Trimeresurus tenasserimensis, Idiiatullina & Nguyen & Pawangkhanant & Suwannapoom & Chanhome & Mirza & David & Vogel & Poyarkov, 2024

Idiiatullina, Sabira S., Nguyen, Tan Van, Pawangkhanant, Parinya, Suwannapoom, Chatmongkon, Chanhome, Lawan, Mirza, Zeeshan A., David, Patrick, Vogel, Gernot & Poyarkov, Nikolay A., 2024, An integrative taxonomic revision of the Trimeresurus popeiorum group of pitvipers (Reptilia: Serpentes: Viperidae) with descriptions of two new species from the Indo-Burma Biodiversity Hotspot, Vertebrate Zoology 74, pp. 303-342 : 303

Trimeresurus tenasserimensis sp. nov.

Figs 10 , 11; Tables 3, 4

Trimeresurus Chresonymy.

Trimeresurus gramineus (non Coluber gramineus Shaw, 1802) - Pope and Pope (1933: 9, in part).

Trimeresurus popeiorum (non Trimeresurus popeiorum Smith, 1937) - Smith (1943: 518-519, in part); Nabhitabhata (2000: 142, in part); Gumprecht (2001: 20-30, in part), Leviton et al. (2003: 446-447, in part); Malhotra and Thorpe (2004: 97, in part); Vogel et al. (2004: 19, in part); Sanders et al. (2004: 183-184, in part); Castoe and Parkinson (2006: 105, in part); Sanders et al. (2006: 361, in part); Leviton et al (2008: 80-81, in part); Das (2010: 307, in part); Malhotra et al. (2010: 175, in part); Chanhome et al. (2011: 325-326, in part); Chuaynkern and Chuaynkern (2012: 148, in part); Wallach et al. (2014: 575-576, in part); Chan-ard et al. (2015: 345-346 in part); Zug and Mulcahy (2020: 164); Poyarkov et al. (2023: 392, in part), Uetz et al. (2024, page " Trimeresurus popeiorum ", in part).

Trimeresurus popeiorum popeiorum - Regenass and Kramer (1981: 186-187, in part).

Trimeresurus sp. nov. - Mulcahy et al. (2017: 310-311).

Trimeresurus cf. popeiorum - Platt et al. (2018: 93).

Popeia sp. 2 - Mirza et al. (2023: 94).

Trimeresurus stejnegeri (non Trimeresurus stejnegeri Schmidt, 1925) - Leviton et al. (2003: 448, in part).

Viridovipera stejnegeri - Leviton et al. (2008: 91-92, in part).

Popeia fucata (non Trimeresurus fucatus Vogel, David & Pauwels, 2004, now Trimeresurus sabahi fucatus ) - Leviton et al. (2008: 78-79, in part), Pauwels and Chan-ard (2006: 100, 103), Pauwels et al. (2009: 14).

Trimeresurus cf. popeiorum 2 - Idiiatullina et al. (2023: 701); Idiiatullina et al. (2024: 17).

Holotype.

ZMMU Re-17668 (adult male) from Suan Phueng District, Ratchaburi Province, Thailand (13.55358°N, 99.20528°E; elevation 640 m) collected by P. Pawangkhanant on 7 June 2019.

Paratypes

(n = 4). Thailand. ZMMU Re-17671 (adult female) collected on 3 June 2019, same information than the holotype. - Myanmar. Tanintharyi Region: NHMUK 1924.5.20.38 (adult male) from Paya Taung Mt., Dawei City; CAS 247870 (adult male) and CAS 247754 (adult female) from Kawthaung District.

Referred specimens

(n = 5). Thailand. ZMMU Re-17672 (subadult male) and ZMMU Re-17670 (subadult female) collected on 3 June 2019, ZMMU Re-17673 (subadult male) collected on 17 July 2019, all same information with holotype. - Myanmar. Taninthayi Region: NHMUK 1856.5.6.105 from Myeik Is., Myeik District; NHMUK 1940.3.9.43 (adult male) from Kisseraing Is, Myeik District.

