Onychodactylus fuscus, Yoshikawa, Natsuhiko & Matsui, Masafumi, 2014

Yoshikawa, Natsuhiko & Matsui, Masafumi, 2014, Two new Salamanders of the genus Onychodactylus from Eastern Honshu, Japan (Amphibia, Caudata, Hynobiidae), Zootaxa 3866 (1), pp. 53-78 : 68-74

Onychodactylus fuscus sp. nov.

(Japanese name: Tadami-hakone-sanshou-uwo) (English name: Tadami clawed salamander) ( Figs. 10 & 11 )

Etymology. The specific epithet “ fuscus ”, a Latin word meaning dark or black, is derived from unstriped, uniformly dark dorsal coloration of the new species, which is quite unique among species in the O. japonicus species complex. Suggested Japanese and English names are after Tadami-machi (Tadami Town), where the type locality is located.

Holotype. KUHE 48284, an adult male from environs of Mt. Yogai (139o18'E, 37o21'N, 430 m a.s.l.) in Tadami-machi, Fukushima Prefecture, Japan, collected by N. Yoshikawa and O. Inaba on 9 November 2013.

Paratypes. A total of 10 specimens: four males ( KUHE 48282–48283, 48285 and 20131109-1[stored at the Tadami Beech Center]) and one female ( KUHE 48129), collected on 9 November 2013 by N. Yoshikawa and O. Inaba) from the type locality; one female ( KUHE 48286 collected on 9 November 2013 by N. Yoshikawa and O. Inaba) from environs of Mt. Hiraishi, Tadami-machi, Fukushima Prefecture; one male and three females ( KUHE 44847 and KUHE 44848–44850, respectively, collected on 2 June 2011 by Y. Misawa) from Shionofuchi, Sanjoshi, Niigata Prefecture.

Referred specimens. See APPENDIX 1.

Diagnosis. The new species is a member of the genus Onychodactylus diagnosed by the characteristics listed for O. intermedius . It is further assigned to a member of the O. japonicus species complex by the genetic evidence, although this species completely lacks dorsal stripe which is a diagnostic characteristic of the complex. Dorsum uniformly dark-brown without stripe, sometimes with slight indistinct ochre small flecks; slightly large body size with mean SVL (±1SD) of 69.5±3.0 mm in males and 69.0± 4.8 mm in females; tail longer than SVL in males, but nearly equal in females; hindlimb comparatively short; head and internarial space comparatively wide; usually lacking wedge-shaped dark marking on chest; ventrum purplish brown or purplish gray, with silvery white dots; presacral vertebrae including atlas 18 or 19; costal grooves 12 or 13; right and left vomerine tooth series interrupted by gap, series tending to curve shallowly, with comparatively small number of teeth, 12–15 on one side of series.

Description of holotype. An adult male with SVL 69.0 mm ( Fig. 10 A–B); body moderately stout; skin smooth; head oval and depressed, longer than wide; neck slightly narrower than head; snout rounded, projecting beyond lower jaw; nostril close to eye; eye large, shorter than snout, prominently protruded; gular fold posteroventral to head; parotoid gland well developed, oval, ca. 1.6 times longer than wide, projecting more posteriorly than gular fold; postorbital groove obvious; vomerine teeth in two transverse, shallowly curved archshaped series with a gap in between ( Fig. 6 B); 15 teeth on right and 14 on left side of series; few dark pigments scattered around vomerine tooth series; forelimb thin; relative length of fingers I<IV<II<III; hindlimb slightly longer and distinctly more robust than forelimb; relative length of toes I<V<II<III=IV; adpressed limbs touching each other; secondary sexual characters obvious; dermal flap on posterior edge of hindlimb extremely developed; black horny claws on tips of fingers and toes; black tubercles and asperities on palm and sole; trunk elongated and cylindrical but slightly depressed; middorsal groove indistinct; well-developed 13 costal grooves on both sides of trunk; presacral vertebrae including atlas numbering 18; base of tail including cloacal region well swollen; cloaca longitudinal slit, length 11.3% SVL, with anterior two-fifth of its edge slightly swollen, forming inverse shallow Vshaped precloacal skin fold; precloacal skin fold as wide as length of cloaca; a series of small black spines lining along front edge of precloacal skin fold; tail long, 127.8% length of SVL, cylindrical at base, increasingly compressed posteriorly; tail slightly lowered toward tip, laterally compressed posterior two-thirds and extremely at tip, forming finny shape; tip of tail rounded in lateral view; tail highest (11.3% SVL) at base.

