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A new species of mole of the genus Euroscaptor (Soricomorpha, Talpidae) from northern Vietnam

Shin-ichiro Kawada, Nguyen Truong Son, Dang Ngoc Can
DOI: http://dx.doi.org/10.1644/11-MAMM-A-296.1 839-850 First published online: 28 June 2012

Abstract

A new species of talpine mole from northern Vietnam is described and compared with other species of the genus Euroscaptor. This small mole was assigned to the genus Euroscaptor on the basis of its dental formula, but it also shows unique morphological and karyological characteristics. The new species is externally similar to E. parvidens from southern Vietnam, possessing warty protuberances on the muzzle not seen in other members of this genus. The tail of the new species is much shorter than in E. parvidens and E. malayana, both known to have short tails. The tail is not visible under the fur in the dorsal view, giving it an almost tailless appearance. The skull of the new species is similar to that of E. longirostris, but the palate is characteristically wider. The molars of the upper jaw are of a simple triangular shape, and there is no hypoconulid in the lower molars. The diploid number of the new species was determined to be 2n = 38, which is a new karyotype for this genus. This mole inhabits the lower elevational areas of northern Vietnam and is partially peripatric with E. longirostris in the type locality. Because of the distribution of another taxon in northern Vietnam, Mogera latouchei, the ecological relationships among 4 species of Vietnamese moles also is discussed.

Key words
  • Insectivora
  • karyotype
  • morphology
  • new species

Four genera of talpine moles are known from eastern Asia (Hutterer 2005). All genera possess unique dental characters, that is, considered to be primitive in the genus Euroscaptor (i 3/3, c 1/1, p 4/4, m 3/3, total 44) through the genus Parascaptor (i 3/3, c 1/1, p 3/4, m 3/3, total 42) to the genus Scaptochirus (i 3/3, c 1/1, p 3/3, m 3/3, total 40 [Stroganov 1948]). Another genus, Mogera, with dentition i 3/2, c 1/1, p 4/4, m 3/3, total 42, is considered to be of unique origin (Stroganov 1948). The genus Euroscaptor was 1st described by Miller (1940) with the type species Talpa klossi Thomas, 1924, originating in Thailand. Seven species of the genus Euroscaptor were subsequently recognized (Hutterer 2005; Kawada et al. 2008): E. grandis, E. klossi, E. longirostris, E. malayana, E. micrura, E. mizura, and E. parvidens.

Three talpine moles have been described from Vietnam (Can et al. 2008). Kawada et al. (2009) attributed these moles to the genera Euroscaptor and Mogera as follows: the longnosed mole, E. longirostris, in the northern highlands; the small-toothed mole, E. parvidens, in the southern Annamese mountains; and Latouche's mole, M. latouchei, from the northern lowlands. Two of the 3 species are geographically separated between the high and low mountain areas of northern Vietnam. In Sa Pa of Lao Cai Province, E. longirostris occupies the high mountain forest areas at 2,800 m above sea level, whereas M. latouchei occupies the relatively low-elevation mountain farm areas (Kawada et al. 2009). A similar separation of habitats is known in Cao Bang Province, with the boundary between these 2 species located around 800 m above sea level.

We recently undertook expeditions to the low-elevation mountain forest area near Tarn Dao National Park, located about 150 km north of Hanoi City. This area is a famous highland mountain resort, and the town of Tarn Dao is nestled on the southern slope of the mountain at an elevation of 1,000 m above sea level. This town also is known as the habitat of the mole E. longirostris (Kawada et al. 2009), and no other mole species were thought to be present in the lower area. However, a local guide informed us about a smaller species of mole in this area. Based on morphological and karyological studies, we determined that this small mole is distinct from any other known species of talpine mole. We also examined specimens at the Institute of Ecology and Biological Resources (IEBR), Vietnam Academy of Science and Technology, Hanoi, collected from a location somewhere between northern and middle Vietnam. The morphological characters of these specimens coincided with those of 6 small moles collected from the Tarn Dao area. In this paper, we describe this mole and identify it as a new species.

Materials and Methods

In 2006 we obtained information from Mr. Nguyen Huu Trung (a local guide living in the Hiep Hoa Commune) about a small mole found at the foot of Tarn Dao Mountain. According to Mr. Trung's information, the mole that inhabits the mountain forest at 200–300 m above sea level is much smaller than the mole found in the town of Tarn Dao (1,000 m above sea level). According to Mr. Trung, this mole could be collected using 4-cm-diameter handmade traps constructed from bamboo. With the assistance of Mr. Trung, we performed 2 field surveys in the forest near the Hiep Hoa Commune, Son Duong District, Tuyen Quang Province, Vietnam. These surveys were conducted in December 2007 and 2008. SK made 20 mole traps of polyvinyl chloride pipe attached to wire and spring that were set on the trails along the stream to capture individuals of this smaller mole species. Trapping was conducted in accordance with the guidelines approved by the American Society of Mammalogists (Sikes et al. 2011).

Materials.—Six moles (5 males and 1 female) were collected. Five of them underwent skin and skeletal preparation for use in the morphological studies. One male was fixed in ethanol and was therefore not used for the quantitative skull comparison. We also examined 3 fluid-preserved specimens of moles collected from Na Hang Nature Reserve, Tuyen Quang Province, and from Pu Huong Nature Reserve, Nghe An Province. These specimens were measured, and the skulls were removed for further study.

