Tuesday 16 February 2021

Achalinus zugorum: A new species of Odd-Scaled Snake from Ha Giang Province, Vietnam.

The family Xenodermidae is a Late Cretaceous diverging group (stem age) of Caenophidian Snakes composed of five poorly known genera; Achalinus, Fimbrios, Parafimbrios, Stoliczkia, and Xenodermus. Odd-scaled Snakes, Achalinus, are an aptly named group of nocturnal Xenodermid Snakes distributed throughout Japan, China, Taiwan, and Vietnam, characterized by a unique nonimbricate scale organisation where the dorsal scales form a dissociated and non-overlapping pattern. The secretive nature of Snakes in the genus Achalinus could perhaps explain why the group is so rarely detected and thus consequently why studies concerning ecology and natural history of Achalinus are almost nonexistent.

Recently, an increasing number of species descriptions has brought further attention to Achalinus, suggesting that diversity within Odd-scaled Snakes was highly underestimated. Currently, minimal genetic data (e.g. single locus mitochondrial DNA) exist for only 10 of the 13 recognized species of Achalinus; Achalinus ater, Achalinus emilyae, Achalinus formosanus, Achalinus hainanus, Achalinus jinggangensis, Achalinus juliani, Achalinus meiguensis, Achalinus niger, Achalinus rufescens, Achalinus spinalis, Achalinus timi, Achalinus werneri, and Achalinus yunkaiensis. Furthermore, our cumulative understanding of Odd-scaled Snake distributions is rather poor owing to infrequent observations. The bulk of diversity is contained in mainland China (Achalinus ater, Achalinus jinggangensis, Achalinus meiguensis, Achalinus rufescens, Achalinus spinalis, and Achalinus yunkaiensis) with three of those species also ranging into northern Vietnam (Achalinus ater, Achalinus rufescens, and Achalinus spinalis). Of the 13 species currently recognized, six are known from Vietnam, including three endemic species recently described from provinces in the northern portion of the country. The recent detection of novel species of Achalinus in Bac Giang, Cao Bang, Quang Ninh, and Son La provinces further underscores the likelihood of undiscovered species elsewhere in northern Vietnam.

Bordering Cao Bang immediately to the west is Ha Giang Province, a province of similar size with a diverse but still poorly characterised herpetofaunal assemblage. Ha Giang lies east of the Red River and is characterised by precipitous limestone formations coupled with rolling mountains and valleys that dominate the subtropical landscape. The province is drenched in approximately 2400 mm of rainfall annually, with as much as 515.6 mm falling during July. Ha Giang falls into the ‘South China’ subunit of the Indo-Malayan Realm, a biogeographic area which conjoins southern China and northeastern Vietnam. In Ha Giang, this area contains tropical semi-evergreen rainforest, subtropical lowland moist forest, and limestone forest, however, the lowlands of this region are fairly populated (94 person/km²) thus much of the primary lowland forest has been cleared and converted for agricultural purposes. Consequently, much of the intact forest is restricted to more montane regions.

Prior surveys of the region have brought the total number of recognised Reptile species from Ha Giang to 57, although the province has been most recently highlighted in the literature for its increasingly known Amphibian diversity.

To better characterise herpetofaunal diversity within the region and northeastern Indochina more broadly, Aryeh Miller of the Department of Vertebrate Zoology at the Smithsonian National Museum of Natural History, and the Department of Biology at the University of North Carolina Asheville, Hayden Davis of the Department of Biology and Center for Biodiversity and Ecosystem Stewardship at Villanova University, and the Department of Biology and Burke Museum of Natural History and Culture at the University of Washington, Anh Mai Luong, Quyen Hanh Do, and Cuong The Pham of the Institute of Ecology and Biological Resources at the Vietnam Academy of Science and Technology, Thomas Ziegler of Aktiengesellschaft Zoologischer Garten Köln, and the Institute of Zoology at the University of Cologne, Justin Lee and Kevin de Queiroz, also of the Department of Vertebrate Zoology at the Smithsonian National Museum of Natural History, Graham Reynolds, also of the Department of Biology at the University of North Carolina Asheville, and Truong Quang Nguyen, also of the Institute of Ecology and Biological Resources and of the Graduate University of Science and Technology at the Vietnam Academy of Science and Technology, conducted several rapid inventory surveys in Bac Me District, which is in the southeastern portion of Ha Giang Province. During the course of the surveys, Miller et al. collected a single Xenodermid Snake matching the diagnosis of Achalinus. Subsequent comparisons of morphology and mitochondrial DNA sequence data with currently recognised Odd-scaled Snake species led Miller et al. to describe this specimen as representing a previously unknown species, in a paper published in the journal Copeia on 7 December 2020.

