Research Article |
Corresponding author: Anh The Nguyen ( vietnamwildlife2012@gmail.com ) Corresponding author: L. Lee Grismer ( lgrismer@lasierra.edu ) Academic editor: Uwe Fritz
© 2022 Anh The Nguyen, Tang Van Duong, Perry L. Wood Jr., L. Lee Grismer.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Nguyen AT, Duong TV, Wood Jr. PL, Grismer LL (2022) Two new syntopic species of wolf snakes (genus Lycodon H. Boie in Fitzinger, 1826) from an imperiled ecosystem in the Song Giang River Valley of southern Vietnam (Squamata: Colubridae). Vertebrate Zoology 72: 371-384. https://doi.org/10.3897/vz.72.e82201
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An integrative taxonomic analysis of species in the colubrid genus Lycodon Fitzinger, 1826 recovered two new syntopic species of the L. rufozonatus complex from the imperiled Song Giang River valley in Khan Hoa Province, of Southern Vietnam. Although L. truongi sp. nov. and L. anakradaya sp. nov. are syntopic, they are not particularly closely related and can be differentiated from each other and all other species in the L. rufozonatus complex on the basis of meristics, morphometrics, color pattern, and uncorrected pairwise genetic distance based on the mitochondrial gene cytochrome b. The discovery of these two new range-restricted species and a previously described range-restricted gekkonid in the genus Cyrtodactylus Gray, 1828 from the same valley, underscores the necessity of continued field work in the Song Giang River valley so as to catalog the unrealized herpetological diversity in this area and establish research-based conservation programs.
Colubrid, conservation, integrative taxonomy, Khanh Hoa Province, Southeast Asia
The colubrid snake genus Lycodon Fitzinger, 1826 comprises a large radiation of at least 71 non-venomous, terrestrial to arboreal, nocturnal species that occupy a range of forested habitats extending from the Caspian Sea to Sulawesi (
Recent field work in the imperiled riparian habitats of the Song Giang River Valley in Khanh Hoa Province of Southern Vietnam (Fig.
The general lineage concept (GLC:
Morphological and color pattern data were taken from three specimens from Song Giang River Valley (12.37079°N, 108.83643°E; at elevation 500 m a.s.l.), Khanh Trung Commune, Khanh Vinh District, Khanh Hoa Province, Vietnam and from literature on Lycodon banksi Luu, Bonkowski, Nguyen, Le, Calame and Ziegler, 2018; L. cathaya Wang, Qi, Lyu, Zeng, and Wang, 2020; L. chapaensis (Angel and Bourret, 1933); L. flavozonatus (Pope, 1928); L. futsingensis (Pope, 1923); L. meridionalis (Bourret, 1935); L. rufozonatus Cantor, 1842; and L. septentrionalis (Günther, 1875) of the L. rufozonatus complex (
All body measurements were made to the nearest millimeter. Morphometric data include snout-vent length (SVL), tail length (TaL), total length (ToL), head length, width, and height (HL, HW, and HH, respectively), eye diameter (ED), snout length (SnL), eye to narial distance (EN), and internarial distance (IND). Meristic data include maxillary teeth (MT); supralabial and infralabial scales (SL and IL, respectively); of SL contacting the eye (SL-E), loreals (LoR); LoR contacting the eye (LoR-E); preoculars (PrO); postoculars (PtO); anterior temporals (aTMP); posterior temporals (pTMP); dorsal scale rows one head length posterior to the head, at midbody, and one head length anterior to the vent presented in that order; ventral scales (VEN); subcaudal scales (SC); light-colored body bands (BB); and light-colored tail bands (TB). Discrete characters evaluated were body scale texture, cloacal plate divided or single, adult head color pattern, presence or absence of a wide nuchal-occipital collar in adults and/or juveniles, dorsal ground color, body bands thin (1–3 scales rows) or wide (> three scales rows), color of body bands, ventrolateral body pattern, and ventral pattern. The institutional acronym SIEZC refers to the Zoological collection of the Southern Institute of Ecology in Hochiminh City, Vietnam.
