Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 June 2024 | 16(6): 25385–25399
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.8935.16.6.25385-25399
#8935 | Received 31
January 2024 | Final received 29 May 2024 | Finally accepted 13 June 2024
First record of two species of
venomous snakes Bungarus suzhenae and Ovophis
zayuensis (Serpentes: Elapidae, Viperidae) from India
Jason Dominic Gerard 1,
Bitupan Boruah 2, V. Deepak 3 &
Abhijit Das 4
1,2,4 Wildlife Institute of India, Chandrabani, Dehradun, Uttarakhand 248001, India.
3 School of Natural and
Environmental Sciences, Newcastle University, Newcastle upon Tyne NE1 7RU, UK.
3 Natural History Museum, London
SW7 5BD, UK.
1 jasondg95@gmail.com, 2 bitupan.kaz@gmail.com,
3 veerappandeepak@gmail.com, 4 abhijit@wii.gov.in
(corresponding author)
Editor: S.R. Ganesh, Kalinga Foundation, Agumbe, India. Date
of publication: 26 June 2024 (online & print)
Citation: Gerard,
J.D., B. Boruah, V. Deepak & A. Das (2024). First record
of two species of venomous snakes Bungarus suzhenae and Ovophis
zayuensis (Serpentes: Elapidae, Viperidae) from India. Journal of Threatened Taxa 16(6):
25385–25399. https://doi.org/10.11609/jott.8935.16.6.25385-25399
Copyright: © Gerard et al. 2024. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: 1. Science and Engineering Research Board (SERB), Govt. of India; 2. National Geographic Society.
Competing interests: The authors declare no competing interests.
Author details: Jason D. Gerard is a researcher with interest in taxonomy and ecology of reptiles. Bitupan Boruah is a
PhD scholar whose interests are systematics and biogeography of lesser-known fauna such as amphibians and reptiles. V.
Deepak is a researcher whose work predominantly focuses on the evolution and systematics of lizards, snakes and turtles in southern Asia. Abhijit Das is a scientist and faculty involved in teaching, training and research in Herpetology.
Author contributions: JDG and BB equally contributed to this work. BB, AD and JDG carried out field work for this study. JDG and BB examined the specimens. AD and BB conceptualized the study. BB and DV contributed to the phylogenetic analyses and data verification. All authors contributed equally to the writing and editing of this
manuscript.
Acknowledgements: We are grateful to the state Forest Department of Nagaland and
Arunachal Pradesh for permitting us to carry out the study (via CWL/GEN/81/580
dated 31 August 2012 and CWL/GEN/355/2021/3178 dated 28th September 2021, respectively). We thank Taluk Rime (DFO, Anini), Kashok Solung (RFO, Anini), and Basant Taye (Forester, Anini) for their support during the field study. We are thankful to SERB-DST
(CRG/2018/000790) for financial support and the National Geographic Society for the award of the National Geographic Explorer Grant
(NGS-74044R-20). We are thankful to the director and dean of the Wildlife
Institute of India, Dehradun for their support. We thank Neelam Dutta, Naitik G. Patel, Santanu Dey, Saurabh Dutta, Rajiv N.V., Gaurav Rai Pariyal, Hachi Molo, Dochi Meli, and Bhaiti for their help during fieldwork. We thank A. Madhanraj, Surya Prasad Sharma, Surya Narayanan, and Kumudani Bala Gautam for their help. We thank Fred Pluthero and section editor, JoTT for their valuable comments in the earlier
version of this manuscript.
Abstract: We report Bungarus
suzhenae Chen, Shi, Vogel, Ding & Shi, 2021
and Ovophis zayuensis
(Jiang, 1977) for the first time from India. Specimens of B. suzhenae and O. zayuensis
were collected during our field surveys in north (Arunachal Pradesh) and south
(Nagaland-Manipur border) of the river Brahmaputra. Species identity was
supported by partial cytochrome b (cyt b),
and 16s mitochondrial gene. We provide a detailed morphological description and
a key to the two genera of this region. This report extends the westernmost
distribution of B. suzhenae by ca. 300 km from
Myanmar, and the southernmost range of O. zayuensis
by 170 km from Tibet. Until now eight species of Bungarus
and only one Ovophis species have been
reported from India. Ovophis species are
recently reported to be medically important venomous snakes whose venom
properties have not been investigated in depth.
Keywords: Krait, northeastern India, pit
viper, range extension, taxonomy.
INTRODUCTION
Northeastern India is part of the
Indo-Burma biodiversity hotspot (Tripathi et al. 2016) and home to
approximately 21 species of venomous snakes from the families Viperidae and Elapidae (Ahmed et al. 2009; Captain et al. 2019; Mirza et
al. 2020; Rathee et al. 2022; Biakzuala
et al. 2023 and 2024). Biodiversity explorations are continuing to reveal new
information on snake diversity (Elangbam et al. 2023;
Biakzuala et al. 2024). The Elapid genus Bungarus Daudin, 1803
consists of 18 species (Uetz et al. 2024),
distributed from Iran and Pakistan eastwards to China and Indonesia (Chen et
al. 2021). Eight species of Bungarus have been
reported from India, namely, B. andamanensis
Biswas & Sanyal, 1978, B. caeruleus Schneider, 1801, B. sindanus
Boulenger, 1897, B. walli
Wall, 1907, B. lividus Cantor, 1839, B. fasciatus Schneider, 1801, B. niger
Wall, 1908, and B. bungaroides Cantor, 1839,
of which the latter four are found in northeastern India (Ahmed et al. 2009;
Das & Das 2017; Das 2018; Biakzuala et al. 2021).
