Research Article |
Corresponding author: Tan Van Nguyen ( tan.sifasv@gmail.com ) Corresponding author: Patrick David ( patrick.david@mnhn.fr ) Corresponding author: Gernot Vogel ( gernot.vogel@t-online.de ) Corresponding author: Nikolay A. Poyarkov ( n.poyarkov@gmail.com ) Academic editor: Uwe Fritz
© 2024 Sabira S. Idiiatullina, Tan Van Nguyen, Parinya Pawangkhanant, Chatmongkon Suwannapoom, Lawan Chanhome, Zeeshan A. Mirza, Patrick David, Gernot Vogel, Nikolay A. Poyarkov.
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Citation:
Idiiatullina SS, Nguyen TV, Pawangkhanant P, Suwannapoom C, Chanhome L, Mirza ZA, David P, Vogel G, Poyarkov NA (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: 303-342. https://doi.org/10.3897/vz.74.e113347
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Abstract
Despite recent progress in our understanding of diversity within the genus Trimeresurus Lacépède, 1804, the subgenus Popeia Malhotra & Thorpe, 2004, distributed across most parts of East and Southeast Asia, remains taxonomically challenging. We applied an integrative taxonomic approach including analyses of morphological data and four mitochondrial genes (12S and 16S rRNA, cytochrome b, and NADH dehydrogenase subunit 4), along with examination of available type material, to address longstanding taxonomic questions in one clade within Popeia, the T. popeiorum group, and reveal a high level of hidden diversity of these snakes in the Indo-Burma Biodiversity Hotspot. We confirm that T. popeiorum Smith, 1937 sensu stricto is restricted to Northeast India, eastern Nepal, southern Bhutan, southeastern Bangladesh, western Yunnan Province (China), and northern and southwestern Myanmar. We further confirm that the recently described species T. yingjiangensis Chen et al., 2019 is a junior synonym of T. popeiorum. In addition, we discovered that the combination Trimesurus [sic] elegans Gray, 1853 is a valid senior synonym of T. popeiorum and threatens the stability of the latter taxon. Therefore, in order to protect the nomen popeiorum and in accordance with Article 23.9 of the International Code of Zoological Nomenclature, we regard the taxon Trimesurus elegans as a nomen oblitum and render Trimeresurus popeiorum a nomen protectum. Examination of a larger series of specimens allows us to describe two new cryptic species of Trimeresurus from the Indo-Burma Region. This study brings the total number of species in the subgenus Popeia to six and also suggests that the subspecific taxonomy of the T. sabahi complex requires further investigation. We urge adequate actions regarding the conservation of the newly discovered species and recommend further studies on their toxicology.
Asia, Biodiversity, Crotalinae, ICZN, Indochina, molecular phylogeny, morphology, mtDNA, nomen protectum, nomenclature, Popeia, systematics
The genus Trimeresurus Lacépède, 1804 has long included most pitvipers of eastern and southeastern Asia (e.g.,
The proposal by
Of particular interest to us is the subgenus Popeia (type species T. popeiorum, by original designation), which was originally defined by
Trimeresurus popeiorum Smith, 1937, as currently defined (see
Unfortunately,
The taxonomy of what we call the T. popeiorum group within the subgenus Popeia was first addressed by
The T. popeiorum group was further revised by
On the Asian mainland,
Recently,
In the analysis we present below, we used both molecular and morphological data to analyze variation in populations from the whole range of the T. popeiorum group. Pitvipers of the genus Trimeresurus cause a large percentage of the snakebites reported in Southeast Asia and therefore have a high medical relevance (
Fieldwork was carried out in Tak Province, Thailand, by G. Vogel in 2006 and 2007; in Chiang Mai Province, Thailand, by P. Pawangkhanant, N. A. Poyarkov, and C. Suwannapoom in August 2017 and July 2018; in Ratchaburi Province, Thailand, by P. Pawangkhanant, N. A. Poyarkov, and C. Suwannapoom in June and July 2019; in Kachin and Sagaing States of Myanmar, by N. A. Poyarkov and P. Pawangkhanant in July 2018 and July 2019; in Arunachal Pradesh State, India, by Z.A. Mirza in July 2019; and in Mizoram State, India, by G. Vogel in 2013, 2015, 2017, and 2023 (Fig.
Distribution of the species and subspecies of the subgenus 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
Specimen collection and animal use protocols were approved by the Institutional Ethical Committee of Animal Experimentation of the University of Phayao, Phayao, Thailand (certificate number UP-AE64-02-04-005, issued to Chatmongkon Suwannapoom) and were strictly compliant with the recommendations of the Thailand Animal Welfare Act. Fieldwork, including collection of animals in the field, was authorized by the Institute of Animals for Scientific Purpose Development (IAD), Bangkok, Thailand (permit numbers U1-01205-2558 and UP-AE59-01-04-0022, issued to Chatmongkon Suwannapoom).
The General Lineage Concept (GLC:
Total genomic DNA was extracted from ethanol-preserved muscle or liver tissues using standard phenol-chloroform extraction procedures (
For cyt b sequences we used a modification of the PCR protocol by
All amplifications were run using an iCycler thermal cycler (Bio-Rad). PCR products were loaded onto 1% agarose gels in the presence of ethidium bromide and visualized using electrophoresis. The successfully amplified PCR products were purified using a Diatom DNA PCR Clean-Up kit and outsourced to Evrogen (Moscow, Russia) for sequencing. Sequence data collection and visualization were performed on an ABI 3730xl Automated Sequencer (Applied Biosystems).
To estimate the phylogenetic relationships of the genus Trimeresurus, we used the newly obtained cyt b, ND4, 12S, and 16S sequences together with previously published sequences of 95 representatives of the subgenus Popeia, as well as representative sequences of 26 species of other Trimeresurus subgenera and sequences of five species of the sister genus Craspedocephalus as recognized by
We initially aligned the nucleotide sequences in MAFFT online (
Phylogenetic trees were estimated for the combined mitochondrial DNA fragments (cyt b, ND4, 12S, and 16S). We inferred the matrilineal genealogy of Trimeresurus using Bayesian Inference (BI) and Maximum Likelihood (ML) approaches. We used IQ-TREE (
For this study, a total of 159 preserved specimens of taxa in the subgenus Popeia were examined for their morphological characters (Appendix III). Altogether, 45 morphological characters, including the structure of the hemipenes, were examined (see Appendix IV). Not all of these characters were useful to distinguish between the subject species, but all of them were compared because they may be used for further studies on taxonomy and geographical variation in this group of snakes.
