crocidura sapaensis 2013

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Bones and genes: resolution problems in three Vietnamese species ofCrocidura... 61

Bons and gns: rsouon probms n rVnams spcs ofCrocidura (Mammaa,Sorcomorpa, Sorcda) and dscrpon

of an addona nw spcs

Paulina D. Jenkins1, , Alexei V. Abramov2,5, ,Anna A. Bannikova3,, Viatcheslav V. Rozhnov4,5,|

1 Te Natural History Museum, Cromwell Road, London SW7 5BD, UK2 Zoological Institute, Russian Aca-

demy of Sciences, Universitetskaya nab., 1, Saint-Petersburg 199034, Russia3 Lomonosov Moscow State Uni-

versity, Vorobievy Gory, Moscow 119992, Russia4 A.N. Severtsov Institute of Ecology and Evolution, Russian

Academy of Sciences, Leninskii pr., 33, Moscow 119071, Russia5 Joint Vietnam-Russian ropical Research

and echnological Centre, Nguyen Van Huyen, Nghia Do, Cau Giay, Hanoi, Vietnam

urn:lsid:zoobank.org:author:87BF61B6-2D07-441F-ABB0-DB3BD20DDCB7

urn:lsid:zoobank.org:author:7B8F6D34-8E6F-4A7E-9044-A45AA8FAD644

urn:lsid:zoobank.org:author:93950AB1-14C9-4CF8-999D-0E8789D6BD46

| urn:lsid:zoobank.org:author:A3281721-063F-4513-8671-36E5F3D87F34

Corresponding author:Paulina D. Jenkins([email protected])

Academic editor:K. M. Helgen | Received 4 February 2013 | Accepted 20 June 2013 | Published 2 July 2013

urn:lsid:zoobank.org:pub:313A5DC5-B59C-476C-89C3-AED22353FA59

Caon: Jenkins PD, Abramov AV, Bannikova AA, Rozhnov VV (2013) Bones and genes: resolution problems in three

Vietnamese species oCrocidura(Mammalia, Soricomorpha, Soricidae) and the description o an additional new species.

ZooKeys 313: 6179. doi: 10.3897/zookeys.313.4823

Absrac

Recent investigations o Southeast Asian white toothed shrews belonging to the genus Crocidura have

revealed discrepancies between the results o morphological and molecular studies. Te ollowing study

concerns three species oCrociduraoccurring in Vietnam, namelyC. attenuata, C. tanakaeand C. wuchi-

hensis, and an undescribed ourth species revealed by molecular analysis. For many years Crocidura at-

tenuatahas been known to occur in Vietnam but, until very recently, the morphologically similar and

comparably sized C. tanakaewas believed to be restricted to aiwan. Following several molecular studies

over the last ew years, this species is now believed to be considerably more widespread and recognised as

occuring also in Vietnam. Te results o one o these recent molecular studies also revealed the presence

ZooKeys 313: 6179 (2013)

doi: 10.3897/zookeys.313.4823

www.zookeys.org

Copyright Paulina D. Jenkins et al. This is an open access article distributed under the terms of the Creative Commons Attribution License 3.0

(CC-BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Paulina D. Jenkins et al. / ZooKeys 313: 6179 (2013)62

o an undescribed species oCrocidura, similar in size and morphology to Crocidura wuchihensis, which is

herein described. Data are provided on geographical variation in Vietnam and the problems o dening

morphologically similar yet molecularly disparate species are discussed.

KeywordsCrocidura, new species, morphology, molecular analysis, geographical variation

inroducon

From the late 1990s there have been several intensive surveys o the small mammal auna invarious localities in Vietnam, resulting in the discovery o a number o species new to sci-ence. Beore that time only three species oCrocidurahad been recorded rom Vietnam: C.attenuataMilne Edwards, 1872, C. fuliginosa(Blyth, 1855) and C. indochinensisRobinson& Kloss, 1922 (Van Peenen et al. 1969, Heaney and imm 1983). Lunde et al. (2003)recorded the occurrence o a ourth species, C. wuchihensisShaw, Wang, Lu & Chang 1966in northern Vietnam. Tis was ollowed by a spate o descriptions o new species oCroci-durabased entirely on morphology: C. kegoensisLunde, Musser & Ziegler, 2004; C. sokolovi

Jenkins, Abramov, Rozhnov & Makarova, 2007; C. zaitseviJenkins, Abramov, Rozhnov& Makarova, 2007; C. annamitensisJenkins, Lunde & Moncrie, 2009; C. guyJenkins,Lunde & Moncrie, 2009; C. phuquocensisAbramov, Jenkins, Rozhnov & Kalinin, 2008a;C. phanluongiJenkins, Abramov, Rozhnov & Olsson, 2010.