Sequence data from a 1,114 base pair fragment of the cytochrome b gene (cyt b) was obtained from 149 specimens comprising 40 species in GenBank and three specimens (SIEZC 20247–48, and SIEZC 20249) from Song Giang. Ahaetulla prasina (Boie, 1827), Boiga dendrophila (Boie, 1827), Gonyosoma oxycephalum (Boie, 1827, and Oligodon chinensis Günther (1888) were used as outgroups to root the tree following (Liu et al. 2020 in part). Genbank accession numbers for SIEZC 20247–49 are OM674283, OM674284, and OM674282, respectively.
Genomic DNA was isolated from muscle tissue stored in 95% ethanol following
Maximum likelihood (ML) and Bayesian inference (BI) were used to estimate the phylogenetic relationships among the sampled species in our sequence alignment. An ML phylogeny was estimated using the IQ-TREE webserver (
Both the ML and BI analyses recovered trees with the same general topology with high nodal support (Fig.
Uncorrected pairwise sequence divergence among species of the Lycodon rufozonatus complex based on 1114 base pairs of the mitochondrial gene cytochrome b. Bold numbers are intraspecific differences. *** indicates a sample size of one.
banksi | cathaya | chapaensis | flavozonatus | futsingensis | meridionalis | truongi sp. nov. | anakradaya sp. nov. | rufozonatus | septentrionalis | |
banksi | *** | |||||||||
cathaya | 0.098 | 0.000 | ||||||||
chapaensis | 0.078 | 0.070 | 0.008 | |||||||
flavozonatus | 0.090 | 0.094 | 0.063 | 0.008 | ||||||
futsingensis | 0.085 | 0.098 | 0.063 | 0.112 | 0.000 | |||||
meridionalis | 0.094 | 0.092 | 0.069 | 0.023 | 0.104 | 0.007 | ||||
truongi sp. nov. | 0.094 | 0.090 | 0.061 | 0.080 | 0.077 | 0.084 | *** | |||
anakradaya sp. nov. | 0.107 | 0.103 | 0.087 | 0.085 | 0.098 | 0.096 | 0.107 | 0.000 | ||
rufozonatus | 0.112 | 0.082 | 0.090 | 0.072 | 0.111 | 0.082 | 0.096 | 0.042 | 0.026 | |
septentrionalis | 0.081 | 0.056 | 0.040 | 0.061 | 0.047 | 0.053 | 0.043 | 0.064 | 0.067 | 0.034 |
Truong’s wolf snake — Rắn khuyết Trường.
Adult male (SIEZC 20249) collected on 22 December 2020 by Anh The Nguyen from Song Giang River Valley (12.37079°N, 108.83643°E; at elevation 500 m a.s.l.), Khanh Trung Commune, Khanh Vinh District, Khanh Hoa Province, Vietnam.
Lycodon truongi sp. nov. is separated from all other species of the L. rufozonatus complex by having the combination of a maximum SVL length of 700 mm; tail length 195 mm; 17–17–15 dorsal scale rows; 14 maxillary teeth; eight supralabials with the third–fifth contacting the eye; nine infralabials; one preocular; two postoculars; an elongate loreal not contacting the eye; two anterior temporals; two posterior temporals; 200 ventral scales; 91 paired subcaudal scales; a divided precloacal plate; 15 keeled vertebral scale rows from midbody to vent; uniform dark-brown to black adult head pattern; no wide light-colored nuchal-occipital collar in the adult; black dorsal ground color; 19 narrow white body bands; 13 white caudal bands; white dorsal bands on ventrolateral section of body as opposed to a reticulated pattern; anterior one-half of venter white, and posterior of venter bearing white and broken black bands. These characters are scored across all species of the L. rufozonatus complex in Table
Holotype of Lycodon truongi sp. nov. SIEZC 20249 from the Song Giang River Valley Khanh Trung Commune, Khanh Vinh District, Khanh Hoa Province, Vietnam. A Dorsal view of head. B Gular region. C Lateral view of head. D Dorsal view of body. E Ventral view of body. Photographs by Anh The Nguyen.
