Hebius annamensis (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 : 29-35

5. Hebius annamensis (Bourret, 1934)

( Figs. 10–11 )

Parahelicops annamensis Bourret, 1934c: 167 (Separate: p. 3) & 170 (Separate: p. 6), Fig. 2 .—

Type locality. “Bana, station d’altitude située à 1 500 m d’altitude au bord de la Baie de Tourane”, now Ba Na Nature Reserve , Da Nang City, Vietnam, 1,500 m a.s.l.— Holotype. MNHN 1938.0117 , adult male (Muséum National d’Histoire Naturelle, Paris, France); collected and deposited by René Bourret in 1934.

Parahelicops annamensis .— Bourret 1936a: 97, 104, 114 & 125; Bourret 1936b: 122, Fig. 50; Bourret 1939b: 54; Taylor & Elbel 1958: 1158; Campden-Main 1970: 46, Fig.; Welch 1988: 88; Nguyen & Ho 1996: 98; Orlov et al. 1998: 61 & 63; Le 2000: 161; Iskandar & Colijn 2001: 102; Orlov et al. 2003: 232; Nguyen et al. 2005a: 93; Stuart 2006: 167–171; Stuart & Chuaynkern 2007: 35 (implicitely, only generic name cited); Murphy et al. 2008: 180; Stuart & Heatwole 2008: 97; Ziegler et al. 2008: 197, 200, 201; Nguyen et al. 2009: 362; Das 2010: Plate 51 (p. 118), 296; Yang et al. 2011: 62, 65–67; Stuart & Nguyen 2012a: e.T192102A2040117; Teynié et al. 2013: 166, 167, 169, 178 & 182; Wallach et al. 2014: 520; David et al. 2015b: 203–205, 209–213; Kizirian et al. 2018: 1–3; Ren et al. 2018 (implicitely, only generic name cited): 37, 46 (Table 5), 47 & 51.

Opisthotropis annamensis .— Smith 1943: 331 & 334; Bain & Hurley 2011: 104 & 128.

Amphiesma annamense .— Teynié et al. 2013: 178 (generic allocation in error).

Hebius annamensis .— Kizirian et al. 2018: 5; Boundy 2020: 91.

Specimens examined (16).— Vietnam. Da Nang City. MNHN 1938.0117 (holotype of Parahelicops annamensis ), “Bana”, now Ba Na Nature Reserve , elev. 1,500 m ; ZISP NLO-2831, Ba Na Nature Reserve , elev. 1,400 m. Ha Tinh Province. AMNH 147129, Po Mu forest, Rao An, Huong Son District (18°20’26”N 105°14’13”E, 870 m); ZISP NLO-2478, Rao An, Huong Son District , elev. 300 m. Kon Tum Province. IEBR 371, ZISP NLO-3435, Mang Canh village (14°41’950N, 108°14’642E), Kon Plong District , elev. 1,200 –1,250 m. Quang Binh Province. IEBR 4580 (Field number QB.2015.377), Dong Chau Forest , 16°58.104’N, 106°35.579’E, elevation 696 m, Lê Thuy District; ZFMK 86457, ZISP NLO-2714, Phong Nha - Ke Bang National Park , 17°42.654’N, 105°52.708’E, elev. 527 m, Hoa Son Commune, Minh Hoa District . Quang Tri Province. ZISP NLO-3257, Ban Cup, Huong Hoa District , 16°57.434’N, 106°35.329’E, elev. 490 m a.s.l. Thua Thien-Hue Province. ZFMK 83513, Bach Ma National Park; ZISP NLO-2790, Bach Ma National Park , elev. 1,350 m .— Laos. Champasak Province. NCSM 77919. Houay Tad Seua stream, Dong Hua Sao NPA, Pakxong District , 1,245 m a.s.l. Xékong Province. FMNH 258637, Xe Sap National Biodiversity Conservation Area, 16°04’10’’N, 106°58’45”E, Kaleum District , elev. 1,280–1,500 m ; NCSM 78630, Phou Ajol, 15.68239°N, 107°1942°E, Dakchung District , elev. 1,475 m ; NCSM 78632, Phou Ajol, 15.68516°N, 107°1981°E, Dakchung District , elev. 1,450 m .