Molecular studies were also being carried out during this period. Signicant studiesincluded those o Ohdachi et al. (2006) investigating the mitochondrial cytochrome bgene sequences o Soricidae; Esselstyn et al. (2009), Esselstyn and Brown (2009) andEsselstyn and Oliveros (2010) studying mitochondrial and nuclear genes oCrocidura.Tese were broad based studies covering wide geographical regions o Southeast Asia,Indonesia and the Philippines but some samples o Vietnamese Crocidurawere includedin their analyses. Bannikova et al. (2011) studied two mitochondrial genes, cytochromeb (cytb) and cytochrome coxidase subunit I gene (COI), o Vietnamese Crociduracol-lected at various localities ranging rom the north to the south o the country.

While the molecular studies o Vietnamese material conrmed some o the resultso the contemporaneous morphological studies, a number o anomalies were equallyrevealed, indicating the presence o several morphologically similar but molecularly dis-tinct taxa. Investigation o these incongruent results is the subject o this current study.

Background o denfcaon of speces based on DNA analyss

Crocidura attenuataandC. tanakae

Crocidura attenuataMilne Edwards, 1872 described originally rom Szechuan, China,was regarded as a widespread and common species known throughout much o Asia,including many localities rom northern to southern Vietnam.


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Crocidura tanakaeKuroda, 1938 rom aiwan was originally described as a ullspecies but was subsequently considered to be either a synonym or subspecies o C.attenuata(Ellerman and Morrison-Scott 1951, Jameson and Jones 1977, Fang et al.1997, Jiang and Homann 2001, Han et al. 2002). Motokawa et al. (2001) demon-

strated that the karyotype o aiwanese specimens diered rom that oC. attenuatarom mainland southern China and suggested that it might represent a distinct species.

Although Ohdachi et al. (2006) observed phylogenetic dierentiation between the twosamples they used rom aiwan and Vietnam, these authors continued to consider theaiwanese samples as a subspecies oC. attenuata.

Esselstyn and Brown (2009) and Esselstyn et al. (2009) studying Southeast Asianshrews, recognised the relationship between samples oC. tanakaerom aiwan and asample rom northeastern Vietnam, which they identied in these studies as Crocidurac. tanakae. Te ollowing year, Esselstyn and Oliveros (2010) demonstrated the pres-ence o two similar sized species oCrocidurain Vietnam, namelyC. attenuatabasedon samples rom northern Vietnam and C. c. tanakaebased on samples rom ourseparate localities in northern and central Vietnam. Bannikova et al. (2011) includedtheir own recently collected samples rom northern, central and southern Vietnamplus inormation derived rom GenBank. Tey were similarly able to demonstrate thepresence o two separate species, C. attenuataconned to a single locality in northeast-ern Vietnam and C. tanakaewhich was widespread in northern, central and southernlocalities. With a minimum distance o 9.91% between the haplotypes, their cytb treeshowed good support or the distinction o C. tanakae rom a multi-species groupcomprisingC. attenuata, C. dsinezumi, C. indochinensis, C. lasiura, C. tadae kuroda, C.wuchihensis, C. sp. AB1 and C. zaitsevi.

Crocidura wuchihensis, C. indochinensisandC. sp. AB1

Although known rom ew specimens at any one location Crocidura indochinensisRob-inson & Kloss, 1922 was considered to have a wide, disjunct distribution, occuring in

a ew widely separated locations in Vietnam and extralimitally in Myanmar and China(Osgood 1932, Anthony 1941, Heaney and imm 1983, Jiang and Homann 2001,Hutterer 2005, Jenkins et al. 2009). Additional specimens rom southern Vietnam wererecorded recently (Abramov et al. 2009; Jenkins et al. 2010) and tissue samples romthese specimens were included in the molecular analysis by Bannikova et al. (2011).

Crocidura wuchihensisShaw, Wang, Lu and Chang, 1966 was originally describedon the basis o two specimens rom Hainan Island, China. Specimens collected romtwo localities in Vietnam (Lunde et al. 2003; 2004) were reerred to this species andspecimens rom several other locations in Vietnam were also considered to represent C.

wuchihensis(Jenkins et al. 2009). Samples oC. wuchihensisrom Ha Giang Province,Mt. ay Con Linh II, northern Vietnam were included in molecular analyses o Oh-dachi et al. (2006) and Esselstyn and Oliveros (2010). A separate analysis o a samplerom Vinh Phu Province, am Dao, northern Vietnam (Meegaskumbura et al. 2007)


