Hebius chapaensis (Bourret, 1934)

David, Patrick, Vogel, Gernot, Nguyen, Truong Quang, Orlov, Nikolai L., Pauwels, Olivier S. G., Teynié, Alexandre & Ziegler, Thomas, 2021, A revision of the dark-bellied, stream-dwelling snakes of the genus Hebius (Reptilia: Squamata: Natricidae) with the description of a new species from China, Vietnam and Thailand, Zootaxa 4911 (1), pp. 1-61 : 23-29

4. Hebius chapaensis (Bourret, 1934)

( Figs. 8–9 )

Pararhabdophis chapaensis Bourret, 1934a: 131 (Separate: p. 3), Fig. 2 .—

Type locality. “Chapa, province de Laokay (Tonkin), à l’altitude moyenne de 1600 m ”, now Sa Pa, Lào Cai Province, Vietnam, ca. 1,600 m elevation.— Holotype. MNHN 1938.0125 , adult male (Muséum National d’Histoire Naturelle, Paris, France); collected by René Bourret, Summer 1930 or 1931 and deposited in 1934.

Pararhabdophis chapaensis .— Bourret 1935a: 249; Bourret 1936a: 97, 103, 114 & 121; Bourret 1936b: 121, Fig. 49; Bourret 1939a: 44; Bourret 1939b: 54; Smith 1943: 316; Tran et al. 1981: 382; Welch 1988: 88; Nguyen & Ho 1996: 98; Iskandar & Colijn 2001: 103; Nguyen et al. 2005a: 93; Nguyen et al. 2009: 363; Das 2010: 296; Bain & Hurley 2011: 104 & 129; Stuart & Nguyen 2012b: e.T191911A2014449; Pham et al. 2013: 17, 21 & 22: Fig. B; Teynié et al. 2014: 43, 44: Pl. 7B; Wallach et al. 2014: 522; David et al. 2015b: 203, 209, 215, 216 & 219; Le et al. 2018: 103, 106: Fig. 3A & 107.

Hebius chapaensis .— Kizirian et al. 2018: 2, 3 & 5; Ren et al. 2018: 31, 37 & 40; Boundy 2020: 92; T. V. Nguyen et al. 2020: 234: Fig. 8 (A); Wang et al. 2020: 205; Appendix 2: 15.

Specimens examined (10).— People’s Republic of China. Yunnan Province. CIB 110718, Menglun, 21°58’5”N, 101°11’51.46”E, Mengla County, Xishuangbanna Dai Autonomous Prefecture. elev. 567 m. — Vietnam. Lao Cai Province. IEBR 2907–2909, Cat Cat, I Ninh Ho, Sa Pa; MNHN 1938.0125 (holotype of Pararhabdophis chapaensis ), Sa Pa , ca. 1,600 m a.s.l. ; ROM 38195, Lao Cai. Cao Bang Province. ROM 28636, Cao Bang. — Laos. Houaphan Province. NCSM 77924, Phou Louey National Protected Area, near Tad Loi Waterfall, 20.23253°N, 103.2108°E, Viengthong District , elev. 1,186 m ; 1 non preserved specimen, near Viengthong, Viengthong District , elev. 1,050m. Louangphabang (or Louang Prabang) Province; NCSM 77925, Hoay Tala 1, branch of the Nam Madao, 19.30189°N, 102.5736°E, Phoukhoume District , elev. 1,269 m .

Taxonomic comments.— Bourret (1934a) erected the genus Pararhabdophis for the sole included species Pararhabdophis chapaensis Bourret, 1934 , described from a single specimen, on the basis of the following characters: 32 subequal maxillary teeth, of which the three last ones are strongly enlarged, and a small eye with a vertical pupil; other characters included a head well distinct from the neck, 2 internasals and 2 prefrontals, an elongate, slightly laterally compressed body, dorsal scales feebly keeled, without apical pits, in 17 rows, tail long, subcaudals paired and hypapophyses developed throughout along the vertebral column. Smith (1943) accepted the validity of this genus solely on the basis of the vertical pupils of the holotype. Otherwise, Smith stated that he would have placed it in the then large genus Natrix Laurenti. In fact, the diagnosis of the genus has been somewhat biased by Bourret (1934a). The holotype is in bad condition and strongly dessicated. After a careful examination under a powerful incident light, the pupil of the holotype became visible. It is indeed elliptic at left but nearly circular at right, where it is much more difficult to see. Most probably, Bourret was misled by the state of his specimen, perhaps found dead on road. We suspect that the dessication of this specimen may have altered the shape of the eye.