Taxonomic comments. — Bourret (1934c) erected the genus Parahelicops for the sole included species Parahelicops annamensis Bourret, 1934 , described in the same paper from a single specimen, on the basis of the following characters: 25 subequal maxillary teeth, of which the two last ones are enlarged, a small eye with a round pupil, nostrils directed upwards, and a single prefrontal; other characters included a head distinct from the neck, 2 internasals, body elongate, slightly laterally compressed, dorsal scales keeled, without apical pits, in 15 rows, tail long, subcaudals paired and hypapophyses developped throughout the vertebral column. The position of the genus Parahelicops has long been controversial ( David et al. 2015b). Bourret (1934c) stated that this genus was similar to members of the genus Opisthotropis G̹nther, 1872 but differed by its dentition, its head clearly distinct from the neck and its more elongate body.

Smith (1943: 334), although recognizing the validity of the characters on which Bourret (1934c) based his description, synonymized Parahelicops with the genus Opisthotropis in extending the definition of this latter one. In contrast, Taylor & Elbel (1958: 1156) accepted the validity of Parahelicops on the basis of Bourret’s characters and placed in this latter genus a new species from north-eastern Thailand, Parahelicops boonsongi . David et al. (2015b) showed that this species is obviously not congeneric either with P. annamensis , or with any other natricid genera. As a consequence, P. boonsongi was referred to the new genus Isanophis David, Pauwels, Nguyen & Vogel, 2015 .

Stuart (2006), although recognizing the validity of the genus Parahelicops , also suggested a close relationship with Opisthotropis . In contrast, David et al. (2015b), on the basis of morphological characters, considered the genus Parahelicops to be valid and distinct from Opisthotropis . Although “ Parahelicops ” annamensis has usually a single prefrontal, as in most species of Opisthotropis , it differs from the latter genus, as defined by Boulenger (1893a), Pope (1935), Smith (1943), Bourret (1936b) and Brown & Leviton (1961), by several morphological characters such as (1) 2 distinctly enlarged maxillary teeth vs. subequal teeth in Opisthotropis , (2) dorsolateral nostrils vs. directed distinctly upwards in Opisthotropis , and (3) supralabials longer than high vs. distinctly higher than long in Opisthotropis . In contrast, some characters of the genus Parahelicops , i.e., the dentition of the upper maxilla, made of subequal small teeth followed by two enlarged posterior teeth, the average 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, were obviously typical of the genus Hebius as defined by Guo et al. (2014), and especially the “ H. modestus species group”, the group of Indo-Himalayan species which is treated in the present paper. Eventually, Kizirian et al. (2018), on the basis of molecular data, showed that Parahelicops annamensis was nested in the genus Hebius and a synonym thereof. We here follow these authors in referring Parahelicops annamensis to the genus Hebius .

For long, Hebius annamensis has been known from its sole holotype collected in central Vietnam. The second known specimen, and first record from Laos, was described by Stuart (2006). Subsequently, more specimens became available, especially from central Vietnam. David et al. (2015b), in the genus Parahelicops , expanded the description of H. annamensis . This species is monotypic.

Diagnosis.—A moderately sized species of the genus Hebius characterized by the combination of (1) body elongate in males and females; (2) head distinct from the neck; (3) 15 or 17 dorsal scale rows at midbody, moderately keeled at midbody, strongly keeled posteriorly, usually smooth on the 1 st dorsal scale row; (4) scales around the base of the tail very strongly keeled; (5) eye moderate with a round pupil, 1.2–1.4 times the distance between the lower margins of eye and of lip; (6) maxillary teeth 28–34, progressively increasing in size in a continuous series, the last two moderately enlarged and not separated by a diastema from anterior teeth; (7) nostrils piercing dorsolaterally; (8) tail long with a ratio Tal/TL equal to 0.30 and above; (9) VEN 158–172; (10) SC 116–146; (11) internasals distinctly narrowing anteriorly; (12) prefrontal single in most known specimens, (13) 8 or 9 supralabials; (14) 1 anterior temporal, (15) venter pale on its inner three quarters, with tips of ventral scales very dark; (16) background colour chestnut brown, dark brown or dark greyish-brown; (17) dorsal pattern made of isolate, cream or yellowish-ochre blotches (bright orange or rusty-red blotches in life), usually transversally elongate as crossbars anteriorly, then becoming irregular, broken spots posteriorly; (18) a short and narrow, oblique postocular streak reaching the neck behind the corner of the mouth, sometimes extending on the nape as a broad, oblique and elongate cream or yellowish-ochre streak (orange or rusty-red in life); and (19) supralabials dark as the upper head surface, without defined spots or blotches.