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rom a specimen misidentied as C. fuliginosa, also proved to be a representative oC.wuchihensis(see Bannikova et al. 2011). Bannikova et al. (2011) added GenBank datarom samples rom these two localities to their cytb analysis o samples rom northern,central and southern Vietnam. Teir analysis o cytb revealed the presence o three taxa

orming a group with 100% support: C. wuchihensisin the two localities (Ha GiangProvince and Vinh Phu Province) in northern Vietnam; C. indochinensis in a singlelocality (Bi Doup - Nui Ba Nature Reserve) in southern Vietnam; and an unnamedspecies, designated as C. sp. AB1, rom Sa Pa in northern Vietnam. Te average dis-tance on the cytb tree between C. wuchihensisand the combined C. indochinensis/ C.sp. AB1branch was 7.75%. Tep-distance rom the cytb tree separatingC. wuchihensisand C. indochinensisis 7.6%, and separatingC. wuchihensisand C. sp. AB1 was 8.0%.Tere was 100% bootstrap support on the cytb and COI trees or the C. indochinensisand C. sp. AB1 group but these two taxa were respectively separated at p-distances o4.1% (or cytb) and 4.0% (in the COI analysis).

Mehods

Tis morphological study draws on specimens rom a wide range o geographical loca-tions in Vietnam (see Fig. 1) and includes those specimens rom which tissue samples

were analysed in the papers by Ohdachi et al. (2006), Meegaskumbura et al. (2007),Esselstyn et al. (2009), Esselstyn and Brown (2009), Esselstyn and Oliveros (2010) andBannikova et al. (2011). Te specimens included in this study (see supplementary le)are stored in the collections o the American Museum o Natural History, New York(AMNH); Natural History Museum, London (BMNH); Field Museum o NaturalHistory, Chicago (FMNH); Museum o Vertebrate Zoology, University o Calior-nia, Berkely (MVZ); National Museum o Natural History, Smithsonian Institution,

Washington D.C. (USNM); Zoological Institute, Russian Academy o Sciences, Saint-Petersburg, Russia (ZIN).

Measurements in millimetres were taken with digital callipers. Cranial and dental no-

menclature ollows that o Meester (1963), Mills (1966), Butler and Greenwood (1979)and Dannelid (1998). Denitions o skull measurements ollow Jenkins et al. (2009).

Resuls

Crocidura sapaensissp. n.urn:lsid:zoobank.org:act:6016D7F3-D50E-4DBC-B571-EB54E5062D1Ehttp://species-id.net/wiki/Crocidura_sapaensis

Holotype. ZIN 96433, genetic analysis code CVN108, BOLD Accession no. AB-MIV11408, eld no. 132, male, body in ethanol, skull extracted, collected 25 May2006 by A.V. Abramov.
http://zoobank.org/?lsid=urn:lsid:zoobank.org:act:6016D7F3-D50E-4DBC-B571-EB54E5062D1Ehttp://species-id.net/wiki/Crocidura_sapaensishttp://species-id.net/wiki/Crocidura_sapaensishttp://zoobank.org/?lsid=urn:lsid:zoobank.org:act:6016D7F3-D50E-4DBC-B571-EB54E5062D1E


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Fgure 1. Geographical distribution o sampling localities in Vietnam: 1 Lao Cai Province, Ngai io

2 Lao Cai Province, Sa Pa District 3 Lao Cai Province, Van Ban District 4 Lao Cai Province, Tai Nien

5 Lao Cai Province, Pa Kha6 Ha Giang Province, Mt. ay Con Linh II 7 uyen Quang Province 8 Vinh

Phu Province, am Dao 9 Hai Phong Province, Cat Ba Island 10 Ha inh Province, Huong Son District

11 Quang Binh Province, Phong Nha - Ke Bang National Park12 Quang ri Province, Huong Hoa

Nature Reserve 13 Quang Nam Da Nang Provinces, Ba Na Nature Reserve 14 Kon um Province,

Ngoc Linh Mt. 15 Kon um Province, Dak o 16 Lam Dong Province, Da Lat 17 Lam Dong Province,

Bi Doup - Nui Ba Nature Reserve 18 Khanh Hoa Province, Hon Ba Mt.


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Type locality. Vicinity o ram on Station o Hoang Lien National Park, northslope o Phansipan Mt. area, 6 km west o Sa Pa own, Sa Pa District, Lao Cai Prov-ince, Vietnam, 2221'N, 10346'E, altitude 2200m above sea level.