Morphological examination methods.—The collected moles were photographed, measured, and dissected to prepare skin and skeletal specimens. Measurements of the external morphology included body weight (BW), head and body length (HBL), tail length (TL), forefoot length (FFL), forefoot width (FFW), and hind-foot length (HFL). The short and long diameters of the testes in the male specimens and uterine activity in the female specimens also were recorded to determine their respective reproductive condition. Dental abbreviations used include incisor (i), canine (c), premolar (p), and molar (m). This new mole was assigned to the genus Euroscaptor on the basis of its dental formula (i 3/3, c 1/1, p 4/ 4, m 3/3, total 44) as defined by Dobson (1883), because this is a diagnostic character for Asian talpine moles, as previously discussed. Body measurements were subsequently compared with other individuals from the same genus and species. Quantitative morphological characters also were considered.

Fifteen skull characters were measured from the prepared skulls following Kawada et al. (2007) using a Mitsutoyo (Kawasaki, Kanagawa, Japan) digital caliper with an accuracy of 0.01 mm, and compared with 70 specimens of the other species in the genus. These measurements included the greatest length of the skull (GLS), palatal length from the anterior tip of the 1st incisor to the posterior lip of the palate (PL), inner length of the zygomatic arch (LZA), length of the upper toothrow (I1-M3), distance between the upper canine and 3rd molar (C-M3), length of the upper molars (M1-M3), rostral breadth of the canines (RB), breadth between the infraorbital foramina (BIOF), breadth across the upper 2nd molars (BAM), greatest interorbital breadth (IOB), mandible length (ML), mandible height at the coronoid process (MH), length of the lower toothrow (il-m3), distance between the lower 1st premolar and 3rd molar (pl-m3), and length of the lower molars (ml-m3). To evaluate the degree of cranial differentiation among the species, a principal component analysis was performed on the skull measurement data using SPSS for Windows (version 17.0; SPSS Inc., Chicago, Illinois). This analysis was performed using data from 7 species of Euroscaptor to identify the new species of mole from this genus. Males and females were combined in each analysis, because the sexual differences were slight in the Japanese moles (Abe 1967) and because some specimens deposited in the museums did not accompany the record of their sexes.

The postcranial skeletons of moles serve as important indicators for adaptation to living in an underground environment. Three of the collected moles were prepared as skeletal specimens. One fluid-preserved specimen was serially sectioned at 0.01-mm thicknesses by computed tomography using LaTheta Laboratory computed tomography (Aloka, Tokyo, Japan). Three-dimensional images were reconstructed from this series of computed tomography sections using Avizo 6.1 (Mercury Computer Systems Inc., Chelmsford, Massachusetts) and Rapidform 2006 (INUS Technology, Inc., Seoul, South Korea), so that postcranial characters could be assessed (data not shown).

Comparative specimens of the genus Euroscaptor were deposited in the mammal collections of SK (SIK) and at the following museums: the American Museum of Natural History (AMNH); the Natural History Museum, London (BMNH); the Institute of Ecology and Biological Resources, Hanoi (IEBR-M); the Kunming Institute of Zoology, Kunming (KIZ); le Musée National d'Histoire Naturelle, Paris (MNHN); the United States National Museum of Natural History, Washington, D.C. (USNM); and the National Museum of Nature and Science, Tokyo (NSMT-M).

Karyological study methods.—Tissue samples of these moles also were taken and preserved in a medium for karyological study and brought to Japan where they were cultured in the laboratory. Sampled tissues were minced and small amounts of the tissues were planted on culture flasks (Iwaki, Funsbashi, Chiba, Japan) and 6 ml of AmnioMaxII medium (Gibco, New York) was added. Half of the medium was replaced by the tissue once every 7 days. After 20 days, the cells were cultivated by trypsin solution supplemented by ethylenediaminetetraacetic acid (Gibco). Cells were treated with hypotonic solution (0.075 M KCl) for 18 min and then collected into a centrifugal tube by rinsing. Then tube was centrifuged and collected cells were fixed by a modified Calnoy solution. Chromosomal preparations were stained using the standard 4% Giemsa solution for conventional staining. Chromosomes were classified as metacentric (M), subtelocentric (ST), and acrocentric (A), as established by Levan et al. (1964).

Results

Euroscaptor subanura, new species Figs. 1 and 2

Fig. 1

—External morphology of the holotype of Euroscaptor subanura. a) Dorsal, b) ventral, and c) lateral view of total appearance. Magnified pictures of d) lateral, e) dorsal, and f) ventral muzzle show the many tubercular protuberances surrounding the nostrils. Eyes (g) are covered by transparent skin (d) and the upper naked pad is trapezoidal in shape (e).

Fig. 2

—Skull, mandible, teeth, and pelvis of holotype of Euroscaptor subanura. a) Dorsal, b) ventral, and c) left lateral views of cranium; d) left lateral view of mandible; e) occlusal and f) lingual views of left upper toothrow; g) occlusal and h) lingual views of right lower toothrow; and i) dorsal, j) ventral, and k) left lateral views of pelvis.

Holotype and type locality.—An adult male was collected on 12 December, 2008 by SK on the northwestern slope of Tam Dao Mountain (global positioning system: N21°37′52.9″, E105°27′24.0″, 250 m above sea level), near Vuoc Ly Village, Hiep Hoa Commune, Son Duong District, Tuyen Quang Province, Vietnam. The holotype includes a stuffed skin, cranium, mandible, and a nearly complete postcranial skeleton. The holotype specimen code is IEBR-M1798, and it has been deposited in the Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, Hanoi, Vietnam. The field number is SIK0882.