Referred materials from the literature

(n = 4). Myanmar. Tanintharyi Region: USNM 587920 (subadult female), USNM 587921 (adult male) from Kawthaung District; USNM 587588 (adult female) Lenya Area; and USNM 587919 (adult female) from Ywahilu Village (see detail from Mulcahy et al. 2017).

Etymology.

The species name " tenasserimensis " is a modern Latin toponymical adjective in nominative singular, adopting the masculine gender of the genus name Trimeresurus, combining the name of the Tenasserim Mountain Range in western Thailand and southeastern Myanmar, where the new species occurs, and the Latin suffix - ensis (- is, - e), meaning “from”. The species nomen therefore means "from Tenasserim". We suggest the following common names for the new species: "Ngu Khiew Hang Mai Thong Khiew Tanao Sri" (งูเขียวหางไหม้ท้องเขียวตะนาวศรี) (in Thai), “Dān nà shā lín zhú yè qīng” (丹那沙林竹叶青) (in Chinese), "Tenasserim green pitviper" (in English), "Tenasserim Bambusotter" (in German), “Trimérésure vert du Tenasserim" (In French) and "Tenasserimskaya bambukovaya kufiya" (in Russian).

Diagnosis.

Trimeresurus tenasserimensis differs from other members of the subgenus Trimesurus Popeia by the combination of the following morphological characters: (1) dorsal surfaces deep green, with faint dark, interstitial crossbands; (2) in males, a wide, bicolored ventrolateral stripe, bright red ventrally, white dorsally; in females, ventrolateral stripe thin, pale yellow anteriorly, whitish posteriorly; (3) in males, a conspicuous, bicolored postocular streak, white and thin ventrally, broad and bright red dorsally, covering two or three temporal scales; in females, streak absent or only white; (4) eyes red to deep red in both males and females; (5) 21 dorsal scales rows at midbody, strongly keeled except those of the first dorsal scale row, always smooth; (6) 159-176 ventrals (159-170 in males, 154-176 in females); 57-74 subcaudals with slightly overlapping sexual dimorphism (66-74 in males, 57-66 in females), all paired; (7) first supralabial entirely separated from the nasal scale by a distinct suture; (8) supraoculars relatively narrow, narrower than internasals, separated by 9-11 cephalic scales; (9) internasals not in contact, separated by one scale; (10) 10-11 cephalic scales between the supraoculars in both sexes; (11) relative tail length 0.20-0.23 in males, 0.14-0.16 in females.

Description of the holotype

(Fig. 10A-F ). Adult male, specimen in a good state of preservation. Especially, it had still retained its color in life at the time of writing this paper.

Morphology.

Body cylindrical, long, and laterally compressed (SVL 502 mm, TaL 127 mm, TL 629 mm, TaL/TL 0.202). Head triangular in dorsal view, elongate, clearly distinct from the neck (HL 30.2 mm, HL/SVL 0.06), snout elongate, flattened and rounded when seen from above, rather rectangular when seen from lateral side, with a very distinct and sharp canthus rostralis; loreal pit present, triangular in shape. Eye average (ED 3.3 mm, SnL 8.4 mm, ED/SnL 0.39); pupil vertically elliptic.

Body scalation.

Dorsal scales in 21-21-15 rows; dorsal scales all moderately keeled, except the first row of which scales are smooth; 160 ventrals (plus two preventrals); cloacal plate single; 66 subcaudals, all divided.

Head scalation.