Paratypes. ZIN 96262, genetic analysis code CVN93, GenBank no. HM587005,

BOLD no. ABMIV100 08, eld no. 13, male, collected 8 December 2005; ZIN 96264,genetic analysis code CVN94, GenBank no. HM587006, BOLD no. ABMIV101 08,eld no. 15, emale, collected 8 December 2005; ZIN 96269, genetic analysis codeCVN99, BOLD no. ABMIV106 08, eld no. 32, male, collected 15 December 2005;ZIN 96271, genetic analysis code CVN101, BOLD no. ABMIV108 08, emale, col-lected 16 December 2005; ZIN 96274, genetic analysis code CVN102, BOLD no. AB-MIV109 08, eld no. 45, male, collected 17 December 2005; ZIN 96275, genetic analy-sis code CVN103, BOLD no. ABMIV110 08, eld no. 46, male, collected 17 December2005; ZIN 96276, genetic analysis code CVN104, BOLD no. ABMIV111 08, eld no.66, emale, collected 22 December 2005; ZIN 96432, genetic analysis code CVN107,BOLD no. ABIOW074 08, eld no. 131, male, collected 25 May 2006; ZIN 96434,genetic analysis code CVN109, BOLD no. ABIOW075 08, eld no. 133, male, collected25 May 2006; ZIN 96436, genetic analysis code CVN111, BOLD no. ABMIV116 08,eld no. 136, male, collected 28 May 2006; ZIN 96438, genetic analysis code CVN113,BOLD no. ABMIV117 08, eld no. 138, emale, collected 28 May 2006; ZIN 96439,genetic analysis code CVN114, BOLD no. ABMIV118 08, eld no. 139, emale, collect-ed 28 May 2006; ZIN 96442, genetic analysis code CVN117, BOLD no. ABIOW06908, eld no. 144, male, collected 31 May 2006; ZIN 99779, eld no. 24, male, collected10 May 2010. All bodies in ethanol, skulls extracted, collected by A.V. Abramov and A.V.Shchinov rom the same locality as the holotype, altitude 19302200m above sea level.

Other material. FMNH 39029 Chapa [Sa Pa], Lao Cai Province; BMNH1925.1.1.24; BMNH 1925.1.1.27 Ngai io, Lao Cai Province, 2236'N, 10340'E.

Diagnosis.A small shrew distinguished by the mitochondrial genes cytochromeb (cytb) and cytochrome oxidase csubunit I (COI) and by the shape o the talonid othe third lower molar (m3).

Description.Size small (see able 1) with a moderately long tail relative to head

and body length (6284%). Dorsal pelage dark greyish brown; tail dark grey dor-sally, slightly paler below (see Fig. 2). Skull with a rounded, short rostrum: moderatelybroad interorbital region; rounded, relatively deep braincase with subangular superiorarticular acets and lambdoid crests just evident laterally near the junction with themastoid (see Fig. 3). Te rst upper incisor is slender with a relatively small posteriorcusp, less than hal the height o the rst upper unicuspid; posterolingual border oupper premolar (P4) deep and rounded, in close contact with the anterolingual margino M1 in occlusal view; last upper molar (M3) relatively narrow. Lower incisor withtwo distinct cusps on the occlusal surace in unworn dentition; posterolingual cuspid

present on lower premolar (p4); talonid basin o m3 broad and deep with an entoconidridge and low entoconid (see Fig. 4).

Comparison with other species. Crocidura sapaensis averages larger than thevery small species oCrocidurarecorded rom Vietnam. Te condyloincisive length is


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Fgure 2. Photograph o adult male Crocidura sapaensis(ZIN 99779).

greater than that oC. guy, C. annamitensisand C. kegoensis, within the upper part othe range oC. zaitseviand the braincase is deeper than that o all our small species.Crocidura wuchihensisand C. sapaensisare in the same size range. Crocidura sapaensisis smaller than or at the lower end o the size range oC. indochinensiswith a relativelyshorter tail (see able 1 and Fig. 5).

Crocidura sapaensisand C. wuchihensisare distinguished by dierences in cytb se-quences. Crocidura sapaensisdiers rom C. zaitseviand C. indochinensis in the cytband COI gene sequences.

Dierences in the shape o the talonid o m3 in northern Vietnamese populationsserve to distinguish C. sapaensisand C. wuchihensis(see Fig. 4). In specimens oC. sa-

paensisrom northern Vietnam the talonid basin is broad and deep with an entoconidridge and low entoconid, whereas in C. wuchihensisthe talonid basin is narrow. In C.indochinensisthe talonid basin is broad and deep with a hypoconid, entoconid and

marked entoconid ridge (see Fig. 4).Etymology.Te new species is named ater Sa Pa, the capital o Sa Pa District inLao Cai Province o northern Vietnam, with the Latin sux - ensis(belonging to).