Measurements were taken with a slide-caliper to the nearest 0.1 mm, except body and tail lengths, which were measured to the nearest of 1 mm with a measuring tape. The number of ventral scales was counted according to
For comparison with other taxa, we relied on data previously published for the subgenus Popeia, including
Abbreviations. Morphology and morphometry: ASR: number of dorsal scale rows on the neck; CEP: number of cephalic scales between the supraoculars; CLP: condition of the cloacal plate; DSR: number of dorsal scale rows before vent; ED: eye diameter; G: pairs of gular scales; HL: head length; IL: infralabials; IN: internasals; MSR: number of dorsal scale rows at midbody; PV: preventrals; SbS: number of scales between supraoculars; SC: number of subcaudals excluding terminal scute; SC/SpOc: number of scales surrounding the supraocular; SL: number of supralabials; SN: snout length; SO: number of supraoculars; SVL: snout–vent length, from tip of snout to last posterior edge of the last ventral scale; TaL: tail length, from posterior edge of the cloacal plate to the tip of the tail; TL: total length, SVL + TaL; TaL/TL: ratio of tail length to total length; VEN: number of ventrals.
Other abbreviations. asl.: above sea level; Mt: Mountain; NP: National Park; WS: Wildlife Sanctuary; Is: Island.
Museum acronyms. AUP: School of Agriculture and Natural Resources, University of Phayao, Phayao, Thailand;
All statistical analyses were conducted in STATISTICA v8.0 (StatSoft Inc.). Univariate analyses were ran separately on males and females to reduce the effects of sexual dimorphism. Multivariate analyses were run on the male dataset because we lacked sufficient sample sizes for females. We used Shapiro-Wilks Tests and Levene’s Tests to test for normality and heteroscedasticity, respectively. We used Mann-Whitney U Tests and Student’s T Tests to compare quantitative differences between species. Tests for sexual dimorphism within species were performed using Mann-Whitney U Tests. For all univariate statistics, differences between characters were determined to be statistically significant when p-values were ≤ 0.05. After univariate analyses, we log-transformed the dataset and conducted a Principal Components Analysis (PCA) on the remaining residuals to determine whether there was visible structure in the morphological variation observed between species. We ran Mann-Whitney U Tests on PCA 1 and PCA 2 factors using the same procedures described above to determine if the PCA centroids of the two taxa were also significantly different. All data used in the PCA were scaled to standard deviation prior to analysis to help eliminate the effects of covariance and ensure the data were normally distributed. The following morphological characters were used for univariate and multivariate statistical analyses (abbreviations in parentheses): ASR, CEP, DSR, ED/HL, HL/SVL, IL, MSR, Sc, SC/SpOc, SL, SnL/HL, TaL/TL, VEN, and VEN+SC.
A total of 2205 aligned base pairs (1150 from cyt b, 853 from ND4, and 1352 from the 12S and 16S rRNA fragments) were obtained. Protein-coding sequences were translated into amino acids to confirm that no pseudogenes had been amplified. We deposited the newly obtained sequences in GenBank under accession numbers OR470534–38; OR470543–46; OR470550–57; OR470561–64; OR470571–80; OR471621–25; OR471630–43; OR999082–99; PP032774–811 (see Appendix II). Sequence characteristics, including the estimated transition / transversion bias, nucleotide frequencies, and suggested models of DNA evolution for each genetic marker are summarized in Appendix V.
ML and BI analyses recovered trees with very similar topologies and nodes that were reconstructed differently were not important to the analysis (Fig.
Maximum Likelihood (ML) phylogenetic tree of Trimeresurus from the analysis of 12S rRNA, 16S rRNA, ND4, and cyt b mitochondrial DNA gene sequences. Part 1 (subgenus Popeia). For voucher specimen information and GenBank accession numbers see Appendix II. Numbers at tree nodes correspond to ML UFBS / BIPP support values, respectively; an en-dash denotes no support. Colors of clades and locality numbers given in brackets after specimen ID correspond to those in Figure
Within the subgenus Popeia, the populations currently assigned to ‘T. popeiorum’ comprise three OTUs and are recovered as paraphyletic. Populations from the northern part of the group’s range in Northeast India, northern Myanmar (Kachin and Sagaing States), and the westernmost part of Yunnan Province form Clade E (100/1.0), which corresponds to OTU1 (T. popeiorum s. str.; Fig.
Populations from eastern Myanmar, northern Thailand, Laos, and southernmost China form OTU2, corresponding to Clade A (99/1.0, Fig.
OTU3 includes populations from the southern part of the group’s range in the Tenasserim Mountains of northern Peninsular Thailand and southeastern Myanmar, and forms a distinct clade (Clade F; 99/1.0) with sister relationships to all other members of the subgenus Popeia (69/0.91; not significantly supported). The populations of OTU3 from the eastern slopes of the Tenasserim Mountains in Thailand and from the western slopes in Myanmar (see Fig.
The phylogenetic positions of T. nebularis (Clade B, 100/1.0), T. phuketensis (Clade C, 100/1.0), and T. sabahi (Clade D, 100/1.0) remain essentially unresolved, but with each species forming a distinct and well-supported clade (Fig.
The uncorrected p distances for the cyt b gene fragment among the examined members of the subgenus Popeia are presented in Appendix VI. Intraspecific distances among Popeia species varied from 3.4% (between Clade C of T. phuketensis and Subclade A1 of OTU2 from northern Indochina) to 8.4% (between Clade E of OTU1 [T. popeiorum s. str.] and Clade B of T. nebularis). Genetic differentiation between the three main OTUs presently assigned to ‘T. popeiorum’ was significant and varied from 3.7–4.8% (between Clade A1 of OTU2 and Clade F of OTU3) to 7.6% (between Clade E of OTU1 and Subclade A1 of OTU2). The inter-group genetic differentiation varied from identity (in T. s. sabahi, T. s. buniana, and T. s. toba) to 2.1% (between Subclades F1 and F2 of OTU3) and 2.3% (between specimens in Subclade A2 of OTU2).
Five characters (VEN, SC, VEN+SC, CEP, ASR) exhibited normal distributions in all datasets. Univariate analysis revealed statistically significant differences between the members of the T. popeiorum group, including the three OTUs presently assigned to ‘T. popeiorum’, including OTU1 (= T. popeiorum s. str.), OTU2, and OTU3. Resulting p-values from univariate morphological analyses comparing OTU1 with OTU2 from northern Indochina and OTU3 from the Tenasserim Range are summarized in Table S2. Univariate analyses for both male, female, and combined datasets showed significant differentiation in the number of body scales (except SL), in relative tail and snout lengths, and relative eye-nostril distance between three OTUs of the complex (Table S2).
