Trimeresurus kuiburi, Sumontha & Suntrarachun & Pauwels & Ngkhanant & Chomngam & Iamwiriyakul & Chanhome, 2021

Sumontha, Montri, Suntrarachun, Sunutcha, Pauwels, Olivier S. G., Ngkhanant, Parinya Pawa-, Chomngam, Nirut, Iamwiriyakul, Prapanth & Chanhome, Lawan, 2021, A new karst-dwelling, colorful pitviper (Viperidae: Trimeresurus) from northern Peninsular Thailand, Zootaxa 4974 (2), pp. 307-332 : 309-326

Trimeresurus kuiburi sp. nov.

( Figures 1–6 )

Trimeresurus sp. — Sumontha et al. 2017a: 561.

Holotype. QSMI 1500 (field number MS 703); adult male collected by Montri Sumontha, Nirut Chomngam, Parinya Phawangkhanant and Prapanth Iamwiriyakul on 27 November 2016 near Ban Thung Noi (ca. 12.084500 N, 99.948556 E), Khao Daeng Sub-district , Kui Buri District, Prachuap Khiri Khan Province, Peninsular Thailand.

Paratypes (5). AUP-02005 (field number MS 701), PSUZC-R 734 (MS 704) and PSUZC-R 735 (MS 731), adult males collected on 9 August 2015, 20 June 2014 and 3 October 2020, respectively (all preserved with everted hemipenes). QSMI 1501 (MS 702) and AUP-02006 (MS 732), adult females collected on 20 June 2014 and 26 June 2020, respectively. Same locality and collectors as the holotype.

Diagnosis. Trimeresurus kuiburi sp. nov. can be distinguished from all other congeneric species by the combination of its red/purple bands on a green dorsum; white concave suborbital stripe in males; white, spaced vertebral dots in males; pale green belly lacking dark dots or stripe on the lateral sides of the ventrals; partially fused 1 st supralabial and nasal scale; 19 dorsal scale rows at midbody; 164–171 ventrals; 63–65 subcaudals in males, 51–53 in females; maximal known SVL of 451 mm; and long, papillose hemipenes.

Description of holotype. Adult male ( Figures 1–2 ). Body cylindrical, long and thin; SVL 376.4 mm; tail length 88.2 mm; total length 464.6 mm. Pupil vertically elliptical. Loreal pit present. Head triangular in dorsal view, elongate, clearly distinct from the neck; head length 18.0 mm; head width 13.4 mm; HW/HL 0.74; distance between nostrils 3.7 mm. Snout elongate, 34% of HL, 1.78 times as long as horizontal diameter of eye, obliquely truncated when seen from lateral side, flattened and rounded when seen from above, with a distinct canthus rostralis. Distance between eye and nostril 4.4 mm on both sides. Rostral slightly visible from above, triangular; rostral width 2.9 mm, rostral height 2.0 mm. Nostril completely enclosed in nasal scale; nasal scale partially fused with first supralabial. Shield bordering anterior edge of pit fused with second supralabial, lacking any small scales between it and nasal. Long, thin, crescent-like subocular scale, in contact with third supralabial, separated from the 4 th and 5 th supralabials by one row of scales, separated from the 6 th supralabial by 1/2 scales. Two upper preoculars above the loreal pit, elongated, and in contact with the single loreal which separates the upper preoculars from the nasal; lower preocular forming the lower margin of the loreal pit; 1/1 postocular. Eleven/ten supralabials, 3 rd supralabial largest; 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. Six pairs of gulars aligned between the chin shields and the preventral. One pair of enlarged internasals, in contact above the rostral. Length of the single, unfragmented supraocular 4.1/ 4.1 mm; width of supraocular 1.3/ 1.3 mm; ratio SOL/SOW 3.15. Supraoculars slightly indented on their inner margin by the upper head scales. At least nine scales between the supraoculars. Scales on snout and in the interorbital region smooth, irregular, subimbricate; temporal and occipital scales moderately keeled. Dorsal scales in 21-19-15 rows. Scale row reduction from 21 to 19 rows resulted from the fusion of the 4 th and 5 th rows above ventrals 30/31; reduction from 19 to 17 from the fusion of the 4 th and 5 th rows above ventral 108; and reduction to 15 rows by fusion of the 5 th and 6 th rows above ventral 121 on the left side, and of the 4 th and 5 th rows above ventral 122 on the right side. Dorsal scales all moderately keeled, except the first row which is unkeeled. One preventral + 166 ventrals. Anal scale single; 65 subcaudals, all divided. Hemipenes long, papillose (holotype preserved with everted hemipenes). Tail distinctly prehensile.