Natural history.Te series o type specimens was collected rom a variety ohabitats in the vicinity o ram on Station o Hoang Lien National Park: mixedevergreen orest; orested banks o small streams; open grassy glades (Fig. 6); pri-mary orest with large trees at an elevation 19302200m (Abramov et al. 2008b).During 20052010 a total o 190 shrews was captured in this area, including 4species (Crocidura sapaensis, Blarinella griselda Tomas, 1912, Anourosorex squa-

mipesMilne Edwards, 1872, and Episoriculus leucops(Horseld 1855)). Crocidurasapaensiswas the most numerous species (90% o the total captures), ollowed byA.squamipesand B. griselda(5.3% and 4.2% respectively), while only one E. leucops

was captured (Abramov et al. 2010). Crocidura sapaensis was more abundant in


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slightly disturbed mixed orest (2.23.0 specimens per 100 trap/nights), the occur-

rence in open glades, amongst shrubs on stream banks and in undisturbed primaryorest was 0.32.6 specimens per 100 trap/nights. Te proportion o males to e-males in C. sapaensiswas greater in all seasons; on average the male to emale ratiois 2.3. Pregnant emales were recorded rom May to mid-July. Mean litter size in C.sapaensiswas 3.0 (2-4, n=15).

Distribution. Conrmed specimens oC. sapaensisare recorded rom Lao CaiProvince, Sa Pa District on the basis o cytb analysis and morphology o m3. On thebasis o morphology, specimens rom the northern part o Lao Cai Province, Ngai io(elevation 1450m) and rom the vicinity o Cat Cat Village near Sa Pa own (eleva-

tion 14001450m) in relatively close geographical proximity also probably belong tothe same species.

Populations oC. wuchihensisidentied on the basis o cytb and those probablyrepresenting this species on the basis o morphology (rom Pa Kha and Tai Nien,

Fgure 3. Comparison o crania oCrocidura wuchihensis(AMNH 274153), Crocidura sapaensis(ZIN96433) and Crocidura indochinensis(ZIN 97668). op row rom let to right: dorsal views o the skulls oC. wuchihensis, C. sapaensisand C. indochinensis, ventral views o the skulls in the same order. Lower row:let lateral view o skulls and mandibles rom let to right oC. wuchihensis, C. sapaensisand C. indochinensis.


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Fgure 4. Occlusal (let) and lingual (right) views o right lower third molar to show dierences in devel-

opment o the talonid. Upper row let Crocidura wuchihensisAMNH 274168; upper row right Crocidura

sapaensisZIN 96439; lower rowCrocidura indochinensisZIN 97671. Scale equals 1 mm.

table 1. Comparison oCrocidura indochinensis, C. wuchihensisand C. sapaensis. Crocidura guyand

C. zaitseviB are included as representatives o the very small species in Vietnam. Measurements in mil-limetres are presented as the mean, standard deviation and range, ollowed by sample size in parentheses.

CharacterCrocidura zaitsevi

B Bi Doup &Hon Ba

CrociduraguyNa Hang

CrocidurawuchihensisMtTay Con Linh II

Crocidurasapaensis

Sa Pa

Crociduraindochinensis

Bi Doup

Condyloincisivelength

15.4 0.2814.9-15.8 (15)

15.4 0.0515.3-15.4 (4)

16.4 0.515.7-17.1 (6)

16.6 0.4115.6-17.2 (20)

18.1 0.3617.5-18.7 (10)

Condylobasal length14.8 0.31

14.2-15.3 (15)14.9 0.06

14.8-14.9 (4)15.7 0.47

15.0-16.4 (6)15.9 0.42

15.0-16.5 (20)17.4 0.37

16.8-17.8 (10)

Upper toothrowlength

6.5 0.146.3-6.8 (15)

6.5 0.146.4-6.7 (4)

7.0 0.256.6-7.2 (6)

7.0 0.176.5-7.2 (21)

7.7 0.237.3-8.0 (10)

Maxillary breadthat M2

4.5 0.194.2-4.9 (15)

4.5 0.144.4-4.7 (4)

4.9 0.064.8-5 (6)

4.8 0.184.4-5.1 (21)

5.2 0.075.1-5.3 (10)

Braincase breadth7.2 0.15

6.9-7.5 (15)7.2 0.177.0-7.4 (4)

7.5 0.167.3-7.8 (6)

7.7 0.197.4-8.1 (19)

8.2 0.157.9-8.4 (10)

Braincase height3.7 0.13

3.5-3.9 (14)3.6 0.143.5-3.8 (4)

4.0 0.153.7-4.1 (6)