Diagnostic characters of Lycodon truongi sp. nov. and L. anakradaya sp. nov. that differentiate them from each other and all other species of the L. rufizonatus complex. Green cells denote characters that separate L. truongi sp. nov. and L. anakradaya sp. nov. from the other species. Orange cells denote characters separating L. anakradaya sp. nov. from all other species. Blue cells denote characters separating L. truongi sp. nov. from all other species. Data for previously described species come from Jansen et al (2019),
anakradaya sp. nov. | truongi sp. nov. | meridionalis | rufozonatus | flavozonatus | banksi | cathaya | chapaensis | septentrionalis | futsingensis | |
---|---|---|---|---|---|---|---|---|---|---|
Maximun SVL (mm) | 790 | 700 | 1295 | 980 | 901 | 415 | 730 | 890 | 990 | 663 |
DSR | 18–17–15 | 17–17–15 | 17–17–15 | 17/19–17–15 | 17–17–15 | 17–17–15 | 17–17–15 | 17-17-15 | 17 | 17–16/17–15 |
MT | 12 | 14 | 11 | 11–13 | 13 | ?/ | 10 | 11 or 12 | 8 | 12–15 |
SPL | 8 | 8 | 8 | 8 | 8 | 8 | 8 | 7 or 8 | 8 | 7–8 |
SPL-E | 3rd–5th | 3rd–5th | 3rd–5th | 3rd–5th | 3rd–5th | 3rd–5th | 3rd–5th | 4th–5th | 2nd–3rd | 2–4; 3/4–5; 4–6 |
IFL | 9 or 10 | 9 | 10 | 9–10 | 10 | 10 | 9 | 8–10 | 9 | 9–11 |
PrO | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
PtO | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2–3 |
Lor | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
Lor-E | no | no | no | no | no | no | no | no | no | no |
aTMP | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 1–2 |
pTMP | 3 | 2 | 3 | 3 | 2–3 | 3 | 3 | 2 or 3 | 3 | 2–3 |
VEN | 225–232 | 200 | 227–240 | 184–225 | 211–221 | 241 | 199 or 200 | 200–225 | 207–212 | 193–208 |
SC | 87 | 91 | 96–106 | 53–98 | 80–88 | 26 (broken tail) | 78 | 74–84 | 78 | 72–87 |
PrC | divided | divided | divided | entire | entire /divided | entire | entire | entire | entire | entire |
BSC | 5 keeled vertebral rows from midbody to vent | 15 keeled vertebral rows from midbody to vent | 10–12 medial rows distinctly keeled | weakly keeled posteriorly | 7 keeled medial rows | 6 central scales of posterior 1/3 weakly keeled | smooth | posterior vertebral row weakly keeled | keeled | smooth |
Adult head pattern | uniform dark-brown/black | uniform dark-brown/black | black w/ yellow sutures | dark-brown w/ reddish sutures | black w/ yellow markings | uniform dark-grey | uniform dark-brown to black | uniform black | uniform black | greyish brown |
Dorsal ground color | dark-brown/black | black | black | dark-brown/black | black | dark-brown/black | black | black | dark-brown/black | dark-brown |
Ventrolateral body pattern | banded | banded | reticulated | reticulated | reticulated | reticulated | reticulated | banded | banded | banded |
Ventral pattern | orangish anteriorly grading to brown posteriorly | white anteriorly black and white banded posteriorly | / | / | / | unicolor grey-cream | / | / | ||
Wide nuchal-occipital band in adults | absent | absent | absent | absent | absent | absent | present | absent | absent | present |
Wide nuchal-occipital band in juveniles | absent | / | absent | absent | absent | / | present | absent | present | present |
Light-colored BB | 12 or 13 | 19 | 84–115 | 44–52 | 51–78 | 87 | 31–35 | 28 | 33–35 | 19–33 |
Body bands narrow or wide | wide | thin | thin | thin | thin | thin | thin | thin | thin | wide |
Color BB in adults | orangish | white | yellow (adult) | reddish | yellow | yellow | light-rose | white | white | light-rose |
Light-colored TB | 5–7 | 13 | 25–35 | 20 | 17–24 | 15 | 13–16 | 11 | 19 | 8–19 |
(Figs
Body elongate, somewhat laterally compressed; SVL 700 mm; TaL 195 mm; ToL 895 mm; 200 ventrals, 91 paired subcaudals; cloacal shield divided; dorsal scales in 17–17–15 rows with 15 keeled vertebral rows from midbody to vent; vertebral row not enlarged; no apical pits.