PCA plots revealed that the taxa of the T. popeiorum group are generally well-separated in morphospace, with members of the T. sabahi complex clearly distinct from OTU1–3 of the T. popeiorum group from Indo-Burma (Fig.
In summary, the combined univariate and multivariate analyses show that the three OTUs of the T. popeiorum group from the Indo-Burma Biodiversity Hotspot, corresponding to clades A, F and E of our mtDNA-based genealogy (Fig.
Results from our molecular phylogenetic analysis are generally consistent with those of
Based on our morphological and molecular analyses, we recognize the three OTUs from Indo-Burma, which have so far collectively been identified as ‘Trimeresurus popeiorum’, as three distinct species:
(1) OTU1 (mtDNA Clade E) encompasses populations from Northeast India, Kachin State and the Sagaing Region in Myanmar, as well as the western Yunnan population (formerly known as T. yingjiangensis). According to the type locality of T. popeiorum, this clade corresponds to T. popeiorum s. str. as defined by
(2) OTU2 (mtDNA Clade A) contains populations inhabiting southwestern China, northern and western Thailand, northern Laos, and southeastern Myanmar. As first indicated by
(3) OTU3 (mtDNA Clade F) includes populations from the northern Tenasserim Mountains, in the peninsular part of southwestern Thailand and southeastern Myanmar. The identification of this clade strongly supports the hypothesis of
The three mainland Asian OTUs of the subgenus Popeia are superficially similar in external morphology and coloration relative to other members of the subgenus, and are characterized by a green dorsal background color with varying degrees of patterning, SL1 separated from the nasal by a distinct suture, comparatively small cephalic scales (i.e., not enlarged into plates), and long and slender, deeply forked and calyculate hemipenes. Based on our results, we therefore recognize three distinct species-level taxa in the Indo-Burma Region, namely T. popeiorum s. str. and two undescribed species, which we formally describe below.
Synonymy.
Trimesurus
[sic] elegans Gray, 1853: 391. – Holotype:
Trimeresurus popeiorum
Smith, 1937: 730. – Lectotype:
Trimeresurus yingjiangensis
The species name is a patronym, in genitive plural, created in honour of Clifford H. Pope (1899–1974) and his wife Sarah H. Pope (1901–1995); see below for a discussion of the correct spelling. We recommend the following common names for this species: “Pō pǔ zhú yè qīng” (坡普竹叶青) (in Chinese), “Pope’s green pitviper” (in English), “Ngu Khiew Hang Mai Thong Khiew Assam” (งูเขียวหางไหม้ท้องเขียวอัสสัม) (in Thai), “Trimérésure vert des Pope” (in French), “Popes Bambusotter” (in German), and “Bambukovaya kufiya Poupov” (in Russian).
Before
We take this opportunity to mention the taxon Coluber viridicaeruleus La Cépède, 1789, which
A nomenclatural problem arose when
This taxon has long been forgotten or considered a synonym of Trimeresurus gramineus. For example,
The brief original description of Trimesurus elegans does not allow a formal identification of the species. However, its holotype (
For this reason, in order to protect the binomen Trimeresurus popeiorum Smith, 1937, we here make use of Art. 23.9 of the Code to reverse precedence (ICZN 1999). In order to apply this Article, two conditions must be fulfilled: Art. 23.9.1.1 states that the senior synonym must not have been used as a valid nomen after 1899; and Article 23.9.1.2 states that the junior synonym must have been used for a particular taxon, as its presumed valid nomen, “in at least 25 works, published by at least 10 authors in the immediately preceding 50 years and encompassing a span of not less than 10 years” (ICZN 1999).
In the present case, the first condition is met because to the best of our knowledge, the specific epithet elegans, as proposed by
In order to fulfil the second condition, the epithet popeiorum should have been used as valid in the genus Trimeresurus, even if under the erroneous spelling popeorum, by at least 25 authors since 1972. We provide below a list of 25 works published from 1972 onwards in which the epithet popeiorum (or popeorum) has been used as valid:
The foregoing sources allow to conclude that Art. 23.9 can be applied to Trimesurus elegans and precedence can be reversed. We therefore declare Trimesurus elegans Gray, 1853 to be a subjective senior synonym of Trimeresurus popeiorum Smith, 1937 and a nomen oblitum. In so doing, Trimeresurus popeiorum Smith, 1937, and also becomes a nomen protectum and the binomen can be used for green pitvipers from Southeast Asia.
(n = 15). Nepal.
Trimeresurus popeiorum differs from all other members of the subgenus Popeia by the combination of the following morphological characters: (1) dorsal surfaces in various shades of green, bluish-green or even turquoise blue; (2) in males, a vivid, wide bicolored ventrolateral stripe, bright and deep red below, white above; in females, stripe thin, white or yellow; (3) males with a conspicuous, bicolored postocular streak, thin and white ventrally, wide and bright red dorsally; streak absent in females; (4) eyes red to deep red in both males and females; (5) 21 dorsal scale rows at midbody, more or less strongly keeled in males, weakly keeled in females, scales of the first dorsal scale row always smooth; (6) first supralabial entirely separated from nasal scale by a distinct suture; (7) supraoculars much narrower than internasals; (8) internasals never in contact, separated by one or two scales; (9) 159–173 ventrals; 55–76 subcaudals, all paired; (10) hemipenes long and forked, reaching at least to the 25th subcaudal, without spines; (11) 11–13 cephalic scales between the supraoculars in males, 10–12 in females; (12) relative tail length 0.18–0.21 in males, 0.14–0.19 in females.
(
Body cylindrical, long, and laterally compressed (SVL 322 mm, TaL 62 mm, TL 384 mm, TaL/TL 0.161). Head triangular in dorsal view, elongate, clearly distinct from the neck (HL 18.4 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 3.1 mm, SnL 5.2 mm, ED/SnL 0.58); pupil vertical, elliptic.
Dorsal scales in 25-21-15 rows; dorsal scales all moderately keeled, except the first row, the scales of which are smooth; 167 ventrals (plus single preventral); cloacal plate single; 61 subcaudals, all divided.
