Research Article |
Corresponding author: Ashok Kumar Mallik ( ashokgene@gmail.com ) Academic editor: Uwe Fritz
© 2021 Ashok Kumar Mallik, Achyuthan Needamangalam Srikanthan, Sumaithangi Rajagopalan Ganesh, Seenapuram Palaniswamy Vijayakumar, Patrick D. Campbell, Anita Malhotra, Kartik Shanker.
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:
Mallik AK, Srikanthan AN, Ganesh SR, Vijayakumar SP, Campbell PD, Malhotra A, Shanker K (2021) Resolving pitfalls in pit viper systematics – A multi-criteria approach to species delimitation in pit vipers (Reptilia, Viperidae, Craspedocephalus) of Peninsular India reveals cryptic diversity. Vertebrate Zoology 71: 577-619. https://doi.org/10.3897/vz.71.e66239
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Abstract
Asian pit vipers belonging to the genus Craspedocephalus are a complex group of vipers, distributed in South and Southeast Asia. Their taxonomy is unresolved in many lineages across their distributional range. Here, we reassess the taxonomy and systematics of pit vipers of the genus Craspedocephalus in Peninsular India based on extensive field sampling, in particular in the Western Ghats. We build and expand on the previous findings of genetic relatedness between the peninsular Indian lineages with the Sundaic clade (C. puniceus complex) with greater evidence, based on additional taxa sequenced herein. We reconstruct the phylogeny of the group using three mitochondrial genes and delineated lineages using coalescent species delimitation methods. We then used multiple criteria including genetic divergence and separation in morphological and geographic space to designate taxonomic units. Our work revealed the presence of a South Asian radiation of the clade Craspedocephalus, with a few Sundaic members. Our study reveals the systematic relationships of four Peninsular Indian species of Craspedocephalus, including Peltopelor macrolepis and C. strigatus, sequenced here for the first time, that are classified or confirmed as members of Craspedocephalus. Hence, we place the genus Peltopelor in the synonymy of Craspedocephalus. Using our multi-criteria approach, we delimit four new cryptic evolutionary lineages within the Western Ghats escarpment of Peninsular India. These cryptic lineages belong to the C. malabaricus, C. gramineus and C. macrolepis complexes and are geographically and/or ecologically (in terms of habitat association) distinct from their sister lineages across their distributional range, while others are separated in morphological space. Our new phylogenetic tree and delimitation analysis thus reveals the presence of multiple clades with several cryptic lineages separated by geographical barriers or habitat association.
Craspedocephalus, cryptic species, geographical barriers, phylogenetics
Pit vipers are a group of venomous snakes that comprise several genera of vipers with a facial pit; they are terrestrial and arboreal in habit and predominantly found in wet, humid forests and montane habitats as well as in a few dry forest habitats in the Oriental realm. Pit vipers of the genus Craspedocephalus Khul & Hasselt, 1822 are a taxonomically complex group of venomous snakes and comprise nine recognized species distributed in South and Southeast Asia, mainly in forested and mountainous tracts (
Some of the first members of the group to be named were from the Indian peninsula such as Coluber gramineus (now Craspedocephalus gramineus) by
In a pioneering attempt to reconstruct a molecular phylogeny of the snakes of the Trimeresurus radiation, Malhotra & Thorpe (2004) recovered a tree revealing close clustering of southern Indian and Sri Lankan taxa with some Indo-Malayan ones (see their ‘Clade E’). They also established molecular relationships of two Peninsular Indian congeners, C. gramineus and C. malabaricus. Malhotra & Thorpe (2004) allocated most southern Indian taxa to the genus Trimeresurus, with one lineage (macrolepis) assigned to the genus Peltopelor Günther, 1864, based mainly on scalation and hemipenial characters that were jointly diagnostic of the mitochondrial clades (Malhotra & Thorpe, 2004). This was further reinforced by osteological characterisation of the skull (
The following taxa recognized as valid (
Though previous genetic studies on the Trimeresurus radiation have included Peninsular Indian taxa, a dedicated study with comprehensive geographic sampling and a robust phylogenetic analysis is still lacking. Prompted by the morphological variations and informed by biogeographic processes, this study approaches the systematics of Peninsular Indian species using a multi-criteria approach. Here, we assess and delimit species boundaries in pit vipers of Peninsular India to reassess species diversity within this group and implement formal nomenclatural changes.
Sampling was carried out in Peninsular India, including in the Western Ghats (WG) and the Eastern Ghats (EG), and in Northeast India as part of Indo-Chinese sub-region. Field surveys and collections were carried out in all possible habitat types, across environmental gradients and at different elevations, as well as type locality locations to maximize the sampling of both rare and range-restricted species, and to capture intra-species variability. Snakes were captured alive and tissue and scale samples were collected by non-intrusive methods and stored in 95% ethanol; snakes were released unharmed after sample collection and measurement. We also collected samples from dead specimens encountered on roads; voucher specimens and samples were collected and preserved in 95% alcohol. The specimens were deposited at Bombay Natural History Society (BNHS). The fieldwork was carried out with the prior written permission from the state forest departments of Maharashtra, Kerala, Karnataka, Tamil Nadu, Odisha, Andhra Pradesh, Arunachal Pradesh and Meghalaya.
Total genomic DNA was extracted from all available tissue samples stored in 95% absolute alcohol. Genomic DNA was extracted using commercially available DNEasy extraction kit (QIAgen) as well as Phenol-Chloroform-Isoamyl alcohol protocol (
Sequences were edited and visually corrected using MEGA v5.2 (
We reconstructed the phylogeny of pit vipers to understand the relationships of pit vipers of Peninsular India including endemic species (C. strigatus and C. macrolepis) from the Western Ghats, which had not been included in earlier work (Malhotra & Thorpe 2004). The 2154 bp matrix was analysed with codon partitions where different codon positions of cyt b and ND4 genes were considered as different partitions using PARTITIONFINDER v1.1.1 (
Morphological data were collected from all sampled specimens. Pholidosis analysis was carried out in the field as well as in the laboratory on preserved specimens (See Supplementary File 3: Table S3). Morphometric measurements were carried out with Mitutoyo Vernier calipers (to the nearest to 0.1 mm). We also examined specimens that were morphologically different in scalation or colour as potential ecomorphs. Sampling was carried out in every possible habitat type and along the environmental gradient to scrutinize the possible morphological space shared by individuals with respect to distance and isolation. We recorded the body colouration of individuals belonging to each population and examined both overall colour from head to tail as well as change in colour, if any occured. Colour variation of ventral scales along with any blotches and speckles present on the ventral shields were also recorded.
We recorded geographic locations for each individual sample collected with the help of a GPS (WGS84) to identify isolation and geographic barriers between lineages if any.
For identification of putative species and delimiting species boundaries between clades, we used a multi-criteria approach including phylogeny, coalescent species delimitation (bPTP), genetic distance, morphological characters, and geographic and ecological isolation (
We calculated genetic p-distance between clades for three mitochondrial loci (cyt b ND4, and 16S rRNA) separately in MEGA, and designated deep and shallow divergent lineages. There is shallow genetic divergence (e.g 1.9 % at cyt b, 1.5% at 16S, 2.2 % at ND4) between a few closely-related sister species (e.g. Trimeresurus andersoni vs. Tri. purpureomaculatus and Tri. erythrurus) of pit vipers with clear morphological differentiation, which were used as a benchmark for comparison. We considered distances of > 7 % at cyt b to be deeply divergent and such lineages were treated as independently evolving and designated as species on the basis of depth of genetic divergence alone. Other lineages were further examined (using additional individuals) along the other axes of morphology and geography to determine whether they should be designated as species. Shallow divergent lineages were designated as species only if they differed in morphology and were geographically isolsated.