The new species is named Achalinus zugorum, in honour of George Zug and Patricia Zug. George is commemorated for his contributions to herpetology, especially within Southeast Asia, and for his mentorship to two of the authors (Aryeh Miller and Justin Lee) and many young scientists before them. Miller et al. also celebrate Patricia for her contributions to herpetology, as well as her ever endearing and compassionate spirit which continues to inspire the authors.

Achalinus zugorum differs from all other species of Achalinus by the following combination of morphological characteristics: dorsal scales elliptical; one dorsal scale directly above each ventral scale; absence of everted labial scales; preocular absent (fused with prefrontal or loreal scale); maxillary teeth 28, all teeth curved and equal in size; internasal suture distinctly longer than that between the prefrontal suture; internasals not fused to prefrontals; loreal fused with prefrontals; seven infralabials; mental very narrow, separated from anterior chin shields; two elongated anterior temporals, in contact with eye, and two posterior temporals; dorsal scales in 25–23–23 rows, keeled; ventrals 173; subcaudals 70, unpaired; a maximum known total length of 458 mm, Tail length/Total length ratio of 0.23; dorsum purple to jet black in life and in preservative, lower and posterior portions of head pink-gray, ventral surface iridescent and uniform black with margins of ventral scales pink-gray.

 
(A) Dorsal and (B) ventral views of the holotype of Achalinus zugorum, new species (IEBR 4698), after preservation. White bar is 10 mm. Miller et al. (2020).

The single known specimen is an adult male with a body moderately elongate and subcylindrical, head oblong and slightly distinct from neck dorsally covered with large head scales. Scales across dorsal portion of head distinctly striated; eyes small, round with vertically subelliptical pupils; nostrils large compared to nasal scale and elliptical. Tail elongate (slightly over one-fifth of total body length), tapering to round blunt tip. Rostral scale small, subpentagonal in frontal view, barely visible from above. Posterior scale suture of rostral with internasals ‘gull-wing’ shaped (broad obtuse angle). Mental scale much smaller and narrower than rostral, subrectangular. Internasals paired, rounded. Suture between internasals 1.4 times longer than prefrontal suture; prefrontals paired, subrectangular, 1.7 times wider than long. Frontal scale shield-shaped with weak crease along midline, 0.9 times longer than wide; anterior angle formed by suture of frontal bordering prefrontals straight (180°); posterior angle formed by the sutures producing the posterior vertex of the frontal a weak obtuse angle (100°). Supraoculars rectangular, 2.1 times longer than wide. Supraoculars shorter than frontal. Parietals paired, weakly subtrapezoidal, 2.5 times longer than wide. Parietal suture 2.0 times longer than frontal; anterior parietal angle formed by the sutures between the parietal plus frontal and the suture between the supraocular plus parietal moderately obtuse (112°) with the lateral ray of the angle pointing posterolaterally. Parietals bordered by one elongate nuchal (second row of posterior temporal) scale on each side; nuchals blocked from contacting at midline by one small scale, each scale in contact with first row of posterior temporals. Loreal scale fused with prefrontal scale; nasal scale divided below nostril, posterior portion of nasal larger than anterior. No preocular or postocular. Supralabials 6/6, first very small, contacting mental, afterwards gradually increasing in size. Supralabials 1–3 contacting nasal, 3–4 contacting fused loreal-prefrontal, 4–5 contacting orbit, 4th in narrow contact, 5th in broad contact, 6th supralabial largest, 2.6 times as long as 5th supralabial, broadly subrectangular. Infralabials 7/7, first pair in contact, blocking mental from contacting anterior pair of genials; infralabials 1–3 in contact with anterior pair of genials; 1st infralabial smallest, increasing in size until 6th infralabial, which is the longest; the 7th infralabial is significantly smaller than the 6th infralabial; both scales are elongate and contact the 6th supralabial, and is thus considered an infralabial based on this characteristic. Genial scales wider than long, subrectangular and asymmetrical. Posterior genials longer than anterior genials, right posterior genial divided into anterior and posterior scales.

 
(A), (B) Lateral, (C) dorsal, and (D) ventral views of the head of the holotype (IEBR 4698) of Achalinus zugorum, new species, after preservation. Each white bar is 5 mm. Miller et al. (2020).