Recently, Chen et al. (2021) described B. suzhenae
from China that is currently known from the type locality Yingjiang
County, Yunnan Province, China, and the adjacent Kachin State of Myanmar.
There are eight species in the
viperid genus Ovophis (Burger, 1981), namely:
O. makazayazaya (Takahashi, 1922); O. jenkinsi Qiu et al., 2024; O.
malhotrae Zeng, Li, Liu, Wu, Hou,
Zhao, Nguyen, Guo & Shi, 2023; O. monticola (Gunther,
1864); O. okinavensis (Boulenger,
1892); O. tonkinensis (Bourret,
1934); and O. zayuensis (Jiang, 1977)
(Malhotra et al. 2011; Zeng et al. 2023; Qiu et al.
2024; Uetz et al. 2024). The southernmost
record of O. zayuensis is from Zayu, Motuo, Xizang province,
China. During a herpetological field survey in northeastern India in 2012,
2022, and 2023, we came across one individual of Bungarus
and two individuals of Ovophis. They
were collected and based on morphological evaluation we identified them as B.
suzhenae and O. zayuensis.
Additionally, we generated new DNA sequences and compared them with published
sequences of these species, including their types (B. suzhanae
CIB 116088 from Yingjiang County, Yunnan
Province, China, and O. zayuensis CIB 013375
from Chayu Co., Xizang, China), based on which we
report here the first country records for India.
MATERIALS AND METHODS
We carried out field surveys
during October 2012 in the Nagaland-Manipur border, between June and July
2022–2023 in Arunachal Pradesh, northeastern India (Figure 1). Collected
specimens were fixed in formalin, washed, stored in 70% ethanol, and housed in
the repository at the Wildlife Institute of India, Dehradun (WII-ADR1241,
WII-ADR3316 and WII-ADR3491). Before fixation, live snakes were photographed,
and liver tissues were collected and stored in absolute ethanol at -20°C.
Molecular phylogenetic analysis
Genomic DNA was extracted from
liver tissue samples using DNeasy Blood and Tissue
Kit (Qiagen™, Germany). For the Bungarus specimen
(WII-ADR1241), we amplified and sequenced fragments of one mitochondrial gene,
cytochrome b (cyt b) using the primers
L14910 (5’-GACCTGTGATMTGAAAACCAYCGTTGT-3’) and H16064
(5’-CTTTGGTTTACAAGAACAATGCTTTA) (Burbrink et al.
2000). Polymerase Chain Reaction (PCR) conditions followed was initial
denaturation at 95°C for five minutes, followed by 35 cycles of denaturation at
95°C for 45 sec, annealing at 54°C for 45 sec, and extension at 72°C for 55
sec. The final extension was at 72°C for 10 min. For the Ovophis
sample (WII-ADR3491) we amplified and sequenced fragments of 16s gene, using
the primers 16Sar (5’-CGCCTGTTTATCAAAAACAT-3’) + 16Sbr
(5’-CCGGTCTGAACTCAGATCACGT-3’) (Palumbi et al. 1991).
Polymerase chain reaction (PCR) condition followed was initial denaturation at
95°C for five minutes, followed by 35 cycles of denaturation at 95°C for 35
sec, annealing at 55°C for 45 sec, and extension at 72°C for one minute. The
final extension was at 72°C for 10 min.
Amplified PCR products were run on a 2% agarose gel and viewed under a
UV transilluminator. The purified PCR product was sequenced directly in an
Applied Biosystems Genetic Analyzer 3500 XL in both directions using BigDye v3.1 kit.
We manually checked bidirectional
sequences using the CHROMAS v2.6.6 software
(http://technelysium.com.au/wp/chromas/) and aligned using ClustalW
(Thompson et al. 199) with default prior settings implemented in MEGA v7.1
(Kumar et al. 2016). For the protein-coding gene (cyt
b), we checked for unexpected stop codons by translating the sequence to
amino acids in MEGA v7.1 (Kumar et al. 2016). We used Naja
atra and Protobothrops
mucrosquamatus as outgroup for phylogenetic
analyses of Bungarus and Ovophis, respectively. The newly generated
sequences were aligned with the sequences downloaded from GenBank (Benson et
al. 2009) (Appendix 1).
We performed maximum likelihood
(ML) analyses using IQ-TREE (Nguyen et al. 2015), implemented in the web server
version (http://iqtree.cibiv.univie.ac.at) (Trifinopoulos
et al. 2016). For cyt b, the dataset was
partitioned by codon positions using Modelfinder (Kalyaanamoorthy et al. 2017), to find the best-fit
partitions and models of sequence evolution for each partition (Appendix 2).
Support for internal branches was quantified using the bootstrap approximation
(UFB 1000 pseudoreplicates) (Minh et al. 2013).
Uncorrected P-distance was calculated in MEGA v7.1 (Kumar et al. 2016) with
pairwise deletions of missing data and gaps.