Coloration in life. Dorsal surface of head dark green with many scales also partly or entirely dark red, especially on the snout, and the interorbital, temporal and occipital regions. A contrasting white stripe begins under the loreal pit, forms a concave curve under the eye, then continues straight from the 7 th to the last supralabial where it stops. Black vertical pupil; iris copper. The background color of the dorsum is dark green, similar to that of the head, with about 62 irregular, dark red crossbands. These red bands are about two dorsal scales long mediodorsally, but narrower on the lower flanks where they are about one dorsal scale long. At the level of the vertebral row, the red bands are generally separated by one dorsal scale. The vertebral row exhibits an interrupted line of white dots, spaced by five or six dorsal scales. Each scale of the lowest dorsal scale row shows a horizontally elongate white spot, forming a continuous white line from the neck to the end of the tail. Most of the scales of the first row also exhibit a smaller red dot, forming a dotted red line. Above the white stripe of the first dorsal scale row, the tail is red, except some thin lighter bands. The infralabials are green and white; the underside of the head is mostly white. The belly is uniformly pale green, of a lighter tone than the background color of the dorsum.

In preservative the background dorsal color turned to brownish, with poorly contrasted darker marks on the head and bands on the dorsum; the belly color became greenish grey. The suborbital concave white stripe remained contrasted, as well as the white stripe on the first dorsal scale row.

Variation. The main meristic, morphometric and chromatical characters of the type-series of Trimeresurus kuiburi sp. nov. are presented in Table 3 . All paratypes and other specimens show a nasal scale partially fused with the first supralabial, similarly to the holotype ( Figures 1 , 2A , 5A & 5B , 6A & 6B ). Scale row reduction from 21 to 19 rows and from 19 to 17 rows generally result from the fusion of the 4 th and 5 th dorsal rows, less frequently from the fusion of the 5 th and 6 th rows. All individuals, similarly to the holotype, show a pale green belly and lack a dark stripe or a dark dot on the lateral tips of the ventrals. Trimeresurus kuiburi sp. nov. shows a strong sexual dimorphism in the number of subcaudals (63–65 in males vs. 51–53 in females). All males exhibit a concave white suborbital stripe ( Figures 1 , 2A , 5A & 5B ), while in females this stripe is straight, and less contrasted or sometimes not visible ( Figures 1 , 6A & 6B ). The spaced white vertebral dots are present in all males, and absent in all females; they are regularly spaced by 5 to 6 vertebral scales. The number of dark bands on dorsum varies from 59 to 68 among the preserved types, without apparent sexual dimorphism; the highest number we observed was 70 in an adult female that we caught and released at the type-locality. All paratypes lost most of their dorsal pattern once in preservative; such a drastic color fading was also observed after a short time in preservative for Trimeresurus kanburiensis and T. venustus ( Malhotra & Thorpe 2004b) .

Distribution and natural history. The type-locality of Trimeresurus kuiburi sp. nov. ( Figure 7 ) is situated along the border with the southern tip of Khao Sam Roi Yot National Park where we also observed the new species. It is locally an abundant snake. Adults are found foraging at night on karst boulders ( Figure 8 ). Young individuals are generally found on small bushes growing among the boulders. Several individuals in pre-shedding phase were found perched high on taller bushes.

This pitviper is not aggressive if gently approached or handled. Nothing is known about its diet in the wild, except that one adult individual regurgitated a Cyrtodactylus samroiyot just after capture. Trimeresurus kuiburi sp. nov. is probably a generalist predator, as captive individuals ate geckos ( Hemidactylus murrayi Gleadow , H. frenatus Duméril & Bibron and H. platyurus (Schneider)) , frogs ( Fejervarya limnocharis (Gravenhorst) and Polypedates leucomystax (Gravenhorst)) and mice. Mating was observed in captivity in the morning of 4 October 2020, after a rain shower. The preserved female QSMI 1501 contains nine eggs.

We found the following squamates in direct proximity to the new pitviper species: Calotes versicolor (Daudin) (Agamidae) , Cnemaspis lineogularis Wood, Grismer, Aowphol, Aguilar, Cato, Grismer, Murdoch & Sites , Cyrtodactylus samroiyot , Dixonius kaweesaki and D. siamensis (Boulenger) , Gekko gecko (Linnaeus) , Gehyra fehlmanni (Taylor) , Hemidactylus frenatus and H. platyurus (Gekkonidae) , Ahaetulla sp. , Dendrelaphis subocularis (Boulenger) , Lycodon capucinus (Boie) and Lycodon davisonii (Blanford) (Colubridae) , Calliophis cf. maculiceps (Günther) (Elapidae) and Indotyphlops braminus (Daudin) (Typhlopidae) .