Rostral slightly visible from above, triangular; one large pair of enlarged internasals, separated by a one small scale; nostril completely included in nasal scale; nasal scale completely separated from the first supralabial; 1/2 small scales between nasal and second supralabial; scales on the upper snout surface and in the interorbital region smooth, irregular, barely imbricate; temporal and occipital scales strongly keeled; two elongate upper preoculars above the loreal pit; lower preocular forming the lower margin of the loreal pit; one supraocular on each side, large, broader than the internasals; 13 irregular cephalic scales between the supraoculars; one long, thin, crescent-like subocular scale (Fig.
Trimeresurus popeiorum in preservative – specimen
Body green, beneath paler, whitish; scales of the back moderate, smooth, not keeled, the lateral series rather broader, the first lateral series green, with a small white spot on the hind part of the upper edge forming an interrupted lateral line.
(
Body cylindrical, long, and laterally compressed (SVL 758 mm, TaL 167 mm, TL 925 mm, TaL/TL 0.181). Head triangular in dorsal view, elongate, clearly distinct from the neck, snout elongate, flattened, and rounded when seen from above (Fig.
Trimeresurus popeiorum in preservative – specimen
Dorsal scales in 23-21-15 rows; dorsal scales all moderately keeled, except the first row, the scales of which are smooth; 165 ventrals (plus single preventral); cloacal plate single; 70 subcaudals, all divided.
Rostral slightly visible from above, triangular; one large pair of enlarged internasals, separated by one small scale (Fig.
Color uniform green above; paler green below. First row of scales on each side brown with yellow tip, second row yellow below the median keel. The narrow bicolor lateral stripe thus formed ending just behind head anteriorly and at vent posteriorly, incompletely developed on tail. Tip of tail pale reddish. Head without pattern or postocular stripe (Fig.
(
An adult male in a very good state of preservation.
Body cylindrical, long, and laterally compressed; SVL 594 mm, TaL 148 mm, TL 742 mm, TaL/TL 0.199. Head triangular in dorsal view, elongate, clearly distinct from the neck (HL 29.8 mm, HW 18.1 mm, HL/SVL 0.05); 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 12.9 mm); pupil vertically elliptic.
Dorsal scales in 21-21-15 rows; dorsal scales all moderately keeled, except the first row the scales of which are smooth; 164 ventrals (plus single preventral); cloacal plate single; 76 subcaudals, all divided. Hemipenes long, reaching to 23–24 SC, forked opposite fifth to sixth subcaudal scale, no spines (Fig.
Trimeresurus popeiorum in preservative – specimen
Rostral slightly visible from above, triangular, broader than high; one enlarged internasal on each side, internasals separated by one small scale behind the top of rostral (Fig.
(Fig.
The dorsal surface of the head and temporal region are bluish-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 distinctly paler than the dorsal surface of the head, namely pale bluish-green (pale green in life); thin and short bicoloured postocular strip (red and white), runs from the posterior part of the subocular to the angle of the jaw. The chin and throat are pale sea-green (yellow green in life), uniform but with few faint darker areas on infralabials sometimes. The eye is grey but it was deep fire-red in life. The venter is uniform pale sea-green (yellow green in life); dorsal tail heavily mottled with dark red blotches, the dark red blotches contiguous posteriorly; the ventral surface of the tail is as the venter anteriorly, tip of tail red on dorsal while dark salmon on ventral.
This description is based on the ten specimens examined by us, supplemented by data from 15 specimens published by
The maximum known total length is 925 mm in males (
Dorsal scales rhombohedral, more or less strongly keeled in males, weakly keeled in females, in 21-21-15 (73%) or 23-21-15 (23%) rows (exceptionally in 25-21-15 rows; 4%); scales of the first dorsal scale row smooth and not enlarged; 159–173 ventrals (plus one or two preventrals), rounded; 57–76 paired subcaudal scales with overlapping sexual dimorphism (64–76 in males, 57–70 in females); cloacal plate entire.
Rostral much broader than high, triangular, well visible from above; nasal subrectangular, entire, elongate, longer than high; one internasal on each side, pentagonal, curved, wide, transversely elongate, separated by one (90%) or rarely two (10%) small scales; four or five canthal scales, slightly larger than adjacent snout scales, bordering the canthus rostralis between the internasal and corresponding supraocular; one relatively large triangular loreal between the upper preocular and nasal; two 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; one supraocular on each side, entire, elongate and rather narrow, about 2.7–3.3 times longer than wide, about 0.5–0.9 times as wide as the internasals, indented on their inner margins by the upper head scales; cephalic scales relatively small, irregular or slightly rounded, juxtaposed, flat and smooth; 10–13 cephalic scales on a line between supraoculars; occipital scales rhombohedral, moderately or more frequently distinctly keeled in males, smooth or weakly keeled in females; temporals rhombohedral, distinctly keeled or less frequently smooth in males, always smooth in females; on each side, one thin, elongate, subocular scale, crescent-shaped; 2–3 small postoculars; 9–13 (usually 10–12) supralabials; first supralabial short, entirely separated from the nasal by a distinct suture; second supralabial tall, always forming the anterior border of loreal pit, separated from the nasal by one or two small scales; third supralabial the longest and highest, rather tall, usually separated from the subocular by one scale on each side (77.8%), rarely in contact (22.2%); fourth supralabial as long as high, lower than third supralabial, separated from subocular by one scale; fifth supralabial smaller than the fourth one, separated from the subocular by one or two scales of similar size; 10–15 (generally 12 or 13) infralabials, those of the first pair in contact with each other, the first three pairs in contact with the chin shields.
In life, the body is uniform bright green, grass-green, deep green, bluish-green or even turquoise blue (
The dorsal surface of the head and temporal region are uniform green or bluish-green like the body; the side of the head below the eye, i.e., the lower sides of the snout, nasal scale, and anterior supralabials and lower temporals, is distinctly paler than the dorsal surface of the head, generally pale green, yellowish-green or pale bluish-green; in males, a vivid, broad, bicolored postocular streak, the lower part narrow and white, the upper part broad and bright red, rusty-red or brownish-red, present at any age, extends from the postoculars obliquely towards the angle of the mouth then to the lower side of the neck where it connects to the ventrolateral stripe; in females, the postocular streak is usually absent, or present as a white and thin line. The chin and throat are generally pale yellowish-green, with infralabials sometimes bright yellow or marked with green. The eye is bright red, fire-red or deep red in life in adult specimens of both sexes (Fig.