Morphological character scoring
and identification
Total length, snout-vent length,
and tail length were measured with a thread and a metre
tape in millimetre (mm). Morphometric measurements
were taken with the help of a digital calliper
(Mitutoyo TM) to the nearest 0.1 mm. Length and width of head scales were measured
at the longest and the widest points of the respective scales. Morphological
comparisons follow Das et al. (2021). All measurements were taken on the
specimen’s right side and scales were counted on both sides for bilateral
scales. Morphometric and meristic characters were examined with the help of the
Olympus SZX10 microscope. Dorsal scale rows (DSR) were counted at one head
length behind the head, at midbody, and at one head length anterior to the anal
scute. Ventral scales were counted following Dowling
(1951). Bilateral scale counts separated by a comma are given in left, and
right order. Abbreviations used are WII-ADR: Wildlife Institute of India
Abhijit Das Reptile collection.
RESULTS
Molecular phylogeny
Based on mitochondrial gene cyt b, the specimen of Bungarus
from Northeastern India clustered with the type sequences of B. suzhenae with strong bootstrap value (100) (Figure 2).
Uncorrected P-distance between the newly collected Indian samples of Bungarus and the type series of B. suzhenae from the type locality varied 0.015–0.019
(Table 1). The inferred ML tree based on cyt–b
showed B. suzhenae as a sister lineage to the
cluster containing B. caeruleus, B. ceylonicus, B. lividus,
and B. sindarus with low bootstrap value (48)
(Figure 2).
Based on 16s gene, the Ovophis sample from Arunachal Pradesh nested with
the Ovophis zayuensis
sequence from Xizang province, China (with strong bootstrap value, (97)
(Figure 3) along with two other samples from Yunnan province, China and Chin
state, Myanmar. These samples altogether form a sister relationship with the
samples of O. zayuensis from Tongmai and Xizang provinces, China with low node support
(Figure 3). Uncorrected P-distance between our newly collected samples of Ovophis and samples of O. zayuensis
from China and Myanmar was minimal (Table 2).
Morphology
We confirmed the new krait
specimen as Bungarus suzhenae
based on the following set of diagnostic morphological characteristics (Chen et
al. 2021): enlarged hexagonal vertebral scale rows present, dorsal scales in
15:15:15 rows, anterior chin shields are slightly larger than the posterior
chin shields, dorsal body black with 34 white bands, ventral scales connected
with the black bands of the dorsal body by small dark patches, the ventral surface
uniform white, underside of tail white with tiny brown dots in the middle.
The two viper specimens we
collected were confirmed as Ovophis zayuensis based on the following set of diagnostic
morphological characteristics (Che et al. 2020): the third supralabial
larger is than the fourth, the second supralabial is
fused with the loreal, internasal scales are separated by two scales; the
ventral scale count is 169–172, dorsal scale count is 23 or 25:23:19 rows, the
subcaudal count of 34–48, mostly single and some are paired, anal scale is
single.
Description of Bungarus suzhenae (WII-ADR1241)
(Image 1,2)
An adult male specimen. Body
nearly triangular in cross-section, broader at midbody, more tapering
posteriorly. Head slightly distinct from the neck and longer than broad (head
width/head length = 0.5); head dorsally depressed at the parietal region, frontal
area flat, gradually sloping towards snout from prefrontals;
loreal region concave; supralabial sloping towards
outer margin; snout rounded in dorsal and lateral view; eyes with rounded
pupil; external nares oval, smaller than eye diameter; nasal large and divided;
prenasal touches first supralabial,
rostral and internasal; postnasal touches first and second supralabial,
preocular, internasal and prefrontal; postnasal-preocular suture short and
straight; pre-ocular one, hexagonal on right side and pentagonal left side,
bordered by second and third supralabials, postnasal,
prefrontal and supraocular; internasals
two, wider than long, in contact with rostral, nasals and pre-frontals; prefrontals large, slightly wider than long; internasal
suture shorter than prefrontal suture length and not aligned with latter;
frontal shield-shaped, pointing posteriorly, 1.3 times longer than wide,
bordered by prefrontals, supraoculars
and parietals; supraoculars small, 1.5 times longer
than wide, in contact with preoculars, upper postoculars,
prefrontals, frontal and parietals; parietals large,
longer than broad, bordered by frontal, supraoculars,
upper postoculars, anterior temporal and upper
posterior temporal on each side, and three smalls nuchal scales on pos-terior margins, posterolateral margins of parietals
bordered by one enlarged elongate scales that anteriorly contact upper
posterior temporals on each side; postoculars two on
each side; temporals 1+2; supralabial seven on both
side, third and fourth touches eye, lower postocular
touches by fourth and fifth supralabials on each
side; anterior temporal bordered by two postoculars,
fifth and sixth supralabial, parietal, and two
posterior temporals; lower posterior temporal in contact with sixth and seventh
supralabial; rostral wider than long and triangular;
mental smaller than rostral, bordered by first pair of infralabials;
infralabial seven on both sides, fourth largest; first pair of chin shields
slightly larger than the second pair chin shields; first chin shield is in
contact with four infralabials on the right side and three infralabials on the
left side; second chin shields contact with fourth infralabial on both sides,
posteriorly bordered by three scales on the right side and fourth scales on the
left side. Dorsal scales on body and tail smooth, no keel and apical pit;
vertebral scale row enlarged and hexagonal; dorsal scale rows 15:15:15; ventrals 219; anal plate single; subcaudals 57, undivided;
terminal scute conical; snout-vent length 664 mm and
tail length 109 mm. Details of the morphometric and meristic characters of the
specimen (WII-ADR1241) are given in (Table 3).
The hemipenes
of the newly reported specimen of B. suzhenae
from India agree with the description provided by Chen et al. (2021). Hemipenis can be divided into three distal calyculate region, middle spinose region, and basal region.