4.1 0.173.9-4.4 (19)

4.4 0.144.1-4.5 (10)

Head and bodylength

52.7 2.7949-59 (15)

49.5 2.2747-53 (4)

60.6 2.758-65 (5)

57.4 3.9150-65 (20)

63.5 3.8156-68 (10)

ail length31.8 1.230-34 (15)

35.9 1.434-37 (4)

39.8 2.2837-42 (5)

41.6 2.4837-47 (20)

55 2.7950-58 (10)

Ratio o tail length tohead and body length

0.61 0.020.55-0.65 (15)

0.73 0.030.69-0.77 (4)

0.66 0.040.63-0.72 (5)

0.73 0.060.62-0.84 (20)

0.87 0.050.81-0.98 (10)

Ratio o tail length tocondyloincisive length

2.1 0.062.0-2.2 (15)

2.3 0.092.2-2.4 (4)

2.4 0.142.2-2.6 (5)

2.5 0.142.2-2.7 (20)

3.1 0.122.9-3.2 (10)


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Fgure 5. Bivariate plot to show dierences in skull size and relative tail length. Horizontal axis: condy-

loincisive length; vertical axis: ratio o tail length to condyloincisive length.

Fgure 6. Habitat typical o the area where Crocidura sapaensiswas ound.


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both in Lao Cai Province) all occur in northeastern Vietnam in localities to the easto the Song Hong (Red River). Te observation that this river marks the borderbetween the two species, with C. wuchihensis to the east and C. sapaensis to the

west, was made by Bannikova et al. (2011), however this apparent biogeographical

separation is based on ew locality records. Tese authors also observed that, in thecytb analysis, the two northern Vietnamese populations oC. wuchihensis(rom Mtay Con Linh II [2246'N, 10449'E] and am Dao [2127'N, 10538'E]) wereseparated by ap-distance o 2.1% suggesting that they probably represent distinctgeographic populations.

Te population oC. wuchihensisrecorded rom Huong Son, Ha inh Provincein the southern Annamites by Lunde et al. (2004) and Jenkins et al. (2009), doeso course, occur west o the Song Hong and samples have not been included in anyo the previous molecular studies. Specimens rom Mt ay Con Linh II are largeron average (CIL 15.717.1, mean 16.4) than those rom Huong Son (CIL 15.8-16.4, mean 16.0). Te Canonical Variate Analysis reported in Jenkins et al. (2009:Fig. 10) shows that these two groups respectively rom northern Vietnam and thesouthern Annamites are moderately well separated rom each other. In view o theproblems outlined in this paper, lacking urther evidence rom molecular studies,it is impossible to predict i the population rom Huong Son is correctly assignedto C. wuchihensis, could belong to C. sapaensis, or might indeed represent a urtherundescribed species.

Crocidura attenuataandC. tanakae

Characters separatingC. attenuataandC. tanakae

Te population rom Mt ay Con Linh II, Ha Giang Province in northern Vietnamrecognised by molecular analysis o cytb as C. attenuata, alls within the size rangeoC. tanakaeand both species are morphologically very similar in appearance. Te

two species may be separated by the ollowing characters. Te basioccipital regionin C. attenuatais narrow and ridged particularly anterior to the position o the ba-sioccipital suture, whereas in C. tanakaethe basioccipital region is broad and fat toconcave (see Fig. 7). Te palatal suture in C. attenuatais a rounded to fat-topped nshape, whereas in C. tanakaethe suture is a shallow to more marked m shape (seeFig. 8). Te two species also dier in the shape o the talon o the upper premolar(P4). In occlusal view, the talon oC. attenuatais broader and more angular thanthat oC. tanakae, the lingual border is straight to concave, with the posterior bor-der shallowly indented so that the whole tooth looks larger in occlusal view. In C.

tanakaethe lingual border o P4 is rounded and the posterior border o the tooth isdeeply indented (see Fig. 8).


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Geographical variation in C. tanakae

Esselstyn and Oliveros (2010) did not provide detailed results about Vietnamesesamples in the text o their analysis o Asian C. tanakae, nevertheless they demon-

strated apparent geographical variation in Vietnam. Teir illustration o a statisticalparsimony network o mitochondrial haplotypes (Esselstyn and Oliveros 2010: Fig. 4)shows northeastern Vietnam samples rom am Dao (2127'N, 10538'E) and uyenQuang (2220'N, 10525'E) grouped relatively closely, separated rom each other by

Fgure 7. Comparison o crania oCrocidura tanakae(ZIN 91190) and Crocidura attenuata(AMNH274152). op row rom let to right: dorsal views o the skulls o C. tanakaeand C. attenuata, ventral

views o the skulls in the same order. Lower row: let lateral view o skulls and mandibles rom let to right

oC. tanakaeand C. attenuata.