The mitochondrial tree topology derived from Maximum Likelihood analysis of the combined dataset is similar to the tree topology obtained in earlier studies on Trimeresurus (Malhotra & Thorpe 2004,
Maximum Likelihood tree reconstructed from a concatenated dataset of three mitochondrial genes (cyt b, ND4 and 16S) for almost all the species of pit vipers found in Peninsular India and the Indo-Burmese sub region. The tree shows two separate major clades (Clade A & B). Clade A includes all peninsular Indian species along with a few taxa from Southeast Asia, while clade B predominantly comprises species from other parts of central India, China and Southeast Asia.
A Maximum Likelihood tree generated from three mitochondrial genes shows the Peninsular Indian, Sri Lankan (I) and Southeast Asian (II) clades. In the Peninsular Indian group (I), the new lineages (L1–L7) are marked with different green bars, which represent the different criteria used to delimit the species boundary. P represents the putative species predicted by bPTP analysis, while GD, M and G represent genetic distance, morphology and geographic isolation. All clades are supported with >70% parametric bootstrap value (see Fig.
All Peninsular Indian taxa are clustered within a single clade along with two species from Southeast Asia. Based on our results, we refer to this clade henceforth as the genus Craspedocephalus. Peltopelor is nested within the Craspedocephalus clade and since Craspedocephalus Khul & Van Hasselt, 1822 has nomenclatural priority over Peltopelor Günther, 1864, the generic name for all Peninular Indian taxa sampled here should continue to be Craspedocephalus.
The two species from Southeast Asia, C. borneensis and C. puniceus (clade I) are sister to the Peninsular Indian and Sri Lankan group (clade II) consisting of C. macrolepis, C. strigatus, C. malabaricus and C. gramineus from Peninsular India and C. trigonocephalus from Sri Lanka. Within clade II, the Craspedocephalus macrolepis species complex is sister to the other taxa distributed in Peninsular India and Sri Lanka (clade III). Within clade III, clades IV and V share a sister relationship. Clade IV comprises the C. malabaricus species complex, which is distributed throughout the Western Ghats and is represented by three separate lineages. Two of these lineages are distributed in the southern Western Ghats; the other is in the northern and central Western Ghats, separated by the Palghat Gap from the two southern lineages. Clade V consists of C. strigatus and a clade comprising C. trigonocephalus and the C. gramineus species complex. The C. gramineus group has two separate evolutionary lineages, which are distributed across the Indian peninsula.
We delimited species boundaries of the Craspedeocephalus populations in Peninsular India (Fig.
The three new lineages in the C. malabaricus species complex have low levels of morphological divergence but strong genetic differences due to geographic isolation (Fig.
Similarly, there is a shallow genetic break, morphological separation and geographical isolation between the populations of C. macrolepis. The lineages are divided by the Shencottah gap as a physical barrier. There is a higher ventral shield count in the southern lineage (L7) than the northern lineage (L6) (Fig.
Viperidae Oppel, 1811
Crotalinae Oppel, 1811
Craspedocephalus Khul & Hasselt, 1822
This species complex can be distinguished from regional congeners as follows: head scales large, shield-like (vs. as small as body scales in the C. gramineus, C. malabaricus complexes and C. strigatus); midbody dorsal scale rows < 19 (vs. 21 or more in the C. gramineus, C. malabaricus complexes and C. strigatus); last rows of costal scales abutting ventrals on either side smaller than rest of the dorsal scale rows (vs. larger in all other congeners throughout the range of the genus); 2nd supralabial bordering the anterior margin of loreal pit (vs. not so in C. strigatus); supraoculars undivided (vs. frequently divided in the C. malabaricus complex); subcaudals of the tail tip bluish (vs. blackish in the C. malabaricus complex).
Trimeresurus macrolepis Beddome, 1862
Peltopelor macrolepis (Beddome, 1862) – Günther, 1864; Malhotra & Thorpe, 2004
Trimeresurus macrolepis
– Hutton, 1949; Malhotra & Davis, 1991;
Trimeresurus (Peltopelor) macrolepis
Beddome, 1862 –
Craspedocephalus macrolepis (Beddome, 1862) (this work)
Lectotype, NHMUK 1946.1.18.72 (formerly BMNH 1861.12.30.80), a male (R.H. Beddome, 1857–1862), designated by Toriba in Golay et al. (1993: 101).
Specimen series: Lectotype – NHMUK 1946.1.17.72 from “Anamallay Mountains, at 6000 feet” collected in 1857–62 by R. H. Beddome; CESS014, CESS015 from Vellimala, Periyar and CESS190 from Rajamalai, Kerala, collected in 2011, by Ashok Kumar Mallik; CESS170 from Uppupara, Goodrickal Range-west, Kerala, CESS256 from Devarmala, Tamil Nadu, collected in 2011, by Saunak P. Pal; BNHS2543 from Shenbaganur, Tamil Nadu and BNHS2545 from Paralai, Valparai collected in 1909, by Maj. Frank Wall.
“Anamallay Mountains; at 6,000 feet elevation” [= Anaimalai Hills, Western Ghats India, ca. 10°22’N; 77°08’E] by lectotype designation (
Within the C. macrolepis complex, C. macrolepis s. str. (L6) can be distinguished as follows: in having higher dorsal scale rows: 13–19 (vs. 10–14 in L7); lower ventral count 133–140 (vs. 150 in L7). Craspedocpehalus macrolepis (L6) is allopatric with its sister taxon (L7), from which it has a shallow genetic divergence (3.7% at cyt b and 0.7–1.0% at 16S rRNA). The low level of genetic divergence is the lowest genetic break between any the lineages inferred here (See Supplementary File 5: Table S4). This shallow genetic break coincides with a physical barrier (Shencottah gap) for these lineages.
A medium sized pit viper (recorded till 920mm by
Specimens in life are in a uniform dark green throughout the dorsal surface, often with a black post ocular stripe that extends to 2 scale rows; the postocular stripe continues to a white to creamy white lateral stripe that stops at the vent; uniform creamy to light green ventrals with hints of light blue, that continues to the mandibular portion that is either yellow, light green, light blue or creamy white in colour; tail after the vent continues with dark green, feeble blue bands at the end of the tail, the terminal scale black or greyish with feeble white bands.
Specimens in preservative show a range of variation in colour depending on the preservative; range from dark to light green on the head and dorsum with hints of or blue black bordering the scales; tail tip banded with grey and white bands, tail darker blue bands with bluish green.
A typically arboreal (rarely terrestrial) species (Ganesh et al. 2010) that is found in high elevation shola forests (tropical montane stunted rainforests) and forests bordering high elevation grasslands. Due to anthropogenic changes to the landscape, this species is also sometimes found in cultivated landscapes such as tea estates and cardamom plantations, found at elevations from about 1100 m asl to 2600 m asl.
Endemic to the southern Western Ghats. The revised distribution restricts this species to the high elevation landscapes of its range, the northern most limit being south of the Palghat gap, in the Nelliampathi hills, Anaimalai, with Palni hills being the eastern-most end of its distribution, extending southwards across High Wavy’s or Meghamalai, Kottaimalai Ranges in the Srivilliputhur-Periyar landscape, to the Sivagiri-Devarmalai range, ending north of the Shencottah gap.
Trimeresurus macrolepis
(not of Beddome, 1862) –
Specimen series: Holotype (BNHS 3593) from Chemunji, Peppara, Agasthyamalai, 08°40.7’N; 77°11.55’E, collected in 2010, by Saunak P. Pal & S.P. Vijayakumar. — Paratype (BNHS 2950) from Tirunelveli Hills (Agasthyamalai), collected in 1976 by Romulus Whitaker.