Rostral slightly visible from above, triangular; one internasal on each side, pentagonal, distinctly transversely elongate, internasals separated by one small scale behind the top of rostral (Fig. 10E ); nostril completely included in nasal scale, pentagonal, entire, elongate, as long as high; nasal scale completely separated from the first supralabial; one small scale between nasal and the second supralabial; scales on the upper snout surface and in the interorbital region smooth, irregular, barely imbricate; 4/4 canthal scales, slightly larger than adjacent snout scales, bordering the canthus rostralis between the internasal and corresponding supraocular; temporal and occipital scales distinctly but obtusely keeled; one relatively large triangular loreal between the upper preocular and the nasal; two elongate upper preoculars above loreal pit, lower one bordering the upper margin of loreal pit, upper one visible from above, both elongate and in contact with loreal; lower preocular forming lower margin of loreal pit (Fig. 10C, D ); one supraocular on each side, long, much longer than wide, 0.7/0.8 times as wide as the internasals; cephalic scales relatively small, irregular or slightly rounded, juxtaposed, flat and smooth; ten irregular cephalic scales between the supraoculars; one long, thin, crescent-like subocular scale; occipital scales rhombohedral, distinctly but obtusely keeled (Fig. 10E ); 2/2 small postoculars; 10/11 supralabials, first supralabial short, entirely separated from the nasal by a distinct suture; second supralabial tall, forming the anterior border of loreal pit; third supralabial largest and in contact with the subocular on each side; fourth and fifth supralabials, much lower than the third one, separated from the subocular by one scale on each side (Fig. 10C, D ); 13/12 infralabials, those of the first pair in contact with each other behind the mental, the first three pairs in contact with the single pair of chin shields. Five pairs of gulars aligned between the chin shields and the first preventral (Fig. 10F ).

Coloration in life

(Fig. 10A-F ). The body is uniform bright grass-green, with faint darker areas forming crossbands due to the darker interstitial skin; a conspicuous, bicolored ventrolateral stripe extends from the beginning of the neck to the vent, bright deep red ventrally, this color covering a large part of the scales of the first dorsal scale row except their upper posterior corner or half that is white, and dorsally white on the lower half of scales of the second row; the large white areas on the red first dorsal scale row makes this ventrolateral stripe seeming red alternately with white; elongate white dots, faint, one scale long, widely spaced on scales of the vertebral row, more visible anteriorly. The tail is bright green like the dorsum, ornate above and on its sides by about 15, distinct large blotches crossing the vertebral line of the tail, hexagonal or subrectangular, bright rusty-red, extending downwards to the mid-height of the sides, in contact each with the other on the vertebral row, progressively fused posteriorly as an irregular stripe; the ventrolateral stripe of the body extends at least up to half of the tail length before vanishing as red blotches; near its end, the dorsal surface of the tail is irregularly mottled with rusty-red.

The dorsal surface of the head and the temporal region are bright grass-green like the body; the side of the head below the eye, i.e., the sides of the snout, nasal scale, anterior supralabials and lower temporals, is paler green than the dorsal surface of the head; a broad, bicolored postocular streak, its ventral part narrow and white, covering the lower part of the second row and, posteriorly, the first lower row of temporals, its upper part, broader, covering the second and third rows of temporals, bright rusty-red, extends from the postoculars obliquely towards the angle of the mouth; the postocular streak does not connect with the ventrolateral stripe. The chin and throat are uniform pale green. The eye is deep brownish-red.

The venter is uniform pale green; tips of ventrals of the same green color, not red. The ventral surface of the tail is as the venter anteriorly, with the bright red ventrolateral stripe on each side, becoming greenish-grey near its tip with reddish-brown dots but not completely reddish-brown.

Variation

(see also Table S3). The longest-known specimen is 736 mm long (SVL 587 mm, TaL 149 mm; male, CAS 247870). The longest-known female is 532 mm long (SVL 452 mm, TaL 80 mm; USNM 587919). The body is quite slender in males, more robust in large females, laterally compressed; head triangular, elongate, wide posteriorly, flattened in males, moderately thick in females, clearly distinct from the neck; snout elongate, distinctly flattened, rounded seen from above, angular and obliquely truncated in profile view, with a distinct canthus rostralis; nostril centered in the nasal scale; size of the eye average, 0.7-0.9 times the distance between the lower margin of the eye and the border of the upper lip; tail average to long, progressively tapering and distinctly prehensile; TaL/TL 0.177-0.230 in males, 0.136-0.161 in females.

Body scalation.