Comparison. In preservative, specimens of Hebius annamensis may be easily misidentified as H. modestus (G̹nther, 1875), an Indo-Himalayan species unknown east of Myanmar. However, H. modestus has 19 scale rows at midbody vs. 17, 143–163 ventrals vs. 158–172, and a ochre or pale brown venter.

With its typical dorsal and ventral pattern and its long tail, Hebius annamensis cannot be confused with any species of the genus Hebius with 17 dorsal scale rows, from which it differs as follows:

Hebius annamensis readily differs from H. chapaensis by the characters given above in the account of this latter species. The main characters are (1) internasals distinctly narrowing anteriorly (vs. abruptly truncated); (2) number of subcaudals, 116–146 vs. 90–114 subcaudals in H. chapaensis ; (3) venter largely pale, with only tips of ventral scales dark vs. nearly entirely dark in H. chapaensis ; (4) a distinct dorsal pattern, consisting of pales blotches, usually arranged as crossbars anteriorly in H. annamensis vs. bright, pale blotches on a faint dorsolateral stripe in H. chapaensis ; and (5) head with short and narrow postocular streak in H. annamensis , as well as with dark supralabials, without defined blotches vs. strong postocular streak in H. chapaensis , with pale supralabials, edged with dark, or divided into a pale and a dark areas.

Hebius annamensis differs from both H. taronensis and H. nigriventer by its venter largely pale vs. entirely black or so in these species, plus by characters given in the key above.

Hebius annamensis differs from H. venningi especially by (1) a prefrontal usually single vs. always double; (2) the number of postoculars, 2 (rarely 3) in H. annamensis vs. usually 3 (rarely 2) in H. venningi ; (3) venter largely pale, with only tips of ventral scales dark 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 ; (4) dorsal pattern made of isolate, bright orange or rusty-red blotches, usually horizontally elongate or vertically elongate as crossbars anteriorly vs. dorsal surface distinctly chequered by the presence on sides and upper part of the body of diffuse blackish-brown or very dark grey blotches, and with a dorsolateral series of irregular blotches, yellow-ochre or yellowish-brown (bright yellowish-ochre in life), enlarged and forming a chain on the first quarter to third of the body; (5) the distribution range, Vietnam and southern Laos vs. Northeast India and North Myanmar for H. venningi .

Description.—Body moderately robust but elongate, somewhat thinner in males, and cylindrical; head oval, rather short, moderately distinct from the thick neck, flattened anteriorly; snout long, flat, blunt or slightly round seen from above, subrectangular seen in profile, 2.0–2.2 times as long as horizontal diameter of eye; no canthus rostralis; nostril directed dorsolaterally, small, round, piercing in the middle of the divided nasal; eye moderately sized or small, its diameter about 1.2–1.4 times the distance between the lower margins of eye and of lip, with a round pupil; tail long, thin and tapering.

The maximum known length is 796 mm for a male (SVL 528 mm, TaL 268 mm; specimen ZISP NLO 3257). The longest known female is 685 mm long (SVL 465 mm, TaL 220 mm; ZISP NLO 2831).

Ratio TaL/TL 0.297 –0.337, without clear sexual dimorphism (6 males: 0.301 –0.337; 3 females: 0.297 –0.321).

Dentition. 28–34 maxillary teeth, gradually enlarging in a continuous series, the last 2 teeth moderately enlarged, without diastema.

Body scalation. DSR: 17–19-15–17-15–17 rows; scales rhomboedric, normal in shape, distinctly 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 on 1 st row smooth anteriorly, feebly keeled posteriorly.

The number of dorsal scale rows is quite variable in this species. In our sample of 15 specimens, the dorsal scale row formulas are: 18–15–15 (1 specimen), 19–15–15 (4), 17–17–17 (1), 18–17–15 (2), 18–17–17 (2), and 19–17–17 (5).

VEN: 158–172 (plus 1 or 2 preventrals), with a sexual dimorphism (see below); SC: 116–146, all paired, with a sexual dimorphism; cloacal plate divided.

Ratio VEN/SC 1.18–1.44.

Position of the reduction to 6 scale rows around the tail: SC 4–16, with a strong sexual dimorphism (see below); ratio: length of the portion of tail with 6 dorsal scale rows/length of the portion of tail with 4 dorsal scale rows: 0.10–0.64.