Chemmunji, in Peppara Wildlife Sanctuary, a part of Agastyamalai Hill Complex, Southern Western Ghats.
Named after Günther’s erstwhile generic nomen that alludes to the shield-like, large scales (peltē: shield/scale, pelor (o)-: a term meaning monstrous [or literally huge], in Greek).
A lineage belongs to the C. macrolepis complex. Differs from C. macrolepis in having lower dorsal scale rows 10–14 (vs. 13–19); higher ventral scale counts 150 (vs. 133–143). The new species is geographically separated from C. macrolepis by the Shencottah gap in the Southern Western Ghats. Craspedocephalus peltopelor sp. nov. (L7) has a shallow genetic divergence (3.7% at cyt b and 0.7–1.0% at 16S) from C. macrolepis (L6).
Holotype in good condition, dissected, with a slender, cylindrical body of snout to vent length (SVL) 263mm and a prehensile tail of length (TL) 57 mm; dorsal scales keeled with anterior dorsal scale rows (DSR) 17, mid body scale rows (MSR) 15 and posterior scale rows (PSR) 10; head prominent, of length 20.5mm, clearly distinguished from the neck with large, smooth dorsal shields on the head; rostral scale triangular with the upper side roughly half the size of the lower side with the tip visible from above; supraoculars of length 5.46 mm and frontal separated by pair of scales on both sides and nasal scales separated by three scales from above; five scales other than the pre and post ocular scales bordering the supraoculars on both sides, with three scales between the posterior edge of the supraoculars; canthus rostralis distinct with 3/3 canthal scale; three preoculars, a postocular and a thin elongated crescent shaped subocular, in contact with a small scale, encompassed by the third and fourth supralabial scale; eye with a distinct elliptical pupil, vertical diameter of the eye 2.94 mm and horizontal diameter 3.52mm; temporal scales smooth; aperture of the nostril completely covered by the nasal scale, undivided and subrectangular; nasal scale bordering the first supralabial; loreal pit present in contact with the second supralabial with two scales between the nasal and the second supralabial; eight supralabials and 12 infralabials, with six scales between the last supralabial, including the last supralabial till the start of the ventral scales; 1st, 2nd and 3rd infralabial scale in contact with the first pair of genials; a gap of four scales including the posterior genials followed by 150 ventrals, laterally separated from the dorsal scale rows by a slightly broader row of dorsal scales; anal scale undivided, followed by 59 divided subcaudals scales; terminal scale on the tail larger than the previous scale, blunt at the tip.
The paratype, of SVL 504mm and TL 145mm, is discoloured with a uniform dark greenish to black colour throughout the specimen in its current preservation state. It differs from the holotype with respect to pholidosis by having 14 DSR, 14 MSR, 11 PSR, 150 ventrals and 64 subcaudals; a distinct head of length 27.5 mm with supraoculars that are separated by one scale from above; two canthal scales on the canthus rostralis, and 3 cephalic scales from above; 11 infralabials on both sides.
Dark to verdant green on the dorsal surface of the head that fades into a lighter green throughout the body dorsally up to the tail and along the lateral sides of the body including the head; a prominent, 2-scale wide, white lateral stripe runs from the creamy white mandibular region; small hints and patches of blue visible on the head and dorsal scales, with the tail tip banded with dark blue or sometimes fully covered with dark blue or black; the last 11 scale rows of the tail banded with black to dark blue and white to yellow; creamy white to yellow mentum fades into a light creamy green throughout the ventrals, sometimes separated by the white ventral stripe from the lateral part of the body.
Greyish green on the head dorsum that fades into a bluish green shade throughout the body; lateral parts of the head light green to bluish green; mentum creamy yellow that blends with creamy green ventrals, separated by the white lateral stripe; tail tip with grey and white bands, tail bluish green with darker blue bands.
A typically arboreal (rarely semi-terrestrial) species (
Endemic to the southern Western Ghats, south of the Shencottah gap. Geographically separated from its sister species, C. macrolepis that inhabits the ranges to the north of the Shencottah gap. Found throughout the high elevations of the Agasthyamalai hills.
This species complex can be distinguished from regional congeners as follows: head scales as small as body scales (vs. large, shield-like in the C. macrolepis complex); midbody dorsal scale rows 21–23 (vs. <19 in the C. macrolepis complex); last rows of costal scales abutting ventrals on either sides larger than rest of the dorsal scale rows (vs. smaller in the C. macrolepis complex); 2nd supralabial bordering the anterior margin of loreal pit (vs. not so in C. strigatus); supraoculars often divided or scale sutures with an indented margin (vs. undivided in the remaining, regional congeners); subcaudals of tail tip blackish (vs. bluish in the C. gramineus and C. macrolepis complexes). Lineages within Craspedocephalus malabaricus group appear to be morphologically cryptic, and do not differ in scalation or external morphological characters, but show geographical separation and are deeply genetically divergent.
Trigonocephalus (Cophias) malabaricus Jerdon, 1854
Trigonocephalus (Cophias) wardii Jerdon, 1854
Lachesis coorgensis Rao, 1917
Trimeresurus malabaricus – Smith, 1943
Lachesis anamallensis (non Günther, 1864) – Wall, 1919, 1924 part
Craspedocephalus malabaricus
–
The specific epithets, mostly toponyms, also suggest the same: C. malabaricus: from ‘Malabar’ i.e. north Kerala and Coimbatore / Nilgiris, in the Western Ghats; C. anamallensis: from Anamalai hills of the Southern Western Ghats; Lachesis coorgensis: from ‘Coorg’ (=Kodagu) a part of Malnad region in Central Western Ghats. The only remaining nomen in its synonymy is Tri. wardii of Jerdon, 1854. Our perusal of historical literature reveal that this eponym could only be named after Samuel Neville Ward (18th June 1813 – 31st January 1897). Samuel M. Ward was with the Madras Civil Service (1832–63) and had a final appointment as Judge of Koyambatur (=Coimbatore). He had reportedly been corresponding with naturalists such as Charles Darwin, Edward Blyth, as well as T. C. Jerdon, who described Tri. wardii. Ward had been reported to have visited Sirsi, in North Canara for his work on Indian wildlife, mostly butterflies and birds (Pittie, 2016 and references therein).
Syntypes lost (after Smith, 1943; also see
Specimen series: Neotype: ZSI-18161 from Coorg, Karnataka, 12°24.82’N; 75°43.85’E by C.R. Narayan Rao in 1917, the holotype of Lachesis coorgensis Rao, 1917. — Other referred material: BNHS 2609-778 from Kotagiri, Tamil Nadu and BNHS 2069–781 from Coonoor, Tamil Nadu by A. M. Kinloch in 1907. Additional comparative material collected for this study - CESS053, CESS055 from Amboli, Maharashtra; CESS063, CESS065 from Saklespura Karnataka; CESS273 from Coorg, Karnataka; CESS086 from Thirunelli, Kerala by Ashok Kumar Mallik between 2009-11 and CESS141 from Silent valley by Saunak Pal and Mrugank Prabhu in 2010; BNHS 2609A from Kotagiri and BNHS 2609B from Coonor, Nilgiris, Tamil Nadu by A.P Kinloch in 1907; BNHS 2596 from Sirsi, Karnataka by Charles McCann in 1938; BNHS 2599 from Mahabaleshwar, Maharashtra by H. Abdulali in 1953; BNHS 2601 from Castle Rock, Karnataka by Mrs. H. Pearson in 1907.
