Bungarus suzhenae, Chen & Shi & Vogel & Ding & Shi, 2021

Chen, Ze-Ning, Shi, Sheng-Chao, Vogel, Gernot, Ding, Li & Shi, Jing-Song, 2021, Multiple lines of evidence reveal a new species of Krait (Squamata, Elapidae, Bungarus) from Southwestern China and Northern Myanmar, ZooKeys 1025, pp. 35-71 : 35

Bungarus suzhenae sp. nov. Figs 6G, H , 7G, H , 8A-C , 9J-K , 10 , 11 , 12 , 13

Bungarus multicinctus multicinctus - Yang and Rao 2008, specimen from Yingjiang, Yunnan, China

Type material.

Holotype. CIB 116088 (Fig. 9 ), subadult male, collected from a road through rice fields in Yingjiang County, Yunnan Province, China (97.584451, 24.662632, 922 m A.S. L), by Ding Li, in 2017. The holotype was a victim of roadkill and was fixed and stored in 80% ethanol .

Paratypes. One adult male CIB 116089 (24.466941°N, 97.648691°E, 934 m A.S. L), one adult female CIB 116090 (24.634715°N, 97.762291°E, 1559 m A.S. L), one sub-adult male CIB 116091 from Yingjiang County (24.560296°N, 97.827170°E, 798 m A.S. L). The specimens were preserved in 80% ethanol .

Diagnosis.

Assigned to genus Bungarus based on the presence of a row of enlarged, hexagonal scales on the vertebral scale row, enlarged prezygapophyseal accessory process and relatively high neural spine ( Slowinski 1994). The new species differs from its congeners by having a combination of the following characters: (1) posterior maxilla teeth three, slightly curved behind (Fig. 8A-C ); (2) fangs feebly curved; (3) dorsal scales in 15 rows; (4) ventrals 220-229 (n = 4); (5) subcaudals undivided, 51-54 (n = 3); (6) anterior chin shields larger than the posterior ones (Fig. 10E ); (7) prefrontal suture 2.7-3.4 (n = 3) times length of internasal suture (Fig. 10C, D ); (8) adult and subadult heads uniform black (Figs 10 - 12 ); (9) dorsal body color black, with 39.3 ± 4.7 (26-38) white narrow bands present on midbody, covering 1.5 ± 0.4 (1.0-2.0) vertebral scales; (10) ventral surface uniform white, underside of tail white with tiny brown dots in the middle or immaculate (Figs 10 - 12 ); (11) ventral scales connected with the black bands of the dorsal body by small dark patches in lateral view, patches smaller than half the width of a dorsal scale; (12) tail relatively long, TaL/TL = 0.136 -0.150 (n = 3); (13) hemipenes reaching 7th subcaudal; (14) large, elongated and pointed spines on hemipenes, in fang-shaped (Fig. 9J-L ); (15) tips of the large spines strongly keratinized, without distinct boundary with the main body of large spines.

Comparison.

Comparisons of Bungarus suzhenae sp. nov. with other Bungarus species are shown in Table 1 . Bungarus suzhenae sp. nov. differs from B. flaviceps by: (1) dorsal scales in 15 rows (vs. 13 rows); (2) dorsal body and tail black with white bands (vs. body black with or without light vertebral and paraventral stripes, tail bright red); (3) head uniform black (vs. head red or yellowish-tan).

Bungarus suzhenae sp. nov. differs from B. fasciatus by: (1) subcaudal scales 51-54 (n = 3) (vs. 23-39, n =?); (2) dorsal body black with white bands (vs. with broad yellow rings between the dark rings); (3) dorsal head uniform black (vs. with V-shaped marking on the posterior of the head).

Bungarus suzhenae sp. nov. differs from B. bungaroides by: (1) subcaudals undivided (vs. divided); (2) Dorsum with 26-38 white bands (vs. 40-60 narrow white rings composing of small white spots); (3) ventral body uniform white (vs. blackish with irregular yellowish white pattern in every 3 to 4 scale intervals).