Trimeresurus popeiorum, T. nebularis, and T. phuketensis in life. – Trimeresurus popeiorum: A Buxa Tiger Reserve, West Bengal, India (adult male); B Karimganj, Assam, India (adult female); C Aizawl, Mizoram, India (adult female); D Inn Gyin Taung Mt., Kachin, Myanmar (male); E Yingjiang, Yunnan, China (adult male); T. nebularis: F, G Cameron Highlands, Pahang, Malaysia (adult male and adult female, respectively); T. phuketensis: H Phuket Is., Phuket, Thailand (adult male); I Sri Phang Nga NP, Phang Nga, Thailand (adult male). Photos by: P. Ray (A), R. Gassah (B), G. Vogel (C, E-G), N. A. Poyarkov (D), R. Grassby-Lewis (H), and S. Plongnui (I)
The venter is uniform yellowish-green or pale green; tips of ventrals red as the lower part of the ventrolateral stripe. The ventral surface of the tail is as the venter anteriorly, becoming rusty-red on its posterior half to third.
The organ is long and thin, deeply forked, extending to the 25th or 26th subcaudal scale in situ, forked opposite at the level of the sixth to eighth subcaudal scales; the base of the organ, up to the point of bifurcation, is entirely smooth with longitudinal folds, except for the sulcus spermaticus; from the point of bifurcation up to the tip of the organ, each fork is finely calyculate. The sulcus is prominent; it divides near the base of the organ and ends near the tip of the fork (based on
Maxilla with one functional and 5–6 replacement fangs; palatine with four teeth, pterygoid with eight teeth, 10–12 dentary teeth (based on
(Fig.
Trimeresurus popeiorum inhabits hilly and montane regions covered with humid tropical and subtropical submontane and montane evergreen forests and semi-evergreen forests.
Chresonymy.
Trimeresurus gramineus
(non Coluber gramineus Shaw, 1802) –
Trimeresurus popeiorum
(non Trimeresurus popeiorum Smith, 1937) –
Popeia popeorum
[sic] –
Trimeresurus popeiorum popeiorum
(non Trimeresurus popeiorum Smith, 1937) –
Popeia
sp. 1 –
Trimeresurus cf. popeiorum
1 –
AUP-00180, an adult male from Siriphum Waterfall, Doi Inthanon National Park (18.5467°N, 98.5124°E; elevation 1450 m), Chiang Mai Province, Thailand; collected by P. Pawangkhanant, C. Suwannapoom, and N. A. Poyarkov on 30 August 2017.
(n = 8).
Chiang Mai Province: AUP-00178 (adult male), AUP-01574 (adult female) data same with holotype; FMNH 178656 (adult male), collected by O.G. Young, and
(n = 21). Thailand. Chiang Mai Province:
The new species name “lanna” represents a noun in apposition and is given in reference to the Lan Na Kingdom, or “Kingdom of a Million Rice Fields”. The Kingdom of Lan Na, also known as Lannathai, was centered in present-day northern Thailand from the 13th–18th centuries. The territories and cultural influence of the Lan Na Kingdom spread from easternmost Myanmar to northern Laos and southernmost present-day Yunnan of China, a geographic area that matches well the range of the new species. Though eventually the Lan Na Kingdom was united with the Siamese State in the early 19th century, its culture had a profound influence on different parts of northern Indochina. We suggest the following common names for the new species: “Ngu Khiew Hang Mai Thong Khiew Nua” (เขียวหางไหม้ท้องเขียวเหนือ) (in Thai), “Lán nà zhú yè qīng” (蘭納竹叶青) (in Chinese), “Lanna green pitviper” (in English), “Trimérésure vert du Lanna” (in French), “Lanna Bambusotter” (in German), and “Chiangmaiskaya bambukovaya kufiya” (in Russian).
Trimeresurus lanna differs from other members of the subgenus Popeia by the combination of the following morphological characters: (1) dorsal surfaces deep green, without crossbands; (2) in males, a vivid, wide, bicolored ventrolateral stripe, bright and deep red below, white above; 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 (93.3%) or rarely 20 (6.7%) dorsal scales rows at midbody, strongly keeled except those of the first dorsal scale row, always smooth; (6) 145–167 ventral plates (145–167 in males; 157–166 in females); 56–75 paired subcaudal scales with weak sexual dimorphism (59–75 in males, 56–64 in females); (7) first supralabial entirely separated from the nasal scale by a distinct suture; (8) supraoculars relatively narrow, narrower than internasals, separated by 10–13 cephalic scales; (9) internasals never in contact, separated by one or two scales; (10) hemipenes long and forked, reaching at least 25th SC, without spines; (11) 9–14 cephalic scales between the supraoculars in males, 11–13 in females; (12) relative tail length 0.18–0.21 in males, 0.16–0.17 in females.
(Fig.
Body cylindrical, long, and laterally compressed; SVL 640 mm, TaL 175 mm, TL 815 mm, TaL/TL 0.215. Head triangular in dorsal view, elongate, clearly distinct from the neck (HL 36.8 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 4.5 mm, SnL 11.3 mm, ED/SnL 0.40); pupil vertically elliptic.
Dorsal scales in 23-21-15 rows; dorsal scales all moderately keeled, except the first row the scales of which are smooth; 157 ventrals (plus single preventral); cloacal plate single; 71 subcaudals, all divided.
Rostral slightly visible from above, triangular, broader than high; one enlarged internasal on each side, internasals separated by one small scale behind the top of rostral (Fig.
Trimeresurus lanna sp. nov. in preservative. Specimen AUP-00180 (holotype, adult male): A Dorsal view of the head; B Ventral view of the head; C Lateral view of the head, right side; D General dorsal view. Specimen
(Fig.
The dorsal surface of the head and the temporal region are bluish-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 distinctly paler than the dorsal surface of the head, namely pale bluish-green (pale green in life); a broad, bicolored postocular streak, its ventral part narrow and cream (white in life) covering the lower row of temporals, its upper part, broader (two rows of temporals), pinkish-brown (bright deep red in life), extends from the postoculars obliquely towards the angle of the mouth but the postocular streak does not connect with the ventrolateral stripe. The chin and throat are pale sea-green (pale green in life), uniform but with few faint darker areas on infralabials sometimes. The eye is grey but it was deep fire-red in life. The venter is uniform pale sea-green (pale green in life); tips of ventrals of the same green color, not red. The ventral surface of the tail is as the venter anteriorly, becoming pinking-orange in its posterior quarter (reddish-brown in life).