Originally given as “West Coast, Peninsula of India”. Here restricted to Coorg (12°24.82’N; 75°43.85’E) in Central Western Ghats, by neotype designation.
The specific epithet malabaricus is a toponym, alluding to its type locality - the Malabar region of the Western Ghats.
A lineage of the C. malabaricus complex, C. malabaricus s. str. (L5) is here restricted only to populations north of the Palghat Gap. This nominotypical population is 8.3–9% and 1.2–2.2% divergent at cyt b and 16S respectively, from those south of the Palghat Gap (L3 & L4), recognised here as two nominate taxa: C. anamallensis (Günther, 1864) and Craspedocephalus travancoricus sp. nov. (see below). These taxa are allopatric with respect to each other and C. malabaricus.
Neotype in good condition, small lesion near the nape, possibly caused while collecting and euthanizing the individual; specimen with a slender, cylindrical body of snout to vent length (SVL) 481 mm and a prehensile tail of length (TL) 73 mm; dorsal scales keeled with anterior dorsal scale rows (DSR) 21, mid body scale rows (MSR) 21 and posterior scale rows (PSR) 13; head prominent, of length 24.3 mm, clearly distinguished from the neck with small, mildly keeled scales on the head; rostral scale trapezoid, with the lower side roughly more than twice the size of the upper side with the tip visible from above; supraoculars divided, separated by eight cephalic scales between both supraoculars at its posterior border; seven scales bordering each supraocular. Canthus rostralis distinct with four canthal scales; three preoculars, two postoculars and a thin elongated crescent shaped subocular; eye with a distinct elliptical pupil, vertical diameter of the eye 3.31 mm and horizontal diameter 3.68 mm; strongly keeled temporal scales and cephalic scales in the posterior sides above the mandibular joint; aperture of the nostril completely covered by the nasal scale, undivided and sub-pentagonal shaped, in contact with the first two canthal scales and the 1st and 2nd supralabial; loreal pit present in contact with the second supralabial and the 2nd and 3rd preoculars; nine supralabials and 12 infralabials, with eight scales between the last supralabial, including the last supralabial up to the start of the ventral scales; 1st, 2nd and 3rd infralabial scale in contact with the first pair of genials; a gap of four scales including the posterior genials followed by 148 ventrals, laterally separated from the dorsal scale rows by a slightly broader row of dorsal scales; anal scale undivided, followed by 38 divided subcaudals scales; Terminal scale on the tail larger than the previous scale, blunt at the tip.
The referred materials are of SVL up to 670 mm and TL up to 126 mm with colours varying from dark brownish red to light green throughout the specimens in its current preservation state, differs from the holotype with respect to pholidosis by having 19 to 22 DSR, 19 to 23 MSR, 13 to15 PSR, 145–149 ventrals and 52–54 subcaudals; head distinct with supralabials ranging between 8–10 and infralabials ranging between 10–13; one to three preocular scales, one to two scales (some specimens showing an absence of these scales) between the 3rd supralabial scale and the suboculars, seven to nine cephalic scales and seven to eight scales surrounding the supraoculars from the dorsum.
A highly variable and polymorphic species, with respect to colour, specimens can be found in a variety of colour morphs - greenish blue-cyan, bright yellow, green, rufous brown, bright orange and red coloured specimens have been encountered during this study; head characterized with a thick dark brown to black postocular stripe till the nape, labials sometimes marked with blotches and a highly variable pattern above the head, sometimes fully dark, some individuals with no markings at all, body with alternating zig-zag saddle shaped markings with the last rows of scales on the tail banded with different colour; these markings vary from brick reddish, dark brown to black, sometimes intermixed with spots of other colours such as green, yellow and blue; the base colour of the body varies from light brown in juveniles, light cream, orange, yellow, brick red, bluish green and sometimes morphs mottled with all or some of the aforementioned colours; ventrals sometimes vary from the colour of the dorsum, complementing the variety of vibrant dorsal colours, but often are coloured similar to the dorsum; colour change is also observed to be seasonal (
Fairly faded specimen with a light brown dorsum, ventrals and tail; scales bordered with dark brown; temporal stripe visible on the right side of the specimen in dark brown, left side with no visible temporal stripe; body with barely distinguishable dark brown saddle shaped markings throughout the body; tail with dark brown stripes from the vent up to the tip.
An arboreal species, commonly found on bushes and in undergrowth in forests and near streams in evergreen forests to moist deciduous and lowland riparian forests. Due to anthropogenic changes to the landscape, this species is also abundantly found in agricultural landscapes such as coffee plantations, from 100-1800m MSL.
Restricted to the central and northern Western Ghats from Mahabaleshwar – Koyna in Maharashtra to the Nilgiris and Elivalmalai hills, north of the Palghat Gap. Known to occur sympatrically with C. occidentalis comb. nov. in Nilgiris and Coorg, with C. gramineus in Amboli and may have some overlap with C. strigatus in the mid to high elevations of the western slopes of the Nilgiris (at the upper limit of its altitudinal distribution).
Trimeresurus anamallensis Günther, 1864
Lachesis anamallensis - Boulenger, 1896; Wall, 1919 part
Craspedocephalus anamallensis (Günther, 1864)
Lectotype (here designated): NHMUK 1946.1.19.93 from Anamallay hills (=Anamalai hills) collected by R.H. Beddome. — Paralectotypes: NHMUK 1946.1.18.73–74, NHMUK 1946.1.19.82, NHMUK 1946.1.19.89, NHMUK 1946.1.19.94–95, and NHMUK 1946.1.20.3, from Anamallay hills (=Anamalai hills) collected by R.H. Beddome. — Other specimens: CESS178 from Topslip, Anamalai Tiger Reserve, Tamil Nadu, by Ashok Kumar Mallik, 2011; CESS181, Orukomban Range, Parambikulam, Kerala by Ashok Kumar Mallik in 2011; CESS166 from Goodrickal Range, Kakki, Periyar Tiger Reserve, Kerala, by Saunak P. Pal, 2011.
Anamalai hills, Southern Western Ghats, Tamil Nadu, India; same type locality for the type series of C. anamallensis.
The specific epithet anamallensis is a toponym, alluding to its type locality - the Anamalai hills of the Southern Western Ghats.
A cryptic lineage belonging to the C. malabaricus complex, this lineage (L3) is genetically divergent from C. malabaricus (L5) by 8.3% & 1.2%, and from C. travancoricus sp. nov. (L4) by 7.1% and 1.5% at cyt b and 16S respectively. This lineage is geographically isolated from C. malabaricus to the North (separated by Palghat Gap) and to the south the boundary broadly lies in the Periyar Plateau, between Gudrikal range (its southern limit) and Devarmalai (northern limit of its sister lineage C. travancoricus sp. nov.).
Lectotype in a generally good condition, entire with a cylindrical body of SVL 505mm and a prehensile tail of TL 87mm; dorsal scales mildly keeled with DSR 21, MSR 21 and PSR 15; head of length 29mm prominent and clearly distinguished from the neck with strongly imbricate small scales; tip of the rostral scale visible from above, with the upper end roughly half the size as the lower; divided supraoculars with nine cephalic scales between both the supraoculars; nine scales surrounding each divided pair of supraoculars on both the sides with nine scales between the posterior border of the supraoculars; distinct canthus rostralis with four scales on the canthal ridge; two preoculars and two postoculars, an elongated cresent shapend subocular; strongly keeled temporals and keels continue to be present in other head scales behind the oculars except the supralabials towards the posterior; eye with a distinct elliptical pupil of vertical diameter 3.3 mm and a horizontal diameter of 3.98 mm; nostril aperture completely covered by the nasal scale, undivided and pentagonal-sub rectangular in shape, in contact with the first three canthal scales, first and second supralabial; nine supralabials and eleven infralabials, with eight scales between the edge of the mouth and the first ventral scale; 1st, 2nd and 3rd infralabial scale in contact with the first pair of genials; a gap of six scales in between the first genial and ventrals; 157 ventrals separated laterally from the body scales by a row of slightly broader dorsal scales; anal scale undivided followed by 55 divided caudals; terminal scale rounded and blunt at the tip, slightly larger than the previous scale.