Meristic, morphometric, and discrete color pattern and scale morphology characters of the type specimens of Lycodon truongi sp. nov. and L. anakradaya sp. nov. All measurements are in millimeters.
anakradaya sp. nov. | truongi sp. nov. | ||
NAT21-11 holotype | NAT21-8 paratype | ||
SVL | 790 | 230 | 700 |
TaL | 190 | 55 | 195 |
TL | 980 | 285 | 895 |
HL | 27.8 | 11.8 | 16.0 |
HW | 18.0 | 7.1 | 12.9 |
HH | 11.8 | 4.6 | 7.6 |
ED | 4.0 | 2.3 | 2.5 |
SnL | 8.2 | 3.5 | 6.3 |
EN | 5.2 | 2 | 4.8 |
IND | 6.0 | 2.6 | 5.6 |
MT | 12 | 12 | 14 |
DSR | 18–17–15 | 17–17–15 | 17–17–15 |
Keeled vertebral rows | 3 | 0 | 15 starting at midbody |
VEN | 225 | 232 | 200 |
SC | 87 | 91 | |
Cloacal plate | divided | divided | divided |
SL (right and left) | 8 | 8 | 8 |
SL-L | 2nd–3rd | 2nd–3rd | 2nd–3rd |
SL-E | 3rd–5th | 3rd–5th | 3rd–5th |
LoR | 1 | 1 | 1 |
LoR-E | 0 | 0 | 0 |
PrO | 1 | 1 | 1 |
PtO | 2 | 2 | 2 |
aTMP | 2 | 2 | 2 |
pTMP | 3 | 3 | 2 |
IL (right and left) | 10 | 9 | 9 |
BB | 13 | 12 | 19 |
TB | 7 | 5 | 13 |
Head pattern | uniform dark-brown | dark-brown plates edged with white | uniform dark-brown |
Wide nuchal-occipital band in juveniles | absent | absent | absent |
Dorsal ground color | dark-brown | black | black |
Ventral pattern | orangish anteriorly grading to brown posteriorly | white anteriorly grading to dark-brown banding posteriorly | white anteriorly, black and white banded posteriorly |
Ventrolateral body pattern | banded | banded | banded |
Wide nuchal-occipital band in adults and juveniles | absent | absent | absent |
Body bands narrow or wide | wide | wide | thin |
Color of body bands | orange | white | white |
(Figs
The specific epithet “truongi” is a patronym honoring Professor Dr. Quang Truong Nguyen for his long-standing extensive contributions to the herpetology of Vietnam and his broad international collaborations.
(Fig.
(Table
Rhade wolf snake – Rắn khuyết Ê đê.
Adult male (SIEZC 20247) collected on 21 December 2020 by Anh The Nguyen from Song Giang River Valley (12.37079°N, 108.83643°E; at elevation 493 m a.s.l.), Khanh Trung Commune, Khanh Vinh District, Khanh Hoa Province, Vietnam.