Bungarus suzhenae sp. nov. differs from B. slowinskii by: (1) subcaudals undivided (vs. divided); (2) anterior chin shields larger than the posterior chin shields (vs. anterior chin shields similar with posterior chin shields); (3) dorsal head uniform black (vs V-shaped marking present on head); (4) dorsal body and tail with black bands, ventral body uniform immaculate yellowish-white (vs. body with pattern of dark and white rings).

Bungarus suzhenae sp. nov. differs from B. ceylonicus by: (1) subcaudal scales 51-54 (n = 3) (vs. 34-40, n =?); (2) ventral body uniform immaculate yellowish white (vs. ventral body with broad dark crossbands).

Bungarus suzhenae sp. nov. differs from B. lividus Cantor, 1839 by: (1) vertebral scales distinctly enlarged (vs. only slightly enlarged on the anterior body); (2) subcaudal scales 51-54 (n = 3) (vs. 41, n = 1); (3) dorsal body black with white bands (vs. no bands or rings or with narrow white rings).

Bungarus suzhenae sp. nov. differs from B. niger by: (1) dorsal body black with white bands (vs. no bands or rings on body) ( Wall 1908); (2) tail relatively longer (TaL/TL = 0.136 -0.150 n = 3 vs. 0.132 n = 1).

Bungarus suzhenae sp. nov. differs from B. magnimaculatus by: (1) more subcaudal scales (51-54 n = 3 vs. 40-48); (2) dorsum with 26-38 white bands, narrower than black bands in between (vs. 11-14 broad, white crossbars, as wide as the black interspaces).

Bungarus suzhenae sp. nov. differs from B. andamanensis Biswas & Sanyal, 1978 by: (1) more ventral and subcaudal scales (220-229 n = 4 and 51-54 n = 3 vs. 192-197 n = 4 and 45-47 n = 4); (2) a shorter tail (TaL/TL = 0.136 - 0.150 n = 4 vs. 0.155- 0.16 n = 4); (3) dorsum with 26-38 white bands (vs. 44 white linear arches or bars, mottled with brown); (4) head uniform black (vs. head is chocolate); (5) ventral body uniform white (vs. anterior and lateral margin of ventral scales tinged with brown).

Bungarus suzhenae sp. nov. differs from B. sindanus by: (1) fewer dorsal scale rows (15 vs. 17); (2) dorsal body colouration (black with white crossbands, and bands mostly complete vs. black with crossbands formed by series of white spots and interrupted).

Bungarus suzhenae sp. nov. differs from B. walli Wall, 1907 by: (1) fewer dorsal scale rows (15 vs. 17 rows); (2) dorsal body coloration (black with white crossbands, and bands mostly complete vs. body black above with crossbands formed by series of white spots and interrupted); (3) a higher number of ventral scales (220-229 n = 4 vs. 198-207 n = 8).

Bungarus suzhenae sp. nov. differs from B. persicus Abtin, Nilson, Mobaraki, Hooseini & Dehgannejhad, 2014 by: (1) fewer dorsal scale rows (15 vs. 17); (2) fewer ventral scales (220-229 n = 4 vs. 236-238 n = 2); (3) loreal plate absent (vs. present); (4) dorsal body coloration (black with white bands vs. body with crossbars ending in pairs of small rectangular whitish dots or short crossbars).

Bungarus suzhenae sp. nov. differs from B. caeruleus by: (1) dorsal body coloration (black with white crossbands, and bands mostly complete vs. narrow transverse white streaks or with small white spots); (2) white bands not in pairs (vs. at least some white bands occurring in pairs).

Bungarus suzhenae sp. nov. is morphologically most similar to phylogenetically closest congeners in B. candidus / Bungarus multicinctus / Bungarus wanghaotingi complex. However, it differs from the latter by multiple morphological characters. See hemipenis and maxilla comparisons in Tables 2 , 3 . The new species differs B. multicinctus by: (1) fang shape (less distinctly curved vs. distinctly curved); (2) lesser posterior maxilla teeth (three vs. four); (3) relatively longer prefrontals suture (length 2.7-3.4 times of internasals suture n = 3 vs. 1.3-2.3 times, n = 16); (4) ventral body coloration in adults (immaculate white, n = 4 vs. white scattered with dense brown pigments, n = 19); (5) black bands on body (large, length 4-7 times of vertebral scales on middle body, not reaching ventrals or just stained the edges of it, ventrals with black edges smaller than half of outer dorsal scales vs. black bands on body moderate, length 3-4 times of vertebral scales, intruding to ventrals for 1.2 to 2 times of width of outer dorsal scales); (6) ventral tail colouration (white with tiny brown dots in the middle or immaculate vs. with dense black bands or patches); (7) relatively shorter hemipenis (reaching 7th subcaudal vs. 9th subcaudal); (8) shape of large spines on hemipenes (elongated, fang-shaped, pointy vs. papilla-like and blunt); (9) tips of large spines on hemipenis (strongly keratinized, without distinct boundary with the main body of large spines vs. weakly keratinized, in shape of short bar, with a distinct boundary with main body of large spine).