The top of the hemipenis is slightly bilobed. The calyculate region is covered with well-developed small
calyces. The spinose zone is covered with fang-shaped large keratinized spines
and the basal region is covered with tiny spines; the basal region is nearly
smooth towards the proximal end.
Dorsally head, body, and tail are
uniformly dark brown. The rostral upper half is dark brown, the lower half
(below the level of the lower edge of external nares) white; the nasals are
also white below the level of the lower edge of external nares; supralabials are partly dark brown on the upper part and
lower part (more than half of the scales) white; 34 narrow white cross bands on
the dorsal body; bands widening on the flank before meeting the ventrals; a dark spot present at the junctions where the
white bands meet the ventrals; white bands 5–7, 13,
15, 18–26, 28, and 31–33 are broad at mid dorsum with a central dark spot
forming a white semicircle; white band 27 is incomplete; black bands wide and
not intruding to venter; 13 white cross bands on the tail; ventrally white
including infralabials, mental, chin shields, gular scales, ventrals,
and subcaudals; the edge of the ventrals with
slightly dark brown patch; tail ventrally white with tiny brown dots in the
middle. The specimen is dorsally dark brown with white transverse bands on the
body and tail. Interstitial skin white. Ventrally white, subcaudals with tiny
brown dots in the middle (Image 2). Difference between the newly reported
specimen and original description of B. suzhenae: Notable
difference between the type specimen (based on the original description) and
our newly reported specimen (WII-ADR1241) is a lower number of ventrals in the new specimen (219 vs. 220–229), the higher
number of subcaudals in the new specimen (57 vs. 51–54).
This newly reported specimen was
encountered along Jessami–Meluri
road (25.63930N, 94.57910E, elevation 599 m), at the
Nagaland-Manipur border ca. 6 km from Meluri,
Nagaland towards Jessami, Manipur. This individual
was found while it was crossing the road at around 2100 h on 20 October 2012.
The Tiji River flows ca. 20 m away from the
collection locality. A roadkill Bungarus niger was also recorded 100 m away from the location of
B. suzhenae indicating their sympatric
occurrence. The surrounding landscape was mostly with secondary vegetation with
extensive jhum cultivation areas. While photographing, the snake showed
head-hiding behaviour and bit the snake bag in defence.
Description of Ovophis zayuensis (WII-ADR3316
and WII-ADR3491) (Image 3,4)
Both the specimens are adult
females. Specimens are in good condition, latero-ventral incision between
ventral scale 99–102 in WII-ADR3316 and between ventral scale 66–70 in
WII-ADR3491. Head triangular, body stout and the dorsal scales are strongly
keeled, ventrally plain pale yellow or orangish in color with no patterns.
There are faint black blotches on the anterior dorsal region of the body and the
blotches are dark on the posterior dorsal region. After preservation, the
specimen’s colour changed into smokey
grey with black blotches on the dorsal side. Dorsally head is completely
covered with small scales. The head length ranges 34.2–37.9 mm, the head width
is 23.1–25 mm, the eye diameter is 2.5–2.6 mm, the eye-to-nostril distance is
5.5–7.3 mm, and the snout length is 10.1–11.3 mm. No supralabials
touching the eye, one preocular and three postocular
present. Nasal single and undivided in both specimens. There is no
distinguishable temporal, parietal, and frontal scales present. The second supralabial is fused with the loreal pit. The total length of the specimens is 826–900
mm, SVL 699–746 mm, tail length 127–154 mm, ventral scales 166–167 mm, anal
scale single and undivided, subcaudals 46–49 with 5–6 paired. WII-ADR3491 has
nine supralabials on the left, third is
the largest measuring 4.3 mm; eight supralabials on the right, third is the largest measuring
3.6 mm. Infralabials 10 on the left, the fourth is the largest measuring 3.2 mm; 11 infralabials on the right and the
sixth is the largest measuring 2.8 mm, dorsal scale rows 25:23:19. WII-ADR3316
has nine supralabials on both sides, third is the
largest measuring 3.7 mm. Infralabials nine on both sides, on the right sixth
is the largest measuring 3.5 mm, and on the left, fifth is the largest
measuring 3.3 mm, dorsal scales rows 23:23:19.
The individual WII-ADR3491 was
recorded at Dri River bank (28.80560N,
95.93210E, elevation 1,288 m), near Etabe
village (~2.5 km north-east from Anini), Dibang Valley district, Arunachal Pradesh. This individual
was found while it was moving on the ground along the edge of a first-order
stream on 16 August 2022 at 2000 h. The stream edge was covered with small to moderate-sized
boulders covered with moss and leaf litter, fern, and other vegetation. The
recorded locality was ~100 m from the Dri river near Etabe village. Along the stream, we observed a few anuran
species such as Xenophrys sp. and
Amolops beibengensis
on the vegetation and also an unidentified rodent species. The second
individual WII-ADR3316 was collected from the newly constructed Chigu Pani road, Anini, Dibang Valley (29.01820N,
95.97550E, elevation 1,800 m). The habitat in this region was
disturbed due to the recent construction of roads, small streams were blocked
by retaining walls. It was found perched in a bush 50 cm above the ground
around 1900 h between the walls, blocking the stream. There was a mild yet
constant drizzle throughout the night. Many Amolops
froglets were found near the blocked stream and on the road. This individual
was a bit aggressive while trying to bag, it puffed up, flattened its body, and
struck the snake hook. The next day around 2000 h on the same road, close to a
small stream two other individuals of O. zayuensis
male and female were spotted crossing the road from both sides. The blocked
streams were seen to be harbouring tadpoles of
multiple species of frogs including Amolops
sp. and Megophrys sp. These two snakes
were removed from the roadside and released by the stream.