Measurements (in mm) of the holotype. SVL 69.0, HL 15.8, HW 10.1, TAL 88.2, AGD 34.7, FLL (L) 18.8, FLL (R) 18.7, HLL (L) 20.1, HLL (R) 20.0, UEL (L) 4.1, UEL (R) 4.2, IOD 3.4, END (L) 2.3, END (R) 2.2, ICD 6.1, IND 5.1, SL (L) 5.5, SL (R) 5.4, CW 9.8, BTAH 7.8, BTAW 8.2, MTAH 6.6, MTAW 4.4.

Color: In life, dorsum uniformly dark-brown with a few indistinct ochre flecks; dorsal stripe completely absent; lateral and ventral sides of body dark-brown with silvery white dots, but background color sometimes gradually fading toward grayish ventrum; iris mottled with dark-brown and gold in upper half, uniformly darkbrown in lower half. In alcohol, color and pattern fading generally, but no obvious change except for bleach of dorsal ochre flecks.

Variation. The following description of variation is based on the maximum number of six adult males and five adult females. Morphometric data are summarized in Table 1 together with those of seven congeneric species.

In O. fuscus sp. nov., there was no significant difference in SVL (t = 0.183, p = 0.859) between males (69.5±3.0 mm, n = 6) and females (69.0± 4.8 mm, n = 5: Table 1). In values relative to SVL, sexes significantly differed in longer tail and shorter trunk in males than females (Table 1). As seen in other congeners, males had more robust hindlimb and posteriorly more projecting distal end of fibula than females.

Adult specimens showed the following characteristics in the breeding season: well-developed dermal skin fold on posterior edge of hindlimb, black tubercles and asperities on palm and sole, cloaca well swollen, and precloacal skin fold forming inverse V-shaped in males; precloacal skin fold forming inverse narrow U-shaped in females; black claws on fingers and toes, parotoid gland well swollen, black precloacal spine series, and tail laterally compressed in both sexes, more remarkable in males.

The number of costal grooves was significantly largerer in males (mode = 13 in males vs. 12 in females: t = 2.455, p = 0.036 for each side: Table 2). The number of presacral vertebrae including atlas varied from 18 to 19 (Table 2) and was not sexually different (t = 0.980, p = 0.353). The number of vomerine teeth, tended to be larger in females (9 to 15, mean = 12.4± 1.7 in males and 11 to 19, 15.0±3.0 in females), but the difference was not significant (t = 1.755, p = 0.113). Gap between left and right vomerine tooth series was present in both sexes except for a single female (present in 90.9%). Short anteriorly directed sub-branch of vomerine tooth series at inner meeting occurred in 27.3% of specimens that were all females (Table 3), and the frequency between sexes was significantly different (p = 0.033).

Color pattern in life was stable among individuals, only amount of ochre flecks on dorsal and ventral sides of the body varied, but neither stripe nor distinct markings was present. Density of silvery white dots on venter also varied from moderate to dense, frosted appearance. On lateral to ventral sides, the ground color was same as dorsum or fading to purplish-gray.

Larva. We could only find five larvae of O. fuscus sp. nov. All the specimens were at premetamorphic stage (stage 69–70), and 36.1–43.1 mm in SVL and 33.0– 41.8 mm in TAL, with the resultant TL of 69.1–84.9 mm. General morphological characteristics are as follows ( Fig. 12 A–B): head rectangular and blunt at snout; body relatively stout; eye slightly prominent; three pairs of short external gills; labial fold well developed at posterior half of upper jaw; caudal fin relatively well-developed dorsally and ventrally; dorsal fin higher than ventral fin; origin of dorsal fin at level of posterior hindlimb to cloaca; ventral fin originating from around posterior one-sixth to two-thirds of tail; tail tip moderately rounded; skin fold on posterior edge of limb; surfaces of palm and sole with dark asperities; digits with acute and curved black claws; dorsum uniformly dark-brown, sometimes with indistinct ochre flecks and/or pale spots; ventrally whitish or grayish without markings.