Bungarus suzhenae sp. nov. differs B. candidus by: (1) fewer posterior maxilla teeth (three vs. four); (2) white bands on dorsal body more and narrower (26-38 white bands on dorsal body, width covering 1.0-1.5 vertebral scales on middle dorsum, n = 4 vs. 19-26 white bands on dorsal body, width covering 3.0-5.0 vertebral scales, n = 18); (3) prefrontal suture relatively longer (2.7-3.4 times length of internasals suture, n = 3 vs. 1.4-2.4 times, n = 17); (4) coloration on the upper head surface and neck (uniform black on adults and juvenile vs. temporal area and lateral neck light brown in adults, lateral necks and dorsal head posterior to eyes of immatures creamy white; (5) ventral tail colouration (white with tiny brown dots in the middle or immaculate vs. with broad dark crossbands); (6) black bands on body (not intruding to ventral body, ventrals with narrow black edges smaller than half of outer dorsal scales vs. intruding to the ventral body, narrow black edges on ventrals with width 1-2 times of outer dorsal scales).

Bungarus suzhenae sp. nov. differs from typical B. wanghaotingi by: (1) slightly curved fangs (slightly curved and arc-like vs. distinctly curved); (2) fewer posterior maxilla teeth (three vs. four); (3) shorter hemipenis (reaches 7th subcaudal vs. 9th subcaudal); (4) shape of large spines on hemipenis (elongated, fang-shaped (vs. relatively short and blunt); (5) the degree of keratinization of the large hemipenial spines (strongly keratinized vs. weakly keratinized).

Description of holotype.

(Fig. 10 ). Subadult male. Head relatively long, length 21.0 mm, maximal head width at anterior temporals 12.3 mm; maximal head height 8.7 mm, head 1.7 times longer than wide, distance between eyes 9.3 mm. Body length 620 mm; tail complete, 109 mm; total length 729 mm.

Body scalation.

Ventrals 221, preventrals 3, anterior edge of first ventral starting at level of oral rictus; azygous scale immediately anterior to cloacal scale, half in width of the ventrals. Cloacal plate undivided. Subcaudals 53 undivided, tail complete. Dorsal scales smooth, in 15-15-15 rows; vertebral scales distinctly enlarged, largest and hexagonal at midbody, slightly wider than long.

Head.