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relatively ew steps but separated by multiple steps rom samples rom the other two lo-calities, Ha inh (1821'N, 10513'E) and Quang Nam (1512'N, 10802'E), whichorm a looser group. In their analysis o the COI gene, Bannikova et al. (2011) demon-strated the presence o two clearly dened haplogroups within Vietnamese C. tanakae:C. tanakaeB restricted to the northern part o the country (Hoang Lien Mountains,Van Ban District) and C. tanakaeA which was more widespread in Central and SouthVietnam (Huong Hoa, Phong Nha-Ke Bang, Ngoc Linh, Hon Ba and Bi Doup). Teuncorrectedp-distance between these two groups using the COI gene was about 2.5%.

Populations oC. tanakaein Vietnam show a distinct clinal variation in skull size,

populations at higher latitudes averaging smaller in size than those at lower latitudes(see able 2). Although sample sizes are small, this observation is a possible example othe converse Bergmanns rule where body size decreases with latitude.

Geographical variation in C. attenuata

Abramov et al. (2012) demonstrated apparent geographical variation oC. attenuatain southern China and northern Vietnam. Genetic dierentiation oC. attenuata is

notable and reveals a phylogeographic structure with our haplogroups. Te specimensrom Cat Ba Island (Hai Phong Province, northeastern Vietnam) ormed a single clus-ter closely related to the group o specimens rom northern Vietnam (Ha Giang Prov-ince) and southeastern China (Guangxi Province). Te genetic distance (p-distance)

Fgure 8. Above: occlusal view o let upper premolar oCrocidura tanakae(ZIN 91205) let and Cro-

cidura attenuata(AMNH 274232) right. Below: palatal sutures o the same specimens in the same order.

Scales equal 1 mm.


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between specimens rom Cat Ba / Ha Giang as well as Cat Ba / Guangxi is about 2.1%.Te specimen oC. attenuatarom the more north-eastern region o China (HunanProvince) appears basal among all samples oC. attenuatarom China and Vietnam.Tus, the genetic distance between two specimens rom China (Hunan / Guangxi) is4.3%, which is nearly the same as the distance between C. indochinensisand C. sapaen-sis(see Bannikova et al. 2011).

Distribution

While C. attenuata in Vietnam appears to occur only to the east o the Song Hong(Red River), in northeastern Vietnam (Bannikova et al. 2011, Abramov et al. 2012),C. tanakaedoes not appear to be so constrained and has been recorded on both sides

o the river in northern Vietnam and also in central and southern Vietnam (Esselstynand Oliveros 2010, Bannikova et al. 2011, this study).

Dscusson

For sister species that are recognised on the basis o morphology, cytb distance valuestypically exceed 5% (Baker and Bradley 2006). Tep-distance values o at least 9.91%between haplotypes belonging to the C. tanakaeand C. attenuatagroups, o 7.6%

separatingC. wuchihensisand C. indochinensis, and o 8.0% separatingC. wuchihensisand C. sapaensisprovide compelling evidence in support o their taxonomic distinc-tion (Bannikova et al. 2011). Te lowerp-distance values o 4.1% separatingC. in-

table 2. Latitudinal size variation in Crocidura tanakae. Measurements in millimetres are presented as

the mean, standard deviation and range, ollowed by sample size in parentheses.

CharacterLao Cai Prov.,Van Ban Dist.

2158'N

Ha TinhProv., HuongSon 1821'N

Quang TriProv., HuongHoa 1656'N

Kon TumProv., Ngoc

Linh 1505'N

Lam DongProv,. Bi Doup

1211'N

Condyloincisivelength

19.3 0.4718.520.0 (14)

19.7 0.4718.420.4 (24)

20.1 0.3819.620.6 (5)

20.6 0.3620.120.9 (4)

20.4 0.5219.621.3 (11)

Condylobasallength

18.8 0.4817.919.4 (14)

18.9 0.4817.719.6

(24)

19.2 0.3618.819.6 (5)

19.8 0.2919.420.0 (4)

19.5 0.5218.820.6 (11)

Upper toothrowlength

8.3 0.187.98.6 (14)

8.5 0.228.29.0 (24)

9.0 0.248.69.3 (5)

9.1 0.148.99.2 (4)

9.0 0.238.59.4 (11)

Maxillary breadthat M2

5.9 0.175.66.3 (14)

6.0 0.195.66.4 (24)

6.2 0.176.06.4 (5)

6.3 0.186.16.5 (4)