DISCUSSION
There are over 400 known species
of snakes in India (Uetz et al. 2024), where 1.2
million snakebite deaths were recorded during the years 2000–2019 (Suraweera et al. 2020). The Mountain Pit Viper Ovophis monticola Günther,
1864 has recently shown to cause medically significant envenoming (Ralph et al.
2023) while the Bungarus species have
always been among the big four snakes of medical importance from India (Simpson
& Norris 2007; Suraweera et al. 2020; Sunagar et al. 2021). Bungarus
suzhenae and Ovophis
zayuensis are two venomous snakes being reported
for the first time from India, from the border of Nagaland-Manipur and
Arunachal Pradesh, respectively.
Among the 18
known species of Bungarus, the maximum
diversity is congregated in southeastern Asia. Until now eight species of Bungarus have been reported from India and are known
for frequently causing fatal envenoming in the region (Suraweera
et al. 2020; Sunagar et al. 2021). Despite several
fatalities by other Bungarus species, the
commercial antivenom is manufactured only against the most widespread congener B.
caeruleus (Sunagar et
al. 2021). This new finding reported here also indicates the lack of systematic
studies on this group of snakes especially in northeastern India.
Identification of Bungarus species is still a
challenge which is evident by the recent discovery of B. suzhenae
from China and Myanmar. Bungarus species with
white cross bands—B. andamanensis Biswas &
Sanyal, 1978; B. bungaroides
Cantor, 1839; B. caeruleus Scheider, 1801; B. multicinctus
Blyth, 1861; B. sindanus Boulenger, 1897; B. slowinskii
Kuch, Kizirian, Nguyen,
Lawson, Donnelly & Mebs, 2005; B. suzhenae Chen, Shi, Vogel, Ding & Shi, 2021; B. walli Wall, 1907; B. canidus
Linnaeus, 1758; B. magnimaculatus Wall
& Evans, 1901; and B. persicus Abtin, Nilson, Mobaraki, Hosseni & Dehgannejhad, 2014—are most complex and difficult to
identify only based on external appearance (Leviton et al. 2003; Chen et al.
2021).
The genus Ovophis
has eight known species globally (Malhotra et al. 2011), and now two
species from India, namely: O. monticola and O.
zayuensis. Though not commonly found in conflict
with humans some species of Ovophis are
capable of delivering a severely painful or life-threatening bite (Ralph et al.
2023). The venom composition of these less medically significant snakes and
their clinical effects on humans still need to be studied (Tan et al. 2021).
The current distribution range of O. zayuensis extends
into the upper region of Dibang Valley, Arunachal
Pradesh, Northeast India. However, it is important to carefully look into the
distribution of O. zayuensis from the rest of
Arunachal Pradesh. Being in the transition zone, the geographical range of
these and other such species is likely to overlap in northeastern India.
Therefore, proper identification of such venomous species and understanding of
geographic distribution is crucial for general awareness, venom research as
well as development of lifesaving antivenin.
Northeastern India is known to
have Tibeto-Yunanese, Indo-Malayan, and its own
unique faunal elements (Das 1996; Giri et al. 2019; Lalronunga et al. 2020; Vogel et al. 2020; Deepak et al.
2021; Das et al. 2021). The new record of B. suzhenae
from India indicates the possibility of the occurrence of other Bungarus species reported from Myanmar such as B.
magnimaculatus, B. wanghaotingi,
and B. flaviceps. Therefore, a systematic
study is necessary across northeastern India to document the diversity of
medically important snakes. With the present report of B. suzhenae, the number of Bungarus
species in India increases to nine, and the distribution range of B. suzhenae is extended by ca. 321 km north-west from the
nearest known locality, Yingjiang County, Yunnan
Province, China. The geographical area of occurrence of B. suzhenae is currently ca. 38,000 km2 within
China, Myanmar, and northeastern India. In earlier documentation, other Bungarus species such as B. bungaroides,
B. fasciatus, and B. niger
were reported from Nagaland (Ao et al. 2004; Dasgupta
& Raha 2006; Das 2018). Singh (1995) and Sinate et al. 2021 also reported B. fasciatus
and B. niger from Manipur respectively. Since
the present specimen of B. suzhenae was
encountered at the Nagaland-Manipur border, there is a possibility of the
occurrence of the species in other parts of Manipur. In a herpetofaunal
biodiversity report of Nagaland, Grewal et al. (2011) provided a photograph of
a road-killed unknown Bungarus sp. from Pungro-Shatuza road (nearest distance ca. 13 km from the
present locality) which is similar to B. suzhenae (based
on the lower number (<40) of unpaired white cross bands on body). Therefore,
the distribution range of this medically important snake is likely to be wider
than hitherto known in the region. Despite several reports of fatal snake bites
by other species, commercial Indian antivenoms are only manufactured against Daboia
russelii, Naja naja, Echis carinatus,
and Bungarus caeruleus.
Hence, it is important to recognise other
medically important Indian snake species as it also has great significance in
the field of snake antivenom design and manufacture (Simpson & Norris
2007).
Table 1.