Cephalic scales smooth. Rostral near Λ-shaped, width 1.6 times of height visible from above. Nasals large, constricted and divided into one prenasal and one postnasal on both sides at border with internasals and first supralabial, prenasals irregular-shaped while postnasals crescent-shaped. External nares large, vertical oval-shaped, slightly smaller than eye diameter. Postnasal-preocular suture short and straight. Preocular hexagonal, bordered by third and fourth supralabials. Internasals two, 1.1 times wider than long, in contact with rostral, prenasals and postnasals, preoculars, and prefrontals. Prefrontals large, slightly wider than long; internasals suture short, prefrontals suture length 2.9 times of internasals suture and not aligned with latter. Frontal shield-shaped, pointing posteriorly, 1.3 times longer than wide, bordered by prefrontals, supraoculars and parietals; anterior suture of frontal pointed toward prefrontal suture, dividing posterior ends of prefrontals; supraoculars small, 1.7 times longer than wide, in contact with preoculars, upper postoculars, prefrontals, frontal and parietals. Parietals large and long, distance between end of parietals to preoculars 1.5 times the length of frontal; bordered by frontal, supraoculars, upper postoculars, one anterior temporal and two upper posterior temporals on each side, and three smalls nuchal scales on posterior margins. Posterolateral margins of parietals bordered by 1/1 enlarged elongate scales that anteriorly contact upper posterior temporals. Posterior extension of parietals pointed, divided in the middle by one of those three small dorsal scales. Preoculars 1/1, long hexagon, bordering with postnasal, second and third supralabials, prefrontal, and supraocular. Eyes small, oval, horizontal diameter 2.3 mm, vertical diameter 1.9 mm. Postoculars 2/2; relatively small with half size of preoculars; each lower postocular bordered by fourth and fifth supralabials, orbit, anterior temporal, upper postocular; each upper postocular bordered by lower postocular, orbit, supraocular, parietal but not anterior temporal. Anterior temporals 1/1, long and hexagonal, length 2.9 times of width; each bordered by fifth and sixth supralabials, lower postocular, parietal, posterior temporals. Posterior temporals 2/2, bordering parietals, anterior temporals, sixth and seventh supralabials, and enlarged elongate scales bordering posterolateral margin of parietals. Supralabials 7/7, the third and fourth supralabials forming lower margin of orbit; first supralabials small, triangular, with pointed extension behind, not reaching preoculars, 1.4 times higher than wide; other supralabials in different subpentagonal shapes; second supralabials long and pentagonal-shaped, larger than the first, 1.8 times higher than wide; third supralabials larger than the former two, and the fourth, 1.5 times higher than wide; the fourth supralabials more or less rectangular, 1.6 times higher than wide; fifth and sixth supralabials are among the two largest, both 1.1 times higher than wide and similar in size, but fifth supralabials wider at lower part while the sixth supralabials is wider at the upper part; seventh supralabials height equal to width. Mentals moderate, width slightly shorter than width of rostral, triangular, bordering first infralabials, mental groove distinct. Infralabials 7/7 first infralabials pentagonal-shaped, long and narrow, in broad contact behind the mental and anterior chin shields; second infralabials in form of a square, half size of the first; the third and fourth enlarged; first, second, and third infralabials in broad contact with anterior chin shields, fourth infralabials in broad contact with posterior chin shields. Anterior chin shields larger than the posterior chin shields, the two pairs of chin shields in form of butterfly wings; anterior chin shield suture 3.5 times the length of the posterior chin shield suture; posterior chin shields 1.6 times longer than wide, bordered by anterior chin shields, fourth infralabials, 2/2 sublabials, and three gulars. Four gulars between first ventral and posterior most extension of each posterior chin shield; one gular and three preventrals between first ventral and suture of posterior chin shields, preventrals wider than half of first ventrals, gradually larger from first preventral to third.

Coloration in preservative.

Dorsal surface of head, upper part of sides of the head, including upper part of supralabials, uniform black; lower half of head, including lower part of supralabials and rostral yellowish-white; ventral head uniform yellowish-white; iris dark black.

Dorsal body black with 38 white narrow crossbands (including incomplete bands). White bands on body scattered with tiny dark patches. Length of bands 1.0 to 2.0 times vertebral scales (average 1.2 ± 0.2), bands widening on flanks before joining the ventral surface, which is uniform white. 10 out of 38 bands incomplete, only present on one side of the dorsal body. First band starts at the 13th ventral, nine vertebral scales between first and second band; following bands gradually denser and brighter, three vertebral scales between 37th and 38th band. Most bands wider on outer row of dorsal scales, a dark spot present at junctions where the white bands meet the ventrals; black bands on body wide, covering 5-6 vertebral scales on middle body, not intruding to venter, ventrals with narrow black edges smaller than half of lateral dorsal scales. Venter immaculate yellowish-white, lateral edges of ventrals between dorsal white bands black.

Dorsal surface of tail black; 12 immaculate white bands present on dorsal part, width about equal to the width of one vertebral. Ventral portion of tail yellowish white, 23 of intermittent subcaudals with small brown dots; subcaudals between white bands margined with brown laterally (Fig. 10 ).

Variation.