The following characters vary within the specimens of the examined type series. Variations in pholidosis between the specimens were: supralabials 9–10 and infralabials 11–13, preoculars 2–3, ventrals 144–145 and subcaudals 50–62, about 8–12 scales between the edge of the mouth and the ventral scales; 21–22 scale rows around the neck; the post ocular stripe sometimes extends to 2 rows of scales.
Black dorsal head scales with the anterior scales with hints of light green and posterior head scales bordered with yellow, up to the postocular eye stripe, that extends untill the nape; light bluish green on the lateral parts of the head that fades into a creamy yellow to white underside, from the mandibular region up to the ventrals; ventral scales creamy yellow scales alternating with light greenish yellow scales, consecutively larger gaps between the lighter scales filled with the greenish yellow scales towards the tail - these correspond to the alternating between creamy yellow and green scales in the column that separates the ventrals and dorsal scales; caudal scales yellow, bordered and often blotched with black scales; black blotches throughout the dorsum with a gap of 3–4 scale rows.
Head dorsum almost completely covered black to dark brown and scales bordered with light faded green; black/ dark brown postocular stripe about 2 scales wide, a preocular/ temporal stripe that continues to the loreal pit and ends at the supralabials below; black markings on the labials below the suboculars; body in light faded green with black saddle shaped markings, the markings centered with faded brown marbled markings; the row dorsal of scales that meet the ventrals alternate between the dorsal light faded green and dark brown/ black markings with a gap of two to three scales in between them; ventrals plain light creamish yellow; subcaudals in black with yellow blotches.
Similar to C. malabaricus, an arboreal species, commonly found on bushes and in the undergrowth in forests and near streams in moist evergreen forests to deciduous and lowland riparian forests. Due to anthropogenic changes to the landscape, this species is also often found in cultivated landscapes such as coffee plantations, from 100–1800 m asl.
Endemic to the southern Western Ghats, south of the Palghat Gap and north of the Shencottah Gap. We recorded this species in the Nelliamapthy, Anamalai and Palni hills, Cardamom hills, and northern sections of the Periyar plateau. Craspedocephalus anamallensis has been recorded to be sympatric with C. macrolepis at the highest limit of its elevational range (see Malhotra & Davis, 1991).
Craspedocephalus anamallensis in life, showing: (A) brown morph front view, from Top Slip, (B) green morph, from Kottaimalai, (C) grey morph, from Nelliyampathy, (D) & (E) olive morphs from Top Slip; entire dorsolateral views, (F) green morph head lateral view, (G) green morph, head dorsal view; from Parambikulam region.
Trimeresurus anamallensis (not of Günther, 1864) - Ferguson, 1895
Trimeresurus malabaricus
(not of Jerdon, 1854) -
Holotype: BNHS 3595 (CESS074) from Bonnakard, Peppara, Kerala by Saunak Pal and S. P. Vijayakumar in 2010; BNHS 2607 from Thiruvananthapuram, collector and year unknown. — Paratype: BNHS 3594 (CESS257) from Devarmalai, Tamil Nadu by Saunak Pal and Mrugank Prabhu in 2011.
Peppara (8°39.7167’N; 77°10.7167’E), Kerala, a part of the Agasthyamalai Hill complex of the Southern Western Ghats.
Toponym, named after its distribution in the far south of the Western Ghats, in the southern parts of the ‘Travancore’ hill ranges.
As previously elaborated and clarified (see C. malabaricus account), historical collections and typifications (both prevailing and previously synonymized treatments) did not involve the population circumscribed here as a distinct lineage. Therefore, this innominate population, previously cited (see
A cryptic lineage belonging to the C. malabaricus complex, this lineage (L4) is genetically divergent from C. malabaricus (L5) by 9% & 2.2% and from C. anamallensis (L3) by 7.1 & 1.5% at cyt b and 16S respectively. This lineage is also allopatric with its related taxa C. malabaricus occurring north of the Palghat Gap and is immediately allopatric with C. anamallensis distributed just north of its distribution range, north of the Shencottah Gap.
Holotype in good condition, dissected, with a slender, cylindrical body of snout to vent length (SVL) 345 mm and a prehensile tail of length (TL) 61 mm; dorsal scales keeled with anterior dorsal scale rows (DSR) 21, mid body scale rows (MSR) 23 and posterior scale rows (PSR) 14-15; head prominent, of length 20.28 mm, clearly distinguished from the neck with small, juxtaposed dorsal scales on the head; rostral scale sub triangular with the upper side roughly half the size of the lower side with the tip visible from above supraoculars of length 3.64 mm and width 1.0 mm, separated by seven scales, between the posterior edge of the supraocular scales; canthus rostralis distinct with four canthal scales on the ridge; three preoculars, two postoculars and a thin elongated crescent shaped subocular, in contact with a small scale, encompassed by the third and fourth supralabial scale; eye with a distinct elliptical pupil, vertical diameter of the eye 2.6 mm and horizontal diameter 3.4 mm.; temporal scales mildly keeled; aperture of the nostril completely covered by the nasal scale, undivided and subrectangular; nasal scale bordering the first supralabial; loreal pit present in contact with the second supralabial with two scales between the nasal and the second supralabial: nine supralabials and 11 infralabials, with nine scales between the last supralabial, including the last supralabial till the start of the ventral scales; 1st, 2nd and 3rd infralabial scale in contact with the first pair of genials; a gap of three scales including the posterior genials followed by 147 ventrals, laterally separated from the dorsal scale rows by a slightly broader row of dorsal scales; anal scale undivided, followed by 55 to 56 divided subcaudals scales; terminal scale on the tail larger than the previous scale, blunt at the tip.
The paratypes have SVL upto 282 mm and TL 65 mm, and differ from the holotype with respect to pholidosis by having 20 to 21 DSR, 21 MSR, 14 to 15 PSR, 157 ventrals and 55 subcaudals; three to four canthal scales on the canthus rostralis, and seven to nine cephalic scales from above; 10 to 12 infralabials on both sides.
Head dorsum almost covered with dark brown to purplish brown colour with scales bordered with light yellowish green; postocular and preocular stripe almost indistinguishable from the head dorsum colour, separated with a faded yellowish green stripe; dark brown postocular stripe about 3 scales wide, a preocular/ temporal stripe that continues to the loreal pit and ends at the supralabials below; black border markings on the labials below the suboculars and anterior supralabials; body in light faded green and brown marbled scales with 28 brown saddle shaped markings, the markings centered with faded brown marbled markings; the row dorsal of scales that meet the ventrals alternate between the dorsal marked with faded yellow and dark brown with a gap of two to three scales in between them; ventrals plain light creamish yellow; subcaudals in black with yellow blotches; tail with 13 yellowish green bands on dark brown to black; eyes silverish with a tinge of yellow, rufous red blotches throughout the eye, concentrated towards the middle, perpendicular to the pupil, almost forming a cross.
Similar to colouration in life with brighter colours faded dull and yellows throughout the body bleached to a creamish white colour; pupils bluish white, dilated.
Similar to other members of the C. malabaricus group, an arboreal species, commonly found on bushes and in the undergrowth in forests and near streams in moist evergreen forests to deciduous and lowland riparian forests, from 100–1800 m asl.