Generally 23-21-15 dorsal scale rows (50%), less frequently 21-21-15 (30%) or 22-21-15 (20%) dorsal scale rows; 154-176 distinctly keeled ventrals (159-170 in males, 154-176 in females); scales of the first dorsal scale row smooth and not enlarged; subcaudals sexually dimorphic with slight overlap, 66-74 in males, 57-66 in females; total number of VEN+SC: 222-242; cloacal plate entire.

Head scalation.

The head scalation is as described for the holotype, with the following variation: internasals separated by one small scale in all examined specimens; four or five canthal scales bordering the canthus rostralis between the internasal and corresponding supraocular; one supraocular on each side, entire and rather narrow, about 0.7-0.9 times as wide as the internasals, indented on its inner margin by the upper head scales; cephalic scales juxtaposed, flat and smooth; 9-14 (10-11 in most examined specimens) cephalic scales on a line between supraoculars; occipital scales rhombohedral, distinctly obtusely keeled in males, weakly keeled or even smooth in females; temporals generally moderately but distinctly keeled in most males (71.5%), sometimes smooth (28.6%); smooth in all examined females; 9-11 supralabials; third supralabial the longest and highest, rather tall, in contact with the subocular or separated from this latter scale by one scale; fourth supralabial separated from the subocular by one scale in all examined specimens; fifth supralabial smaller than the fourth one, separated from the subocular by one or two scales of similar size; 11-14 (generally 12 or 13) infralabials, those of the first pair in contact with each other.

Coloration and pattern

(Figs 10 - 11 ). In life or in freshly preserved animals, the body is uniform bright green, grass-green or emerald-green (in preservative, the general background color remains green or turns to bluish-green or brown); dark, transversal interstitial crossbands faint in males, absent in females; white, elongate vertebral dots present in males; in males, the broad, bicolored ventrolateral stripe is as described above, bright red or fire-red on its lower part, on most scales of the first dorsal scale rows, white above, on scales of the second dorsal scale row and on the upper posterior part of scales of the first row, always present and conspicuous; in females, the ventrolateral stripe is absent (83.3%) or sometimes present as thin white line (16.7%). The tail is of the same green color than the dorsum, with above and on the sides a series of 15-25 large, bright rusty-red blotches, subrectangular or hexagonal, crossing the vertebral line of the tail, either distinct throughout the tail or progressively fused together posteriorly as an irregular stripe.

The dorsal surface of the head and the temporal region are uniform bright green or deep green like the body; the sides of the head below the eye, are more or less distinctly paler than the dorsal surface of the head, namely usually pale yellowish-green or pale green; in males, the vivid, broad, bicolored postocular streak associating a thin and white ventral part with a broad and bright red, rusty-red dorsal part, is always present (Fig. 10C, D, G, H ); in females, the postocular streak is usually absent or present as a thin, faint white line. The chin and throat are pale yellowish-green or pale sea-green, uniform or with some darker green areas. The eye is bright red, fire-red, or deep red in specimens of both sexes.

The venter is uniformly pale green or pale yellowish-green; tips of ventrals usually green like the venter but we saw a male, especially colorful, in which the bright red part of the ventrolateral stripe also extended onto the outer parts of ventral plates. The ventral surface of the tail is like the venter with the tips of the red dorsal blotches extending onto the outer parts of some subcaudal scales; posterior part of the tail mixed rusty-red and green.

Comparisons.

Trimeresurus tenasserimensis is distinguished from T. lanna (described above) by having: (1) lower max TL in both sexes (736 mm in males, 532 mm in females vs. 815 mm in males, 854 mm in females); (2) slightly higher total number of VEN+SC in males (226-242, x̄ = 235.3 vs. 213-241, x̄ = 227.8 in males; p = 0.018); (3) a slightly lower ratio ED/SnL in males (0.39-0.62, x̄ = 0.50 vs. 0.46-0.66, x̄ = 0.58 in males; p = 0.05); (4) elongate, white vertebral spots generally present in juvenile and subadult specimens in both sexes (vs. absent).