Paratypes largely resemble the holotype in scalation and color but differ in the following characters: upper postoculars of one adult male (CIB 116090) and one subadult male (CIB 116091) bordered by the anterior temporal on both sides. Ventral tail of CIB 116089, CIB 116090 (for remaining part) and CIB 116091 immaculate instead of mottled with small dots. First to 10th and the 12th white crossbands on dorsum of CIB 116090 disconnected, forming moderate white dots covering two vertebral scales. Posterior chin shields suture of CIB 116090 barely exist. The dorsal bands are fewer in CIB 116091 (Fig. 12 ).

Cranial osteology.

The premaxilla of B. suzhenae sp. nov. is quite small and blunt, the ascending process of the premaxilla is well-developed, meeting the nasals at its dorsal edge. The nasal process of the premaxilla is not conspicuous. The nasal is peltate, with a blunt process on the lateral margin. The mesial process of the prefrontal is quite slender and pointed, narrowly reach the anterior tip of the frontal. Frontal triangular in shape from dorsal view. The distal process of the postorbital is slender and slightly anteriorly pointed, the basal part is in contact with the posterolateral marge of the frontal. A fenestra notch present on the posterolateral marge of the frontal. Two sides of the anterior surfaces of the parietal form the angle of approximately 120 degrees. The parietal is approximately “T” shaped; the lateral process is conspicuous and rectangular. The dorsal ridge of the parietal is more conspicuous in adults than in juveniles. The posterior end of the dorsal ridge merges at the mesial of the parietal in adults whereas separated in juveniles. The prefrontal surface of maxilla conspicuously upheaved. The supratemporal is flexed whereas the angular surface to the quadrate is obviously incrassated. The quadrate is quite short and stubby, the anterior angular surface to the supratemporal is extended. The ventral process of the basioccipital is trifurcate. The maxilla process (lateral process) of the palatine quite small whereas the choanal process is absent. The pterygoid is slender and medially curved, with the ectopterygoid process lost. The compound bone is quite stocky, the mesial crest and lateral crest are low and inconspicuous.

The first fang is canaliculated and feebly curved behind. There are four or five replacement fangs posterior to the first. Three small solid teeth ranged on the posterior end of maxilla, decrease in size posteriorly and separated from the fang by a very large diastema. Palatine teeth 10 (11), pterygoid teeth 10 (9); dentary teeth 16 (15), 2, 3 and 4 largest, decrease in size posteriorly. (Fig. 13 ).

The DOI numbers for ADMorph: 10.12112/ R. 0003 ( CIB 116088 , holotype) and 10.12112/ R . 0004 ( CIB 116090 , paratype) .

Hemipenes.

Description is based on the adult male paratype CIB 116089 (Fig. 9J-L ; SVL 1,140 mm). Hemipenis reaches 7th subcaudal, slightly bilobed near top. Three zones of similar length of ornamentation exist: a distal calyculate zone, a spinose zone proximal to the sulcus bifurcation, and a basal zone. The line of demarcation between the calyculate zone and spinose zones is poorly defined. The calyculate zone is capitate; calyces well developed, gradually smaller and lesser keratinized towards the distal end; calyces nearest the sulcus intruding to the spinous zone by few ranks. The spinose zone is covered with large spines; large, elongated and pointed spines on hemipenes, in fang-shaped, gradually thinner from bases to tips; tips of large spine strongly keratinized, without distinct boundary with the main body of large spines; the spines adjacent to the calyces are nearly twice as large as the most proximal ones in a sulcate view. The hemipenis slightly constricts between the spinose zone and the basal zone. The basal zone is covered with numerous minute spines on the larger distal part, and smooth proximal region. The sulcus is forked distally along the spinose zone, with the bifurcation originating at a distance of about one large spine length; lips bearing calyces in calyculate zone, and small spines throughout the spinose region.

Etymology.

The specific epithet of the new species was named after Su-Zhen Bai, a famous powerful goddess of Chinese myth The legend of the White snake (白蛇传), in honor of her courage to true love and kindness to people. The common name is suggested as “Suzhen’s krait" in English and "素贞环蛇 ( sù zhēn huán shé)” in Chinese.

Distribution and ecology.

Bungarus suzhenae sp. nov. was found in rice fields, streams in monsoon forest at elevation from 800 m to 1,560 m. This species is distributed in Yingjiang Country, Yunnan Province, China and Kachin State, Myanmar (Fig. 1 ). In captivity, they prey on eels like Monopterus albus and small snakes such Xenochrophis flavipunctatus , Pareas spp., but refuse mice and frogs .