Comparisons. Morphological data are summarized in Tables 1–4, and some data are from Poyarkov et al. (2012) and Yoshikawa et al. (2013). Onychodactylus fuscus sp. nov. is different from the continental O. fischeri , O. koreanus , O. zhangyapingi , and O. zhaoermii in complete lack of distinct dorsal markings (vs. presence of distinct spots, mottlings, or indistinct stripe in continental species).

Onychodactylus fuscus has smaller SVL, relatively shorter trunk, longer forelimb and hindlimb, longer and wider head, and larger IND, END, and CW (Table 1) in both sexes, and relatively shorter tail in females, than O. fischeri . Onychodactylus fuscus also has smaller numbers of presacral vertebrae and costal grooves than O. fischeri (Table 2).

Oncychodactylus fuscus differs from O. koreanus in having shorter tail, smaller number of presacral vertebrae in both sexes, relatively shorter hindlimb, wider internarial space and chest (Table 1), and a smaller number of vomerine teeth in males (Table 3), as well as fewer costal grooves in females (Table 2).

Onychodactylus fuscus is different from the other species of the O. japonicus complex in possession of uniformly dark-brown dorsum with slight, indistinct ochre flecks and completely lacking markings (vs. possessing distinct dorsal stripe or markings). In addition, the gap between vomerine tooth series is much more frequently present (90.9% of specimens) than in other species (6.3–41.7%).

Onychodactylus fuscus differs from O. japonicus in: larger SVL in males (69.5 mm vs. 65.7 mm in O. japonicus ); relatively shorter tail (121.9% of SVL in males and 99.7% in females vs. 125.0% and 106.7%) in both sexes; wider head (15.5% of SVL vs. 14.8%) and narrower intercanthal space (57.1% of HW vs. 59.6%) in females; and larger number of costal grooves in males (mode = 13 vs. 12). In coloration, O. fuscus has a uniformly dark-brown dorsum lacking markings which differs from O. japonicus with dorsal markings (99.3% of specimens had dorsal markings). A pair of dark markings on the chest tends to be absent in O. fuscus (present in 18.2% of specimens vs. 68.6% present in O. japonicus ).

Oncychodactylus fuscus significantly differs from O. kinneburi in having: smaller SVL in females (69.0 mm vs. 78.4 mm); wider internarial space (51.3% of SVL vs. 49.1%) in males, wider head (15.5% of SVL vs. 14.5%) in females, and wider chest (13.5% of SVL in males and 13.8% in females vs. 12.3% and 12.2%) in both sexes. Onychodactylus fuscus also differs from O. kinneburi in having significantly smaller numbers of presacral vertebrae in both sexes (mode = 18 or 19 in males and 18 in females vs. 19 in both sexes in O. kinneburi ) and costal grooves in females (mode = 12 vs. 13 in O. kinneburi ). In coloration, O. fuscus has uniformly dark-brown dorsum and silvery-dotted ventrolateral sides, and differs from O. kinneburi which has yellowish-orange dorsal stripe or blotches (100% of specimens examined) and no ventrolateral silvery dots.

Oncychodactylus fuscus differs from O. nipponoborealis in having larger SVL in males (69.5 mm vs. 64.2 mm), and shorter tail (99.7% of SVL vs. 106.7%) in females, and wider internarial space (51.3% of HW vs. 49.7%) in males. In coloration, O. fuscus is different from O. nipponoborealis in lacking dorsal markings (vs. usually having dorsal markings [97.8%]). Dark marking on chest is also less frequently observed in O. fuscus (present in 18.2% of specimens) than in O. nipponoborealis (65.2%: Table 4).