Paratypes.—Five paratypes consisting of 1 female (IEBR-M1799, field number SIK0883) and 4 males (IEBR-M1734 [SIK0875], IEBR-M1735 [SIK0876], IEBR-M1800 [SIK0884], and IEBR-M1801 [SIK0885]) were collected by the authors at the type locality. Paratypes IEBR-M1734, IEBR-M1735, IEBR-M1799, and IEBR-M1800 include skins, crania, mandibles, and nearly complete postcranial skeletons. One paratype (IEBR-M1801) is deposited as a fluid-preserved whole-body specimen.

Distribution and ecology.—Euroscaptor subanura is found in semideciduous forest of the low-elevation limestone mountains located in northern Vietnam (Fig. 3). Unlike other talpine moles, this species is not found in farms or grasslands around the forest. In addition to the type locality, this mole has been found in Na Hang Nature Reserve, Tuyen Quang Province, and Pu Huong Nature Reserve, Nghe An Province. The ecological requirements of this species are unknown, but are thought to be similar to those of other talpine moles, based on the experiences of the researchers during specimen collection. This species only constructs huge mounds, but many surface runnings are seen in the trails and specimens are easily collected there. The specimens collected in November–December at the type locality had undeveloped testes and uteri. However, the male specimens collected in January from Na Hang Nature Reserve had well-developed testes and penises. Female specimens did not display any fetuses or have placental scars; therefore, it is possible that the reproductive season may occur after January.

Fig. 3

—The distribution map of 4 species of Vietnamese moles, Euroscaptor subanura (closed diamonds), E. longirostris (triangles), E. parvidens (squares), and Mogera latouchei (stars).

Etymology.—The tail of this species is the shortest among known talpids. The species name subanura means almost no tail, in reference to the diagnostic characteristic.

Diagnostic characters.—Euroscaptor subanura is a small mole with a very long and slender body. The tail is quite shorthand not much of it is visible under the fur in the dorsal view. The lateral part of the nostrils contains many protuberances corresponding to vibrissae. The nose is slender, and the naked portion is trapezoidal in shape. The skull is typical, but a bit smaller than that of others. The anterolateral edge of the external acoustic pore projects forward. Protocones of the molars are anteriorly positioned, and hypoconulids are absent in the lower molars. The ribs are broad and closely spaced. The pelvis is short, especially the ischia. The diploid chromosome number is 2n = 38.

Description of the Holotype

External morphology.—The skin is dark brown on the dorsal side and silvery brown on the ventral side. Parts of the neck, forearm, and abdomen are stained dark orange by a secretion. The overall shape is similar to that of E. parvidens, because the holotype is small in size with a long trunk and extremely short tail (4.0 mm). The tail ratio is 3.2%, and the tail is almost not visible under the fur in the dorsal view, and is covered with a few scattered hairs 3–4 mm in length. When the hip hairs are pushed aside, the rounded tip of the tail can be seen.

The eyes are covered by thin transparent skin, and the surrounding area is hairless. The muzzle is long and slender, with the naked portion of the upper side posteriorly broadening into a trapezoidal shape, which is bordered by a rounded hairline in the back. In the ventral view, warty processes corresponding with whitish vibrissae are radially arranged and clearly visible. The arrangements of these processes are well identified as wrinkles. The periphery of the mouth also is hairless with only scattered vibrissae. The nostrils open anterolaterally, and the upper pad is rounded and protruding.

Skull.—The skull is smaller, shorter, and thicker than in E. longirostris and E. parvidens. The zygomatic arch originates postlaterally from the jugal bone and is curved at one-fourth of the length, causing it to be almost parallel on both sides. The center of the auditory bulla is swollen, and the anterolateral edge of the external acoustic pore projects forward. The infraorbital bridge is weakly developed, and is positioned above the paracone of M3. The edge of the palate is conspicuously constricted between P2 and P4. The palatal foramen is located in front of the protocone on each side of M1. The coronoid process is longitudinally thick. The lamina between the condylar and coronoid processes is well developed.

Teeth.—The I1 is the largest of the incisors, and projects forward. I2 is only slightly larger than I3, as compared to other species in which I2 is significantly larger. The incisor row has a triangular arrangement similar to that of E. longirostris, whereas it is rounded in E. parvidens.

The upper canines and all premolars have 2 roots. P1 is a lanceolate tooth without any clear subcusp. P2 and P3 are similar in shape, but the height of P2 is the lowest in the premolar row. The parastyle of P1 is more developed than in other Euroscaptor species. P2 is smaller than P1 and P3, which are small but almost equivalent in size. P4 has a well-developed protocone with an associated small tubercle located anteriorly to it. The parastyle of P4 is rudimentary.

The paracone heights of M1 and M2 are lower than the metacones, whereas in E. parvidens they are almost the same height, and in E. longirostris they are slightly lower than the metacone. In M3, the paracone and metacone are of equal height. The mesostyle of Ml to M3 is not divided as it is in E. parvidens. The metaconules of M1 and M2 are weakly developed and clearly distinguishable on the postprotocristae. The protocones of Ml to M3 are positioned forward of the line between the left and right paracones of each molar.

The i1 and i2 are almost the same size, whereas i3 is much smaller. The lower canine is narrower than in E. longirostris, and the crown does not broaden.

The p1 is about 1.5 times the height of the lower canine, whereas in other species it is twice the height of the canine. The anterior subcusp of p1 is unclear, whereas the posterior subcusp is conspicuous with a rounded constriction from the paracone. p2 and p3 lack clear mesial subcusps, but the distal subcusps are clearly visible. Crown heights are not greatly different, but are slightly higher in p3. p4 is developed and the line of the crowns of p2 and p3 are not linearly arranged with that of p4.