The status of this genus has not been re-evaluated between 1934 and 2018 and it has been constantly considered to be valid (see the references cited above), probably by lack of additional specimens. Indeed, for long, this species has been known from its sole holotype, collected in north-western Vietnam. Subsequently, three specimens were obtained from Laos ( Teynié et al. 2014). David et al. (2015b) examined a total of nine specimens of Pararhabdophis chapaensis and confirmed the validity of the species. All these specimens agree in all points with the holotype but have a round pupil. The posterior maxillary teeth are strongly enlarged. In the family Natricidae , this condition is met in the genus Rhabdophis and in Amphiesma stolatum (Duméril, Bibron & Duméril) , sole species of the genus Amphiesma following the revision of Guo et al. (2014). It appears also in the Himalayan species currently referred to the genus Herpetoreas G̹nther by Guo et al. (2014).

Eventually, on the basis of molecular data, Kizirian et al. (2018) showed that Pararhabdophis chapaensis is nested within the genus Hebius Thompson, 1913 . Barely one month later, Ren et al. (2018) reached the same conclusions on the basis of both morphological and molecular data. We here follow these authors in referring Pararhadophis chapaensis to the genus Hebius . The dentition of the upper maxilla, made of subequal small teeth followed by two enlarged posterior teeth, the average-sized eye with a round pupil, the dorsolateral nostrils, the keeled dorsal scales, the long, keeled tail, the supralabials longer than high and the general pattern, are typical of the genus Hebius as defined by Guo et al. (2014). This species is monotypic.

Furthermore, Ren et al. (2018) reported the occurrence of this species in China on the basis of a single specimen collected from Pingbian Miao Autonomous County, Honghe Hani and Yi Autonomous Prefecture, Yunnan Province, at about only 21 kilometres from the Sino-Vietnamese border along the Vietnamese province of Lào Cai. These authors also examined seven additional specimens from north-western Vietnam (Sa Pa, Lao Cai Province).

Diagnosis.—A moderately sized species of the genus Hebius characterized by the combination of (1) a body elongate in both sexes; (2) head distinct from the neck; (3) 17–18 (rarely 19)-17-17 dorsal scale rows, distinctly keeled at midbody, strongly keeled posteriorly, especially before vent but smooth or feebly keeled on the 1 st dorsal scale row; (4) scales around the base of the tail very strongly keeled; (5) eye average with a pupil variable in shape, i.e., usually round but also elliptic or even asymmetrically and irregularly shaped, 1.0–1.2 times the distance between the lower margins of eye and of lip; (6) 29–34 maxillary teeth, progressively increasing in size in a continuous series, the last two or three abruptly and strongly enlarged, not separated from anterior teeth by a diastema; (7) nostrils piercing laterally or slightly dorsolaterally; (8) tail long but with a ratio Tal/TL lower than 0.30; (9) 159–177 VEN; (10) 90–114 subcaudals, paired; (11) internasals abruptly truncated; (12) 2 prefrontal scales, (13) 1 anterior temporal, (14) venter dark, blackish-brown or black, with some paler, more or less faint longitudinal streaks and sometimes a pale blotch or streak on the outer margin of ventrals; (15) background colour dark brown or blackishbrown; (16) dorsal pattern made of more or less elongate cream, pale yellow or pale orange-brown blotches on a faint dorsolateral stripe; (17) an elongate, cream or pale ochre-yellow blotch, or isolated blotches on the nape; (18) a strong postocular streak; (19) upper head surface with strong, yellow vermiculations; and (20) supralabials cream, ochre-yellow or pale yellowish-brown, edged with dark brown, or divided into a pale and dark area.

Comparison. Among species with 17 dorsal scale rows, Hebius chapaensis readily differs from H. annamensis by (1) internasals abruptly truncated (vs. distinctly narrowing); (2) its venter nearly entirely dark vs. entirely pale with only tips of ventral scales dark in H. annamensis ; (3) a distinct dorsal pattern; and (4) a shorter tail, ratio TaL/ TL 0.28–0.30 vs. 0.30–0.34 in H. annamensis ; see also below in the account of H. annamensis .