In comparison with O. tsukubaensis , O. fuscus differs in having longer tail in both sexes (121.9% of SVL in males and 99.7% in females vs. 102.3% and 90.4%) and wider head in females (54.7% of SVL vs. 52.4%), and wider internarial space in males (51.3% of HW vs. 48.3%) and wider interorbital space in both sexes (32.2% of HW in males and 30.8% in females vs. 28.3% and 27.8%). Onychodactylus fuscus had the gap between vomerine tooth series more frequently than O. tsukubaensis (90.9% present in O. fuscus vs. 6.3% in O. tsukubaensis ). In coloration, O. fuscus differs from O. tsukubaensis by lacking dorsal markings (vs. typically having dorsal stripe [93.8%]).

In comparison with O. intermedius , O. fuscus differs in having significantly larger SVL in males (69.5±3.0 mm vs. 63.0±4.9) and tendency of larger SVL in females (69.0± 4.8 mm vs. 65.5±4.1), significantly wider internarial space relative to HW in males (51.3% vs. 49.4%) and narrower intercanthal space relative to HW in females (57.1% vs. 59.3%). Relative HLL also tended to be shorter in both sexes (30.0% in males and 30.9% in females vs. 31.5% and 32.1%).Number of vomerine teeth was significantly larger in O. fuscus than O. intermedius in males (12.4±1.7 vs. 15.9±2.4). Presence of the gap between vomerine tooth series is more frequent in O. fuscus than in O. intermedius (90.9% present in O. fuscus vs. 29.6% in O. intermedius ). In coloration, O. fuscus differs from O. intermedius by lacking dorsal markings (vs. having dorsal stripe or mottlings).

At the larval stage, O. fuscus is morphologically similar to the other congeneric species, but has uniformly dark-brown dorsum with some small ochre flecks, and it can be distinguished from larval O. japonicus , which is sympatric in one locality ( Fig. 12 C–F). In O. japonicus larvae of neighboring or sympatric populations, there are two morphotypes, striped and unstriped types, and striped type can easily be distinguished from O. fuscus . The unstriped O. japonicus larvae has a varying amount of black mottlings on yellowish-gray background and it differs from uniformly dark-brown O. fiscus . From the other species in the O. japonicus complex, O fuscus larvae can be distinguished by the presence of various types of dorsal markings (distinct stripe, continuous or discontinuous series of blotches, or varying amount of mottlings). However, we would like to note that these diagnoses of O. fuscus are provisional, and future collection of more larval specimens and detailed comparisons are necessary to understand morphological characteristics of O. fuscus larvae.

Karyotype. No karyotypic information is available for O. fuscus .

Genetic characteristics. Onychodactylus fuscus sp. nov. forms a distinct clade, Subclade II-C, which is newly reported in this study ( Fig. 2 ). Based on the mitochondrial phylogeny, the new species is a sister taxon of O. intermedius described above (Subclade II-A), and is also closely related to O. tsukubaensis (Subclade II-B) with mean pairwise p-distances between them for cytb gene of 4.15% (3.59–4.73%) and 5.51% (5.35–5.70%), respectively. Within the species, pairwise p-distances varied up to 1.75%, and two distinct haplotype groups were recognized although they showed no meaningful geographic genetic structure. The new species is sympatric in some localities with O. japonicus , but is genetically distinct from it, with a large p-distance of 8.18% (7.71–8.85%). Analysis of microsatellite loci also showed substantial difference between these sympatric species, and indicated presence of a high degree of reproductive isolation between them at least in these instances of sympatry.

Fecundity and natural history. Breeding habits of O. fuscus sp. nov. is not fully understood, but it is certain that the species breeds in late autumn to early winter. It is unknown if this species also breeds in summer as known in some congeners, or breeds biannually (summer and winter) as seen in O. japonicus in Ishikawa Pref. ( Akita, 1989). In the type locality, assemblage of breeding adults (seven males and two females) was observed on 9 November 2013, and newly laid egg sacs were confirmed on 23 November 2013 ( Y. Nakano, personal communication). Egg sacs were strongly adhered under the rock by gelatinous stalks in complete darkness in the underground flowing water at a headstream (water temperature 9.3°C).