Recorded mostly from Agasthyamalai with a single isolated record from Devarmalai hills, across the Shencottah gap. This species may occur sympatrically with C. peltopelor sp. nov. in the highest elevations of Agasthyamalai.
Craspedocephalus travancoricus sp. nov. in life, showing: (A) brown morph entire front view, (B) green/brown morph entire dorsal view, (C) orange morph front view, (D) green morph lateral view, (E) green morph dorsal view, (F) brown morph lateral view, (G) grey/black morph dorsolateral view; from Ponmudi hills, Kerala.
This species complex can be distinguished from regional congeners as follows: head scales as small as body scales (vs. large, shield-like in the C. macrolepis complex); midbody dorsal scalerows 21–23 (vs. <19 in C. macrolepis complex); last rows of costal scales abutting ventrals on either sides larger than rest of the dorsal scale rows (vs. smaller in the C. macrolepis complex); 2nd supralabial bordering the anterior margin of loreal pit (vs. not so in C. strigatus); supraoculars undivided (vs. often divided or with indented scale in the C. malabaricus complex); subcaudals of tail tip bluish (vs. blackish in the C. malabaricus complex).
Coluber gramineus Shaw, 1802
Coluber viridis (nec Trimeresurus viridis Lacépède, 1804) Bechstein, 1802
Vipera viridis (nec Trimeresurus viridis Lacépède, 1804) Daudin, 1803
Trigonocephalus fario Jan, 1859 (nomen nudum)
Colubar gramineus – Mason, 1860 (nomen incorrectum)
Bothrops viridis fario Jan, 1863 (nomen nudum)
Bothrops viridis genei Jan, 1863 (nomen nudum)
Lachesis graminea – Wall, 1919 part
Trimeresurus gramineus – Whitaker & Captain, 2004 part
Craspedocephalus gramineus
–
Later
Coluber viridis Bechestein, 1802 and Vipera viridis Daudin, 1803 are both objective junior synonyms of Coluber viridis Shaw, 1802, all being described on the basis of the very same type specimen described and illustrated by
Holotype (iconotype), a 762 mm specimen described and illustrated in
“hills in the vicinity of Vizagapatam, coast of Coromandel, India” [= Vishakhapatnam, Andhra Pradesh, India, 17°41’N; 83°13’E].
gramineus, ‘grassy’ in Latin, alluding to its grass-green dorsal colouration.
NHMUK 1946.1.19.87 from Cuddapa Hills, Andhra Pradesh, by R.H. Beddome paratype of Trimeresurus occidentalis Pope & Pope, 1933; CESS033 from Gandagan, Orissa by Ashok Kumar Mallik; CESS100, CESS101, CESS102 from Naneghat, Maharashtra by Ashok Kumar Mallik in 2010; AFS96.13 from Masinagudi, and AFS96.14 Gingee, Tamil Nadu by Anita Malhotra in 1997; BNHS 2627 from Khandala, Maharashtra by Charles Mc Cann in 1941, BNHS 2764 from Ahwa, Dangs, Gujarat by Dr. E.M. Shull in 1963 and BNHS 3275 from Sirumalai hills, Tamil Nadu by S.P. Vijayakumar, 2001; CESS526 from Shevroys, Tamil Nadu by Achyuthan Srikanthan and M.V. Shreeram in 2019.
A cryptic lineage (L1) belonging to the C. gramineus complex, it is distinguished from C. occidentalis (L2) as follows: lower ventral scale count 158–179 (vs.142–154). It is genetically divergent from C. occidentalis by 8.1 % and 1.0 % at cyt b and 16S respectively. This lineage is far more widespread than its parapatric sister taxon C. occidentalis, occuring almost throughout peninsular India from Odisha in the east, southern Gujarat to the north-west and as far south as the Srivilliputhur hills.
A species with a slender, cylindrical body of snout to vent length (SVL) up to 679 mm and a prehensile tail; dorsal scales keeled with anterior dorsal scale rows (DSR) 19–21, mid body scale rows (MSR) 19–21 and posterior scale rows (PSR) 15; head prominent, clearly distinguished from the neck with small, juxtaposed scales on the head; rostral scale sub triangular with the upper side roughly one fourth the size of the lower side with the tip visible from above; supraoculars separated by 8–11 scales, between the posterior edge of the supraocular scales; canthus rostralis distinct with three to four canthal scales on the ridge; two to three preoculars, two to three postoculars and a thin elongated crescent shaped subocular; eye with a distinct elliptical pupil; temporal scales mildly keeled; aperture of the nostril completely covered by the nasal scale, undivided and subrectangular; nasal scale bordering the first supralabial; loreal pit present in contact with the second supralabial with two scales between the nasal and the second supralabial; 10–12 supralabials and 11–13 infralabials, with 9–13 scales between the last supralabial, including the last supralabial up to the start of the ventral scales; ventrals 158–179, laterally separated from the dorsal scale rows by a slightly broader row of dorsal scales anal scale undivided, divided subcaudals 54–67; terminal scale on the tail larger than the previous scale, blunt at the tip.
Head and dorsum colour from verdant green to leaf green, sometimes bluish green with black, alternating saddle shaped markings on the dorsum; preocular/ temporal stripe in black, sometimes green fading into black; ventrals with bright yellow, creamish yellow to a dirty white colour; the region where the ventrals meet the dorsum alternating with the ventral colour once every 2–3 scales.
A highly arboreal species found in dry scrub, dry deciduous, semi evergreen and lowland riparian forests from 100-1600 m asl.
Endemic to Peninsular India. Found in the Eastern Ghats (Simlipal hills, Chota Nagpur plateau southwards upto Sirumalai hills) and hills of Central India (Pachmahri, Seoni hill ranges) as well as the Western Ghats from Surat Dangs, southwards till the Shencottah gap.
Trimeresurus occidentalis Pope & Pope, 1933
Trimeresurus viridis (nec Coluber viridis Bechestein, 1802) - Beddome, 1862 part
Lachesis graminea – Wall, 1919 part
Craspedocephalus occidentalis (Pope & Pope, 1933)
Pope & Pope (1933), in an effort to fix the status of Southeast Asian taxa of superficially similar green Trimeresurus species, worked out the systematics of the Indian group. Unfortunately, they were mistaken in allocating the nomen Coluber gramineus Shaw, 1802 to the East Asian species (see
Among the four paratypes attributed to this taxon in its original description (Pope & Pope, 1933), one male from Brahmagiri, Western Ghats is currently attributable to this species based on the phylogenetic position of topotypical samples. The distribution of C. occidentalis, as defined here, encompasses the provenance of the holotype (Mudumalai, Wayanad, and the Nilgiri hills in general). We refer three other paratypes, two females originating from the Cuddapa hills and the Shevaroys in the Eastern Ghats and one male from Matheran to C. gramineus (Shaw, 1802) based on the phylogenetic placements of topotypical samples. However, as paratypes have no name-bearing function and status, the nomen Craspedocephalus occidentalis is available in toto for being conferred to this Western Ghats population.
Holotype, NHMUK 1982.8.26.40, an immature male, collected by R.H. Beddome.
Mudumallay, near Wayanad [i.e., Mudumalai hills, in Nilgiris dt., Tamil Nadu, India] in the Western Ghats (fide Pope & Pope 1933).
Latin, for ‘western’, in allusion to its western distribution range, compared to S.E. Asia.
Holotype, NHMUK 1982.8.26.40 from Wayanad, Tamil Nadu by R.H. Beddome; CESS040 from Brahmagiri, Karnataka by S.P. Vijayakumar in 2009; CESS272 from Tadiendamol, Karnataka by Ashok Kumar Mallik in 2011.
