Hebius chapaensis (Bourret, 1934)

Ren, Jin-Long, Wang, Kai, Nguyen, Tao Thien, Hoang, Chung Van, Zhong, Guang-Hui, Jiang, Ke, Guo, Peng & Li, Jia-Tang, 2018, Taxonomic re-evaluation of the monotypic genus Pararhabdophis Bourret, 1934 (Squamata: Colubridae: Natricinae) with discovery of its type species, P. chapaensis, from China, Zootaxa 4486 (1), pp. 31-56 : 40-51

Hebius chapaensis (Bourret, 1934)

( Figs. 3–8 )

Pararhabdophis chapaensis Bourret, 1934 . Bull. Gén. Instr. Publ. Hanoi 14 (7): 131–132, fig. 2. Type locality. “ Chapa , province de Laokay ( Tonkin ), à l’altitude moyenne de 1.600 m., Indochine française” [= Sa Pa, NW Lao Cai Prov., ext. N Vietnam, 22°21’N, 103°50’E, elevation 1500–1600 m]. Holotype. MNHN 1938.0125 (formerly RLB M.270), a 690+ mm male (Collected by R.L. Bourret, collected around 1930–1931) .

Referred specimens. Data of 28 specimens of H. chapaensis were referred: Vietnam (n = 24). Lao Cai Province. MNHN 1938.0125 (holotype of Pararhabdophis chapaensis ), Sa Pa, 1,600 m; IEBR 2907–2909, Sa Pa, I Ninh Ho, Cat Cat; ROM 38195, Lao Cai; VNMN 0 5791, VNMN 06102–106, Sa Pa, 22°23'6.07" N, 103°47'7.56" E, 1,759 m; VNMN 3277, Bat Xat, Y Ty, 22°36'44" N; 103°38'39" E; 2,030 m. Cao Bang Province. ROM 28636, Cao Bang. Yen Bai Province. HNUE MCC.2017.43–44, HNUE MCC.2017.70, HNUE MCC.2017.72, Mu Cang Chai Species and Habitat Conservation Area, Che Tao Commune, Che Tao Village, 21°45'47.16" N; 104°1'7.68" E; 1,134–2,046 m. Son La Province. TBU-PAR 30–32, Copia nature reserve, Co Ma and Long He; TBU-PAR 52–55, Sop Cop nature reserve, Huoi Mot.— Laos (n = 3). Houaphan Province. NCSM 77924, Viengthong District, Phou Louey National Protected Area, near Tad Loi Waterfall, 20°13'57.11" N, 103°12’38.88" E, 1,186 m; one non preserved specimen, Viengthong District, near Viengthong, 1,050m.—Louangphabang Province. NCSM 77925, Phoukhoume District, Hoay Tala 1, branch of the Nam Madao, 19°18'6.80" N, 102°34'24.96" E, 1,269 m. —China (n = 1). Yunnan Province, YBU 14026, Honghe Prefecture, Pingbian County, Daweishan Nature Reserve, 103°42'16.06" N, 22°54'40.21" E, 1,993 m. Of these, eight specimens were physically examined (see Materials and Methods), and data of 20 other specimens were obtained from the literature ( Bourret 1934a; David et al. 2015b; Le et al. 2018; Pham et al. 2013).

Diagnosis. The species can be diagnosed from other morphologically similar species by a combination of the following characteristics: (1) Body elongate and slender, TL 390–899 mm; (2) tail relatively long, TaL/TL 0.20– 0.31; (3) head subtrapezoid, moderately distinct from neck; (4) maxillary teeth 29–34, last 2–3 strongly enlarged, without any diastema; (5) nostrils directed dorsolaterally; (6) prefrontal paired, seven upper head scales as typical for colubroids; (7) internasals truncated anteriorly, sutures between them not in contact with prefrontal sutures; (8) supralabials nine, 4th, 5th and 6th entering orbit; (9) dorsal scale rows 17:17:17, weakly keeled anteriorly, strongly keeled posteriorly; (10) ventrals 15 9–177; (11) subcaudals 83–114; (12) hemipenis reaching subcaudals 5–6, spinose throughout, not forked; (13) head brownish black, with irregular and complex golden stripes and spots, (14) anterior parts of supralabials 1–8 with a thicker upright or oblique stripe; (15) dorsal scales of row 5 and row 12 with pale orange blotches anteriorly and longitudinal rodlike pattern, forming two light discontinuous or continuous dorsolateral stripes along each side; (16) venter glossy black, with scream or pale yellow longitudinal streaks, tending to become fainter posteriorly ( Fig. 7 ; Table 3).