Lower molars lack a hypoconulid, but it exists in other talpids. Very small cusps (parastylid or mesiostylid) exist on the mesial sides of m2 and m3, but are much smaller than in related taxa. Protoconids are twice the height of the hypoconids, and are posteriorly positioned, resulting in narrower trigonids as compared with other species.

Postcranial skeleton.—Vertebral formula is 7 C, 13 T, 6 L, 6 S, 9 Ca, total 41, as is typical for the genus Euroscaptor (Yoshiyuki 1986). This species has a characteristically low number of tail vertebrae; the tail is very short. Each rib is very thick and they are closely arranged, with the proximal part of each rib strongly curved backward. Spinous and transverse processes of the lumbar vertebrae are weaker than those of other species.

The pelvic girdle is very short and slender, particularly the ischium. The posterior extreme of the ischium is not very wide, and is rather similar to the ischium of Parascaptor leucura. The ischium has a rounded lateral outline. One pair of sciatic foramina is present dorsally. About two-thirds of the total length of the pelvis consists of a fused area between the ilium-ischium and sacrum. The cranial articular processes of the sacrum are well developed.

The humerus is typical for talpine moles, but is more slender than in E. longirostris and shorter than in E. parvidens. The “scalopine ridge” is well defined, but not as distinct as in other species. The clavicle has a cube-shaped bone with a hole, which is a common character of Asian talpids.

Karyotype.—The male karyotype of E. subanura is shown in Fig. 4. The diploid number and autosomal fundamental number of E. subanura were determined to be 2n = 38 and NFa = 56, respectively. This is a new diploid number for Asian talpid species. The karyotype consisted of 14M + 6ST + 16A autosomes and sex chromosomes. The X chromosome was small and metacentric and Y the chromosome was made up of dot-shaped minute chromosomal bodies.

Fig. 4

—The conventional karyotype of male Euroscaptor subanura, paratype IEBR-M1735.

Variation.—Body weight ranged from 33.8 to 43.0 g. The tail length was notably short in all specimens, ranging from 4.0 mm to 5.0 mm. All type specimens had small skulls (30.60-31.39 mm). Most of the external and skeletal morphologies are coincident with those of the holotype. However, the P3 of paratype IEBR-M1735 possesses a clear protocone. The morphology of P4 also was variable among the specimens. The holotype has an accessory tubercle in front of the protocone that also is present in paratypes IEBR-M1799 and IEBR-M1800, but is absent in other paratypes. Paratypes IEBR-M1734 and IEBR-M1799 are older individuals, and therefore the dental characters are not prominent. The tail of IEBR-M1735 is composed of 8 bones, rather than the usual 9.

We compared 3 specimens from 2 locations outside of the type locality, Na Hang Nature Reserve and Pu Huong Nature Reserve; all specimens had the same external, skull, dental, and postcranial characteristics. The male skulls from Na Hang Nature Reserve (n = 2) measured 30.79 and 32.03 mm, and the female skull from Pu Huong Nature Reserve (n = 1) measured 31.61 mm. Thus, the 3 specimens that we compared were relatively larger than the type specimens. The size of female skulls overlapped the range in size of males; therefore, sexual size variation was not prominent.

Comparison of Euroscaptor subanura with Other Species of the Genus

Descriptive comparison of species.—The body of E. subanura was, on average, the smallest of the continental Asian Euroscaptor species, with the exception of the 1 Japanese species, E. mizura, which was much smaller (Table 1). This Japanese E. mizura had characters quite distinct from the continental species of Euroscaptor, and was therefore excluded from further examination.

View this table:
Table 1

Comparison of external measurements among 6 species of the genus Euroscaptor previously collected by SK.

Measurementsa
SpeciesBWHBLTLFFLFFWHFLTR (%)
Euroscaptor subanura (n = 8)b
̄38.97122.884.3814.7514.3814.003.6
Range33.8–13.0113.0–130.04.0-5.014.0–15.513.0–15.513.5–15.5
SD3.685.510.440.460.740.38
Euroscaptor parvidens (n = 10)
̄52.98143.756.9515.3015.4014.604.8
Range37.3–63.5135.0–148.55.5–9.014.5–16.515.0-16.513.5–15.5
SD7.283.751.090.630.610.66
Euroscaptor longirostris (n = 19)
̄59.62138.4515.3716.2615.9515.5511.1
Range42.3–76.7133.0–144.014.0–17.015.0–17.514.5–17.014.5–16.5
SD10.183.391.010.770.710.50
Euroscaptor malayana (n = 9)
̄57.36131.155.7015.8016.4015.504.4
Range43.6–71.5128.5–134.54.5–8.515.0–16.515.5 –17.014.5–16.5
SD7.721.941.090.420.570.62
Euroscaptor klossi (n = 2) ̄51.65132.7510.0016.2516.0015.007.5
Range47.8–55.5130.0–135.59.5–10.516.0–16.516.015.0
SD5.443.890.710.350.000.00
Euroscaptor mizura (n = 1)28.6102.02214.51414.521.6
  • a BW, body weight (g); HBL, head and body length (mm); TL, tail length (mm); FFL, forefoot length (mm); FFW, forefoot width (mm); HFL, hind-foot length (mm); TR; tail ratio (%).

  • b Six individuals were measured for body weight.