Trimeresurus tenasserimensis is distinguished from T. popeiorum by having: (1) lower max TL in both sexes (736 mm in males, 532 mm in females vs. 925 mm in males, 884 mm in females); (2) slightly lower ratio TaL/TL in females (0.136-0.161, x̄ = 0.152 vs. 0.14-0.19, x̄ = 0.166; p = 0.017); (3) bicolor postocular streak in males very broad, covering 2-3 temporal scales (vs. thin, covering 1-2 temporal scales); (4) temporals strong keeled in males (vs. feebly keeled). Furthermore, T. tenasserimensis is widely separated from T. popeiorum on a geographical basis as this latter species inhabits only northeastern India, Nepal, Bhutan, Bangladesh, southwestern China, and northern Myanmar. Moreover, the ranges of both species are separated by that of T. lanna .

Trimeresurus tenasserimensis is distinguished from T. nebularis by having: lower max TL in both sexes (736 mm in males, 532 mm in females vs. 1002 mm in males, 948 mm in females; (2) higher total number of VEN+SC in both sexes (226-242, x̄ = 235.3 vs. 210-218, x̄ = 214.0 in males; p = 0.02; 222-242, x̄ = 231.0 vs. 197-210, x̄ = 205.6 in females; p = 0.01); (3) eye bright or deep red in both sexes vs. usually green; (4) bicolored postocular streak present in males vs. absent; (5) ventrolateral streak present in females vs. absent; (6) ventral color green vs. usually yellowish in both sexes.

Trimeresurus tenasserimensis differs from T. phuketensis by having: (1) higher max TL in males (736 mm vs. 640 mm), but lower max TL in females (532 mm vs. 748 mm); (2) lower ratio TaL/TL in both females (0.14-0.16, x̄ = 0.15 vs. 0.17-0.18, x̄ = 0.17; p = 0.003); (3) higher total number of VEN+SC in males (226-242, x̄ = 235.3 vs. 242-249, x̄ = 246.4; p = 0.004); (4) eye color deep red in both sexes vs. copper; (5) no dorsal crossbands vs. irregular, conspicuous reddish-brown crossbands usually present.

Lastly, T. tenasserimensis can be further differentiated from the five subspecies of T. sabahi as follows:

- from T. s. barati by having: (1) higher total number of VEN+SC in both sexes (226-242, x̄ = 235.3 vs. 208-225, x̄ = 217.7 in males; p = 0.0006; 222-242, x̄ = 231.0 vs. 201-219, x̄ = 207.0 in females; p = 0.001); (2) 21 dorsal scales rows at midbody vs. 17-19; (3) eye color deep red in both sexes vs. deep orange; (4) bicolored postocular streak present in males vs. absent;

- from T. s. buniana by having: (1) lower total number of VEN+SC in males (226-242, x̄ = 235.3 vs. 246-250, x̄ = 248.0; p = 0.02); (2) lower number of cephalic scales in both sexes (9-11, x̄ = 10.0 vs. 11-12, x̄ = 11.7 in males; p = 0.03; 11-13 vs. 14 in female); (3) eye color deep red in both sexes vs. copper; (4) dorsum uniform bright green vs. dark bluish-green or verdigris with conspicuous reddish-brown or violet, irregular crossbands; (5) bicolored postocular streak, red and white, in males vs. postocular streak reddish-brown;

- from T. s. fucatus by having: (1) lower max TL in both sexes (736 mm in males, 532 mm in females vs. 834 mm in males, 826 mm in females); (2) lower ratio TaL/TL in females (0.14-0.16, x̄ = 0.15 vs. 0.16-0.19, x̄ = 0.17; p = 0.002); (3) eye color deep red in both sexes vs. copper; (4) solid dorsal crossbands in males absent vs. present; (5) wide bicolor postocular streak, red and white, present in males vs. sometimes absent, or white, or thin, white with a dark red upper part;

- from T. s. toba by having: (1) lower max TL in females (532 mm vs. 798 mm); (2) slightly higher total number of VEN+SC in females (222-242, x̄ = 231.0 vs. 204-218, x̄ = 212.5; p = 0.02); (3) eye color deep red in both sexes vs. deep orange; (4) in males, ventrolateral stripe bicolored, wide, vs. white and thin.