6.2 0.215.96.6 (11)

Braincase breadth8.7 0.31

8.39.2 (14)8.9 0.19

8.39.1 (24)9.0 0.148.79.1 (5)

9.2 0.368.99.6 (4)

9.3 0.268.99.6 (11)


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dochinensisrom C. sapaensisare somewhat less convincing, were it not or the readymorphological distinction o the two species. Te conundrum is the morphologicaldistinction yet relatively low molecular separation between C. indochinensisand C.sapaensis, in contrast to C. wuchihensisand C. sapaensiswhich are not easily dened

by morphological eatures but are distinguished by high molecular values. Similarsituations are ound in the literature, or example amongst dierent species oEumopsMiller, 1906 (bonneted bats) (McDonough et al. 2008). It is possible to speculate thatthis implies a relatively closer relationship between C. indochinensisand C. sapaensisbut morphological convergence o C. wuchihensis and C. sapaensis to meet similarecological requirements.

Crocidura tanakae is currently recognised as being widely distributed in South-east Asia including southern China, Vietnam, aiwan and the Philippines (Esselstynand Oliveros 2010, Bannikova et al. 2011). Crocidura attenuatahas a more northerlydistribution (Esselstyn and Oliveros 2010) and urthermore evidence suggests that, atleast in Vietnam, the distribution may be more restricted than ormerly understood(Bannikova et al. 2011, this study). It is conceivable that these two morphologicallyconvergent species have secondarily come into contact with each other as there is evi-dence that the two species are sympatric in at least one Chinese locality (Esselstyn andOliveros 2010, Judith Eger pers. comm.).

Acknowledgemens

Te eld studies in Vietnam were possible due to the support o the Joint Vietnam-Russian ropical Research and echnological Centre. We are grateul to the adminis-tration o the Hoang Lien National Park or providing us with an opportunity to carryout eld surveys. AA thanks A.V. Shchinov, A.E. Anichkin, Vu Van Lien, A.L. Monas-tyrskii, S.V. Kruskop or their help and scientic expertise during the eld work. Tisstudy was supported in part by the Russian Foundation or Basic Research (projects11-04-00020, 12-04-93005).

PJ particularly thanks Darrin Lunde, National Museum o Natural History,Smithsonian Institution, Washington D.C. or generously allowing access to speci-mens collected at pivotal localities in Vietnam and or many discussions over the prob-lems o identiying morphologically conservative shrews. For providing access to thecollections in their care, we are especially grateul to Eileen Westwig and Neil Duncan,

American Museum o Natural History, New York; to James Patton and Chris Con-roy, Museum o Vertebrate Zoology, University o Caliornia, Berkeley and to Wil-liam Stanley and John Phelps, Field Museum o Natural History, Chicago. As always,grateul thanks to Phil Hurst, Photographic Unit, Natural History Museum, London,

or specimen photography and to Roberto Portela Miguez, Mammal Group, NaturalHistory Museum, London or scanning documents. We thank two anonymous re-viewers or their helpul and constructive comments and criticisms.


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Appendx

Specimens included in the morphological study. (doi: 10.3897/zookeys.313.4823.app). File ormat: Microsot Word document (doc).

Explanation note: Te supplementary le contains a list o all specimens included inthis study.

Copyright notice: Tis dataset is made available under the Open Database License(http://opendatacommons.org/licenses/odbl/1.0/). Te Open Database License(ODbL) is a license agreement intended to allow users to reely share, modiy, and usethis Dataset while maintaining this same reedom or others, provided that the originalsource and author(s) are credited.

Caon: Jenkins PD, Abramov AV, Bannikova AA, Rozhnov VV (2013) Bones and genes: resolution problems in three

Vietnamese species oCrocidura(Mammalia, Soricomorpha, Soricidae) and the description o an additional new species.

ZooKeys 313: 6179. doi: 10.3897/zookeys.313.4823Specimens included in the morphological study. doi: 10.3897/

zookeys.313.4823.app
http://dx.doi.org/10.3897/zookeys.313.4823.apphttp://dx.doi.org/10.3897/zookeys.313.4823.apphttp://opendatacommons.org/licenses/odblhttp://dx.doi.org/10.3897/zookeys.313.4823http://dx.doi.org/10.3897/zookeys.313.4823.apphttp://dx.doi.org/10.3897/zookeys.313.4823.apphttp://dx.doi.org/10.3897/zookeys.313.4823http://opendatacommons.org/licenses/odblhttp://dx.doi.org/10.3897/zookeys.313.4823.apphttp://dx.doi.org/10.3897/zookeys.313.4823.app

crocidura sapaensis 2013

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