Dorsal scale rows 25–23–23, all dorsal scales elliptical and distinctly keeled posterior to nape, outermost dorsal scale row slightly enlarged from innermost rows. Ventrals smooth, border with dorsal scales a broad obtuse angle. 173 ventrals with no preventrals; cloacal plate single; subcaudals 70, unpaired.

Maxillary teeth 28, anterior teeth equal in size, all curved. Mandibular and palatine teeth all equally sized and similar in shape to those of maxilla.

Hemipenes small, partially everted organ extending 5–6 subcaudal scales in length, retracted back to 2–3 subcaudal scales after preservation. Organ bilobed, semicapitate based on partial eversion; shape uniform but inflated on the sulcate side near point of lobular bifurcation. The sulcus spermaticus is forked, at centrifugal position, dividing at point of bifurcation and extending across the lobes towards the apex. Sulcus lips elevated, naked, creating large channel. The lobes of each hemipenis have not been fully prepared but are mostly naked except for a few small horizontal flounces; on the left organ, a few spinous calyces are present on the lobes; the base of the organ is somewhat flounced, without other ornamentation.

The colour pattern of the holotype in life was similar to the colouration after preservation. The dorsum is blackish and dark purple; interstitial skin between the dorsal scales dark gray; head same color as dorsum; underside of gular region dark brown, margins of labial scales dark brown; venter uniform jet black with the outer margins of each ventral scale dark gray, strong iridescence also present.

After formalin fixation and subsequent preservation in 70% ethanol for six months, dorsum uniform dark purple throughout entire body; dorsal portion of head same as dorsum, interstitial skin of dorsal and head scales violet-brown; medial portion of labial scales around mouth pinkish-gray; ventral region of snout dark purple, strongly iridescent; dark violet-gray along gular region; ventral ground color of body dark purple, margins of ventral scales pinkish-gray, also strongly iridescent.

The holotype of Achalinus zugorum was collected on a small gravel road running through Lùng Càng Village, Minh Ngọc Commune, Bac Me District, Ha Giang Province, Vietnam at an elevation of 228 meters above sea level. So far, the species is known only from the type locality and no specimens have been collected since its discovery. Nothing is known about the ecology, behavior, diet, or preferred microhabitat of this species, though it is presumably a semi-fossorial species that was drawn out by recent heavy rainfall prior to collection. The habitat surrounding its collection location consisted primarily of secondary forest with medium to small hardwoods on karst. The mean annual temperature in Ha Giang Province is 23.38°C, with a dry season typically extending from October to March and the rainy season lasting April until September.

 
(A) Map of all type localities for Odd-scaled Snakes, Achalinus, and (B) province-level map of Vietnam with type localities in that country. Black arrow indicates location of Ha Giang Province. All type localities of recognised Achalinus are included with the exception of that for Achalinus spinalis, which is geographically imprecise. Miller et al. (2020).

As only a single specimen of Achalinus zugorum is thus far known, it is impossible to infer demographic parameters. However, Ha Giang Province, like much of Vietnam, is hurtling towards an increasingly ecologically fragmented and destabilised community as deforestation resulting from logging, agricultural expansion, and residential development, as well as limestone quarrying, continue to threaten the regional biota. The surrounding lowland habitat beyond the secondary forest at the type and only known locality has been heavily deforested and converted for agricultural use, thus the immediate area is seriously threatened. However, it would be inappropriate to assert that this species is a microendemic occurring only at its type locality, as many species of Achalinus are known to occur across broader geographic areas, but their secretive habits make estimating population sizes and distributions exceedingly difficult.

Odd-scaled snakes appear vulnerable to desiccation; a likely consequence of their non-imbricate scutellation where more interstitial skin is exposed, thus habitat modification (such as agricultural activities) could force odd-scaled snakes to drier forest edge habitats (where Achalinus zugorum was encountered), which would represent a formidable threat to this group. Populations of Achalinus formosanus chigirai are in decline for this reason exactly. In 1929, Clifford Pope and Walter Granger stated upon collection of Achalinus spinalis in Fujian Province, China that the specimens were ‘extremely delicate’ and that it ‘dries and hardens in a most unusual way’, further signifying the importance of moist, humid forest habitats for this group.

Currently available data are inadequate to make a sound decision concerning the distribution, abundance, and population status of this species, thus Miller et al. are unable to assess extinction risk.Miller et al. therefore recommend classifying Achalinus zugorum as Data Deficient under the International Union for the Conservation of Nature's Red List of Threatened Species criteria. The Data Deficient categorisation is based on the paucity of data to make an appropriate classification in another Red List category, but with sufficient concern to suggest that the species is facing threats owing to development and habitat modification near the type locality.

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