Crocidura sapaensis, Jenkins, Paulina D., Abramov, Alexei V., Bannikova, Anna A. & Rozhnov, Viatcheslav V., 2013

Jenkins, Paulina D., Abramov, Alexei V., Bannikova, Anna A. & Rozhnov, Viatcheslav V., 2013, Bones and genes: resolution problems in three Vietnamese species of Crocidura (Mammalia, Soricomorpha, Soricidae) and the description of an additional new species, ZooKeys 313, pp. 61-79 : 63-71

Crocidura sapaensis sp. n.

Holotype.

ZIN 96433, genetic analysis code CVN108, BOLD Accession no. ABMIV114-08, field no. 132, male, body in ethanol, skull extracted, collected 25 May 2006 by A.V. Abramov.

Type locality.

Vicinity of Tram Ton Station of Hoang Lien National Park, north slope of Phansipan Mt. area, 6 km west of Sa Pa Town, Sa Pa District, Lao Cai Province, Vietnam, 22°21'N, 103°46'E, altitude 2200m above sea level.

Paratypes.

ZIN 96262, genetic analysis code CVN93, GenBank no. HM587005, BOLD no. ABMIV100-08, field no. 13, male, collected 8 December 2005; ZIN 96264, genetic analysis code CVN94, GenBank no. HM587006, BOLD no. ABMIV101-08, field no. 15, female, collected 8 December 2005; ZIN 96269, genetic analysis code CVN99, BOLD no. ABMIV106-08, field no. 32, male, collected 15 December 2005; ZIN 96271, genetic analysis code CVN101, BOLD no. ABMIV108-08, female, collected 16 December 2005; ZIN 96274, genetic analysis code CVN102, BOLD no. ABMIV109-08, field no. 45, male, collected 17 December 2005; ZIN 96275, genetic analysis code CVN103, BOLD no. ABMIV110-08, field no. 46, male, collected 17 December 2005; ZIN 96276, genetic analysis code CVN104, BOLD no. ABMIV111-08, field no. 66, female, collected 22 December 2005; ZIN 96432, genetic analysis code CVN107, BOLD no. ABIOW074-08, field no. 131, male, collected 25 May 2006; ZIN 96434, genetic analysis code CVN109, BOLD no. ABIOW075-08, field no. 133, male, collected 25 May 2006; ZIN 96436, genetic analysis code CVN111, BOLD no. ABMIV116-08, field no. 136, male, collected 28 May 2006; ZIN 96438, genetic analysis code CVN113, BOLD no. ABMIV117-08, field no. 138, female, collected 28 May 2006; ZIN 96439, genetic analysis code CVN114, BOLD no. ABMIV118-08, field no. 139, female, collected 28 May 2006; ZIN 96442, genetic analysis code CVN117, BOLD no. ABIOW069-08, field no. 144, male, collected 31 May 2006; ZIN 99779, field no. 24, male, collected 10 May 2010. All bodies in ethanol, skulls extracted, collected by A.V. Abramov and A.V. Shchinov from the same locality as the holotype, altitude 1930-2200m above sea level.

Other material. FMNH 39029 Chapa [Sa Pa], Lao Cai Province; BMNH 1925.1.1.24; BMNH 1925.1.1.27 Ngai Tio, Lao Cai Province, 22°36'N, 103°40'E.

Diagnosis.

A small shrew distinguished by the mitochondrial genes cytochrome b (cyt b) and cytochrome oxidase c subunit I (COI) and by the shape of the talonid of the third lower molar (m3).

Description.

Size small (see Table 1) with a moderately long tail relative to head and body length (62-84%). Dorsal pelage dark greyish brown; tail dark grey dorsally, slightly paler below (see Fig. 2). Skull with a rounded, short rostrum: moderately broad interorbital region; rounded, relatively deep braincase with subangular superior articular facets and lambdoid crests just evident laterally near the junction with the mastoid (see Fig. 3). The first upper incisor is slender with a relatively small posterior cusp, less than half the height of the first upper unicuspid; posterolingual border of upper premolar (P4) deep and rounded, in close contact with the anterolingual margin of M1 in occlusal view; last upper molar (M3) relatively narrow. Lower incisor with two distinct cusps on the occlusal surface in unworn dentition; posterolingual cuspid present on lower premolar (p4); talonid basin of m3 broad and deep with an entoconid ridge and low entoconid (see Fig. 4).

Comparison with other species.

