Trimeresurus (Popeia) popeiorum Smith, 1937

Mirza, Zeeshan A., H. T. Lalremsanga,, Bhosale, Harshal, Gowande, Gaurang, Patel, Harshil, Idiatullina, Sabira S. & Poyarkov, Nikolay A., 2023, Systematics of Trimeresurus popeiorum Smith, 1937 with a revised molecular phylogeny of Asian pitvipers of the genus Trimeresurus Lacepede, 1804 sensu lato, Evolutionary Systematics 7 (1), pp. 91-104 : 91

Trimeresurus (Popeia) popeiorum Smith, 1937

Figs 2 , 3 , 4

Trimeresurus popeiorum Smith (1937).

Popeia popeorum Malhotra & Thorpe (2004a), Wallach et al. (2014), Guo et al. (2015).

Trimeresurus (Popeia) popeiorum David et al. (2011).

Trimeresurus yingjiangensis Chen, Zhang, Shi, Tang, Guo, Song & Ding, (2019), syn. nov.

Type material.

Lectotype: NHMUK 72.4.17.137, a male from 'Khasi Hills’ now in Meghalaya State, India. Designated by Taylor and Elbel (1958).

Additional material.

‘India’.

Diagnosis.

A Trimeresurus bearing 21 (rarely 19) dorsal scale rows at midbody with an overall bright green colour, lacking bands; males may bear a bicoloured postocular stripe and a bicoloured ventrolateral stripe is always present. SVL 414-692 mm in males, 417-710 mm in females. Hemipenis deeply forked, reaching the 25th subcaudal. Ventrals 158-170 in males, 161-169 in females; subcaudals 62-76 in males, 55-66 in females; nasal and first supralabial separate. TaL 107-194 mm in males, 75-139 mm in females; TaL/TL 0.18-0.22 in males, 0.14-0.19 in females. Palatine with four teeth; pterygoid with eight teeth; 10-12 dentary teeth. Maxilla with one functional and 5-6 replacement fangs.

Description based on examined specimens

(n = 19). Body long and moderately stout, SVL 414-600 mm; head triangular and elongate, head length 20-24.3 mm (HL/SVL 0.04-0.05); head width 13.4-21 mm; (HW/HL 0.64-0.88) clearly distinct from neck; distance between nostrils 3.8-7 mm; distance between preoculars 8.6-12.8 mm; distance between the tip of snout and anterior border of eye 6.6 mm; distance between nostril to eye 5.1-6.7 mm. Canthus rostralis distinct; a single large scale between the nasal and supraocular. Rostral subtriangular, slightly visible when viewed from above; nasal and first supralabial separate, wider than tall; three internasals, the outer pair of internasals larger than the one in the middle, and the one in the middle less than half the width of the outer ones. bordered by six scales on its posterior margin; two small scales separate the third supralabial from the nasal; second and third supralabial and three preoculars encompass the loreal pit; the lower preocular forms the lower margin of the loreal pit; one elongate and narrow supraocular; cephalic scales (CEP) small, irregular, subimbricate, smooth; longitudinal cephalic scales 27-31, gradually increasing in size towards the posterior part of the head; 10-11 CEP between anterior edge of the supraoculars and 14-17 at the posterior edge; occipital scales smooth; seven rows of scales between the internasals and anterior border of the supraoculars flat and irregular in their shape; the rows towards the posterior part of the head gradually show a feeble keel; temporals feebly keeled and subequal; subocular crescent shaped; 9-13 supralabials; SL1 not fused with nasal scale, 2nd much higher than 1st, 3rd highest among the supralabials; 4th widest, separated from the subocular by a single row of smooth scales and the lower loreal scale; 4th supralabial separated from the subocular by two rows of smooth scales; the remaining supralabials slightly decreasing in size posteriorly and in contact with temporal scales; 10-13 infralabials, the first pair in contact with each other; the first three pairs in contact with anterior chin shields; six pairs of chin shields, each pair in contact medially; separated from infalabials by 1-5 scale rows.

Body scalation.