TABLE 4. Morphological comparison of Hebius chapaensis specimens from different localities in present study. (1) Abbreviations are listed in Material and Methods except for L–orbit: loreal enter orbit, SpL–orbit: supralabial enter orbit, IfL–aCS: infralabial contact with anterior chin shield, aTEM: anterior temporal, pTEM: posterior temporal format; (2) “+” indicates tail incomplete; (3) “-” indicates missing data; values given in brackets indicate infrequent condition.

Description. Body cylindrical, rather elongated, slenderly built, TL 390–899 mm; tail relatively long, TaL/TL 0.20–0.31, thin, tapering, without clear sexual dimorphism; head small, subtrapezoid-shaped, HL/HW 1.10–1.47, moderately distinct from the poorly defined neck, dorsally depressed; snout short, SL/SW 0.55–0.78; eye moderate or large, EW/SOL 1.00–1.79, EW/HL 0.13–0.19; pupil shape rather variable, vertically elliptic, round, or irregular, usually asymmetric; interorbital distance medium, IOD/HW 0.41–0.56; nostril crescentic, somewhat kidneyshaped, piercing upper middle of nasal, directed dorsolaterally.

Dentition. Maxillary teeth 29–34, progressively increasing in size, last 2–3 strongly enlarged without diastema.

Hemipenis. Hemipenis in everted condition short and subcylindrical, not forked, reaches subcaudal 5–6, spinose and calyculate throughout, spines more or less uniform in size; sulcus spermaticus simple, reaching tip of each organ.

Body scalation. Dorsal scale rows 17:17:17; vertebral not enlarged, smooth anteriorly, weakly keeled from row 5 to row 13 at midbody, strongly keeled posteriorly; ventrals 159–177, precloacal not divided (half divided in VNMN 06105); cloacal divided, subcaudal 83–114, paired, with single terminal rod.

Head scalation. Rostral broad, width approximately 1.5 times as long as high, curved onto upper snout surface, visible from above; nasals subrectangular, in contact with rostral, internasals, prefrontals, loreals and supralabials 1–2 (1–3 on left side in VNMN 06104), not divided, furrow from inferior nostril to lower edge of nasals; internasals trapezoid, truncated anteriorly, not in contact with loreals, internasal sutures curved on both ends, not in contact with prefrontal sutures; prefrontal paired in all specimens, in contact with nasals, loreals and preoculars laterally, lengths of prefrontal sutures about equal to internasal sutures; frontal subtriangular or subpentagonal, longer than wide, penetrate into parietals posteriorly, length equal to snout length and parietal sutures; parietals large, nearly 1.7 times as long as wide, much longer than frontal. Loreal 1/1, subrectangular, approximately twice as long than high, not entering orbit (except for VNMN 0 6104, where loreal enters orbit on left side), in contact with nasals anteriorly, with prefrontals dorsally, with preoculars posteriorly, and with supralabials 2–3 or 2–4 (only on single side of head in four of eight examined specimens) ventrally (3–4 on left side in VNMN 06104); preoculars 2/2, upper pair much larger, length about 2 times longer than lower ones, preoculars partly fused together on left side in VNMN 3277, fused with loreal on left side in VNMN 06104; postoculars 2/2 (3 on right side in YBU 14026), upper pair subrectangular, about 1.3 times as high as long, shape of lower pair variable, trapeziform or comma-shaped, smaller than upper pair; supraoculars 1/1, longer than wide; subocular absent. Supralabials 9/9, fourth, fifth and sixth entering orbit (only fifth and sixth entering orbit on right side in VNMN 06104), supralabials slightly higher than long, except for seventh, eighth and ninth, which are distinctly enlarged; eighth supralabials largest, upper part distinctly broader, in contact with temporals dorsally; infralabials mostly 10/ 10 (9 on single side of head in VNMN 0 6103 and VNMN 0 6104 only), first five in contact with anterior chin shields (first four only on left side of head in VNMN 0 5791, VNMN 0 6102, and VNMN 06103); temporals directed obliquely, anterior temporal single in all specimens, number of posterior ones variable, usually asymmetric, 1, 1+2, 1+3, 2 or 2+3; two pair of chin shield present, anterior one shorter, posterior chin shields separated from each other by 1+2 scales (1+1+ 2 in VNMN 0 6103 and VNMN 06104). Minute granular asperities observed on head scales especially on supralabials and temporals.