Head scalation. Arrangement of upper head scales complete but prefrontals modified, including 2 internasals, 1 or 2 prefrontals (see below), 2 supraoculars, 1 frontal, and 2 parietals. Rostral hexagonal, wider than high, barely visible from above; nasal subrectangular, elongate, vertically divided by a furrow, with the fore and hind parts of similar size, altogether about 1.3–1.5 times longer than high; internasals distinctly subtriangular, elongate, in broad contact with each other, 1.2–1.4 times longer than wide, distinctly narrowing anteriorly with anterior margin about 0.4–0.5 times the width of the posterior margin; 1 prefrontal (in 12/ 15 specimens), shield-like and broad, or 2 prefrontals (3/15), subrectangular, in both cases broader than long and 0.9–1.2 times as long as internasals, in broad contact with loreal; frontal hexagonal, shield-like, rather wide but short, its apex directed posteriorly, 1.0–1.2 times longer than wide, 1.7–2.0 times longer than prefrontals; on each side 1 entire, subtriangular supraocular, rather broad, 1.8–2.2 times longer than wide, slightly narrower than internasals, about 0.5 times as wide as frontal; parietals large, long and wide, 1.7–2.1 times longer than frontal and in contact for a length 1.2 times as long as the frontal length; large, rectangular loreal scale, elongate, 1.5–1.8 times longer than high, in broad contact with the nasal; 2 subequal preoculars on each side in all examined specimens; 2 or rarely 3 small postoculars, the upper one largest; 8 or 9 supralabials, 1 st as long as high, 2 nd– 5 th longer than high, other supralabials as long as high, 1 st– 2 nd supralabials, small and short or, exceptionally 1 st– 3 rd supralabials, in contact with nasal, 2 nd– 3 rd or 3 rd– 4 th supralabials in large contact with the loreal, 4 th– 5 th supralabials, or exceptionally solely 4 th, solely 5 th, 4 th– 6 th or 5 th– 6 th supralabials, entering orbit; 6 th– 7 th or 7 th– 8 th supralabials largest; 1 anterior temporal, narrow and elongate, in all known specimens with complete temporal formulas as 1+1+2 or rarely 1+2+2 or 1+3 (this latter condition only in the type); 10 (rarely 8 or 9) infralabials, 1 st pair in contact with each other behind the mental, 1 st– 5 th infralabials in contact with anterior chin shields, 5 th infralabial largest; mental triangular; anterior pair of chin shields equal to or slightly longer than posterior shields.

Coloration and pattern. In preservative, the dorsal and lateral surfaces of body are dark chestnut brown, dark brown or dark greyish-brown, darker above than on the sides, either nearly uniform or, more usually, profusely variegated with diffuse, darker brown blotches, larger on the upper parts of the sides than on the vertebral region; scales of the lower lateral scale rows usually spotted or marked with diffuse, yellowish-grey blotches or streaks; in 3 out of 13 specimens, a faint dorsolateral stripe is present on 5 th– 7 th dorsal rows, barely paler than the background color and poorly distinct; on each side, a series of about 50 to 70 distinct dorsolateral blotches, cream, ochre, yellowishbrown, pinkish-brown or orange-brown on 5 th– 7 th dorsal rows, separated from each other by 2–3 dorsal scales, forming a discontinuous dorsolateral stripe; the first few blotches are usually vertically elongate and form a few vertical crossbars extending outwards and reaching downwards the level of the 3 rd scale row on the anteriormost part of the body, quickly followed by thick and horizontally elongate blotches extending up to the first anterior quarter to third of the body; progressively these blotches are reduced to irregular or broken spots or even disappear posteriorly; a short, cream ventrolateral stripe on the anterior part of the body, up to 20 th to 30 th ventrals. The upper surface of tail is as the body, either uniform or with only a few pale dots.

The head is dark chestnut-brown, more or less variegated above with ochre yellow or pale yellowish-brown, often with numerous minute scattered dark dots; a ochre yellow or pale yellowish-brown sagittal line present, but faint, or absent; last three posterior supralabials irregularly and faintly edged with ochre-yellow anteriorly; a short, narrow or relatively broad, oblique, more or less distinct postocular streak on anterior and lower posterior temporals, and on top of 8 th and 9 th supralabials, reaching the neck behind the corner of the mouth and extending as a large, cream or yellowish-ochre oblique, elongate blotch on the nape, connecting the posterior end of the postocular streak with the first dorsolateral blotch. The throat, chin and infralabials are cream or pale yellowish-ochre, more or less heavily spotted with dark brown spots; infralabials heavily marbled or spotted with dark brown. Eye deep black in life.