19, 21 or 23 dorsal scales one head length behind the head (rarely 17); 21 dorsal scales at midbody, rarely 19; 13-15 dorsal scales one head length anterior to the vent; dorsal scales rhomboid, moderately keeled except for the first row which is smooth; 0-3 preventrals; ventrals 158-170 in males, 161-169 in females ventral scales; subcaudals 62-76 in males, 55-66 in females subcaudal scales; paired; single cloacal plate. Eye large, with VED/DEL ratio 0.85; tail short; ventrally depressed; TaL 107-194 mm in males, 75-139 mm in females; TaL/TL 0.18-0.22 in males, 0.14-0.19 in females. Tail prehensile. Hemipenis long and deeply forked at the 5-6th subcaudal, extending to the 23-25th subcaudal scales, calyculate throughout the arms of the fork, lacking spines.

Description of the skull

(Fig. 2 ). The skull of T. popeiorum displays the typical shape found in other members of the genus Trimeresurus . The skull is well calcified except for the premaxilla which remains largely cartilaginous, and base of non-functional teeth. The braincase, or neurocranium, is composed of the prefrontals, frontals, jugals, parietal, supraoccipital, prootics, otoccipitals, basioccipital, and parabasisphenoid. The general shape of the braincase is trapezoid in dorsal view (Fig. 2b ); with the main openings well visible in lateral view (Fig. 2a ). Fenestra ovalis (between the otooccipital and prootic), foramina of trigeminal and facial nerves (on the prootic), and the foramen opticum (between the frontal, the parietal, and the basisphenoid) (Fig. 2a ). Columella, or stapes, is well-visible attached to the fenestra ovalis (Fig. 2a ).

Frontals paired, articulated with each other with a straight median suture (Fig. 2b ); ventrally articulated with the parabasisphenoid, anteriorly with the prefrontals and the nasals, and posteriorly with the parietal and the jugals. Dorsally the frontals have a squared shape with slightly convex posterior and anterior margins. The parietal single, anteriorly articulated with the jugals and the frontals, ventrally with the parabasisphenoid and posteriorly with the supraoccipitals and the prootics. The parietal is a large bone which has almost a triangular shape in dorsal view (Fig. 2b ) with almost straight anterior margin, short outward protruding dorsal jugal transverse processes bound by the jugals, and distinct crests seen in the lateral aspect (Fig. 2a ). Parietal foramen is absent. The suppraoccipital is a single bone, anteriorly articulated with the parietal, posterolaterally with the otoccipitals, and anetrolaterally with the prootics. In dorsal aspect the anterior margin of the supraoccipital is triangularly concave (Fig. 2b ); occipital crests straight, directed posterolaterally, forming a narrow angle with the sagittal crest. The prefrontals paired, subrectangular in dorsal view (Fig. 2b ), ventrally articulated with the maxillae, posteriorly with the frontals; with which they are articulated via a long prefrontal caudal ramus. The prefrontals are perforated with a lacrimal foramen. The jugals (in some works referred to as postorbitals, see ( Szyndlar 1984)) are paired bones, medially articulated both with the frontals and the parietal. The jugals are semi-crescent in shape with an irregular posterior margin (Fig. 2a ).

The snout is composed by the nasals dorsally (Fig. 2b ), premaxilla anteriorly (Fig. 2a ), septomaxillae and the vomers ventrally (Fig. 2c ), the latter form the bony capsule of the Jacobson’s organ. Nasals paired, posteriorly articulated with the frontal, ventrally with the septomaxilla; dorsally each nasal triangular in shape, with anterior tip bearing a poorly-ossified anterior process (Fig. 2b ). The dorsal margin of the posterior part of the nasal is gently rounded. The premaxilla is an unpaired, poorly ossified bone, posteriorly articulated with the vomers and the septomaxilla, with an unpaired posterior nasal process (Fig. 2b ). The vomers are bubble-shaped paired bone, containing the Jacobson’s organ. The vomer is dorsally articulated with the septomaxilla, and anteriorly with the premaxilla (Fig. 2c ). The capsular expansion of vomer well-developed, with a wide surface directed anterodorsally. The septomaxilla is a paired bone located in the center of the snout, articulated anteriorly with the premaxilla, dorsally with the nasals, and ventrally with the vomers; it cannot be observed in lateral or ventral aspects of the whole skull.