Juvenile (SIEZC 20248) collected on 21 August 2020 by Anh The Nguyen from Song Giang River Valley (12.37079°N, 108.83643°E; at elevation 580 m a.s.l.), Khanh Trung Commune, Khanh Vinh District, Khanh Hoa Province, Vietnam.
Lycodon anakradaya sp. nov. is separated from all other species in the L. rufozonatus complex by having the combination of a maximum SVL length of 790 mm; TaL 190 mm; 17 or 18–17–15 dorsal scale rows; 12 maxillary teeth; eight supralabials with the 3rd–5th contacting the eye; nine or 10 infralabials; one preocular; two postoculars; an elongate loreal not contacting the eye; two anterior temporals; three posterior temporals; 223–232 ventral scales; 87 paired subcaudal scales; a divided precloacal plate; five keeled vertebral scale rows from midbody to vent; uniform dark-brown to black adult head pattern; no wide light-colored nuchal-occipital collar; dark-brown/black dorsal ground color; 12 wide, orangish body bands; 5–7 orangish caudal bands; orangish dorsal bands on ventrolateral section of body as opposed to a reticulated pattern; and anterior one-half of venter orangish grading into a dark-brown posteriorly. These characters are scored across all species of the L. rufozonatus complex in Table
(Figs
Body elongate, somewhat laterally compressed; SVL 790 mm; TaL 190 mm; ToL 980 mm. 225 ventrals, 87 paired, subcaudals; cloacal shield divided; dorsal scales in 18–17–15 rows with three keeled vertebral rows; vertebral scale row not enlarged; no apical pits.
(Figs
(Figs
Holotype of Lycodon anakradaya sp. nov. SIEZC 20247 from the Song Giang River Valley Khanh Trung Commune, Khanh Vinh District, Khanh Hoa Province, Vietnam. A Dorsal view of head. B Gular region. C Lateral view of head. D Lateral view of a portion of the body. E Dorsal view of body. F Ventral view of body. Photographs by Anh The Nguyen.
Paratype of Lycodon anakradaya sp. nov. SIEZC 20248 from the Song Giang River Valley Khanh Trung Commune, Khanh Vinh District, Khanh Hoa Province, Vietnam. A Dorsal view of head. B Gular region. C Lateral view of head. D Dorsal view of body. E Lateral view of body. Photographs by Anh The Nguyen.
The specific epithet “anakradaya” is given in a reference to the Ede people (“Anak Radaya” in Ede language), an Austronesian ethnic group living in the upland forested areas of southern Vietnam including those that surround the Song Giang River valley.
(Fig.
(Table
The discovery of Lycodon truongi sp. nov. and L. anakradaya sp. nov. brings the total of number of Lycodon in Vietnam to 18. Prior to these descriptions, the newest species to be described from the Vietnam was L. pictus Janssen, Pham, Ngo, Le, Nguyen, & Ziegler 2019 from Cao Bang Province, ~1.300 km overland distance to the north from the Song Giang River Valley. Other than that, the only addition of Lycodon to southern Vietnam was L. cardamomensis
We thank the Bureau of Forestry, Ministry of Agriculture and Rural Development of Vietnam and of administration of Khanh Hoa Province for permitting the fieldwork. Anh The Nguyen thanks Doan Manh Tuan, Vu Long (Center for Biodiversity conservation and Endangered Species) and Bui Huu Manh for numerous support and assistance in during the field surveys. Sincere thanks go to Dr. Le Khac Quyet (Fauna & Flora International), Dr. Nguyen Thien Tao (Institute of Genome Research), Dr. Hoang Minh Duc, and Tran Van Bang (Southern Institute of Ecology). Tang Van Duong expresses his gratitude to Leaders of Vietnam National Museum of Nature (VNMN) for supporting his work in Lab. Molecular analysis of this research were supported by Vietnam National Foundation for Science and Technology Development (NAFOSTED) under grant number 18/2020/STS02.