Crocidura sapaensis averages larger than the very small species of Crocidura recorded from Vietnam. The condyloincisive length is greater than that of Crocidura guy , Crocidura annamitensis and Crocidura kegoensis , within the upper part of the range of Crocidura zaitsevi and the braincase is deeper than that of all four small species. Crocidura wuchihensis and Crocidura sapaensis are in the same size range. Crocidura sapaensis is smaller than or at the lower end of the size range of Crocidura indochinensis with a relatively shorter tail (see Table 1 and Fig. 5).

Crocidura sapaensis and Crocidura wuchihensis are distinguished by differences in cyt b sequences. Crocidura sapaensis differs from Crocidura zaitsevi and Crocidura indochinensis in the cyt b and COI gene sequences.

Differences in the shape of the talonid of m3 in northern Vietnamese populations serve to distinguish Crocidura sapaensis and Crocidura wuchihensis (see Fig. 4). In specimens of Crocidura sapaensis from northern Vietnam the talonid basin is broad and deep with an entoconid ridge and low entoconid, whereas in Crocidura wuchihensis the talonid basin is narrow. In Crocidura indochinensis the talonid basin is broad and deep with a hypoconid, entoconid and marked entoconid ridge (see Fig. 4).

Etymology.

The new species is named after Sa Pa, the capital of Sa Pa District in Lao Cai Province of northern Vietnam, with the Latin suffix - ensis (belonging to).

Natural history.

The series of type specimens was collected from a variety of habitats in the vicinity of Tram Ton Station of Hoang Lien National Park: mixed evergreen forest; forested banks of small streams; open grassy glades (Fig. 6); primary forest with large trees at an elevation 1930-2200m ( Abramov et al. 2008b). During 2005-2010 a total of 190 shrews was captured in this area, including 4 species ( Crocidura sapaensis , Blarinella griselda Thomas, 1912, Anourosorex squamipes Milne Edwards, 1872, and Episoriculus leucops ( Horsfield 1855)). Crocidura sapaensis was the most numerous species (90% of the total captures), followed by Anourosorex squamipes and Blarinella griselda (5.3% and 4.2% respectively), while only one Episoriculus leucops was captured ( Abramov et al. 2010). Crocidura sapaensis was more abundant in slightly disturbed mixed forest (2.2-3.0 specimens per 100 trap/nights), the occurrence in open glades, amongst shrubs on stream banks and in undisturbed primary forest was 0.3-2.6 specimens per 100 trap/nights. The proportion of males to females in Crocidura sapaensis was greater in all seasons; on average the male to female ratio is 2.3. Pregnant females were recorded from May to mid-July. Mean litter size in Crocidura sapaensis was 3.0 (2-4, n=15).

Distribution.

Confirmed specimens of Crocidura sapaensis are recorded from Lao Cai Province, Sa Pa District on the basis of cyt b analysis and morphology of m3. On the basis of morphology, specimens from the northern part of Lao Cai Province, Ngai Tio (elevation 1450m) and from the vicinity of Cat Cat Village near Sa Pa Town (elevation 1400-1450m) in relatively close geographical proximity also probably belong to the same species.

Populations of Crocidura wuchihensis identified on the basis of cyt b and those probably representing this species on the basis of morphology (from Pa Kha and Thai Nien, both in Lao Cai Province) all occur in northeastern Vietnam in localities to the east of the Song Hong (Red River). The observation that this river marks the border between the two species, with Crocidura wuchihensis to the east and Crocidura sapaensis to the west, was made by Bannikova et al. (2011), however this apparent biogeographical separation is based on few locality records. These authors also observed that, in the cyt b analysis, the two northern Vietnamese populations of Crocidura wuchihensis (from Mt Tay Con Linh II [22°46'N, 104°49'E] and Tam Dao [21°27'N, 105°38'E]) were separated by a p- distance of 2.1% suggesting that they probably represent distinct geographic populations.

The population of Crocidura wuchihensis recorded from Huong Son, Ha Tinh Province in the southern Annamites by Lunde et al. (2004) and Jenkins et al. (2009), does of course, occur west of the Song Hong and samples have not been included in any of the previous molecular studies. Specimens from Mt Tay Con Linh II are larger on average (CIL 15.7-17.1, mean 16.4) than those from Huong Son (CIL 15.8-16.4, mean 16.0). The Canonical Variate Analysis reported in Jenkins et al. (2009: Fig. 10) shows that these two groups respectively from northern Vietnam and the southern Annamites are moderately well separated from each other. In view of the problems outlined in this paper, lacking further evidence from molecular studies, it is impossible to predict if the population from Huong Son is correctly assigned to Crocidura wuchihensis , could belong to Crocidura sapaensis , or might indeed represent a further undescribed species.