Uncorrected P-distances (%) of Bungarus
species based on the cyt b sequences.
|
|
1 |
2 |
3 |
4 |
5 |
6 |
|
1. Bungarus
suzhenae (India) |
|
|
|
|
|
|
|
2. B. bungaroides
(AY973270) |
0.188 |
|
|
|
|
|
|
3. B. caeruleus
(AJ749305) |
0.135 |
0.189 |
|
|
|
|
|
4. B. candidus
(AJ749329, AJ749339, AJ749341, MN165133) |
0.098–0.101 |
0.167–0.17 |
0.139–0.142 |
0.003–0.008 |
|
|
|
5. B. ceylonicus
(KC347457) |
0.144 |
0.201 |
0.101 |
0.151 |
|
|
|
6. B. fasciatus
(AJ749350, MW596457) |
0.147–0.154 |
0.171–0.183 |
0.152–0.154 |
0.152–0.154 |
0.174–0.176 |
0.041 |
|
7. B. lividus
(MW596472) |
0.137 |
0.201 |
0.114 |
0.144 |
0.111 |
0.169 |
|
8. B. multicinctus
(AJ749344, MN165136, MN165137, MN165139, MN165138, MN165135) |
0.086–0.090 |
0.169–0.171 |
0.143–0.145 |
0.026–0.031 |
0.147–0.148 |
0.153–0.154 |
|
9. B. niger
(AJ749304, MW596473) |
0.091–0.095 |
0.177–0.181 |
0.135–0.14 |
0.101–0.106 |
0.144–0.146 |
0.152 |
|
10. B. sindanus
(AJ749346) |
0.145 |
0.186 |
0.129 |
0.136 |
0.134 |
0.166 |
|
11. B. slowinskii
(AJ749306) |
0.176 |
0.087 |
0.190 |
0.179 |
0.199 |
0.174 |
|
12. B. suzhenae
(AJ749435, MN165142, MN165140, MN165141, MN165143) |
0.015–0.019 |
0.185–0.187 |
0.133–0.136 |
0.096–0.1 |
0.138–0.142 |
0.151–0.156 |
|
13. B. wanghaotingi
(MN165144, KY952766, MN165146, MN165145, MN165132, AJ749336, AJ749308,
MN165134, AJ749309, MN165131, AJ749331, AJ749337) |
0.092–0.1 |
0.163–0.177 |
0.136–0.144 |
0.018–0.024 |
0.142–0.151 |
0.148–0.161 |
Table 1. continue…
|
7 |
8 |
9 |
10 |
11 |
12 |
|
0.136–0.139 |
0–0.006 |
|
|
|
|
|
0.14–0.143 |
0.102–0.104 |
|
|
|
|
|
0.142 |
0.130 |
0.129 |
|
|
|
|
0.197 |
0.170 |
0.171 |
0.183 |
|
|
|
0.135–0.140 |
0.087–0.091 |
0.091–0.095 |
0.141–0.144 |
0.171–0.176 |
0.002–0.007 |
|
0.134–0.139 |
0.026–0.03 |
0.096–0.102 |
0.126–0.137 |
0.164–0.175 |
0.087–0.097 |
Table 2.
Uncorrected P-distances (%) of Ovophis species
based on the 16s gene sequences.
|
|
1 |
2 |
3 |
4 |
5 |
6 |
|
1. Ovophis
zayuensis (India) |
|
|
|
|
|
|
|
2. O. zayuensis
(HQ325109, HQ325111, HQ325118, HQ325089, MK193194, MK193195) |
0.004–0.019 |
0.0–0.013 |
|
|
|
|
|
3. O. monticola
(HQ326117, HQ325121, HQ325078, MG995792) |
0.05–0.062 |
0.039–0.057 |
0.004–0.017 |
|
|
|
|
4. O. makazayazaya
(HQ325107) |
0.056 |
0.039–0.055 |
0.05–0.054 |
|
|
|
|
5. O. tonkinensis
(HQ325096, HQ325070) |
0.031–0.032 |
0.026–0.032 |
0.049–0.056 |
0.03–0.034 |
0.004 |
|
|
6. O. okinavensis (AB175670) |
0.056 |
0.035–0.046 |
0.057–0.059 |
0.054 |
0.052–0.053 |
|
|
7. O. convictus
(HQ325082, HQ325083) |
0.046–0.052 |
0.032–0.05 |
0.041–0.059 |
0.05–0.052 |
0.042–0.043 |
0.05–0.056 |
Table 3.
Morphometric and meristic data of newly collected specimens of Bungarus suzhenae.
All the measurements are given in millimetre.
Bilateral characters are given in left, and right order separated by comma. “N”
denotes sample size, “-“ indicates data not provided.
|
Voucher ID |
WIIADR1241 |
Chen et al. (2021) |
|
|
Sex |
male |
male (N = 3) |
female |
|
Snout- vent length (SVL) |
664 |
620–1140 |
1310 |
|
Tail length (TL) |
109 |
109–180 |
- |
|
Head length (HL) |
21.6 |
21–39 |
30.2 |
|
Head width (HW) |
10.7 |
12.3–15.5 |
19.4 |
|
Head height (HH) |
6.5 |
8.7–12.8 |
14.2 |
|
Eye diameter |
2.3 |
9.3–10.5 |
14.6 |
|
Ventrals |
219 |
220–229 |
222 |
|
Subcaudals |
57 |
51–54 |
11+ |
|
Anal plate |
single |
single |
single |
|
Dorsal scale row |
15:15:15 |
15:15:15 |
15:15:15 |
|
Supralabial |
7,7 |
7,7 |
7,7 |
|
Infralabial |
7,7 |
7,7 |
7,7 |
|
Preocular |
1,1 |
1,1 |
1,1 |
|
Postocular |
2,2 |
1–2 |
2 |
|
Temporal (anterior + posterior) |
1+2 |
1+2 |
1+2 |
|
Nasal |
divided |
divided |
divided |
|
No. of white bands (body +
tail) |
34+13 |
26–38+9–12 |
34+3 |
Table 4.
