the two egg sacs. Highest numbers of eggs were observed in Manchuria, the lowest in the extreme North East and the Amur and Ussuri river areas (Borkin, 1999). The fertilized egg is gray-brown, a little brighter at the vegetal pole, measuring 1.87 to 2.38 mm in diameter (not including the capsules) (Borkin, 1999). The development of embryo and larva is described and depicted in detail in Sytina et al. (1987).
Depending on temperature the larvae hatch after two to four weeks, at 9-12 mm length, usually in May-June, in the extreme North East from June to early August (Sato, 1993). Color is dark with irregular light spots, growing darker with age. Two balancers present. Young larvae have a peculiar elongated fin between two fingers (Sytina et al., 1987). Larval development up to metamorphosis takes one and a half to three months, depending on the area. The development from egg laying to metamorphosis takes from 83 to 110 days. Length at metamorphosis also varies with location from 23 to 57 mm (Borkin, 1999).
After the breeding season, juveniles disperse on land and adults lead a terrestrial life. They live in burrows and under logs. Some surface activity near the breeding waters can be observed in September before the animals migrate to hibernation refugia (Hasumi & Kanda, 2007). Eggs, larvae and adult newts are preyed upon by a variety of animals. The main predators of eggs and larvae are aquatic insects; adults are mainly eaten by fish, snakes, birds and mammals (Kuzmin, 1999).