A cryptic lineage (L2) belonging to the C. gramineus complex, it can be distinguished from C. gramineus s. str. (L1) as follows: lower ventral scale count 142–154 (vs. 158–179). L2 is genetically divergent from C. gramineus s. str. (L1) by 8.1 % at Cyt b and 1.0 % at16S. This lineage is possibly parapatric with respect to its far more widespread sister taxon C. gramineus, and is endemic to the Wyanad-Bramagiri-Coorg hill complex of the central Western Ghats, at higher elevations (> 1000 m MSL).
Holotype in good condition, entire, with a slender, cylindrical body of snout to vent length (SVL) 400 mm and a prehensile tail of length (TL) 97 mm; dorsal scales keeled with anterior dorsal scale rows (DSR) 23, mid body scale rows (MSR) 21 and posterior scale rows (PSR) 15; head prominent, of length 21.5 mm, clearly distinguished from the neck with small, juxtaposed dorsal scales on the head; rostral scale sub triangular with the upper side roughly one fourth the size of the lower side with the tip visible from above; supraoculars of length 1.85 mm and width 4.15 mm, separated by eight scales, between the posterior edge of the supraocular scales; canthus rostralis distinct with four canthal scales on the ridge; two preoculars, two postoculars and a thin elongated crescent shaped subocular, in contact with a pair of scales scales that are in contact with the third and fourth supralabial scale; eye with a distinct elliptical pupil, vertical diameter of the eye 2.23 mm and horizontal diameter 2.44 mm; temporal scales mildly keeled; aperture of the nostril completely covered by the nasal scale, undivided and subrectangular; nasal scale bordering the first supralabial; loreal pit present in contact with the second supralabial with two scales between the nasal and the second supralabial; nine supralabials and 10 infralabials, with seven scales between the last supralabial, including the last supralabial up to the start of the first ventral scale; 1stand 2nd infralabial scale in contact with the first pair of genials; a gap of six scales including the posterior genials followed by 155 ventrals, laterally separated from the dorsal scale rows by a slightly broader row of dorsal scales; anal scale undivided, followed by 60 divided subcaudals scales; terminal scale on the tail larger than the previous scale, blunt at the tip.
Head and dorsum colour varies from bright green to faded dull green, with no markings on the dorsum; preocular/ temporal stripe absent; ventrals in creamish yellow to dirty white colour; the region where the ventrals meet the dorsum alternating with the ventral colour once every 2–3 scales; the colour of the dorsum and ventrals divides exactly at the pre/postocular stripe area, with an absence of a dark stripe (as opposed to C. gramineus).
Head and dorsum in light faded green; ventrals creamish to dirty white in colour; some of the dorsum scales with a black interscalar colour, more evident in the front half of the body; the colour of the dorsum and ventrals divides exactly at the pre/postocular stripe area, with an absence of a dark stripe (as opposed to Tri. gramineus).
A highly arboreal species found in moist evergreen forests from 1000–1900m MSL, sympatric with C. malabaricus throughout parts of its range.
Endemic to the central Western Ghats, distributed in the Wayanad, Brahmagiri, Coorg hills, at higher elevations (> 1000 m asl).
Atropos darwini Duméril, Bibron & Duméril, 1854
Trigonocephalus (Cophias) neelgherriensis Jerdon, 1854
Lachesis strigatus – Boulenger, 1896
Lachesis strigata – Wall, 1919
Trimeresurus strigatus – Smith, 1943
Protobothrops strigatus
–
Craspedocephalus strigatus
–
Originally in error, mentioned as “Cape of Good Hope?” and “Madras” subsequently emended to Madras Presidency (=Tamil Nadu) by
Latinized from its stem word ‘strigate’ alluding to the pattern streaked with colourful, alternate, transverse bars.
Syntypes NHMUK 1946.1.18.79 and NHMUK 1946.1.18.78 from Nilgiris, Tamil Nadu by T.C. Jerdon in 1850.
Syntypes NHMUK 1946.1.18.79 and NHMUK 1946.1.18.78 from Nilgiris, Tamil Nadu by T.C. Jerdon in 1850; CESS142 from Silent Valley, Kerala by Saunak Pal and Mrugank Prabhu in 2010; BNHS 2617 and BNHS 2618 from Coonor by C.Gray in 1917; BNHS 2619 from Coonor by Maj. Frank Wall in 1911; BNHS 2621 from Ooty by Maj. Frank Wall in 1912.
A species of Craspedocephalus (L8) endemic to the Western Ghats, characterized by having the following combination of characters: 2nd supralabial (usually) not bordering the anterior margin of loreal pit (vs. always bordering in the C. malabaricus, C. gramineus complexes); lacking a prehensile tail and green dorsum (vs. having prehensile tail and green dorsum in the C. gramineus, C. macrolepis complexes); having an undivided supraocular (vs. divided or with indented margins in the C. malabaricus complex).
Relatively stout species with a cylindrical body of snout to vent length (SVL) up to 391 mm and a tail of length (TL) up to 64 mm; dorsal scales keeled with anterior dorsal scale rows (DSR) 20 to 22, mid body scale rows (MSR) 19 to 21 and posterior scale rows (PSR) 15 to 17; head prominent, clearly distinguished from the neck with small juxtaposed scales on the dorsal surface of the head; rostral scale sub triangular with the upper side roughly half the size of the lower side with the tip visible from above; supraoculars separated by 9 to 11 scales on the posterior end; canthus rostralis distinct with three canthal scales; two to three preoculars, two to three postocular and a thin elongated crescent shaped subocular; eye with a distinct elliptical pupil; temporal scales smooth; aperture of the nostril completely covered by the nasal scale, undivided and subrectangular; nasal scale bordering the first supralabial; loreal pit present in contact with the second supralabial with two scales between the nasal and the second supralabial; nine to 10 supralabials and 10 to 12 infralabials, with six to eight scales between the last supralabial, including the last supralabial till the start of the ventral scales; 1st, 2nd and 3rd infralabial scale in contact with the first pair of genials; a gap of three scales including the posterior genials followed by 134 to 142 ventrals, laterally separated from the dorsal scale rows by a slightly broader row of dorsal scales; anal scale undivided, followed by 38 to 44 divided subcaudals scales; terminal scale on the tail larger than the previous scale, blunt at the tip.
Bronze to light brown dorsum blotched with a stark, continuous alternating saddle-shaped pattern in dark brown to black, strikingly similar to the markings on Vipera berus or Gloydius himalayanus; preocular/temporal stripe in dark brown; post ocular stripe in dirty brown continuing towards the loreal pit and the infralabials; another stripe below the subocular stripe fades into the infralabials followed by another blotch towards the end of the infralabials; base colour of the infralabials and ventrals being light creamish to white in colour, often dotted with rufous spots in the supralabials the region where the dorsal scales meet the ventrals in altenating dark brown colour and light brown/bronze colour scales; dorsal bronze scales are dotted with darker brown; the nape is characterized with a prominent horse shoe shaped marking hence earning its common name; in juveniles, the bronze colour is replaced with light brown.
Brown and cream markings dorsally and laterally, occasionally interrupted with silvery/grey scales, tail mostly brown and cream coloured with lighter more vivid cream coloured scales making triangular markings vertically along it (four in total); tip of tail fading to a light cream colour.
A highly terrestrial species found in montane evergreen, moist evergreen and high elevation grasslands.
Endemic to the Nilgiri Massif north of the Palghat Gap, distributed in very high elevations (1700–2600 m asl) (also see Wall, 1919; Bhupathy & Nixon, 2011). This species has the smallest geographic range of all Craspedocephalus in Peninsular India (Ganesh & Chandramouli, 2018).