The size range of E. subanura overlapped with some of the small individuals of E. parvidens and E. longirostris in our comparison (Table 1). Body shape was similar to that of E. parvidens, with a slender body and a very large hip (Fig. 1, and also see figures 4 and 5 of Kawada et al. [2009] for E. longirostris and E. parvidens, respectively). Many warty protuberances (Figs. 1d1f) also were seen in E. parvidens, but not as clearly as in other Euroscaptor species. Forefeet and hind feet were similar in size to those of E. parvidens, and smaller than in E. longirostris, E. malayana, and E. klossi. The tail was the shortest among known talpid species (4–5 mm). Short tails are a common character of E. micrura, E. malayana, and E. parvidens, but the tail of this new species consisted only of a small protuberance originating from the body. Other species had tails with long hairs visible beyond the body fur in the dorsal view (Kawada et al. 2009).

Fig. 5

—Dorsal, ventral, and lateral views of cranium, lateral view of mandible, and pelvis (from top to bottom) of a) Euroscaptor longirostris (IEBR-M1469), b) E. parvidens (IEBR-M1356), and c) E. subanura (holotype). The bar indicates 10 mm.

The GLS of E. subanura overlapped with those of 2 other Vietnamese Euroscaptor species (Table 2). A larger species, E. longirostris, showed a broad range of skull sizes, but 2 of the specimens fit within the size range of E. subanura. Small specimens of E. parvidens also were included in the same size range, but in general E. subanura was smaller than the other species. The mean GLS value in E. subanura was 31.12 mm (range 30.60-32.03 mm, n = 8), which is distinctive from E. longirostris (33.23 mm; range 31.19–34.50 mm, n = 27), and E. parvidens (32.32 mm; range 30.39–34.10 mm, n = 19). One specimen of E. parvidens had a smaller GLS than the range of E. subanura, but the body size of this specimen was within the range of E. subanura. Thus, E. subanura has a relatively larger skull for its body size than does E. parvidens.

View this table:
Table 2

Comparison of skull measurements among 7 species of the genus Euroscaptor. See text for character abbreviations.

SpeciesGLSPLLZAI1–M3C-M3M1–M3RBBIOFBAMIOBMLMHi1–m3p1–m3m1–m3
Euroscaptor subanura (n = 8)
̄31.1211.817.5712.1910.754.974.145.597.486.9419.745.9711.549.475.28
Range30.60–32.0311.12–12.287.05–7.9611.86–12.6210.36–11.344.79–5.233.92–4.405.40–5.787.15–7.866.69–7.3619.06–20.405.70–6.2111.19–11.949.16–9.845.05-5.41
SD0.500.440.300.280.280.130.160.140.200.200.490.170.250.230.12
Euroscaptor parvidens (n = 19)
̄32.3111.978.3111.8210.264.544.225.827.366.8320.145.9511.148.974.78
Range30.39–34.1010.94–12.937.40–9.1611.07–12.699.59–11.084.07–5.223.81–4.445.34–6.356.64–7.795.39–7.1418.46–21.245.44–6.3410.27–11.908.35–9.524.47–5.23
SD0.750.400.550.340.290.300.170.220.290.380.610.270.340.240.22
Euroscaptor longirostris (n = 27)
̄33.2313.028.2813.1111.495.264.135.867.727.2521.106.4012.3710.165.63
Range31.19–34.5012.13–13.886.94–9.2212.26–13.7710.76–11.994.90–5.763.45–4.545.53–6.326.68–8.216.79–7.7719.45–22.035.68–6.9111.50–13.049.52–10.645.25–6.29
SD0.970.450.620.410.340.230.300.200.380.210.830.300.360.250.25
Euroscaptor grandis (n = 4)
̄36.2314.339.3714.6512.956.305.166.979.337.8623.377.1013.8411.396.79
Range35.63–37.1014.00–14.598.95–10.1214.52–14.7512.66–13.136.11–6.475.02–5.286.32–7.239.20–9.577.50–8.0623.02–23.876.99–7.2313.66–14.0811.23–11.586.65–6.93
SD0.620.250.510.110.220.150.110.430.170.250.390.120.170.140.15
Euroscaptor malayana (n = 9)
̄31.3512.348.0712.6711.035.664.286.308.347.3420.056.3511.899.635.93
Range30.54–32.4712.07–12.797.66–8.4712.31–13.0310.68–11.335.40– 5.774.07–4.456.03–6.587.94–8.627.01–7.7319.65–20.736.06– 6.5811.48–12.129.38–9.875.67–6.09
SD0.620.260.290.210.200.120.130.200.260.230.350.160.200.160.12
Euroscaptor klossi (n = 2)
̄32.4812.688.4913.1811.695.944.416.348.207.0520.906.5312.2910.226.23
Range31.54–33.4112.35–13.008.02–8.9613.08–13.2711.64–11.735.80–6.074.23–4.586.30–6.388.05–8.356.65–7.4520.40–21.406.50–6.5612.27–12.3010.10–10.346.11–6.34
SD1.320.460.660.130.060.190.250.060.210.570.710.040.020.170.16
Euroscaptor micrura (n = 9)
̄33.7112.838.4313.1511.545.814.736.578.477.8821.616.4212.409.986.24
Range32.91–34.6112.42–13.387.87–8.9412.84–13.4711.19–11.905.42–6.084.44–5.076.33–6.878.20–8.897.54–8.1920.94–22.145.85–6.8112.05–12.759.67–10.316.10–6.38
SD0.560.290.360.210.230.220.190.180.220.230.440.290.250.240.09

Palate shape also was comparatively examined. Some western species of Euroscaptor have a broad and short palate, whereas the palate of E. subanura is long, similar to that of E. longirostris and E. parvidens. Of these species, E. subanura has the most slender rostrum and widest palate, with the edge of the palate showing a good curve in the position of P4 (Figs. 2a and 5). The palatal foramen is located forward of the line of the protocone on each side of M1, but is on the line in E. longirostris and posterior to the line in E. parvidens.