Hebius chapaensis differs from H. venningi by the characters given in the key above, especially (1) a shorter tail, ratio TaL/TL 0.28–0.30 vs. 0.30–0.35 in H. venningi ; (2) the number of postoculars, mostly 2 (exceptionally 3) vs. 3 in all examined specimens of H. venningi ; (3) venter entirely dark with some pale streaks vs. venter pale mesially at least on the anterior part of the body, clouded with darker hues of brown on the outer parts of ventrals in H. venningi .

Hebius chapaensis differs from H. taronensis especially by (1) its venter entirely dark with some pale streaks vs. venter pale anteriorly with an irregular dark brown crossband on each ventral, dark brown on its posterior half in H. taronensis ; (2) dorsum with large, orange dorsal blotches vs. dorsum overally dark with faint paler blotches and diffuse black spots or blotches forming a complex speckled or irregularly mottled pattern.

Lastly, H. chapaensis is morphologically quite similar to H. nigriventer . These species may be distinguished by (1) a shorter tail in H. chapaensis , 0.28–0.30 vs. 0.29–0.37 in H. nigriventer ; (2) 90–114 subcaudals in H. chapaensis vs. 105–143 SC in H. nigriventer ; (3) dorsal scales strongly keeled on the body (smooth or feebly keeled on the 1 st dorsal scale row) vs. moderately keeled at midbody, strongly keeled posteriorly, but with scales of 1 st DSR smooth; (4) dorsal pattern made of more or less elongate, cream, pale yellow or pale orange-brown blotches (orange or rusty-red in life) on a faint dorsolateral stripe vs. rectangular blotches of the same colours, higher than long anteriorly then more elongate, forming a conspicuous, dorsolateral chain of blotches. Other characters may be found in the account of H. nigriventer .

Description.—Body elongate, slightly laterally compressed, somewhat thicker in females; head elongate, somewhat triangular, distinct from the thick neck, strongly flattened anteriorly; snout elongate, flat, blunt or slightly round seen from above, subrectangular seen in profile, 25.0–31.0 % of HL, or 1.8–2.0 times longer than diameter of eye; nostrils small, round, placed slightly dorsolaterally on the snout and directed dorsolaterally, piercing in between the two parts of divided nasal; eye size average, about 1.0–1.2 times as large as the distance between its lower margin and the margin of the lip, with a pupil variable in shape, i.e., usually round but also elliptic or even asymmetrically and irregularly shaped, according to our specimens and Ren et al. (2018); tail long, thin and tapering.

The maximal known total length is 742 mm (SVL 534 mm; TaL 208 mm; specimen ROM 38195) for a male. The longest known female is 730 mm long (SVL 522 mm, TaL 208 mm long; ROM 28636).

Ratio TaL/TL: 0.280 –0.296, without sexual dimorphism (see below).

Dentition. 29–34 maxillary teeth, gradually enlarging in a continuous series, the last 2 or 3 teeth abruptly and strongly enlarged, without diastema.

Body scalation. DSR: 17(or 18)-17-17 rows; scales rhomboedric, keeled on 2 nd– 10 th, moderately on the anterior part of the body, strongly posteriorly, very strongly in the region of the vent and along the base of the tail; scales of 1 st row smooth anteriorly, feebly keeled posteriorly.

In a sample of 11 specimens, the dorsal scale row formulas are: 17–17–17 (7 specimens), 18–17–17 (3 specimens) and 19–17–17 (1 specimen).

VEN: 159–177 (plus 1 or 2 preventrals); SC: 90–114, all paired, with a weak sexual dimorphism (males: 103–114; females 90–111); cloacal plate divided.

Ratio VEN/SC 1.47–1.77.

Position of the reduction to 6 scale rows around the tail: SC 8–19, with a sexual dimorphism (males: 15–19 th subcaudal; females: 8–13 th subcaudal); ratio: length of the portion of tail with 6 dorsal scale rows/length of the portion of tail with 4 dorsal scale rows: 0.39–0.55.

