A new species of salamander, Hynobius yangi, is described from Kori (=Hyoam-ri), Busanshi, southeastern Korea. It is a lentic breeder belonging to the H. nebulosus species group, and has long been confused with another Korean species H. leechii. The new species, however, is genetically substantially differentiated from Korean and Japanese relatives. Hynobius yangi is morphologically very similar to H. leechii, but could be differentiated from it by the tail shape, degree of limb separation, shape of vomerine teeth series, shape of egg sac, and dorsal coloration.
INTRODUCTION
In the recent decade, presence of several unique populations among a Korean salamander Hynobius leechiiBoulenger, 1887 has been repeatedly reported in South Korea (Lee and Jung, 1993; Cha and Lee, 1995; Yang et al., 1997, 2000; Lee et al., 1998) and distinct specific status of two forms from the nominal species has been suggested (Yang et al., 1997). One of which from Jeju (=Cheju) Island and peripheral islands has already an available name, H. quelpaertensis (Mori, 1928), but another from Kori (= Hyoam-ri and Gilcheon-ri), Busan-shi, has never been formally evaluated taxonomically.
Our morphological survey including the population from Kori and many populations of south Korean H. leechii and H. quelpaertensis, as well as two Japanese relatives, H. nebulosus from Nagasaki and H. tsuensis from Tsushima, proved the former assumption that the salamander from Kori could be constantly distinguished from other species by the combination of several morphological characteristics. In this short article, we describe the salamander from Kori, South Korea as a new species on the basis of the results of morphological analysis and hitherto accumulated information.
SYSTEMATICS
Hynobius yangi sp. nov.
[Korean name : Kori-dorongnyong]
[Japanese name : Kori-sansyouo]
Fig. 1
Dorsal (A) and ventral (B) views of holotype of Hynobius yangi sp. nov. (KUHE 29842). Scale=1 mm.
Hynobius leechii (part): Dunn, 1923. p. 456.
Hynobius leechii (part): Sato, 1943. p. 33.
Hynobius leechii (part): Cha and Lee, 1995. p. 89.
Hynobius leechii Form-C: Yang et al., 1997. p. 253, Fig. 3C.
Fig. 3
Open mouths of Hynobius species showing variations in shape of vomerine teeth series. A: H. yangi sp. nov.; B: H. leechii; C: H. quelpaertensis from Jeju Isl.; D: H. tsuensis. Scales=1mm.
Hynobius leechii (part): Lee et al., 1998. p. 155.
Hynobius sp.: Yang et al., 2000, p. 44.
Holotype:
KUHE (Graduate School of Human and Environmental Studies, Kyoto University) 29842, an adult male from Hyoam-ri, Jangan-eup, Gijang-gun, Busan-shi (129°17′E, 35°19′N, alt. 45m), collected by Jong-Bum Kim on 26 February 2002.
Paratypes:
KUHE 29843-29849 and 29851-29865, 17 males and 3 females, with the same data as the holotype.
Diagnosis:
A member of the lentic breeder of the Hynobius nebulosus group of Sato (1943): living on hilly regions and breeding in still waters in ditches; most similar to some populations of H. leechii in appearance, but is distinguished from it by longer and higher tail relative to snout-vent length (SVL), greater separation of adpressed limbs, slightly deeper vomerine teeth series (Fig. 3A, B), egg sac of coil shape (Fig. 4), light brownish dorsum, and distinct genetic differences. It has smaller SVL, relatively longer head, higher tail, and shorter trunk, and more costal grooves than H. quelpaertensis from Jeju. From H. quelpaertensis from peripheral islands, H. yangi can be differentiated by relatively longer and higher tail and wider head, and by having more costal grooves and narrower separation of limbs. It differs from H. tsuensis by smaller SVL, higher tail, much shallower vomerine teeth series (Fig. 3A, D), and usually unspotted dorsum. From H. nebulosus, H. yangi can be differentiated by smaller SVL, longer tail and wider head relative to SVL, less costal grooves, smaller separation of limbs, much shallower vomerine teeth series, and lack of yellowish light stripes on top and base of the tail.
Description and variation:
The following description is based on the maximum number of 18 adult males and 3 adult females. Morphometric data are summarized in Table 1 together with those of the allied species, H. leechii, H. quelpaertensis, H. tsuensis, and H. nebulosus. Head longer than broad. Males with relatively larger head in length (HL) than in females, when each dimension is converted to percentage ratio to SVL (Mann-Whitney U test, U18,3=3, p<0.05; Table 1). Females with relatively longer trunk than males (U18,3=3, p<0.05). Number of costal grooves including axillary groove 12 to 14, the modal number being 14 in both sexes (Table 2). Limbs short, and when adpressed, they mainly do not overlap. Separation is greater in females (median=2.5 folds) than in males (median=0 fold; U18,3=2, p<0.01, Table 3). Statistically significant sexual dimorphism in tail shape: males with relatively longer (U18,3=0, p<0.01) and higher (U18,3=0, p<0.01) tail than in females. Fifth toe usually present but rudimentary in some specimens. Vomerine teeth in two small, obliquely arched series, nearly touching at midline, and forming shallow “V” shape. Combined series distinctly wider than long (VTW/VTL 1.24–1.89 in males and 1.30–1.52 in females). Shape of vomerine teeth series are not sexually different as shown by comparison of the ratio of VTW to VTL (U16,3=9, p>0.05, Table 4).