Morphometric and meristic data of newly collected specimens of Ovophis zayuensis.
All the measurements are given in millimetre.
|
Voucher ID |
WII-ADR3491 |
WII-ADR3316 |
|
Sex |
female |
female |
|
Snout- vent length (SVL) |
746 |
699 |
|
Tail length (TL) |
154 |
127 |
|
Head length (HL) |
37.9 |
34.2 |
|
Head width (HW) |
25 |
23.1 |
|
Head height (HH) |
14.3 |
14.2 |
|
Eye diameter |
2.6 |
2.5 |
|
Ventrals |
167 |
166 |
|
Subcaudals |
49 |
46 (missing tip) |
|
Anal plate |
single |
single |
|
Dorsal scale row |
25:23:19 |
23:23:19 |
|
Supralabial |
9,8 |
9,9 |
|
Infralabial |
10,11 |
9,9 |
|
Preocular |
1,1 |
1,1 |
|
Postocular |
3,3 |
3,3 |
|
Nasal |
undivided |
undivided |
Identification key to the Bungarus species of northeastern India
Crossbands on body and tail
absent .........................................................................................
1
1A. Mid-dorsal scale distinctly
enlarged ....................................................................................
Bungarus niger
1B. Mid-dorsal scale not enlarged
..............................................................................................
Bungarus lividus
Crossbands present
.....................................................................................................................
2
2A. Crossbands yellow and black
.................................................................................................
Bungarus fasciatus
2B. Crossbands white
....................................................................................................................
3
3A. White crossbands not paired,
26–38 in number ................................................................
Bungarus suzhenae
3B. White crossbands not paired,
46–60 in number .................................................................
Bungarus bungaroides
Identification key to the Ovophis species from India
Ventral scales
A. 135–154
....................................................................................................................................
O. monticola
B. 158–176
..................................................................................................................................
O. zayuensis
For
figures & images - - click
here for full PDF
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Appendix 1.
Details of the GenBank sequences used in this study. The sequence of Bungarus suzhenae and
Ovophis zayuensis
generated in this study is given in bold.
|
Taxa |
Voucher numbers |
Locality |
AccessionNo. (cyt– b) |
Reference |
|
B. bungaroides |
KIZ 98R0186 |
Medog, Medog County, Tibet, China |
AY973270 |
Kuch et al. 2005 |
|
B. caeruleus |
UK H7 |
Pakistan |
AJ749305 |
Kuch 2007 |
|
B. candidus |
UK B39 |
Vicinity of Jambah,
Losarang District, Indramayu
Regency, West Java, Indonesia |
AJ749329 |
Kuch 2007 |
|
B. candidus |
UK BcBa |
Bali Island, Indonesia |
AJ749339 |
Kuch 2007 |
|
B. candidus |
UK B21 |
Vicinity of Jambah,
Losarang District, Indramayu
Regency, West Java, Indonesia |
AJ749341 |
Kuch 2007 |
|
B. candidus |
SYNU R180411 |
Endau Rompin
National Park, Taman Negara, Johor, Malaysia |
MN165133 |
Chen et al. 2021 |
|
B. ceylonicus |
RS-135 |
Sri Lanka |
KC347457 |
Pyron et al. 2013 |
|
B. fasciatus |
UK B24 |
Vicinity of Jolo,
Central Java, Indonesia |
AJ749350 |
Kuch 2007 |
|
B. fasciatus |
MZMU978 |
Mizoram, India |
MW596475 |
Biakzuala et al. 2021 |
|
B. lividus |
YSR187 |
Baridua, Meghalaya, India |
MW596472 |
Biakzuala et al. 2021 |
|
B. multicinctus |
CIB104228 |
Nanning Zoo, Guangxi, China
(locality uncertain) |
MN165137 |
Chen et al. 2021 |
|
B. multicinctus |
UK Bm1 |
Zhejiang, China |
AJ749344 |
Kuch 2007 |
|
B. multicinctus |
CIB DL18090209 |
Wuyi Moutain,
Fujian, China |
MN165138 |
Chen et al. 2021 |
|
B. multicinctus |
CIB DL18090210 |
Wuyi Moutain,
Fujian, China |
MN165139 |
Chen et al. 2021 |
|