The anterolateral part of the auditory bulla in E. subanura protrudes forward (Fig. 2b). This is another diagnostic character, because the auditory bullae in other Euroscaptor species are rounded (Fig. 5).

The tip arrangement of the lower premolars is a good marker for grouping within the genus Euroscaptor. Kawada et al. (2009) observed that in most species, other than E. longirostris and E. parvidens, there is a high gradation between the tips of p2 to p3 and that of p4. In E. subanura this gradation was unclear (Fig. 2g), and E. subanura was morphologically more similar to the western Euroscaptor species (Fig. 5). This character is related to the degree of the development of p3, assigning a middle state between western and eastern groups of Euroscaptor. The parastyle of p4 was of similar size in E. subanura and E. longirostris, but larger than in E. parvidens.

Most of the species in this genus have a deviated mesostyle in the upper molars. A simple mesostyle was observed in this new species and in E. parvidens, although this was not apparent in older individuals. The protocone position in the upper molars was similar among most species of Euroscaptor, Talpa, and Mogera, and is considered the typical morphology. However, in E. parvidens this cusp was located toward the middle of each molar, forming an isosceles triangle,. Furthermore, the western species E. klossi and E. malayana had a well-developed metaconule on their molars, giving the overall appearance of a trapezoid. In contrast, a simple right triangular shape was typical of the new species (Fig. 2f) and E. longirostris.

The cusp arrangement of the lower molars is of great diagnostic value. The molars of known talpid species have 5 main cusps with 2 accessory cusps on both longitudinal sides. In E. subanura, a posterior accessory cusp, considered a hypoconulid, was absent, showing a distinct short diastema between the molars (Fig. 5). In addition, the anterior accessory cusp (possibly the parastylid) was not well developed. The lower molars of this species are very simple in shape, comparative with simple tribosphenic molars. The height difference between the protoconid and hypoconid is also a unique character for this species, because in most Euroscaptor species the development of these cusps is almost equivalent.

Figure 6 shows the arrangements of the ribs in 3 Vietnamese species. Each rib of E. subanura was considerably thicker than other 2 species and closely arranged without the spaces obvious in E. longirostris and E. parvidens, showing “armorlike” appearance. The tail vertebral count was 8 or 9 in the new species, and 12–14 in the others. Transverse processes were observed on the 1st and 2nd caudals, but in other species the 4th caudal vertebra had well-developed transverse processes. This character is prominent in E. parvidens, in addition to the short tail. The pelvic structure of the genus Euroscaptor is characterized by the possession of a single sciatic foramen (Fig. 2i); the so-called caecoid type. The new species possesses this characteristic along with a short and slender pelvic shape, whereas E. longirostris, E. parvidens, and E. klossi have long and wide ilia. The pelvic girdle of E. malayana is comparatively short, but the ischium is very thick and a secondary sciatic foramen has almost developed. The fusion between the ilium-ischium and sacral bones of E. subanura is long relative to the total length of the pelvis (Fig. 5, bottom).

Figure 6

—Left lateral view of anterior postcranial skeletons of a) Euroscaptor longirostris (IEBR-M1467), b) E. parvidens (IEBR-M1346), and c) E. subanura (holotype). The bar indicates 10 mm.

Numerical comparison of species.—Euroscaptor can be separated into 2 groups in scatter plots derived from molar size and palate shape (Fig. 7). One is the western group including E. grandis, E. klossi, E. malayana, and E. micrura, which is characterized by a wide palate coincident with the development of large rectangular molars. The other is the eastern group including E. longirostris, E. parvidens, and the new species described herein, which shows a slender palate and typically small triangular molars.

Fig. 7

—Two-dimensional plots of the breadth across the molar and the length of upper molar to the greatest length of skull in 7 species of genus Euroscaptor. Closed diamonds, E. subanura; squares, E. parvidens; triangles, E. longirostris; crosses, E. grandis; asterisks, E. malayana; closed circles, E. klossi; and pluses, E. micrura. These 7 species can be divided to western and eastern groups.

To elucidate the differences among the 3 species of the genus Euroscaptor, a principal component analysis was performed for the 7 continental Asian species. Table 3 shows the results of the analysis based on 15 skull measurements. The cumulative eigenvalue for principal components 1–3 (PC1–PC3) was 90.9%, accounting for most of the variation in the sample. Eigenvalues of PC1–PC3 were >1, and these were therefore examined for the analysis. Factor loading was positive for all measurements in PCI, indicating size variation in these 7 species. However, PC2 and PC3 showed high loading for the palate width (RB and BIOF) and zygomatic length parameters, respectively. In contrast, molar size was negatively loaded in PC3. According to these factor loadings, Euroscaptor species were mostly separated from each other by the PC scores, but with some degree of overlap. The eastern species of Euroscaptor tended to have high PC values, whereas the known Vietnamese Euroscaptor species could be diagnosed by the low PC scores in this plot (Fig. 8; square: E. parvidens, and triangle: E. longirostris). Interestingly, the position of E. subanura in the scatter plot of PC2 and PC3 was separated from the other 2 Vietnamese species based on a relatively low value of PC3, corresponding to the development of molar rows.

View this table:
Table 3

Eigenvectors of the first 3 principal components axes based on cranial characters. See text for character abbreviations.