Coloration in life. In life, the dorsal surface of head is glossy brownish-black, dorsal head scales densely covered by irregular and vermiculate golden stripes, the remaining head scales interspersed with golden spots or blotches, especially on internasals and prefrontals. Golden or pale yellow thick streaks on anterior part of supralabials 1–8, only a faint deep yellow blotch on the anterior inferior part of ninth supralabial, but a thick, oblique stripe on the posterior superior margin. The latter together with the similar markings on anterior temporals forming a thick “eyebrow” streak pattern. Patterns of infralabials are similar to supralabials, but the stripes being paler and decorated with beige or cream spots posteriorly, almost connected with corresponding supralabial stripes. The background color of the ventral surface of the head is yellowish cream, two pair of chin shields densely speckled with blackish brown spots especially on the center. These densely-set spots forming clusters of blotches on the scales after the posterior chin shields, and are fused to three to four large, spotted-edged black patches on ventrals, especially in the anterior third of body where patches have clear boundaries.

The dorsal body is glossy black, dorsal scales of row 5 and row 12 have pale orange blotches throughout, these rodlike blotches are approximately 2 to 3 scales long and 2 scales wide, every two blotches are separated by a distance of one scale length, producing two light discontinuous dorsolateral stripes along each side. The rodlike blotches are thicker and more distinct anteriorly but thinner and paler posteriorly, nearly in contact with each other on both ends; in some individuals, the blotches posteriorly forming two continuous dorsolateral stripes. More or less pale yellow spots on each dorsal scales, largely forming complex mesh pattern throughout. The venter is glossy black, three to four large black blotches are present on each ventral scale in the anterior third of body, and the interspace of each blotch is cream to off-white, variegated with light yellow, forming 4 to 5 fine streaks longitudinally. The ventral streaks are tending to become fewer and fainter posteriorly, a faint, and narrow cream lateral stripe on each side remains until cloaca. Lower tail surface and venter are glossy black entirely without lateral stripes ( Fig. 7 , 8 ).

Coloration in preservation. For the preserved holotype, the golden, yellow or orange pigmentation of the dorsal head fades significantly and turns to a rusty or brownish yellow coloration, the ventral surface of body fades into uniform brownish with barely observed gloss on ventral scales ( Fig. 3 ). The pattern of the recently preserved specimens still resembles the coloration of live animals, however, all the light ornamentation fade to an off-white hue to different degrees, but the gloss of scales still remains distinct ( Fig. 4C , 5 , 6 ).

Comparison. H. chapaensis can be separated from 33 congeners by having 17 dorsal scale rows at midbody (vs. 19 or 15). For the rest of eight congeners that have 17 rows of dorsal scales at midbody, H. chapaensis differs from H. arquus ( David & Vogel, 2010) and H. groundwateri (Smith, 1922) by having different dorsal scale formulae (17:17:17 vs. 17:17: 15 in H. arquus , and 19:17: 17 in H. groundwateri ); from H. atemporale (Bourret,

TABLE 5. Morphological comparison of the monotypic genus Pararhabdophis with other morphologically similar genera of the subfamily Natricinae .

1934) by the presence of normal anterior temporals (vs. absent or a minute one), more supralabials (9 vs. 6), and more infralabials (10 vs. 7); from H. frenatum (Dunn, 1923) by having more preoculars (2 vs. 1), more supralabials (9 vs. 8), and fewer anterior temporal (1 vs. 2); from H. sarawacense (Günther, 1872) by having 159–177 ventrals (vs. 140–154 ventrals), dorsal scales weakly keeled anteriorly, moderately keeled at midbody, and strongly keeled posteriorly vs. dorsal scales strongly keeled throughout, two preoculars vs. a single preocular; from H. sauteri Boulenger, 1909 by having more maxillary teeth (29–34 vs. 22–26), more ventrals (159–177 vs. 118–147), and more subcaudals (83–114 vs. 61–92); from H. venningi and H. taronense (Smith, 1940) by having a different maxillary condition (posterior maxillary teeth distinctly enlarged vs. gradually enlarged), and fewer postoculars (2 vs. 3).

In addition, H. chapaensis may be confused with Parahelicops , it can be distinguished from the later genus by having (1) a pair of prefrontals without exceptions vs. usually a single prefrontal, (2) a lower number of subcaudals (83–114 vs. 116–146), and (3) a glossy black venter vs. pale-colored (from other morphologically similar genera occurring in China and Vietnam also see diagnostic key provided below).