Etymology. The specific epithet is a noun in apposition, invariable, in reference to the administrative district Kui Buri in which the type-locality lies. We suggest the following common names: งูหางแห้มกุย (Ngu Hang Ham Kui, Thai), Kui Buri Pitviper (English), Trimérésure de Kui Buri (French), and Kui Buri Bambusotter (German).

Comparison to other species. The possession of a long papillose hemipenis and a partially fused first supralabial and nasal scale makes of Trimeresurus kuiburi sp. nov. a member of the Trimeresurus group sensu stricto ( Cryptelytrops group sensu Malhotra & Thorpe 2004a), which currently includes the following 20 species: Trimeresurus albolabris (Gray) , T. andersonii Theobald , T. cantori (Blyth) , T. cardamomensis Malhotra, Thorpe, Mrinalini & Stuart , T. caudornatus Chen, Ding, Vogel & Shi , T. davidi Chandramouli, Campbell & Vogel , T. erythrurus (Cantor) , T. fasciatus (Boulenger) , T. guoi Chen, Shi, Vogel & Ding , T. honsonensis (Grismer, Ngo & Grismer) , T. insularis Kramer , T. kanburiensis Smith , T. labialis Fitzinger in Steindachner, T. macrops Kramer , T. mutabilis Stoliczka , T. purpureomaculatus (Gray) , T. rubeus Malhotra, Thorpe, Mrinalini & Stuart , T. salazar Mirza, Bhosale, Phansalkar, Sawant, Gowande & Patel , T. septentrionalis Kramer and T. venustus Vogel ( David & Vogel 2015; Chandramouli et al. 2020; Chen et al. 2020a –b; Mirza et al. 2020).

Among these species, Trimeresurus kuiburi sp. nov. is readily distinguished from the widespread Trimeresurus albolabris , the Andaman and Nicobar Islands endemic T. andersonii , the Nicobar Archipelago endemics T. cantori , T. davidi , T. labialis and T. mutabilis , the Cardamom Mounts endemic T. cardamomensis , the Chinese T. caudornatus , the Indo-Burmese T. erythrurus , the Indonesian Tanahdjampea Island endemic T. fasciatus , the widespread T. guoi , the Vietnamese Hon Son Island endemic T. honsonensis , the Indonesian T. insularis , the Southeast Asian T. macrops , the southern Vietnamese-Cambodian T. rubeus , the Indian T. salazar and the Himalayan T. septentrionalis by its dorsal pattern made of purple-red bands on a green background ( David & Vogel 2000; David et al. 2003; Grismer et al. 2008; Malhotra et al. 2011; Vogel et al. 2014; Chandramouli et al. 2020; Chen et al. 2020 a –b; Mirza et al. 2020). Its 19 MSR further separate it from Trimeresurus andersonii (21 MSR), T. cantori (27, 29 or 31), T. cardamomensis (21), T. caudornatus (21), T. davidi (21 or 23), T. erythrurus (23 or 25), T. fasciatus (21), T. guoi (21), T. honsonensis (21), T. insularis (21), T. labialis (21 or 23), T. macrops (21), T. mutabilis (21), T. purpureomaculatus (23–29), T. rubeus (21), T. septentrionalis (21) and most specimens of T. venustus (21, rarely 19).

Compared to all members of the Cryptelytrops group, Trimeresurus kuiburi sp. nov. is superficially similar only to T. kanburiensis and T. venustus , two geographically-restricted endemics of western Thailand and the Thai-Malay Peninsula, respectively.

The northernmost published record of Trimeresurus venustus was mentioned by Pauwels et al. (2013; Figure 9B ) who listed the reptile taxa co-occurring at the type-locality of Cyrtodactylus sanook in Muang District, Chumphon Province. At that time we were not aware of the existence of the Kui Buri population and we did not morphologically examine in detail what we believed to be not more than a northern range extension of Trimeresurus venustus . The males of the Chumphon population, contrary to Trimeresurus kuiburi sp. nov., do not show a concave but a straight suborbital stripe, and they show a white vertebral dot every 2 to 4 vertebral scales, while male T. kuiburi sp. nov. show a dot every 5 or 6 scales, and typical male T. venustus do not show white dots ( Figure 9A ).