Head scalation. Arrangement of upper head scales complete including 2 internasals, 2 prefrontals, 2 supraoculars, 1 frontal, and 2 parietals. Rostral hexagonal, wider than high, well visible from above; nasals more or less rectangular, elongate, vertically divided above and below the nostril by a furrow with the fore and hind parts similar in size, altogether about 1.2–1.6 times longer than high; internasals subtriangular, 1.1–1.2 times longer than wide, abruptly truncated with their anterior margin about 0.7–0.58 times the width of the posterior margin, elongate, in broad contact with each other, shorter than the prefrontal; 2 prefrontals, rather large, wide but short, distinctly broader than long, 1.1–1.3 times longer than internasals; in broad contact with loreal; frontal hexagonal, large, shield-like, 1.1–1.3 times longer than wide and 1.7–1.9 times as long as the prefrontals; on each side 1 supraocular, subtriangular slightly narrower than internasals, 1.6–1.8 longer than wide, about 0.5 times as wide as frontal; parietals long and broad, 1.7–2.1 times longer than frontal, or suture between parietals as great as the frontal length; 1/1 loreal, rectangular, elongate, 1.5–1.8 times longer than high, in broad contact with the nasal; 2 (rarely 1) preoculars on each side, 2 subequal preoculars on each side in all specimens examined by us, 1 or 2 scales in specimens examined by Ren et al. (2018); 2 or rarely 3 small postoculars on each side, upper one largest; 9 (rarely 10) supralabials, 1 st– 5 th SL longer than high, other supralabials as long as high, 1 st– 2 nd SL small and short, 1 st– 3 rd SL in contact with nasal, 2 nd– 3 rd or 3 rd– 4 th SL in large contact with the loreal, 4 th– 6 th or rarely 5 th– 6 th SL entering orbit, 7 th– 8 th supralabials largest; 1 anterior temporal, narrow and elongate, in all known specimens; complete temporal formulas as 1+1 or more rarely 1+2; 9–10 (rarely 8) infralabials, first pair in contact with each other behind the mental, 1 st– 5 th (rarely 1 st– 4 th) IL in contact with anterior chin shields, 5 th IL largest; mental triangular; anterior pair of chin shields equal to or slightly longer than posterior shields.

Coloration and pattern. In preservative, upper dorsal surface and body sides are dark brown, dark chestnut brown or deep blackish-brown, with sides below the 5 th dorsal scale row either variegated with cream or yellow, or with most scales of the 1 st to 4 th scale rows marked with irregular longitudinal streaks, cream, ochre or pale brown (see below in life), reduced to dots posteriorly; a large, elongate, crescentic blotch or smaller, isolated cream, pale yellow or pale orange-brown blotches on the nape; a faint or irregular dorsolateral stripe, yellowish-ochre or pale brown, extending from the neck to vent on the 5 th– 7 th dorsal scale rows, often barely distinct or even absent; on the dorsolateral stripe (when present), a series of cream or yellow, elongate, blotches 2 or 3 scale long; the first four to six blotches behind the neck largest, covering scales of the 5 th– 7 th dorsal scale rows, others progressively narrower and forming a chain of vertically narrow, irregular, strongly elongate blotches then turning into a narrow stripe posteriorly. Dorsal surface of tail is the same than the upper body surface, with a row of dorsolateral blotches of same colour as those of the body.

The head is dark brown or blackish-brown as the body above, irregularly but strongly variegated above with paler brown, yellow or yellowish-ochre; sides of the snout distinctly paler, greyish-brown or greyish- or brownishyellow or brown-ochre; anterior supralabials rather brown, others ochre-yellow or pale brown, more or less strongly edged with dark brown or blackish-brown, last three supralabials ochre-yellow on their lower part, dark brown or blackish-brown on much of their middle, pale above, this pattern forming a lower, dark postocular streak; above, a narrow, oblique, more or less distinct cream, pale ochre-yellow or pale brown postocular streak on anterior and lower posterior temporals and top of the 8 th and 9 th supralabials, reaching the neck behind the corner of the mouth but not connected with the large blotch on the nape. The throat, chin and infralabials are cream or pale yellowishochre, more or less heavily spotted with dark brown spots; infralabials heavily marbled or spotted with dark brown. Eye dark golden brown in life.

The venter is dark brown or blackish-brown, with some paler, more or less faint longitudinal streaks; a more or less conspicuous cream spot or streak on the outer part of each ventral, with dark brown or blackish-brown tips. The under surface of tail has the same colour than the venter.