Figures

Figure 1. Distribution map of molecular samples localities of Bungarus in this study.

Figure 6. Dorsolateral head view of adults (left) and juveniles (right) of the Bungarus candidus / Bungarus multicinctus / Bungarus wanghaotingi complex and B. suzhenae sp. nov. A B. multicinctus, adult male, CIB DL 2019051701 from Lishui, Zhejiang, China B B. multicinctus, juvenile female, CIB DL 18090209 from Fujian, China C B. candidus, adult female, NMW 9486: 1 from Pelambang, Java D B. candidus, juvenile female, NMW 27730: 4 from Tasikmalaya, Java E B. wanghaotingi, adult male, CIB MLML 20170801 from Jiangcheng, Yunnan, China F B. wanghaotingi, unknown sex juvenile, CIB JCR 36 from Jiangcheng, Yunnan, China G B. suzhenae sp. nov. adult female, CIB 116090 H B. suzhenae sp. nov. subadult male, CIB 116088.

Figure 7. Body patterns of adults (left) and juveniles (right) of the Bungarus candidus / Bungarus multicinctus / Bungarus wanghaotingi complex and B. suzhenae sp. nov. A B. multicinctus, adult male CIB DL 2019051701 from Lishui, Zhejiang, China B B. multicinctus juvenile female, CIB DL 18090209 from Fujian, China C B. candidus, adult male, NMW 27711: 1 from Bandong, Java D B. candidus, juvenile male, RMNH 11416 from Pelambang, Java E B. wanghaotingi, adult male, CIB MLML 20170801 from Mengla, Yunnan, China F B. wanghaotingi, unknown sex juvenile CIB JCR 36 from Jiangcheng, Yunnan, China G B. suzhenae sp. nov. adult male, CIB 116089 from Yingjiang, Yunnan, China H B. suzhenae sp. nov. subadult male, CIB 116088 from Yingjiang, Yunnan, China.

Figure 8. Maxilla morphology of seven members of subfamily Elapidae. Lateral (A) lingual (B), and ventral (C) view of the left maxilla of CIB 116090 (the paratype of B. suzhenae sp. nov.), compared with other members of the subfamily Elapinae D B. wanghaotingi SYNU R 170408, from Yala, Thailand E B. multicinctus, from Guangdong, China F B. fasciatus, from Guangdong, China G Naja atra from Guangdong, China H N. melanoleuca from Kimpese, Congo I Ophiophagus Hannah from Guangxi, China. Scale bars: 5 mm, note that H and I had been scaled down at 1 / 2. Al = alveoli.

Figure 9. Hemipenial morphology of the Bungarus candidus / Bungarus multicinctus / Bungarus wanghaotingi complex and B. suzhenae sp. nov. Sulcate view (left), asulcate view (middle), spines (right) A-C B. multicinctus, CIB DL 2019051701 from Lishui, Zhejiang, China, body length 993 mm D-F B. candidus, RH 06153 from Quang Binh Province, Vietnam, body length 1200 mm G-I B. wanghaotingi, CIB MLML 20170801 from Mengla, Yunnan, China, body length 1170 mm J-L B. suzhenae sp. nov., CIB 116089 from Yingjiang, Yunnan, China, body length 1140 mm.

Figure 10. Holotype of Bungarus suzhenae sp. nov. (CIB 116088) A dorsal view of body B ventral view of body C dorsal view of head D left lateral view of head E right lateral view of head.

Figure 11. Paratype of Bungarus suzhenae sp. nov. in life (Adult female CIB 116090).

Figure 12. Paratypes of Bungarus suzhenae sp. nov. in preserve A dorsal and ventral B view of adult female CIB 116090 C dorsal view of adult male CIB 116089 D dorsal view of juvenile male CIB 116091.

Figure 13. Three-dimensional reconstructed skull models of the holotype (A-C CIB 116088, subadult male) and paratype (D, E CIB 116090, adult female) of Bungarus suzhenae sp. nov. Dorsal (A, D), ventral (B), lateral (C, E) view. Scale bar: 10 mm.