B. multicinctus |
CIB93923 |
Guangxi, China |
MN165136 |
Chen et al. 2021 |
|
B. multicinctus |
SYNU R180305 |
Haikou, Hainan, China |
MN165135 |
Chen et al. 2021 |
|
B. niger |
Bnig |
Nepal |
AJ749304 |
Kuch 2007 |
|
B. niger |
MZMU975 |
Mizoram, India |
MW596473 |
Biakzuala et al. 2021 |
|
B. sindanus |
Bsin1 |
Pakistan |
AJ749346 |
Kuch 2007 |
|
B. slowinskii |
IEBR 1172 |
Na Hau
Commune, Van Yen District, Yen Bai,Vietnam |
AJ749306 |
Kuch 2007 |
|
B. suzhenae |
CAS 221526 |
Naung Mon Township, Rabaw Kachin State, Burma (Myanmar) |
AJ749345 |
Kuch 2007 |
|
B. suzhenae |
CIB116088 |
Yingjiang, Yunnan, China |
MN165140 |
Chen et al. 2021 |
|
B. suzhenae |
CIB116089 |
Yingjiang, Yunnan, China |
MN165141 |
Chen et al. 2021 |
|
B. suzhenae |
CIB116090 |
Yingjiang, Yunnan, China |
MN165142 |
Chen et al. 2021 |
|
B. suzhenae |
CIB116091 |
Yingjiang, Yunnan, China |
MN165143 |
Chen et al. 2021 |
|
B. suzhenae |
WIIADR1241 |
Nagaland-Manipur border, India |
PP808595 |
This study |
|
B. wanghaotingi |
ROM 35250 |
Quang Thanh, Cao Bang, Vietnam |
AJ749308 |
Kuch 2007 |
|
B. wanghaotingi |
ROM 35256 |
Chi Linh, Hia
Duong, Vietnam |
AJ749309 |
Kuch 2007 |
|
B. wanghaotingi |
UK BT6 |
Nakhon Si Thammarat,
Thailand |
AJ749331 |
Kuch 2007 |
|
B. wanghaotingi |
UK BT8 |
Nakhon Si Thammarat,
Thailand |
AJ749336 |
Kuch 2007 |
|
B. wanghaotingi |
FMNH 255259 |
Hin Nam No National
Biodiversity Conservation Area, Boualapha District,
Khammouan, Laos |
AJ749337 |
Kuch 2007 |
|
B. wanghaotingi |
FMNH 255260 |
Nam Et Phou Louey
Mountain, Phou Louey National Biodiversity,
Conservation Area, Vieng Tong, Huaphahn,
Laos |
AJ749338 |
Kuch 2007 |
|
B. wanghaotingi |
CIB FCDZ20170806 |
Dongzhong, Fangchenggang, Guangxi, China |
MN165131 |
Chen et al. 2021 |
|
B. wanghaotingi |
CIB104227 |
Beiliu, Guangxi, China |
MN165134 |
Chen et al. 2021 |
|
B. wanghaotingi |
SYNU R170408 |
Bang Lang National Park, Yala, Thailand |
MN165132 |
Chen et al. 2021 |
|
B. wanghaotingi |
CIB ML20170801 |
Menglun, Yunnan, China |
MN165145 |
Chen et al. 2021 |
|
B. wanghaotingi |
CIB MLMY20170801 |
Mengla, Yunnan, China |
MN165144 |
Chen et al. 2021 |
|
B. wanghaotingi |
JK20181101 |
Jinghong, Yunnan, China |
MN165146 |
Chen et al. 2021 |
|
B. wanghaotingi |
GP 3375 |
Xishuangbanna, Yunnan Province,
China |
KY952766 |
Xie et al. 2018 |
|
Naja atra |
- |
China |
DQ343648 |
Yan et al. 2008 |
|
O. zayuensis |
WII-ADR3491 |
Dibang Valley district,
Arunachal Pradesh, India |
PP794643 |
This study |
|
O. zayuensis |
GP90 |
Xizang Autonomous Region, China
|
HQ325109 |
Malhotra et al.
2011 |
|
O. zayuensis |
GP92 |
Yunnan Province, China |
HQ325111 |
Malhotra et al.
2011 |
|
O. zayuensis |
CAS 233203 |
Chin State, Myanmar |
HQ325118 |
Malhotra et al.
2011 |
|
O. zayuensis |
CHS099 |
Tibet, China |
MK193914 |
Li, J. N et al.
2020 |
|
O. zayuensis |
CHS101 |
Tibet, China |
MK193915 |
Li, J. N et al.
2020 |
|
O. zayuensis |
GP89 |
Xizang Autonomous Region, China |
HQ325089 |
Malhotra et al.
2011 |
|
O. tonkinensis |
MVZ 226627 |
Vinh Phu
Province, N Viet Nam |
HQ325096 |
Malhotra et al.
2011 |
|
O. tonkinensis |
B581 |
China |
HQ325070 |
Malhotra et al.
2011 |
|
O.monticola makazayazaya |
GP24 |
Yunnan Province, China |
HQ325107 |
Malhotra et al.
2011 |
|
O. monticola |
CAS 224424 |
Kachin State, Myanmar |
HQ325117 |
Malhotra et al.
2011 |
|
O. monticola |
V16 |
North East India |
MG995792 |
|
|
O. monticola |
CAS 234866 |
Chin State, Myanmar |
HQ325121 |
Malhotra et al.
2011 |
|
O. monticola |
ZMB 70216 |
Gandaki Zone, W Nepal |
HQ325078 |
Malhotra et al.
2011 |
|
O. okinavensis |
- |
- |
AB175670 |
Dong & Kumazawa 2005 |
|
O. convictus |
B629 |
Pulau Langkawi, West
Malaysia |
HQ325083 |
Malhotra et al.
2011 |
|
O. convictus |
B628 |
Pulau Langkawi, West
Malaysia |
HQ325082 |
Malhotra et al.
2011 |
|
Protobothrops mucrosquamatus |
B106 |
Vin Phuc
Province, N Viet Nam |
AY294271 |
Herrmann et al.
2004 |