In ventral view (Fig. 2c ) the floor of the skull is formed by the basioccipital and the parabasisphenoid. The parabasisphenoid is a single bone forming the ventral surface of the braincase, ventrally bearing a deep longitudinal cavity with a median crest. It is articulated anterodorsally with the frontals, dorsally with the parietal, posterodorsally with the prootics and posteriorly with the basioccipital. In ventral view, the bone is elongated oval-shaped, with a long and spatulate parasphenoid process; the basisphenoid crest well-developed (Fig. 2c ). The basioccipital is an unpaired bone anteriorly articulated with the parabasisphenoid, anterolaterally with the prootics, and posterolaterally with the otoccipitals. The anterior margin of the basioccipital is gently concave; its’ posterior margin forms the ventral surface of the foramen magnum. The prootic is a paired bone, anteriorly articulated with the parietal, posteriorly with the supraoccipital and the otoccipital, and ventrally with the parabasiphenoid. In lateral aspect, the foramen nervi trigemini is well seen in the middle part of the bone; this bone forms the anterior edge of the foramen ovale (Fig. 2a ). The otoccipital is formed by the ossae opisthotici and the exoccipital (occipitale laterale). This paired bone is articulated with the supraoccipital and the prootic anteriorly, with its controlateral equivalent along a straight suture medially, and with the basioccipital ventrally. It forms the posterior edge of the foramen ovale (Fig. 2a ).

The upper jaw includes the maxilla, the pterygoid, the palatine, and the ectopterygoid which form a movable connection to each other; with only the latter bone lacking teeth. Maxillae are large paired bones, kinetically articulated posterodorsally with the prefrontals and posteriorly with the ectopterygoids. Maxillae are massive bones bearing venom teeth; dorsally with a thick triangular prefrontal process forming the maxillary-prefrontal articulation, and laterally with a large fossa (Fig. 2a ). Maxilla bears one functional and 5-6 replacement fangs (venom teeth); the functional fang is slightly longer than the body of the maxilla. The quadrates and the supratemporals are kinetically connected and put together the neurocranium and the lower jaw (Fig. 2a ). The palatine is a paired short bone, posteriorly kinetically articulated with the pterygoids, bearing from four to five tooth alveoli with four functional teeth (Fig. 2c ). The pterygoid is a large paired bone, anteriorly articulated with the palatine, posteriorly with the quadrate, and posterodorsally with the ectopterygoid. This bone is distinctly dorsoventrally bent and is slightly V-shaped in lateral aspect, bearing a pterygoid crest (Fig. 2a ). Posteriorly the pterygoid bears the facet for the attachment of the ligamentum quadrato-pterygoidei. The anterior half of the pterygoid is slightly curved and slender, it broadens abruptly near the middle of the bone, and flattens out, with an outward curve. The pterygoid bears from 13 to 14 tooth alveoli with eight functional teeth (Fig. 2c ). The ectopterygoid, or transversum, is a paired bone which lacks teecth, and is articulated with the maxilla anteriorly and with the pterygoid posteriorly. The bone is alost spatualte in the anteior part, and gets thinner posteriorly (Fig. 2c ). In dorsal view, the ectopterygoid spans out laterally, nearly half the width of the frontal (Fig. 2b ). The supratemporals are paired, long and relatively thin bones, anteriorly articulated with the prootics, and posteriorly with the quadrates (Fig. 2a ). The quadrate is a paired bone, anterodorsally articulated with the supratemporal and posteroventrally forming a jaw articulation with the compound bone. The trochlea quadrati is a saddle-like articular facet in the posterior part of the quadrate, kinetically articulated with the posterior portion of the compound bone (Fig. 2a ).