In life, the colour and pattern are much more vivid, some specimens being especially colourful (see Fig. 9 ); the dorsal background colour is dark greyish-brown, dark reddish-brown, dark brown or blackish-brown; scales of the sides below the 5 th dorsal scale row variegated with yellow or orange, or scales of the 1 st to 4 th scale rows marked with yellow or bright coral-red longitudinal streaks or dots posteriorly; the large crescentic blotch or the smaller blotches on the nape are yellowish-ochre or reddish-brown; the dorsolateral stripe is yellowish-red, rusty-red or reddish-brown; the dorsolateral blotches, anteriorly, and stripe, posteriorly, are vividly and conspiscuously colored in bright yellowish-red, orange or bright rusty-red. Pale markings on the head, the supralabials, the elongate blotch on the temporal region and the streak obliquely directed upwards and backwards on the hinder part of the head and the neck are yellowish-ochre or yellowish-red. Pale areas of the venter are yellowish-ochre.

Hemipenes.—Based on morphological data of the specimen IEBR2908 and Ren et al. (2018), in everted condition the organ is single, short and subcylindrical, not forked, reaching the 5–6 th SC, spinose throughout; spines more or less uniform in size; sulcus spermaticus simple, reaching the tip of the organ.

Sexual dimorphism. — It is expressed in two characters:

(1) Position of the reduction to 6 scale rows around the tail: males: 15–19 th SC; females: 8–13 th SC.

(2) Number of subcaudals: males: 103–114; females 90–111.

Distribution ( Fig. 3 ).— Vietnam. Cao Bang Province. Cao Bang. Hanoi Municipality. Ba Vi National Park. Dien Bien Province. Muong Nhe Nature Reserve, Muong Nhe District. Lao Cai Province. Lao Cai; Hoang Lien National Park, Sa Pa District; Bat Xat Nature Reserve, Bat Xat District. Son La Province. Copia Nature Reserve, Thuan Chau Dsitrict; Sop Cop Nature Reserve, Sop Cop District. Thanh Hoa Province. Xuan Lien, Thuong Xuan District. Yen Bai Province. Mu Cang Chai Species and Habitat Conservation Area, Che Tao Commune ( Le et al. 2018).— Laos. Houaphan Province. Phou Louey National Protected Area, Viengthong District. Louangphabang Province. Hoay Tala, Phoukhoume District. Xaisomboun Province. Longcheng District (T. V. Nguyen et al. 2020).— People’s Republic of China. Yunnan Province. Daweishan National Nature Reserve, Pingbian Miao Autonomous County, Honghe Hani, Yi Autonomous Prefecture, and Jinhong Prefecture. This distribution includes data from Ren et al. (2018; pers. comm., June 2020).

Biology.—This species inhabits regions covered with tropical and subtropical evergreen montane forests between 900 and 2,046 m a.s.l. ( Ren et al. 2018). All specimens for which data are available were collected in montane, wet evergreen forests and in close association with forest streams. This species is nocturnal and both semiaquatic and terrestrial; no specimen was collected at more than a few meters from water. One specimen from Laos was swimming in submerged vegetation along the bank of a 3 meter wide stream with moderate current; another specimen was seen perched on a tree at 1 meter from a stream. A specimen observed by Ren et al. (2018) was actively preying upon tadpoles of a treefrog species ( Rhacophorus duboisi ) on the edge of a pool. Other data of the biology of Hebius chapaensis , such as reproductive habits, are still unknown. Specimens from Laos did not prove to be aggressive when handled.

Figures

FIGURE 2. Hebius venningi Wall, alive—A & C: specimen from Changlang District, Arunachal Pradesh, India. Photographs: Ashok Captain.—B: specimen CAS 233206, Chun Kyone, Hakha Township, Hakha District, Chin State, Myanmar. Photograph: Hla Tun.

FIGURE 3. Distribution map of species with 15 or 17 dorsal scale rows at midbody. Circles: Hebius annamensis Bourret. Diamonds: Hebius venningi Wall. Inverted triangles: Hebius taronensis Smith. Squares: Hebius nigriventer Wall. Triangles: Hebius chapaensis Bourret.

FIGURE 8. Hebius chapaensis Bourret, holotype (MNHN 1938.0125)—A: dorsal view; B: lateral view of the head, right side. Photographs: Patrick David.

FIGURE 9. Hebius chapaensis Bourret, alive—A: specimen from Yen Bai Province, Vietnam. Photograph: Nikolai Orlov. B: specimen from Thanh Hoa Province. Photograph: Truong Quang Nguyen. C: specimen from Tuyen Quang Province. Photograph: Truong Quang Nguyen.