(based on adult male
The longest known specimen is 845 mm long (SVL 709 mm, TaL 136 mm; female,
Dorsal scales in 23-21-15 (50%), 21-21-15 (36.7%), or rarely 25-21-15 (10%) and 22-21-15 (3.3%) rows, moderately or strongly keeled; scales of the first dorsal scale row smooth and not enlarged; 145–167 ventral plates (plus one or two preventrals), rounded; 56–75 subcaudal scales with a weak sexual dimorphism (59–75 in males, 56–64 in females), all paired; total number of VEN+SC: 213–241, without sexual dimorphism; cloacal plate entire.
The head scalation is as described for the holotype, with the following variation: internasals separated by one (84%) or rarely two (16%) small scales; three or four 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 their inner margins by the upper head scales; cephalic scales juxtaposed, flat and smooth; 10–13 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 (80%), rarely smooth (20%) in males, always smooth in females; on each side, one thin, elongate subocular scale, crescent-shaped; two or three small postoculars; 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; 10–14 (generally 12–13) infralabials, those of the first pair in contact with each other.
(Figs
Trimeresurus lanna sp. nov. in life. Thailand: A Doi Inthanon NP, Chiangmai (mating adult couple); B, C Doi Phu Kha NP, Nan, Thailand; D Doi Suthep-Pui NP., Chiangmai (subadult female); E Doi Luang Mt., Chiang Rai (adult male); F Umphang, Tak (adult male). Laos: G, H Phongsaly (adult male and female, respectively). China: I Mengla, Xishuangbanna, Yunnan, China (adult male). Photos by: P. Pawangkhanant (A, D), T. Smith (B, E, F), R. Jaihan (C), T. Calame (G), P. Brakels (H), and J. Ming (I).
The dorsal surface of the head and the temporal region are uniform green or bluish-green like the body; the sides of the head below the eye, i.e., the lower sides of the snout, nasal scale, and anterior supralabials and lower temporals are distinctly paler than the dorsal surface of the head, pale green or pale bluish-green; in males, the vivid, broad, bicolored postocular streak, white ventrally, bright red, rusty-red or brownish-red dorsally, is always present; in females, the postocular streak is usually absent (85.7%) or present as a white and thin line (14.3%). The chin and throat are pale green or pale sea-green, uniform or with infralabials marbled with green. The eye is bright red, fire-red or deep red in specimens of both sexes. The venter is uniform pale green or pale sea-green; tips of ventrals green. The ventral surface of the tail is as the venter anteriorly, becoming rusty-red on its posterior half to third.
We here compare T. lanna with the four other species of the subgenus Popeia (T. nebularis, T. phuketensis, T. popeiorum, and the T. sabahi complex). The main diagnostic characters separating the new species from these four species are summarized in Table S4.
Trimeresurus lanna is morphologically very similar to T. popeiorum but it is distinguished from this latter species by having: (1) lower max TL in males (815 mm vs. 925 mm), but higher max TL in females (884 mm vs. 854 mm); (2) slightly lower number of ventral plates in males (145–167, x̄ = 159.9 vs. 162–171, x̄ = 165.7; p = 0.0004); (3) slightly lower total number of VEN+SC in males (213–241, x̄ = 227.81 vs. 229–240, x̄ = 234.71; p = 0.0004); (4) bicolor postocular streak in males broad, covering 2–3 temporal scales vs. narrow, covering 1–2 temporal scales; (5) temporals strongly keeled in males (vs. feebly keeled).
Trimeresurus lanna is distinguished from T. nebularis by having: (1) eye color deep red in both sexes vs. usually green; (2) bicolor postocular streak present in males vs. absent; presence of a white ventrolateral stripe in females vs. absent; (3) lower max TL in both sexes (815 mm in males, 854 mm in females vs. 1002 mm in males, 948 mm in females); (4) higher total number of VEN+SC in both sexes (213–241, x̄ = 228.1 vs. 210–218, x̄ = 214.0 in males; p = 0.007; 213–229, x̄ = 221.2 vs. 197–210, x̄ = 205.6 in females; p = 0.021).
Trimeresurus lanna differs from T. phuketensis by having: (1) higher max TL in both sexes (815 mm in males, 854 mm in females vs. 640 in males,748 mm in females); (2) lower total number of VEN+SC in both sexes (213–241, x̄ = 227.8 vs. 242–249, x̄ = 246.4 in males; p = 0.0032; 213–229, x̄ = 221.2 vs. 226–237, x̄ = 230.6 in females; p = 0.015); (3) eye color deep red in both sexes vs. copper; (4) body without dorsal crossbands vs. present and conspicuous.
Trimeresurus lanna can be further differentiated from the five subspecies of T. sabahi as follows:
– from T. s. barati by having: (1) 21 dorsal scales rows at midbody (vs. 17–19); (2) eye color deep red in both sexes vs. deep orange; (3) bicolor postocular streak present in males vs. absent; (4) slightly higher max TL in both sexes (815 mm in males, 854 mm in females vs. 740 mm in males, 720 mm in females);
– from T. s. buniana by having: (1) dorsum uniform bright green vs. dark bluish-green or verdigris with conspicuous reddish-brown or violet, irregular crossbands; (2) eye color deep red in both sexes vs. copper; (3) bicolor postocular streak (red plus white) present in males vs. postocular streak reddish-brown; (4) slightly lower ratio TaL/SVL in both sexes (0.18–0.21, x̄ = 0.20 vs. 0.22–0.23, x̄ = 0.22 in males; p = 0.007; 0.14–0.17, x̄ = 0.16 vs. 0.21 in females); (5) lower total number of VEN+SC in both sexes (213–241, x̄ = 228.5 vs. 246–250, x̄ = 248.0 in males; p = 0.0004; 213–229, x̄ = 221.4 vs. 231 in females);
– from T. s. fucatus by having: (1) slightly lower ratio TaL/TL in both sexes (0.18–0.21, x̄ = 0.20, vs. 0.19–0.24, x̄ = 0.22 in males; p = 0.000002; 0.14–0.17, x̄ = 0.16 vs. 0.16–0.19, x̄ = 0.17 in females; p = 0.05; (2) eye color deep red in both sexes vs. copper; (3) dorsal crossbands absent in males vs. present; (4) white vertebral spots absent vs. present; (5) bicolor postocular streak wide (red plus white) present in male vs. sometimes absent, or white, or white with its upper part dark red and thin;
– from T. s. toba by having: (1) eye color deep red in both sexes vs. deep orange; (2) ventrolateral stripe bicolor, wide in males vs. white and thin; (3) slightly higher max TL in both sexes (815 mm in males, 854 mm in females vs. 730 mm in males, 798 mm in females);
– from T. s. sabahi by having: (1) bicolor postocular streak present in males vs. absent; (2) slightly lower TaL/TL ratio in both sexes (0.18–0.21, x̄ = 0.20 vs. 0.19–0.24, x̄ = 0.21 in males; p = 0.05; 0.14–0.17, x̄ = 0.16 vs. 0.17–0.18, x̄ = 0.18 in females; p = 0.04); (3) slightly higher total number of VEN+SC in females (213–229, x̄ = 221.2 vs. 212–217, x̄ = 214.7; p = 0.034).