Distribution. H. chapaensis is currently known from ten localities ( Fig. 1 ), including northern Vietnam (Lao Cai Province, Sa Pa [type locality]; Lao Cai Province, Bat Xat, Y Ty; Cao Bang Province [ David et al. 2015b]; Yen Bai Province, Mu Cang Chai Species and Habitat Conservation Area, Che Tao Commune, Che Tao Village [Le et al. 2018]; Son La Province, Copia Nature Reserve, Co Ma and Long He [ Pham et al. 2013]; Son La Province, Sop Cop Nature Reserve, Huoi Mot [ Pham et al. 2013]), Laos (Houaphan Province, Viengthong District, Phou Louey National Protected Area, near Tad Loi Waterfall [ David et al. 2015b]; Houaphan Province, Viengthong District, near Viengthong [ David et al. 2015b]; Louangphabang Province, Hoay Tala 1, branch of the Nam Madao [ David et al. 2015b]), and southwestern China (Yunnan Province, Honghe Prefecture, Pingbian County, Daweishan Nature Reserve).

Natural history. H. chapaensis inhabits water bodies in tropical/subtropical forests between elevations of 1,050 m and 2,046 m. The species is nocturnal, thus active and foraging at night. In southern Yunnan Province, a male specimen was observed actively preying upon tadpoles of treefrogs ( Rhacophorus duboisi ) on the edge of water by a static pool ( Fig. 9 ). In the same microhabitat, Feihyla fuhua , Odorrana tiannanensis , Rhacophorus duboisi , Lycodon fasciatus , and Trimeresurus gumprechti were the common amphibians and reptiles observed during the survey period in 2014. H. chapaensis was also observed sympatrically occurring with Gracixalus sapaensis in northern Lao Cai Province.

Etymology. The original generic nomen, Pararhabdophis , is based on the Greek prefix para -, meaning near or similar, and the natricine generic name Rhabdophis , presumably refers to the morphological similarity between two genera, and the gender of this generic name is possibly masculine. The newly referred generic nomen is Hebius , which was erected by Thompson (1913) on the basis of the morphology of the hemipenis. The generic name presumably derived from the Greek noun ἥβη “hebe”, meaning youth or pubescence, maybe refers to the densely spinous hemipenis, which is the salient diagnostic characteristic of this group. The gender of this generic name is masculine. The species name is derived from the type locality of this species (Chapa, = Sa Pa, in Lao Cai Province of Vietnam) and it remains unchanged if the gender of the genus changes. We suggest “SaPa Keelback” as its common name, and “Sha Ba Fu Lian She” (Óffiůmẘ) as its Chinese common name.

Paraphyly of Hebius species from China. Interestingly, the newly generated sequences of H. chapaensis (VNMN 0 5791, 0 6102, 0 6103, 06106) formed a significantly supported clade (clade B, see Fig. 2 ) with two individuals retrieved from GenBank, i.e. H. venningi (GP 1300), H. deschauenseei (AMNH 148575), and uncorrected p -distance within this clade being relatively low (0.0%–1.1%, Table 2), which is much lower than the overall mean distance of selected taxa apart from this clade (12.1%). Since many Hebius species are poorly diagnosed yet and characters highly convergent ( David et al. 2007; 2015a; Guo et al. 2014), we suspect that the specimens previously identified as H. venningi (GP 1300) and H. deschauenseei (AMNH 148575) are misidentifications of H. chapaensis . Moreover, the localities of these two supposedly misidentified specimens (GP 1300, from Yunnan, China; AMNH 148575, from Ha Giang, Vietnam) both fall within or in between the known distribution sites of H. chapaensis ( Fig. 1 ). As taxonomic identification problems of existing Genbank sequences are very common ( Guo et al. 2014; also represented by the multiple paraphyly of Hebius species in our trees), we cannot confirm the sister species of H. chapaensis , as the most closely related species on our tree are both paraphyletic (CAS 234262, H. ‘modestum’ and GP 2468, H. ‘venningi’) ( Fig. 2 ).