PC1PC2PC3
GLS0.8420.1270.469
PL0.909−0.1920.270
LZA0.6530.4120.496
I1-M30.957−0.2580.034
C-M30.933−0.302−0.017
M1-M30.853−0.148−0.386
RB0.7210.605−0.054
BIOF0.7650.430−0.357
BAM0.8470.297−0.312
IOB0.8130.143−0.258
ML0.9180.1000.342
MH0.881−0.0640.072
i1–m30.951−0.2760.044
p1–m30.910−0.3680.042
m1–m30.884−0.134−0.365
Eigenvalue11.0911.3051.243
Cumulative73.94082.64090.925

Karyological comparison of species.—The diploid numbers of E. klossi, E. malayana, E. mizura, and E. parvidens are 2n = 36, with some variation among the species. In addition, the karyotype of E. longirostris from northern Vietnam is comprised of a 34 chromosomal complement. Therefore, the diploid number of E. subanura (2n = 38) is distinct from that of other Euroscaptor species.

Fig. 8

—Scatter plots of the factors in the result of principal component analysis. Symbols indicate respective species described in Fig. 7.

Discussion

Euroscaptor subanura is characterized by a mosaic of features similar to the external morphology of E. parvidens and the skull of E. longirostris. The external morphology of E. subanura is characterized by an extremely short tail (about 4–5 mm long), which visually resembles a wart. A short tail also is an etymological character of E. micrura, but its tail is longer (3/16 inches = 7.6 mm) than that of E. subanura (Jerdon 1874). Blyth (1843) described another species of short-tailed mole, Talpa criptura, but no descriptive text and measurements were presented. Later, Blyth (1850) noted that this “tail-less mole” was collected from Darjiling, eastern India, and that it showed no perceptible difference in the skulls and dentition from E. micrura. Therefore, we consider that E. subanura also is a different species from T. criptura. Kawada et al. (2003, 2008) reported that the Malaysian mole (referred to as E. micrura in 2003, but later renamed as E. malayana in 2008) had a short tail, but its tail length ranges between 5 and 9 mm. Although a short tail (5.5–9.0 mm) also is diagnostic for E. parvidens (Kawada et al. 2009), the tail of E. subanura is much shorter (4.0–5.0 mm). One character shared by E. parvidens and E. subanura is the rump structure, because these species have large rumps extending behind, and most of the tail vertebrae are enclosed within the hips. This character is only shared by these 2 species among known moles, suggesting a close genetic relationship. However, the differences of skeletal and dental characters mentioned above envisage clear distinction between these species. We consider E. subanura to be an endemic relative of the southern Vietnamese species, E. parvidens. Known distributions of these 2 species are presumably separated in the middle of Vietnam (Fig. 3), as evidenced by the occurrence of E. parvidens in Kon Turn and Quang Nam provinces (Abramov et al. 2006; Kawada et al. 2009). These 2 species are likely separate due to as of yet undetermined geographic or genetic factors, or both, and this hypothesis needs to be confirmed by future phylogenetic studies using molecular markers.

The dental morphology of the lower molars of the new species is unique among talpid moles because they lack a small cusp that is present in most talpids; therefore, the lower molars of E. subanura are simplified. Well-documented tooth characters of Euroscaptor show some differences among the species. For example, the arrangement of the lower premolars in the new taxon is similar to that seen in the western Euroscaptor species, E. micrura, E. malayana, and E. klossi, whereas molar shape is triangular as it is in E. longirostris and E. parvidens. In E. subanura the protocone is located in the mesial position; thus, the overall shape resembles a right triangle, as seen in E. longirostris. This shape is different from E. parvidens, which has almost isosceles triangle-like molars with the protocone positioned evenly between the 2 main cusps. Another western Euroscaptor, E. klossi, Emalayana, and E. micrura, has the molar protocone located in the mesial position with a hypoconule developed distal to it, resulting in a trapezoidal shape (Kawada et al. 2008).

Postcranial skeletal characters of E. subanura are quite unique. The ribs of this species are very thick and closely arranged, almost armorlike (Fig. 6). This armorlike morphology is only seen in this species among talpids, and was confirmed in specimens collected from 2 separate localities. The pelvic structure also is distinct from that of other Euroscaptor species (Fig. 5). The pelvis of E. subanura is very short, especially in the caudal part, and the ischia are almost parallel to each other. These 2 postcranial characters have been neglected in previous studies of the genus Euroscaptor, despite pelvic characters being considered as good diagnostic characters in the European genus Talpa (Grulich 1982; Stroganov 1948). In addition, Asian talpine moles have caecoid-type and mogeroid-type pelves as determined by the development of the ossification between the sacrum and the ischia; therefore, pelvic morphology is reflective of the taxonomic position of Asian mole species. Most species of Euroscaptor have caecoid-type pelves, which are considered to be the ancestral type of pelvic structure (Stroganov 1948). The Japanese mole E. mizura has a completely mogeroid-type pelvis (Abe et al. 1991), and in E. malayana the ischia and sacral bones have nearly fused (Kawada et al. 2008). The benefit or purpose of this bone fusion is unknown. Nonetheless, pelvic characters are thought to reflect the adaptive grade of moles to a fossorial lifestyle and are considered an important factor for identifying Asian mole species.

The known distribution of E. subanura is scattered around northern Vietnam. All localities are relatively low-elevation mountains surrounded by plains areas. In the type locality of the Tarn Dao area, this species is distributed between 200 and 300 m above sea level and another species, E. longirostris, occurs at a higher elevation (about 1,000 m above sea level). The higher habitat of moles in the Tarn Dao area includes farms and townships (Kawada et al. 2009), but there is no record of E. subanura from such habitats. Therefore, we consider E. subanura to be adapted to the lowland forests of northern Vietnam.