Table 1
Comparisons of SVL measurements (means±SD, followed by ranges in parenthesis, in mm) and percentage ratios of each character dimension to SVL (medians, followed by ranges in parenthesis) in Hynobius yangi sp. nov., H. leechii, H. quelpaertensis, H. tsuensis, and H. nebulosus.
Table 2
Variation in the number of costal grooves, including the axillary groove, in Hynobius yangi sp. nov., H. leechii, H. quelpaertensis, H. tsuensis and H. nebulosus.
Table 3
Variation in the number of costal folds between adpressed limbs in Hynobius yangi sp. nov., H. leechii, H. quelpaertensis, H. tsuensis, and H. nebulosus.
Table 4
Comparisons of width-length ratio of vomerine teech series (median) in Hynobius yangi sp. nov., H. leechii, H. quelpaertensis, H. tsuensis, and H. nebulosus. Figures in parenthesis indicate variation range.
Color in life:
Dorsum olive without dark speckles (Fig. 2), but some specimens have dark brownish dorsum dotted very finely with yellow speckles. These speckles tend to fuse on sides of the tail. Underside of body lighter than dorsum.
Measurements and counts of the holotype:
An adult male with the following measurements (mm; in preservative): Head width (HW) 10.9, snout to gular fold (HL) 11.8, head depth at posterior angle of jaw 4.2, eyelid length 3.0, anterior rim of orbit to snout 4.2, horizontal orbit diameter 2.1, interorbital distance 3.3, snout to insertion of forelimb 17.4, distance separating internal nares 3.1, distance separating external nares 3.1, snout to anterior angle of vent (SVL) 49.1, axilla to groin 23.4, anterior angle of vent to tip of tail (tail length, TAL) 38.8, tail width at base 5.7, tail height at base 5.6, tail height at middle 5.9, maximum tail height (MTAH) 5.8, axilla to tip of out-streched forelimb 13.9, groin to tip of out-streched hindlimb 15.3, width of vomerine teeth series (VTW) 2.79, length of vomerine teeth series (VTL) 1.77. The holotype has 54 upper jaw teeth, 31 vomerine teeth, 13 costal grooves between axilla and groin, 1.5 costal folds between adpressed limbs, and 5 digits on both hind-limbs.
Etymology:
The specific name “yangi” is a patronymic noun in the genitive singular, honoring Dr. Suh-Yung Yang. He contributed much to the study of South Korean animals. Range: Known so far from the type locality Hyoam-ri and nearby Gilcheon-ri, both in Jangan-eup (=Changan-eub), Gijang-gun (=former Yangsan-gun), Busan-shi (formerly included in Kyungsangnam-do), southeastern South Korea (Fig. 5).
Morphological comparisons:
Limited number of available female specimens prohibited detailed interspecific comparisons and only male specimens were compared. In SVL, H. yangi was significantly smaller than H. quelpaertensis from Jeju, H. tsuensis, and H. nebulosus (Tukey test, p<0.05; Table 1).
By comparing percentage ratios of each character dimension to SVL, the following significant differences (U-test, p<0.05) in body shape were detected. Hynobius yangi was greater in relative TAL (U18,82=430, p<0.01) and relative MTAH (U18,8=204.5, p<0.01) than H. leechii. It had greater values in relative HL (U18,34=202, p<0.05) and relative MTAH (U18,34=121, p<0.01), but had smaller value in relative TRL (U18,34=202, p<0.05) than H. quelpaertensis from Jeju. Compared with H. quelpaertensis from peripheral islands, H. yangi had greater values in relative TAL (U18,36=212.5, p<0.05), relative MTAH (U18,34=105, p<0.01), and relative HW (U18,41=108.5, p<0.01). Hynobius yangi was greater in relative MTAH than H. tsuensis (U18,6=15, p<0.05), and greater in relative TAL (U18,19=5, p<0.05) and relative HL (U18,31=109, p<0.01) than H. nebulosus (Table 1).
In males, H. yangi had limbs more separated than in H. leechii (U18,99=538, p<0.01), but less so than in H. quelpaertensis from peripheral islands (U18,41=247.5, p<0.05) and H. nebulosus (U18,31=72.5, p<0.01) (Table 3).
Hynobius yangi had vomerine teeth series (as expressed by the ratio of width and length) slightly deeper than H. leechii (U15,57=209, p<0.01), but much shallower than H. tsuensis (U15,5=1, p<0.05) and H. nebulosus (U15,31=2, p<0.01) (Table 4).
Hynobius yangi had costal grooves more than H. quelpaertensis from Jeju (U18,34=134, p<0.01) and peripheral islands (U18,39=199.5, p<0.01) and H. nebulosus (U18,31=159.5, p<0.01) (Table 2, Fig. 3A, D).