In any case, Trimeresurus kuiburi sp. nov. is distinct from Trimeresurus venustus sensu auctorum. A striking pattern difference is the concave shape of the suborbital white stripe in male Trimeresurus kuiburi sp. nov. It is straight and bordering the orbit in males of the northern and southern populations of T. venustus (less contrasted or sometimes not visible in females), as can be clearly seen in photographs published in the original description of T. venustus showing specimens from Thung Song, as well as in Manthey & Grossmann (1997: 411, one individual from ‘Süd-Thailand’), Chan-ard et al. (1999: 197–198, an individual from Tai Rom Yen National Park in Surat Thani Prov., and another from Surat Thani Province without locality details, identified as T. kanburiensis ), Gumprecht & Ryabov (2002: 37, a female from Kanchanadit, Surat Thani Prov., as T. kanburiensis ), Vogel (2006: 122–123, five individuals from ‘South Thailand’), Figures 10–11 , and in the museum material we examined (see Appendix).

Many other photographs and some drawings of Trimeresurus venustus s.l. were published without any locality information, but none of them showed a convex suborbital stripe, and as far as we know, none of them was illustrating individuals from Prachuap Khiri Khan Province. This includes among others the individuals illustrated by Thumwipat & Nutphand (1982: 140, identified as T. purpureomaculatus ), Kundert (1984: Fig. 106, as T. sumatranus ), Lim & Lee (1989: 107 top, as T. purpureomaculatus ), Nabhitabhata (1989: 176, implicitly as T. kanburiensis ), Cox (1991: 398, as T. kanburiensis ), Jintakune & Chanhome (1995: 129, as T. kanburiensis ), Cox et al. (1998: 22, as T. kanburiensis ), Jintakune (2000: 151, as T. kanburiensis ), Nutphand (2001: 298–299, as T. purpureomaculatus ; see David et al. 2004a), Chan-ard (2002: 127, as T. kanburiensis ), Sanders et al. (2006: Supplementary material: Fig. 2b ), Anonymous (2010: 3, as T. kanburiensis ), Chanhome et al. (2011: 326), O’Shea (2013: 18), Chan-ard et al. (2015: 287; individuals from Surat Thani or Nakhon Si Thammarat), Suteparuk & Vasaruchapong (2016: Fig. 2 ), Visser (2015: Figs 610, 612–613, 615–622), Oliveri et al. (2016: Fig. 7 A-D) and Fuchs et al. (2019). The latter publication described the medical consequences of the bite by a F2 captive individual of unknown geographic origin; it is stated that this species ( T. venustus ) has 21-21-15 DSR, but these numbers actually come from the internet (http://www.toxinology.com/) and were not verified on the individual in question (J. Fuchs, pers. comm. to OSGP, Oct. 2020).

Besides the differences in the suborbital stripe in males (concave vs. straight) and the lower number of midbody scale rows (19 vs. 21, exceptionally 19), Trimeresurus kuiburi sp. nov. differs from T. venustus by the absence (vs. presence) in both sexes of red dots on the lateral sides of the ventrals, the presence of white vertebral dots every 5 or 6 in males (vs. absence), a shorter tail in females (0.133 –0.135 vs. 0.137 –0.148), and the lower number of ventrals in males (164–166 vs. 166–181) (see Table 4 ). While the internasals are always in contact in Trimeresurus kuiburi sp. nov., they are in contact in only 45% of cases in T. venustus ( David et al. 2004b) .

Trimeresurus kuiburi sp. nov. differs from T. kanburiensis by its smaller maximal SVL (451 vs. 582 mm), internasals always in contact (vs. always separated), generally wider supraocular, higher IOS (9–11 vs. 7–9), lower number of ventrals in males (164–166 vs. 170–178), more subcaudals in males (63–65 vs. 59), more subcaudals in females (51–53 vs. 41–51), distinct dorsal color (red/purple bands on bottle green background vs. dark olive-brown bands on grayish-olive background), concave (vs. straight) suborbital stripe in males, and pale green vs. creamy white belly (see Table 4 ). White vertebral dots in males are more spaced in Trimeresurus kuiburi sp. nov. than in T. kanburiensis (5 or 6 vs. 3–5 scales apart).

Geographically, Trimeresurus kuiburi sp. nov. is well separated from both T. kanburiensis and T. venustus . Trimeresurus kanburiensis is restricted to the area of Sai Yok in Kanchanaburi Province, a part of the Tenasserim Range showing a high endemism in squamates ( Sumontha et al. 2017b), located about 300 km N-NW of the typelocality of T. kuiburi sp. nov. Trimeresurus venustus is separated from T. kuiburi sp. nov. by a gap of at least 180 km (population of Chumphon Province, whose status is not yet established, but similar to T. venustus in pattern; see Figures 9A & 9B ) or at least 350 km (other venustus -like populations).