The egg sacs of O. fuscus are similar to those of O. japonicus ( Akita 1982) and O. tsukubaensis (Yoshikawa et al. 2013) in shape and texture ( Fig. 13 ), and were spindle in shape, with transparent, elastic, and strong outer layer. The egg sacs had very weak, longitudinal grooves on the surface, and short, filamentous structure on free ends. Among six pairs of egg sacs observed, length of sacs excluding stalk ranged 30.0– 36.2 mm (mean±1SD = 32.3±2.3, n = 12). In the egg sac, eggs were arranged in two rows, and the clutch size ranged from 13 to 16 (6– 9 eggs per egg sac). Eggs were large, with diameters of 5.0– 6.5 mm (mean±1SD = 5.9±0.3, n = 87), and completely yellowish white in color.

Larval life history of O. fuscus , including the season and the size at hatching and metamorphosis, is poorly known. Our limited number of specimens suggest that larvae reach at least 43.1 mm in SVL and 84.9 mm in TL. Metamorphosed juveniles would disperse to inhabit forest floor around the stream.

Life history of adults in the non-breeding season is unknown, but they are presumed to inhabit the cool and humid forest floor in the adjacent mountains, as is the case in the other Onychodactylus species. The new species is sympatric with O. japonicus in one locality, and is probably so in its entire distributional range, but detailed distributional patterns and ecological features of these species, as well as mechanisms of their reproductive isolation are unknown.

Range. Known from two localities in western Tadami-machi, Fukushima Prefecture and southern Sanjo-shi, Niigata Prefecture. However, actual distributional range is probably wider. The new species is sympatric with O. japonicus in Sanjo-shi, Niigata Prefecture, where larvae of the two species are found together. In addition, we also found larvae of O. japonicus ( Fig. 12 D–F) from a stream close (ca. 5km distant) to the type locality of O. fuscus .

Conservation. The new species is currently known only from a limited area in Fukushima and Niigata Prefectures, although potential distributional range is much wider. This species seems to be locally abundant and the habitat is generally well conserved, but some parts of the habitat is threatened by recent constructions of roads and dams. Because the known range is small, collection pressure for pets can also be a serious threat, as in O. tsukubaensis , which is now facing the problem of over collection ( O. Inaba, personal communication) shortly after recent description. We propose that the new species to be designated as Vulnerable in the Red Lists of IUCN and Ministry of the Environment of Japan.

Figures

FIGURE 2. The ML trees based on 1141 bp of mitochondrial cytochrome b gene, showing entire shape of the ML tree (A), detail of Subclade II-A (B), and detail of Clade III (C). Values at nodes indicate supports of 1000 bootstrap replicates. Numbers in parenthesis indicate population numbers shown in Appendix 3.

FIGURE 6. Open mouth of holotype of O. intermedius sp. nov. (A: KUHE 47455) and O. fuscus sp. nov. (B: KUHE 48284) showing the shape of vomerine tooth series. Scale bars indicate 1 mm.

FIGURE 10. Dorsal and ventral views of male holotype (A and B; KUHE 48284, SVL = 69.0 mm) and a female paratype of O. fuscus sp. nov. (C and D; KUHE 48129, SVL = 74.8 mm). Scale bar indicates 10 mm.

FIGURE 12. Larvae of O. fuscus sp. nov. (A and B) and a sympatric O. japonicus larva (C) from Sanjo-shi, Niigata Prefecture (In preservation). Larvae of O. japonicus in life (D – F) collected from Tadami-machi, Fukushima Prefecture, near the type locality of O. fuscus sp. nov. Scale bar indicates 10 mm.

FIGURE 11. A male paratype of O. fuscus sp. nov. (KUHE 48283) in life.

FIGURE 13. A pair of egg sacs of O. fuscus sp. nov. in the type locality on 20 December 2013, about one month later from the deposition. Scale bar indicates 10 mm.