Biochemical characteristics:
Hynobius yangi differs from H. leechii completely at Ldh-1 allele and nearly completely at Ldh-2, Gp-2, and Xdh-2 alleles. From H. quelpaertensis, it differs completely at Ldh-1 and Ldh-2 alleles and nearly completely at Aat-2 and Xdh-2 alleles (Yang et al., 1997). In partial sequence of cytochrome b gene (246 bp), H. yangi (as H. leechii from Yangsan) is reported to have mean Kimura's two-parameter distance (Kimura, 1980) of 7.8% from H. leechii and 10.9% from H. quelpaertensis (Lee et al., 1998).
Karyotype:
2N=56 with Ag-NORs constantly at 23rd chromosome, in contrast to great intrapopulation variations in H. leechii (Cha and Lee, 1995).
Fecundity and natural history:
The clutch size of one female was 86. The mean diameter of ten ova just oviposited by one female ranged from 2.70–2.84 (mean±SD= 2.78±0.05) mm. The animal pole is dark brown and vegetal pole is grayish brown in color. Breeding occurs from late February to late March. Egg sacs of coil shape (Fig. 4) lack striations on the surface and are attached to water plants or fallen branches in the still-water.
DISCUSSION
As a by-product of genetic divergence during speciation process, most animal species acquire morphological differences that are suitable for diagnostic purpose, but cryptic species fail to acquire such differences (Mayr and Ashlock, 1991). Korean salamanders of the H. leechii complex (=H. leechii, H. quelpaertensis, and H. yangi) seems to correspond to such a case.
From results of studies using different methods, some Korean authors have already reported that South Korean H. leechii actually includes three putative cryptic species that are morphologically very difficult to distinguish (Yang et al., 1997, 2000; Lee et al., 1998). Of these three species, H. leechii was originally described from Wonsan (Gensan), north Korea (Boulenger, 1877) and actual taxonomic assignment of South Korean populations remains undone because of current political problems. The second species, now called H. quelpaertensis, was originally described from Jeju Island as a subspecies of H. leechii by Mori (1928), but has long been synonymized with the nominotypical subspecies (e.g., Sato, 1943). Close affinities of the populations from islands peripheral to the Korean Peninsula to H. quelpaertensis (see Yang et al., 2000) has been clarified by biochemical studies (Lee and Jung, 1993; Yang et al., 1997). The third putative species represented by the population from Kori (Yang et al., 1997=Yangsan in Lee et al., 1998) had no name until present study.
Among lines of evidence proposed, these species are especially clearly split by several diagnostic allelic differences, and the population from Kori (now H. yangi) is split from H. leechii and H. quelpaertensis with Nei (1972) D of 0.25 and 0.30, respectively (Yang et al., 1997). The minimum genetic distance reported for seven closely related species of lentic-breeding Hynobius is 0.22 (Matsui, 1987), and compared with interspecific genetic differentiations in these Japanese members, genetic divergences among three forms of the Korean H. leechii complex seem to be substantially large to regard each of them as heterospecific.
Also, an analysis of mitochondrial cytochrome b gene partial sequence divergence of the Korean H. leechii complex revealed that H. yangi was separated from H. leechii and H. quelpaertensis at the level ordinary found between different species (Kimura's two-parameter distance >7.8%; Lee et al., 1998). Further, the three putative species differ significantly in some skeletal characters. The population from Kori has been reported to be different from H. leechii and H. quelpaertensis in the numbers of vomerine teeth and coccyx (Yang et al., 1997). In the present comparisons of external morphology of salamanders from Korea and Japan proved that H. yangi could be constantly separated from the other species by the combination of several characters. Thus, distinct specific position of H. yangi is now undoubtful.
Hynobius yangi is isolated in the Milyang sub-basin of the Kyeongsang basin in southeastern Korea, and is split in the north from a population of H. leechii by the Taehwa river and in the south from an islet population of H. quelpaertensis by a small strait (Fig. 5). River basin is regarded as one of intra-continental barriers that might have played an important role in amphibian speciation processes (e.g., Arntzen and Garcia-Paris, 1995; Garcia-Paris et al., 1998), and the Taehwa river in the Milyang sub-basin might have been an important barrier for genetic interchange between H. yangi and H. leechii that inhabit hilly or montane regions. Although distributional and divergence patterns similar to H. yangi and H. leechii have never been reported, future studies of various lower vertebrates in this area might contribute to the understanding of their speciation processes within South Korea.
Acknowledgments
We thank Dr. S.-Y. Yang for his continuous counseling and warm friendship. We thank Prof. H.-Y. Lee, Dr. J.-H. Suh, Mr. S.-H. Cha, and Mr. H.-Y. Suk for help in collecting specimens. This study was supported by the JSPS Postdoctoral Fellowship of Japanese Research Foundation in 2001 (to J.-B. Kim) and by Korean Ministry of Education through Research Fund (BSRI-95-4423, to S.-Y. Yang).