The common paraphyly of Hebius species reflects the need of continuous taxonomic analyses on the group in Asia. As very few taxonomic studies have been conducted for the Natricinae ( David et al. 2007; Guo et al. 2014), the understanding of this subfamily in China and Vietnam remains understudied, and the diagnostic key to all natricine genera in both countries have not been updated in the past decades ( Nguyen & Ho 1996; Nguyen et al. 2009; Pope 1935; Zhao 2006; Zhao & Adler 1993; Zhao et al. 1998). Here based on the best available data, we provide an updated diagnostic key to all known genera of the subfamily Natricinae in China and Vietnam, including a total of 15 genera (14 genera occurring in China /8 genera in Vietnam; 59 species occurring in China /35 species in Vietnam, similarly hereinafter): Amphiesma (1/1), Amphiesmoides (1/1), Atretium (1/0), Hebius (18/12), Herpetoreas (2/0), Macropisthodon (1/0), Natrix (2/0), Opisthotropis (13/9), Parahelicops (0/1), Paratapinophis (1/0), Rhabdophis (10/6), Rhabdops (1/0), Sinonatrix (4/3), Trachischium (2/0), and Xenochrophis (2/2) ( Cai et al. 2015; David et al. 2015a; Murphy et al. 2008; Nguyen et al. 2009; Nguyen et al. 2018; Ren et al. 2017; Wang et al. 2017a; Ziegler et al. 2018).

Figures

FIGURE 1. Map illustrating the distribution of Hebius chapaenis. Star represents the type locality (Sa Pa, Lao Cai Province, Vietnam). Triangle represents Y Ty, Bat Xat, Lao Cai Province, Vietnam. Sqare represents the new country record location in China (Daweishan National Nature Reserve, Pingbian County, Yunnan Province). Circles represent localities previously provided by David et al. (2015b) (No. 1–4), Le et al. (2018) (No. 5), and Pham et al. (2013) (No. 6–7), repectively: 1. Gao Bang Province, Vietnam; 2. Viengthong District, Houaphan Province, Laos; 3. Phou Louey National Protected Area, Viengthong District, Houaphan Province, Laos; 4. Hoay Tala 1, Phoukhoume District, Louangphabang Province, Laos; 5. Mu Cang Chai Species and Habitat Conservation Area, Yen Bai Province, Vietnam; 6. Copia nature reserve, Son La Province, Vietnam; 7. Sop Cop nature reserve, Son La Province, Vietnam.

FIGURE 2. Phylogenetic tree of Natricinae obtained by Maximum likelihood (A) and Bayesian Inference (B), depicting phylogenetic relationships of the genus Pararhabdophis and other natricine snakes. Numbers above branches are BSP and BPP, respectively.

FIGURE 3. The preserved holotype of Hebius chapaensis (MNHN 1938.0125). (A) Body in dorsal view; (B) Body in ventral view; (C) Head in dorsal view; (D) Head in ventral view; (E) Head in lateral view, left side; (F) Close-up view of ventral anal region. Photographs by Antoine Fraysse (MNHN).

FIGURE 4. Comparisons of head scalation and color pattern in different descriptions of Hebius chapaensis. (A) Figures from original description (Bourret 1934a); (B) Figures from Bourret (1936); (C) This work (VNMN 3277, Photographs by JL).

FIGURE 5. Comparisons of the pupil shape on both sides of Hebius chapaensis, row 1: left side; row 2: right side. (A) VNMN 3277; (B) VNMN 06102; (C) VNMN 06105; (D) VNMN 06104; (E) VNMN 06106. Scale bar 1 mm. Photographs by JL.

FIGURE 6. Adult male specimen of Hebius chapaensis (VNMN 06102), in preservative, Sa Pa, Lao Cai Province, Vietnam. (A) Dorsal view; (B) Ventral view; (C) Lateral head view, left side; (D) Dorsal head view; (E) Ventral head view. Scale bar 10 mm. Photographs by JL.

FIGURE 7. General aspect of Hebius chapaensis (YBU 14026; male), showing coloration in life,—Daweishan National Nature Reserve, Pingbian County, southern Yunnan Province, China. (A) Lateral view; (B) Ventral view. Photographs by WK.

FIGURE 8. Aspects of Hebius chapaensis (YBU 14026; male) in life,—Daweishan National Nature Reserve, Pingbian County, southern Yunnan Province, China. (A) Lateral head view, right side; (B) Ventral head view; (C) Dorsolateral color pattern; (D) Hemipenis. Photographs by WK.

FIGURE 9. Habitat of Hebius chapaensis in Daweishan National Nature Reserve, Pingbian County, southern Yunnan Province, China. (A) Microhabitat, showing general view of the dense forest; (B) Microhabitat, showing ephemeral pools with lentic water. Photographs by WK.