The southern limit of this species' range is possibly bounded by Nghe An Province, because the more southern area is occupied by E. parvidens, which lives in a very similar low, mountainous, broad-leaved forest habitat. We estimate that the range limit of these 2 species is located between Nghe An and Quang Nam provinces. The northern limit is unclear, but another mole genus, M. latouchei, is known from the low mountains in Cao Bang and Lao Cai provinces (Kawada et al. 2009). Because 2 mole taxa sharing a similar niche rarely coexist in the same area (Abe 1967), we presume that the northern limit of E. subanura is the present known location in Na Hang Nature Reserve, Tuyen Quang Province (Fig. 3). Within the Japanese genus Mogera, the nature of the border between 2 species can be very complicated and is affected by geological and spatial factors (Abe 1967). A similarly complex distribution pattern also is known for Taiwanese species (Kawada et al. 2007). Therefore, it is important to know the exact distribution of these 2 lowland species to elucidate the phylogeography of Vietnamese moles.

The genus Mogera is thought to be derived from Euroscaptor species based on the dental formula (Abe 1967; Stroganov 1948), as well as recent molecular phylogenetic studies (Shinohara et al. 2003, 2004). Within the context of this hypothesis, E. subanura may have been displaced from its northernmost habitat by the derived and highly developed M. latouchei. Another relic species, E. longirostris, occupies the higher elevations and might possibly be the oldest species inhabiting northern Vietnam. The similar external morphology of E. subanura and E. parvidens sheds some light on the relationship between these species. Presumably these 2 species share their most recent common ancestor within the genus Euroscaptor, which occupied the areas presently inhabited by E. subanura in the north and E. parvidens in the south. E. parvidens is characterized by small, specialized molars, as indicated by the species name, and therefore E. subanura is considered an ancestral species to E. parvidens. Within the evolutionary context of the Asian talpine species, it is also noteworthy that the habitats of the 2 Euroscaptor species in northern Vietnam are segregated by elevation.

Acknowledgments

Authors are grateful to N. Huu Trung for his information about this small mole inhabiting the type locality and his guidance in the field. We thank the Director of IEBR L. Xuan Canh, N. Xuan Dang, H. Endo of Tokyo University, and T. Oshida of Obihiro Agricultural University for their encouragement to conduct the field surveys in northern Vietnam. N. Thien Tao of Vietnam National Museum of Nature presented us a mole collected in Nghe An Province. We are grateful to P. Jenkins and D. Hill of the Natural History Museum, J. Spence of the American Museum of Natural History, Y. Wang of the Kunming Institute of Zoology, C. Callou of Le Muséum National d'Historire Naturelle, and M. D. Carleton of the National Museum of Natural History for kindly permitting SK to examine the specimens that were deposited within each of these museums. O. Hoson of National Museum of Nature and Science supplied the computed tomography images of 1 paratype specimen. We also appreciate N. Kurihara for her useful comments for the species recognition of the moles. This study was partially supported by National Foundation for Science and Technology Development (23501232) from Vietnam, (NAFOSTED):106:12-2011.06, and Grant-in-Aids for Scientific Research 21370033 and the Ministry of Education, Culture, Sports, Science and Technology of Japan.

Appendix I

Specimens compared in this study. Euroscaptor parvidens (n = 19).—MNHN1959-1794, MNHN1959-1795, USNM258342, USNM320530, USNM320532, IEBR-M1344, *1EBR-M1345, IEBR-M1346, IEBR-M1347, IEBR-M1348, IEBR-M1349, IEBR-M1350, IEBR-M1351, IEBR-M1352, IEBR-M1353, IEBR-M1354, IEBR-M1355, IEBR-M1356, IEBR-M1357, IEBR-M1358.

Euroscaptor longirostris (n = 27).—MNHN1870-19bis, BMNH 11.2.1.24, USNM253319, AMNH110505, AMNH110506, AMNH110508, AMNH110507, BMNH33.4.1.148, IEBR-M573, IEBR-M574, IEBR-M575, IEBR-M576, IEBR-M577, IEBR-M578, IEBR-M579, IEBR-M580, IEBR-M581, IEBR-M582, IEBR-M583, IEBR-M584, IEBR-M585, IEBR-M1066, IEBR-M1067, IEBR-M1068, IEBR-M1467, IEBR-M1468, IEBR-M1469, IEBR-M1470.

Euroscaptor grandis (n = 4).— KIZ2, KIZ438, KIZ432, KIZ547.

Euroscaptor malayana (n = 11).—BMNH62.712, NSMT-M34738, NSMT-M34739, NSMT-M34740, NSMT-M34741, NSMT-M34742, NSMT-M34743, NSMT-M34744, NSMT-M34745, SIK0556, SIK0558.

Euroscaptor klossi (n = 3).—BMNH28.5.3.1, NSMT-M34363, NSMT-M 34364.

Euroscaptor micrura (n = 9).—BMNH16.3.25.42, BMNH16.3.25.40, BMNH15.9.1.4.5, BMNHNo.196, BMNH16.3.25.45, BMNH16.3.25.41, BMNH16.3.25.39, BMNH16.3.25.46, BMNH16.3.25.36.

Euroscaptor mizura.—SIK0538.

Footnotes

  • Associate Editor was Ryan W. Norris.

Literature Cited

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