- from T. s. sabahi by having: (1) slightly lower ratio TaL/TL in females (0.14-0.16, x̄ = 0.15 vs. 0.17-0.18, x̄ = 0.18; p = 0.02); (2) higher total number of VEN+SC in both sexes (226-242, x̄ = 235.3 vs. 216-226, x̄ = 222.0 in males; p = 0.01; 222-242, x̄ = 231.0 vs. 212-217, x̄ = 214.7 in females; p = 0.02); (3) bicolored postocular streak present in males vs. absent.

Distribution

(Fig. 1 ). Currently, T. tenasserimensis is likely to be restricted to the northern part of the Isthmus Kra, in the Tennasserim Range of peninsular Myanmar and Thailand. Based on our data, we establish the distribution of this species as follows: Peninsular Thailand (Ratchaburi, Kanchanaburi, Phetchaburi, and Prachuap Khiri Khan provinces), and southeastern Myanmar (Tanintharyi Region).

Natural history notes.

Trimeresurus tenasserimensis inhabits a wide variety of habitats, from lowland bamboo forest and dry evergreen forest to submontane forest, at elevations from 200-1500 m. This pitviper usually occurs near small streams or in wet habitats. In Lampi Marine NP., Tanintharyi Region, Myanmar, this species was found coiled in trailside vegetation (ca. 50 cm above the ground) in undisturbed tropical evergreen forest on ridgeline ( Platt et al. 2018). Arboreal and nocturnal, it is mostly found hanging above streams, sometimes at 6-8 m above water. Breeding starts around August, and newborn snakes appear around mid-December (personal observations). Diet in the wild is mostly based on frogs and geckos such as Cyrtodactylus cf. oldhami (Theobald). Large females sometimes feed on small rodents (personal observations).

Conservation status.

Further research is required to clarify the extent of the distribution, population trends and conservation status of the new species. Trimeresurus tenasserimensis is distributed over a relatively small region, but inhabits several protected areas. Across its range, the new species is quite common. Thus, we tentatively suggest that T. tenasserimensis be assessed as Least Concern (LC) following the IUCN‘s Red List categories (IUCN Standards and Petitions Committee 2019).

Figures

Figure 1. Distribution of the species and subspecies of the subgenus Trimesurus Popeia. Base map created using simplemappr. net. A dot in the center of a colored circle denotes type locality. Colors of circles and locality numbers correspond to those in Figures 2 - 3 and Appendix II; for locality information see Appendix VIII. Type localities of the included taxa are shown in colored clouds; taxon names that are not valid nomina of recognized taxa are shown in quotes.

Figure 10. Trimeresurus tenasserimensis sp. nov. Specimen ZMMU Re- 17668 (holotype, adult male; before preservation): A General dorsal view; B General ventral view; C Lateral view of the head, right side; D Lateral view of the head, left side; E Dorsal view of the head; F Ventral view of the head. Specimen CAS 247870 (paratype, adult male; in preservative): G Dorsal view of the head; H Ventral view of the head. Photos by: N. A. Poyarkov (A-F), and G. Vogel (G-H).

Figure 11. Trimeresurus tenasserimensis sp. nov. in life. Thailand: A - D Khao Kra Jom Mt, Suan Phueng, Ratchaburi, adult male (A, B), adult female (C), and subadult female (D), respectively; E Khao Laem Mt., Suan Phueng, Ratchaburi (subadult male); F - G Kaeng Krachan NP., Phetchaburi (adult male and adult female, respectively); H Namtok Huai Yang NP, Prachuap Khiri Khan (adult female). Myanmar: I Lampi Marine NP., Mergui, Tanintharyi (adult male). Photos by: P. Pawangkhanant (A-E), R. Jaihan (F), A. Tomaszek (G), T. Smith (H), and P. Brakels (I).