Crocidura attenuata and Crocidura tanakae Characters separating Crocidura attenuata and Crocidura tanakae

The population from Mt Tay Con Linh II, Ha Giang Province in northern Vietnam recognised by molecular analysis of cyt b as Crocidura attenuata , falls within the size range of Crocidura tanakae and both species are morphologically very similar in appearance. The two species may be separated by the following characters. The basioccipital region in Crocidura attenuata is narrow and ridged particularly anterior to the position of the basioccipital suture, whereas in Crocidura tanakae the basioccipital region is broad and flat to concave (see Fig. 7). The palatal suture in Crocidura attenuata is a rounded to flat-topped ‘n’ shape, whereas in Crocidura tanakae the suture is a shallow to more marked ‘m’ shape (see Fig. 8). The two species also differ in the shape of the talon of the upper premolar (P4). In occlusal view, the talon of Crocidura attenuata is broader and more angular than that of Crocidura tanakae , the lingual border is straight to concave, with the posterior border shallowly indented so that the whole tooth looks larger in occlusal view. In Crocidura tanakae the lingual border of P4 is rounded and the posterior border of the tooth is deeply indented (see Fig. 8).

Geographical variation in Crocidura tanakae

Esselstyn and Oliveros (2010) did not provide detailed results about Vietnamese samples in the text of their analysis of Asian Crocidura tanakae , nevertheless they demonstrated apparent geographical variation in Vietnam. Their illustration of a statistical parsimony network of mitochondrial haplotypes ( Esselstyn and Oliveros 2010: Fig. 4) shows northeastern Vietnam samples from Tam Dao (21°27'N, 105°38'E) and Tuyen Quang (22°20'N, 105°25'E) grouped relatively closely, separated from each other by relatively few steps but separated by multiple steps from samples from the other two localities, Ha Tinh (18°21'N, 105°13'E) and Quang Nam (15°12'N, 108°02'E), which form a looser group. In their analysis of the COI gene, Bannikova et al. (2011) demonstrated the presence of two clearly defined haplogroups within Vietnamese Crocidura tanakae : Crocidura tanakae B restricted to the northern part of the country (Hoang Lien Mountains, Van Ban District) and Crocidura tanakae A which was more widespread in Central and South Vietnam (Huong Hoa, Phong Nha-Ke Bang, Ngoc Linh, Hon Ba and Bi Doup). The uncorrected p-distance between these two groups using the COI gene was about 2.5%.

Populations of Crocidura tanakae in Vietnam show a distinct clinal variation in skull size, populations at higher latitudes averaging smaller in size than those at lower latitudes (see Table 2). Although sample sizes are small, this observation is a possible example of the converse Bergmann’s rule where body size decreases with latitude.

Geographical variation in Crocidura attenuata

Abramov et al. (2012) demonstrated apparent geographical variation of Crocidura attenuata in southern China and northern Vietnam. Genetic differentiation of Crocidura attenuata is notable and reveals a phylogeographic structure with four haplogroups. The specimens from Cat Ba Island (Hai Phong Province, northeastern Vietnam) formed a single cluster closely related to the group of specimens from northern Vietnam (Ha Giang Province) and southeastern China (Guangxi Province). The genetic distance (p-distance) between specimens from Cat Ba / Ha Giang as well as Cat Ba / Guangxi is about 2.1%. The specimen of Crocidura attenuata from the more north-eastern region of China (Hunan Province) appears basal among all samples of Crocidura attenuata from China and Vietnam. Thus, the genetic distance between two specimens from China (Hunan / Guangxi) is 4.3%, which is nearly the same as the distance between Crocidura indochinensis and Crocidura sapaensis (see Bannikova et al. 2011).

Distribution

While Crocidura attenuata in Vietnam appears to occur only to the east of the Song Hong (Red River), in northeastern Vietnam ( Bannikova et al. 2011, Abramov et al. 2012), Crocidura tanakae does not appear to be so constrained and has been recorded on both sides of the river in northern Vietnam and also in central and southern Vietnam ( Esselstyn and Oliveros 2010, Bannikova et al. 2011, this study).