Each mandible includes the splenial, the angular, the dentary, and the compound bone. The paired compound bone forms the posterior part of the mandible and articulates anteriorly with the dentary, anetromedially with the splenial and angular, and posteriorly is kinetically connected with the quadrate, forming the jaw articulation (Fig. 2a ). The coronoid process of the compound bone is well-developed. The retroarticular process occupies the posteriormost part of the compound bone (Fig. 2a ). This process is well-developed, thick, and medially curved in dorsal and ventral views (Fig. 2b, c ). The saddle-like articular facet for the reception of the quadrate is located anteriorly to the retroarticular process, forming the jaw articulation. In lateral view, the supraangular foramen for the mandibular branch of the trigeminal nerve is seen on the compound bone (Fig. 2a ). The angular is a paired bone, which articulates anteriorly with the splenial and the dentary, and posterolaterally is articulated with the compound bone. The splenial is a paired bone of the mandible, which is anteriorly articulated with the dentary, posteriorly with the angular, and posterolaterally with the compound bone. Both the angular and the splenial are not seen in the lateral, but only on the medial aspect of the mandible. The dentary is a paired bone, articulated with the angular and the compound bone posteriorly and with the splenial posteromedially. In lateral view, the mental foramen is visible on the dentary, it is located closer to the articulation with the compound bone than to the anterior edge of the dentary. The ventral posterior process of the dentary is slightly longer than the dorsal one (Fig. 2a ). The dentary is the only tooth-bearing bone of the lower jaw, and bears from 10 to 12 functional teeth.

Colouration in life

(Fig. 3 ). Males overall in a shade of bright green throughout, slightly lighter ventrally. Scales on the dorsum are green with cyan edges. Bicoloured postocular strip, usually red and white, runs from the posterior part of the subocular to the angle of the jaw. The line extends all the way up to the tail; the outermost dorsal scale row bears a white spot at the tip and is blood red for the rest of the part, bordered by the second row, which is white in its lower half and green on its upper half. The tail in both sexes may be rusty, red or brown. The ventrolateral aspect of the tail in males may bear a discontinuous stripe. The females lack the postocular and ventrolateral stripes. The ventral scales bear a slight yellowish tinge. The males may lack the postocular stripe. The eyes of both sexes are blood red.

Hemipenial morphology

(everted organ n = 2, Fig. 4 ). Trimeresurus popeiorum has a hemipenis pattern corresponding fairly well to the overall pattern of the T. macrolepis group ( Peng and Fuji 2000). Retracted organ is deeply bilobed, extends up to the 25th subcaudal and bifurcates at 6th subcaudal. The organ is bicalyculate with long, slender lobes that are twice the length of the body; capitulum restricted to sulcate and dorsal surface. The lobes are calyculate throughout; dense calyces on the distal half which transits to slightly enlarged, shallow calyces with fleshy, unadorned ridges at the base of the lobes. Sulcus spermaticus simple; the sides of the sulcus spermaticus are smooth; truncus and hemipenial base is completely nude.

Figures

Figure 2. MicroCT scan of the skull of male Trimeresurus popeiorum (NCBS NRC-AA- 0010) in lateral (A), dorsal (B) and ventral (C) aspects, showing osteological features of members of the subgenus Trimeresurus Popeia. Abbreviations: bo. - basioccipital; c. p. - coronoid process; col. - columella (stapes); comp. - compound bone; d. - dentary; ecp. - ectopterygoid (transversum); f. n. t. f. - foramina of trigeminal and facial nerves; f. op. - foramen opticum; f. ov. - fenestra ovalis; f. sa. - supraangular foramen; fr. - frontal; jug. - jugal; me. f. - mental foramen; mx. - maxilla; nas. - nasal; ot. - otoccipitals; p. r. - a. - retroarticular process; pal. - palatine; par. - parietal; pbs. - parabasisphenoid; pmx. - premaxilla; prf. - prefrontal; pro. - prootics; pt. - pterygoid; q. - quadrate; soc. - supraoccipital; st. - supratemporal; t. q. - trochlea quadrati; vom. - vomer.

Figure 3. Images depicting colouration of Trimeresurus popeiorum in life, (a) a complete profile of a male Trimeresurus popeiorum from Kamlang Wildlife Sanctuary, (b) anterior body showing the bicolored postocular and ventrolateral stripe, (c) dorsal view of head, (d) female lacking the stripes from the same locality. Photos by Zeeshan A. Mirza.

Figure 4. Hemipenis of T. popeiorum MZMU 3043. Photo by Andrey Bragin.