Furthermore, in western Laos and northern Thailand T. lanna may be recorded in sympatry with the superficially similar T. (Viridovipera) gumprechti David et al., 2002. The two species can be easily distinguished from each other by hemipenial morphology: in the new species hemipenes are long, slender and deeply forked, reaching in situ at least the 25th subcaudal, lacking spines (vs. hemipenes short, thick, barely forked and strongly spinous, extending at most up to the 13th–15th subcaudals in T. gumprechti). Furthermore the eye of T. lanna is always deep red or fire-red in life in both sexes (vs. eye in life red in males, copper or yellow in females in T. gumprechti); and the head is flat with a distinctly obliquely truncated snout (vs. snout barely obliquely truncated, rather rectangular or rounded in T. gumprechti).
Trimeresurus lanna is currently known from a large expanse in northern Indochina around the infamous “Golden Triangle”, including southeastern Myanmar. Based on our data, we establish the distribution of this species as follows: Myanmar (southeastern part of the country: Mon and Kayah States, and the Bago Region). China (Yunnan Province: Puer, Jinghong, and Mengla Counties). Laos (Houaphan, Luangnamtha, Luangphrabang, Oudomxay, Phongsali, Xaignabouli, and Vientiane Provinces). Thailand (northern and western parts of the country: Chiang Mai, Chiang Rai, Kamphaeng Phet, Kanchanaburi, Lampang, Mae Hong Son, Nan, Tak, and Uthai Thani Provinces; the southern limit of the range is in Sri Sa Wat District, Kanchanaburi). The occurrence of the new species in Shan and Kayin States of Myanmar, in the province of Bokeo in Laos, and in Phayao and Phrae Provinces in Thailand, is strongly anticipated.
Trimeresurus lanna typically inhabits humid tropical submontane primary evergreen and secondary forests, subtropical montane evergreen, semi-evergreen and mixed forests, as well as mixed secondary submontane forest, generally at elevations between 600 and 2000 m but it can be found at much lower elevations in suitable cool and humid habitats. It feels also at home in moist monsoon and other deciduous forests, bamboo thickets, and plantations. In Chiang Mai Province, Thailand, it is normally found in evergreen submontane and montane forest at elevations between 500 and 1700 m. It occurs in regions where winter temperatures can be as low as 3–7°C. The preferred microhabitats of this pitviper are markedly cool, humid, and shaded places. It is generally associated with dense shrubs, thickets, bushes, scrubs, the foliage of low trees, and tall grasses. This species is generally found in the low, humid vegetation of riparian areas, especially in the vicinity of freshwater habitats.
Trimeresurus lanna is arboreal, crepuscular, and nocturnal. It is usually found coiled up above small streams or sometimes as high as 4 or 5 m above the ground. In Tak Province, Thailand, GV observed an individual on the ground in a submontane forest. In Oudomxay Province, Laos,
Further research is required to clarify the extent of the distribution, population size and trends before the conservation status of this new species can be assessed. Trimeresurus lanna is distributed over a large area including many protected areas. Across its range the new species generally seems to be quite common. The density of some populations may be high as
Chresonymy.
Trimeresurus gramineus
(non Coluber gramineus Shaw, 1802) –
Trimeresurus popeiorum
(non Trimeresurus popeiorum Smith, 1937) –
Trimeresurus popeiorum popeiorum
–
Trimeresurus
sp. nov. –
Trimeresurus cf. popeiorum
–
Popeia
sp. 2 –
Trimeresurus stejnegeri
(non Trimeresurus stejnegeri Schmidt, 1925) –
Viridovipera stejnegeri
–
Popeia fucata
(non Trimeresurus fucatus Vogel, David & Pauwels, 2004, now Trimeresurus sabahi fucatus) –
Trimeresurus cf. popeiorum
2 –
(n = 4). Thailand.
(n = 5). Thailand.
(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
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).
Trimeresurus tenasserimensis differs from other members of the subgenus 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.
(Fig.
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.
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.
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.
Trimeresurus tenasserimensis sp. nov. Specimen
(Fig.
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.
(see also Table S3). The longest-known specimen is 736 mm long (SVL 587 mm, TaL 149 mm; male,
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.
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.
(Figs
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).
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.
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.
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.
(Fig.
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 (
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).
The genus Trimeresurus has been one of the most taxonomically challenging groups of Asian snakes. Due to a high degree of morphological similarity between species, many Trimeresurus species have been misidentified in the past, and the interspecific and intrageneric classification of most of its members, including the subgenus Popeia, have remained contentious (
We also provide additional information on the morphological variation and distribution of T. popeiorum and restrict the distribution of this species to northeastern India, eastern Nepal, southern Bhutan, southeastern Bangladesh, western Yunnan (China), and northern and southwestern Myanmar. As a consequence, we propose to remove T. popeiorum from the snake faunas of Thailand, Laos, southern Yunnan Province (China), and southeastern Myanmar. We further describe the mainland Asian populations previously assigned to T. popeiorum as two new species: T. lanna for the populations from southern Yunnan, western Laos, northern Thailand and eastern mainland Myanmar, and T. tenasserimensis for the populations from Tenasserim Mountains in southeastern Myanmar and western Thailand.
Furthermore, we demonstrate that T. lanna consists of two divergent subclades, one in Thailand, Laos, and China, and the other in southeastern Myanmar. These two subclades differ by a significant genetic divergence, with a mean cyt b pairwise distance of 3.4%. The low sample size of the specimens from Myanmar examined in our study and the superficial morphological similarity between the specimens of the two clades of T. lanna hinders further assessment of their taxonomic status. Therefore, further studies are required to elucidate the taxonomic status of T. lanna populations from southeastern Myanmar.