The venter is cream, pale yellowish-ochre or pale brown on the inner half to two thirds of its width, with tips of ventrals dark brown or dark greyish-brown, this dark surface progressively widening posteriorly; often some irregular dark spots scattered on the pale part. The under surface of tail is as the venter but the pale central part is narrower than the dark, outer parts anteriorly, the tail becoming progressively entirely dark below.

In life, the background coloration is chestnut-brown, dark olive-brown or dark brown, more or less iridescent; the upper dorsal dark blotches are blackish-brown or very dark grey whereas the lower lateral scale rows are marked with yellowish-ochre blotches or streaks; when present, the dorsal stripe is rusty-brown; the main dorsolateral blotches are yellowish-ochre, orange or reddish-brown, a colour often still seen in recently preserved specimens; the short ventrolateral stripe is pale yellowish-ochre. Pale markings on the head are yellowish-ochre or dirty, greyish-yellow; the elongate blotch on the temporal region and on the hinder part of the head is yellowish-ochre or sometimes reddish-ochre; behind the head, the streak obliquely directed upwards and backwards on the neck is of the same colour or turns to bright orange or yellowish-red. The background colour of the throat and venter is cream or pale yellowish-grey.

Hemipenes.—In situ, the organ is single, short and subcylindrical, not forked, reaching the 10 th SC, spinose throughout.

Sexual dimorphism. — It is expressed in three characters:

(1) by the difference in the number of ventrals: males: 168–172 (mean = 167.7, s = 1.7); females: 158–167 (mean = 164.2, SD = 3.4).

(2) by the difference in the number of subcaudals: males: 126–146 (mean = 138.7, s = 6.9); females: 116–126 (mean = 119.7, SD = 5.5).

(3) by the position of the reduction to 6 scale rows around the tail: males: 12–16 th SC; females: 4–7 th SC.

Distribution ( Fig. 3 ).—This species has been recorded only from central Vietnam and southern Laos. Vietnam. Da Nang City. Ba Na Nature Reserve. Ha Tinh Province. Huong Son District. Kon Tum Province. Ngoc Linh Nature Reserve, Kon Plong District. Quang Binh Province. Dong Chau Forest, Lê Thuy District; Phong Nha - Ke Bang National Park, Minh Hoa District. Quang Tri Province. Huong Hoa District. Thua Thien-Hue Province. Bach Ma National Park— Laos. Champasak Province. Dong Hua Sao National Biodiversity Conservation Area, Pakxong District. Xékong Province. Sap National Biodiversity Conservation Area, Kaleum District; Dakchung District.

Biology.—This species inhabits regions covered with tropical wet evergreen forest and subtropical montane evergreen forests between about 300 and 1,500 m a.s.l., although most specimens for which elevation data are available were collected between 1,200 and 1,400 m a.s.l. (see also Stuart & Nguyen 2012a). All were collected in primary montane evergreen forests and in close association with fast-running, rocky forest streams.

This species seems to be mainly nocturnal and aquatic, although one specimen was found on the ground. According to Stuart (2006), specimen FMNH 258637 was collected at night (20.30 h) in steep terrain covered by wet evergreen forest between 1,280 –1,500 m elevation. The snake was first observed on land 50 cm from a small, swift, rocky stream, then it dove into the water and swam under a rock on the stream bottom. Specimen ZFMK 86457 was captured at night (20.00–21.00h) in the leaf litter of a forest stream at 510 m a.s.l., with only the snout tip protruding from the surface of the water ( David et al. 2015b). Other biological data of Hebius annamensis , such as its diet and reproductive habits, are still unknown.

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 10. Hebius annamensis Bourret, holotype (MNHN 1938.0117)—A: dorsal view; B: lateral view of the head, right side. Photographs: Patrick David.

FIGURE 11. Hebius annamensis Bourret, alive—A: specimen from Quang Tri Province, Vietnam. Photograph: Nikolai Orlov. B: specimen from Quang Binh Province. Photograph: Nikolai Orlov. C: specimen from Kon Tum Province. Photograph: Truong Quang Nguyen.