The systematics of pit vipers of Peninsular India has been in flux, given their variation in morphology, their distribution in different habitat types and uncertainty of species delimitation criteria (
New lineages (green bars) are depicted within C. gramineus, C. malabaricus and the C. macrolepis species complex along with the other species from the Peninsular India. The clade comprising C. macrolepis and C. peltopelor sp. nov. is sister to the clade comprising all other members of Peninsular Indian Craspedocephalus (II). The Western Ghats C. malabaricus complex includes C. malabaricus, C. anamallensis and C. travancoricus (IV). C. trigonocephalus from Sri Lanka is nested within the Western Ghats sub-clade (III) along with C. strigatus, C. gramineus and C. occidentalis (V). Clade-I comprises species from Southeast Asia.
The phylogeny generated using three concatenated mitochondrial fragments of almost all the populations and species of Craspedocephalus found in Peninsular India is similar to the tree topology published in earlier studies (Malhotra & Thorpe 2004,
The chromatically variable and widely distributed taxon, C. malabaricus, was recovered with three divergent lineages, two of which are distributed in the Southern Western Ghats and are sister to each other, with high genetic divergence from a northern Western Ghats lineage. Considering the type locality of C. malabaricus as the Western Ghats (all west coast forests in Peninsular India) (
This delineation takes into account the geographic ranges of each of the lineages within the C. malabaricus species complex: C. malabaricus (Jerdon, 1854), C. anamallensis (Günther, 1864) and C. travancoricus sp. nov. whose distributions coincide with segments of the Ghats separated by significant gaps. However, there were morphological differences (i.e. strongly keeled dorsal scales) between
Similarly, the C. gramineus species complex comprises two highly divergent lineages (7 % at ND4 and 8 % at cyt b) with significant morphological variation and strong habitat preference in those lineages (authors’ personal observation). Morphologically, they differ in ventral scales and supralabials. Lineage 1 (C. gramineus) is distributed in the drier and low-mid elevations of hill ranges (till ca. 1000 m asl) of Peninsular India while Lineage 2 (C. occidentalis) is distributed in the wet forests of the Western Ghats. These findings are supported by earlier work (Pope & Pope, 1933).
The endemic C. macrolepis was classified as a distinct species with significant morphological differentiation and was found to be nested within the Craspedocephalus clade of Peninsular India, as suggested by earlier studies based on morphology alone (
Our work suggests that there are (at least) eight independent evolutionary lineages in Peninsular India, supported by genetics, morphology, and geography. Besides naming two new lineages, both from the southernmost part of the Western Ghats, this study also clarifies the taxonomic status, distribution and phylogeny of Peninsular Indian Craspedocephalus involving both recognized and synonymized taxa. Of the eight species of Craspedocephalus belonging to Peninsular India, seven are restricted to the wet forests of the Western Ghats. The southern Western Ghats stands out in terms of species richness for Craspedocephalus in Peninsular India with four endemic species, which is evident in other taxa including frogs (Raorchestes -
The Peninsular Indian clade comprises almost all taxa distributed across South Asia except Tropidolaemus huttoni. The phylogenetic relationship of Tro. huttoni with Trimeresurus is unknown. Tropidolaemus huttoni is currently known from two neonate museum specimens, which are underdeveloped sexually. Based on its morphological similarity to Tropidolaemus wagleri, David & Vogel (1998) placed Tro. huttoni in this genus.
This work underscores the indispensable role of genetic studies that enable us to fully document cryptic diversity including in lineages that have remained taxonomically ‘stable’ for over a century (since Rao, 1917). This study also highlights the profound and untested effect of geographic barriers on this group of snakes. Though there were several synonyms and typifications within, for example, the C. malabaricus group between 1854 and 1917, these were primarily driven by morphological variations and not based on geographic rationale. That we uncovered geographically concordant sister lineages within the genus Craspedocephalus in the Western Ghats exemplifies the effectiveness of allopatry as a prezygotic reproductive barrier, one that does not instigate morphological changes in lineages, resulting in a high degree of crypsis, but at the same time leading to deep genetic divergence. This pattern is also observed in vine snakes (Ahaetulla –
KS and AKM thank the Department of Biotechnology, Ministry of Science and Technology, Government of India (BT/PR-14146/BCE/08/814/2010) as the main funding agency for this study; additional support was received from Ministry of Environment and Forests, Government of India (through grants to CES, IISc), DBT-IISc Partnership Programme and Critical Ecosystem Partnership Fund (CEPF). We would like to thank the state forest departments of Maharashtra, Karnataka, Kerala, Tamil Nadu, Andhra Pradesh, Odisha, Chhattisgarh, Meghalaya, Arunachal Pradesh and Jharkhand for providing permission for us to carry out sampling in their states. We would also like to thank the Forest Rangers, Forest Guards, Forest watchers and other field staff without whom this work would not have been possible.
We would also like to thank Jeff Streicher [NHM(UK)], Omkar Adhikari and Rahul Khot (BNHS) for help in the museum specimen examination and deposition; Aditi Jayarajan, Riya Menezes for help in laboratory work; Aritri Sanyal for morphology work; Saunak Pal, Mrugank Prabhu and S. R. Chandramouli for specimen collection; Romulus Whitaker, Gerry Martin, Ishan Agarwal, Vivek Sharma, Jose Louies, Aniruddha Datta-Roy, K. P. Dinesh, Hemant Ogale, Mayavan and Sudhakar for the collection of tissue samples and help in fieldwork. AKM thanks Dr. Lee Grismer for providing location information for a few specimens. For generous contribution of photographs, we wish to thank M.V. Shreeram (C. malabaricus colour morphs), Allipara Sreejith (C. peltopelor sp. nov) & Vivek Philip Cyriac (C. peltopelor sp. nov); and Hugo de Souza, Shreekant Deodhar, Smriti SR and Udita Bansal for specimen photography. SRG thanks the Executive Chairman and Trustees of the Chennai Snake Park for encouraging his research activities. NSA thanks N.V Srikanthan, M. Nandini and M.V. Shreeram for their support.
Table S1
Data type: .pdf
Explanation note: Details of gene regions amplified and PCR primers used in this study. Table indicates DNA sequence length (in base pairs) and PCR protocols used.
Table S2
Data type: .cvs
Explanation note: List of tentative species of Asian pit vipers and outgroups use in this study. The table contains the museum voucher numbers, geographic locations and loci used in this study. ‘*’ Indicates non-lethal sampling. Voucher numbers with parentheses indicate the secondary code number.
Table S3
Data type: .pdf
Explanation note: Morphological characters examined and their abbreviations used to discriminate among species in pit vipers.
Figure S1
Data type: .jpg
Explanation note: The complete Bayesian Poisson Tree Processes (bPTP) output trees from a concatenated dataset of three mitochondrial loci (cyt b, ND4 and 16S) show predictions of putative species across the clades. The values on clades indicate the posterior probability, monophyly (clade of single species) with 1.00, whereas lower values suggest polyphyly (clade with more than one species). The actual number of putative species in the tree is ascertained with help of other delimiting criteria. Blue colored branches indicate monophyly of that lineage and red color indicates individuals clustered together within a species.
Table S4
Data type: .pdf
Explanation note: Uncorrected pairwise genetic distances (in per cent) between lineages (L1–L9) for mitochondrial loci ND4, CYTB and 16S.
Figure S2
Data type: .pdf
Explanation note: Distribution of Craspedocephalus lineages in Peninsular India: (A) Craspedocephalus macrolepis complex, (B) Craspedocephalus malabaricus complex, (C) Craspedocephalus gramineus complex.