As the present study is focused on the taxonomic relationships of the continental populations of the T. popeiorum species group, we do not provide significant insights on taxonomy of the populations inhabiting the islands of Southeast Asia and the Malay Peninsula, which was partially addressed in previous works (e.g.,
Trimeresurus sabahi complex in life. Thailand (T. sabahi fucatus): A Krung Ching Waterfall, Nakhon Si Thammarat (adult male), B, C Ron Phibun, Nakon Si Thammart (adult male and adult female, respectively). West Malaysia: D–E Raub, Pahang (adult male and adult female of T. sabahi fucatus, respectively); F Tioman Is., Pahang (adult female of T. sabahi buniana). East Malaysia (T. sabahi sabahi): G Kota Belud, Sabah (adult male), H Ranau, Sabah, (adult female). Indonesia: I North Sumatra, (adult male of T. sabahi toba), J Karo, North Sumatra, (adult female of T. sabahi toba); K, L West Sumatra (adult male and adult female of T. sabahi barati, respectively). Photos by: R. Grassby-Lewis (A), T. Smith (B, C), R. Harris (D), A. Tomaszek (E, H), O.B. Claesson (F, J), A. Kang (G), and G. Vogel (I, K, L).
In summary, our phylogenetic analyses of the subgenus Popeia suggest that several lineages are still poorly resolved and that most recognized species and subspecies constitute a rapid radiation, which likely speciated during a comparatively short time period. A phylogenetic resolution of the subgenus Popeia would likely require genomic-scale data, which would help establish the degree of isolation and gene flow among the OTUs reported in this work. Overall, the description of T. lanna and T. tenasserimensis brings the total number of species in the subgenus Popeia to six.
The distribution of the subgenus Popeia in mainland Asia seems to be shaped by the physical geography of the region. Trimeresurus popeiorum, according to our data, is distributed across the hilly and mountainous areas of Northeast India, the eastern Himalayas, northern Myanmar, and the westernmost part of Yunnan Province, China. Some other members of the herpetofauna show similar distribution patterns covering the northern part of the Indo-Burma Biodiversity Hotspot (e.g., Than Zaw et al. 2019;
The distribution of T. lanna is restricted to the mountainous areas of the Northwest Thai Uplands and the Northeast Thai–Lao Uplands (see
The distribution of T. tenasserimensis is restricted to the Tenasserim Range, a chain of hills and mountains that exhibit high levels of herpetofaunal diversity and endemism (e.g.,
However, the taxonomic status of the Popeia populations distributed between the Isthmus of Kra and the Khlong – Marui Fault (Ta Pi Line of
Despite receiving much taxonomic interest from the 1930s to the present day, the existing reports on distribution of species of the subgenus Popeia both at the national and regional levels remained highly controversial. Below we will address some long-standing questions of Popeia species distribution in Bhutan, China, Myanmar, Thailand, and Laos.
In Bhutan.
In China.
In Myanmar.
In Thailand.
Similarly,
Previous studies (
In Laos. Under the combination T. popeiorum,
The Indo-Burma Biodiversity Hotspot is known for its rich biodiversity, including herpetofauna (
Furthermore, the Indo-Burma Region, as currently known, hosts the highest number of species of Trimeresurus pitvipers in the world. With the description of two new species of the subgenus Popeia, the present study brings the total number of Trimeresurus species recorded in this region to 32, including: 17 species of the subgenus Trimeresurus: T. albolabris; T. ayeyarwadyensis
Despite recent progress on the taxonomy of Asian pitvipers, our knowledge of the diversity and distribution of several species still remains incomplete. Furthermore, along with the venomous elapid snakes (such as Naja spp. and Bungarus spp.), members of the genus Trimeresurus are responsible for a large percentage of the documented cases of snakebites in Southeast Asia and their medical importance cannot be underestimated (e.g.,
We would like to thank the Laboratory Animal Research Center, University of Phayao and The Institute of Animal for Scientific Purposes Development (IAD), Thailand for permission to do fieldwork. We are deeply grateful to Thanawut Worranuch, Thiti Ruangsuwan, Mali Naiduangchan, Kanokwan Yimyoo, Kawin Jiaranaisakul, Krarok Wongde and Priwan Srisom (Thailand) for help during the field surveys. We thank Nikolai L. Orlov (ZISP, Russia), George R. Zug (USNM, USA), Ton Smits and Rushen Jaihan (Thailand), Rupert Grassby-Lewis (Thailand); Jigme Tshelthrim Wangyal (Bhutan); Peter Brakels (IUCN, Laos), Thomas Calame (Laos); Artur Tomaszek (Hongkong, China), Jue Ming (China); Prajjwal Ray, Rejoice Gassah (India); Otto Bylén Claesson (Sweden); and Albert Kang (Malaysia) for sharing information and providing us photographs of Trimeresurus spp. N. A. Poyarkov thanks the members of MSU HerpLab including Vladislav A. Gorin, Evgeniya N. Solovyeva, Andrei M. Bragin, Alexey V. Trofimets, Nikita S. Klyukin, and Dmitriy V. Akhipov for support and assistance. S. Idiiatullina is thankful to Tanapong Tawan, Sunutcha Suntrarachun, Nararat Laopichienpong, and Apinya Longya (QSMI) for providing some important DNA samples and for helping in the lab. We also warmly thank Ngoc Quynh Nguyen (SIFASV, Vietnam) for help in the preparation of the figures. We thank warmly Patrick D. Campbell (
Tables S1–S4
Data type: .pdf
Explanation notes: Table S1. Species-level scientific names erected for the members of the subgenus Popeia. — Table S2. Resulting p-values from univariate morphological analyses comparing the geographic populations of the Trimeresurus popeiorum group from the Indo-Burma Region: Northeast India, northern Myanmar, and western Indochina. — Table S3. Main measurements and meristic characters of the type series and other specimens of Trimeresurus popeiorum s. str. (OTU1), T. lanna sp. nov. (OTU2), and T. tenasserimensis sp. nov. (OTU3). — Table S4 (Part 1–4). Comparison of morphological characteristics of Trimeresurus lanna sp. nov. (OTU2) and T. tenasserimensis sp. nov. (OTU3) with those of the subgenus Popeia.
Appendices I–VIII
Data type: .docx
Explanation notes: Appendix I. Primers used in this study. — Appendix II. Sequences and voucher specimens of the genus Trimeresurus and outgroup taxa used in This study. Locality number corresponds to those shown on the map in Figure