The analysis of cytochrome b revealed that mean interspecific p -distances between Trimeresurus kuiburi sp. nov. and related Trimeresurus species ranged from 4.57 % to 18.10 %, with the minimum of 4.57 % ± 0.91 % being to T. macrops and the maximum of 18.10 % ± 1.68 % being to P. mucrosquamatus ( Table 5 ). Moreover, 16S rRNA gene was analyzed and showed the interspecific p -distances between T. kuiburi sp. nov. and related Trimeresurus species ranged from 1.23 % to 8.15 %, with the minimum of 1.23 % ± 0.54 % being to T. macrops and the maximum of 8.15 % ± 1.34 % being to T. wagleri ( Table 6). Bayesian phylogenetic inference yielded a well - supported sister relationship between T. kuiburi sp. nov. and T. macrops . These two species are nested within the Trimeresurus clade ( Figure 14 ). Therefore, the molecular results concur with the assignment of our specimens to a new species of Trimeresurus s.s.

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Figures

FIGURE 1. Live adult male holotype of Trimeresurus kuiburi sp. nov. (right) with a conspecific, non-preserved adult female from the same locality. Photograph by M. Sumontha.

FIGURE 2. Preserved holotype of Trimeresurus kuiburi sp. nov. A. Left profile of the head. B. Dorsal view of the head. C. Ventral view of the head. D. Posterior part of the venter and cloacal area. Figures not to scale. Note the drastic fading of colors after preservation. Photograph by M. Sumontha.

FIGURE 3. A. Dorsal view of a preserved male paratype (AUP-02005) of Trimeresurus kuiburi sp. nov. Note the near total loss of dorsal pattern after preservation. B. Dorsal view of a preserved female paratype (QSMI 1501) of Trimeresurus kuiburi sp. nov. Note the eggs and the near total loss of dorsal pattern after preservation. Photographs by M. Sumontha.

FIGURE 4. A. Ventral view of a freshly preserved male paratype (PSUZC-R 735) of Trimeresurus kuiburi sp. nov. B. Ventral view of a freshly preserved female paratype (AUP-02006) of Trimeresurus kuiburi sp. nov. Note the total absence of dots or stripes on the lateral sides of the ventrals in both specimens. Photographs by M. Sumontha.

FIGURE 5. A. Head of an adult male Trimeresurus kuiburi sp. nov. from the type-locality; individual not collected. Photograph by P. Pawangkhanant. B. Male Trimeresurus kuiburi sp. nov. from Khao Sam Roi Yot National Park; individual not collected. Photograph by M. Sumontha.

FIGURE 6. A. Female Trimeresurus kuiburi sp. nov. from the type-locality; individual not collected. Photograph by M. Sumontha. B. Adult female Trimeresurus kuiburi sp. nov. from Khao Sam Roi Yot National Park; individual not collected. Photograph by P. Pawangkhanant.

FIGURE 7. Distribution of Trimeresurus kanburiensis (white circles), T. kuiburi sp. nov. (red asterisk), T. cf. venustus (pink triangles) and T. venustus (blue squares) in Thailand. Map by A. Aksornneam. New localities in Krabi and Phang-Nga provinces are based on our Figures 12 & 13.

FIGURE 8. Microbiotope of Trimeresurus kuiburi sp. nov. within Khao Sam Roi Yot National Park. Photograph by P. Pawangkhanant. Adult individuals forage on the boulders, while young ones are mostly found on the bushes.

FIGURE 9. A. Adult male Trimeresurus cf. venustus from Tham Chang Phueak (ca. 10°26’48.9”N, 99°02’00.7”E), Muang District, Chumphon Province, showing a straight suborbital stripe. B.Adult female Trimeresurus cf. venustus from Tham Sanook (= Sanook Cave, ca. 10°28’53.2”N, 99°04’29.3”E), Muang District, Chumphon Province. Photographs by M. Sumontha.

FIGURE 10. Adult male Trimeresurus venustus from Wat Tham Suea (= Tiger Cave Temple, ca. 8°07’32.6”N, 98°55’23.4”E), Muang District, Krabi Province, showing a straight suborbital stripe. Photograph by M. Sumontha.

FIGURE 11. A. Adult male Trimeresurus venustus from Khao Phanom Wang (ca. 9°05’35.3”N, 99°36’30.9”E), Kanchanadit District, Surat Thani Province, showing a straight suborbital stripe. B. Adult female Trimeresurus venustus from Khao Phanom Wang, Kanchanadit District, Surat Thani Province. Photographs by M. Sumontha.

FIGURE 14. Bayesian inference tree showing inferred phylogenetic relationships of Trimeresurus kuiburi sp. nov. with Trimeresurus spp. and other viperids. Numbers at internal branches represent Bayesian posterior probability.