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Acta Chiropterologica, 13(2): 271­278, 2011
PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/150811011X624758

A new mouse-eared bat (Mammalia: Chiroptera, Vespertilionidae) from South China
M
1Institute

IKHAIL

P. T

IUNOV

1, 4

,S

ERGEI

V. K

RUSKOP

2

, and J

IANG

F

ENG

3

3

of Biology and Soil Science Far East Branch of the Russian Academy of Sciences, Vladivostok 690022, Russia 2 Zoological Museum, Moscow State University, Bolshaya Nikitskaya 6, Moscow 125009, Russia College of Urban and Environmental Sciences, Northeast Normal University, Changchun 130024, People's Republic of China 4 Corresponding author: E-mail: tiunov@ibss.dvo.ru

A small Myotis species belonging to the Myotis siligorensis group was found in four caves in Yunnan province, South China. Twenty specimens of this bat were compared with other East Asian Myotis species. Statistical and physical analysis of this sample demonstrates that, despite their similarity to M. siligorensis, the Yunnan specimens have characteristics of baculum morphology and cranial proportions suggesting that they represent a distinct species. Key words: Myotis sp. nov., taxonomy, baculum, South China

I

NTRODUCTION

The genus Myotis is amongst the largest mammalian genera (Simmons, 2005). Its internal structure is very problematic since the traditionally accepted affiliations between Myotis species were called into question by recent molecular studies (Ruedi and Mayer, 2001; Zang et al., 2009; Lack et al., 2010). Thus the genus includes numerous species complexes with questionable and uncertain taxonomy. One of these is the Myotis `siligorensis' species group. This group was initially proposed for only one species (Tate, 1941), characterized by small size, formal features of the subgenus Selysius, low rostrum, abruptly elevated frontal profile and small canines. Within this species four geographical races were usually recognized (Ellerman and MorrisonScott, 1966; Simmons, 2005). This species group was accepted by e.g. Koopman (1994) but not defined in the latest published checklist (Simmons, 2005). It was considered to be a good taxonomic unit by Borisenko et al. (2008) and an additional species -- Myotis phanluongi -- was described. Here we suggest inclusion into this group of several other Asiatic species of similar size and skull proportions, namely Myotis laniger, M. longipes, M. annamiticus, M. taiwanensis and M. csorbai. This proposal is supported by molecular data (Borisenko et al., 2008; Zhang et al., 2009; Francis et al., 2010). Being

distributed sporadically and not very well represented in scientific collections, bats of this species group are insufficiently investigated taxonomically. In June 2006, during joint field work supported by the Russian Foundation for Basic Research (RFBR) and the National Natural Science Foundation of China (NNSFC), scientific voucher specimens of bats were collected from Yunnan province (southern China). The collection includes several specimens of small mouse-eared bats (genus Myotis) of uncertain taxonomic status. An analysis and comparison of the external and cranial morphological characteristics of these Myotis specimens indicate that they possess features that set them apart from other South Asian representatives of the genus Myotis. In our opinion, these mouse-eared bats, captured in Longxu, Xianren, Dashi, and Huyan caves (Yunnan province), represent a distinct species. M
ATERIALS AND

M

ETHODS

Two males and 12 females of Myotis sp. nov. were captured in a mist net from Longxu Cave (24°30'N, 102°20'E); two females from Xianren Cave at Fagudian Village (24°30'N, 102°20'E); one male and two females from Dashi Cave (24°29'N, 102°22'E); and one male from Huyan Cave at Shuanghechang Village (24°29'N, 102°22'E). All are preserved in 75% ethanol with skulls extracted. Forty-nine specimens of morphologically similar species were used for qualitative and quantitative morphological comparison (adult individuals of both sexes; dry or alcohol


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M. P. Tiunov, S. V. Kruskop, and J. Feng articulated process (LMD), lower jaw height on the level of the tip of the coronoid process (HMD), crown length of maxillary tooth row (MCM3). During statistical processing this list of measurements was restricted to 16 due to missing data. To assess the pattern of variation of quantitative characters, principal component (PC) analyses were performed for cranial measurements, using the factor analysis module of STATISTICA for Windows (StatSoft, Inc., 1999). For PC analysis, measurements were standardized [(raw score - mean)/SD] to decrease the influence of the overall size.

preserved skins with extracted skulls). Acronyms of repositories of the processed collections are as follows: FMNH -- Field Museum of Natural History, Chicago, USA; HNHM -- Hungarian Natural History Museum, Budapest, Hungary; ROM -- Royal Ontario Museum, Toronto, Canada; ZMMU -- Zoological Museum of Moscow State University, Moscow, Russia; IBSS -- Institute of Biology and Soil Science, Far East Branch of the Russian Academy of Sciences, Vladivostok, Russia. Myotis csorbai Topal, 1997 -- Central Nepal (including five paratypes of the species): ZMMU S-164475 , ZMMU S164476 , ZMMU S-164478 , ZMMU S-164481 , ZMMU S-164483 , ZMMU S-164484 , ZMMU S-164485 , ZMMU S-164487 , ZMMU S-164490 . Myotis annamiticus Kruskop and Tsytsulina, 2000 -- Central Vietnam (from the type series of the species): ZMMU S-167123 , ZMMU S167126 , ZMMU S-167127 , ZMMU S-167128 , ZMMU S-167132 , ZMMU S-167134 , ZMMU S-167135 . Myotis cf. annamiticus -- Laos: ROM 110661 . Myotis siligorensis -- Vietnam Central Highlands: ZMMU S-175152 , ZMMU S-175157 , ZMMU S-175159 ; Central Vietnam: ZMMU S-167188 ; Northern Vietnam (Tuen Quang, Sa Pa and Muon Muon; including three females from the type series of M. s. alticraniatus): ROM 107649 , ROM 107652 , ROM 107657 , ROM 107677 , ROM 112447 , ROM 112456 , ROM 112458 , FMNH 32173 , FMNH 32175 , FMNH 32178 ; China, Fujian (= Fokien): FMNH 33858 , FMNH 33859 , FMNH 44109 . Myotis laniger (Peters, 1871) -- Northern Vietnam: ROM 107655, ROM 107665 , ROM 112492 , ROM 111269 , HNHM 93.57.1 ; India: HNHM 92.108.1 , HNHM 92.108.2 , HNHM 92.108.3 ; Southern China: IBSS u-06-75, IBSS u-06-106. Myotis taiwanensis Linde, 1908 -- Taiwan: HNHM 2005.65.43. Myotis muricola (Gray, 1846) -- Southern Vietnam: ZMMU S-173413 , ZMMU S-172616 , ZMMU S-172626 ; Central Vietnam: ZMMU S-165048 , ZMMU S-165055 . External measurements were taken to the nearest 0.1 mm with a dial caliper. A set of 19 cranial measurements was taken in the laboratory to the nearest 0.01 mm with an electronic caliper in combination with a binocular microscope. The following external measurements were taken: head and body length (HB), tail length (T), length of free tail tip (TT), ear length (E), tragus length (Tr), tibia length (Tib), foot length (without claws and including claws (F), measured to the most remote part of claw), forearm length (FA), length of the first digit including claw, length of the metacarpal of the second digit, and lengths of the metacarpals and phalanxes of the third through fifth digits. All wing measurements were taken on the right wing. The following cranial characters were measured (appropriate abbreviations are given in parentheses): condylobasal length (CBL), condylocanine length (CCL), width of the skull at the level of the auditory bullae (W), width of braincase (BCW), height of braincase posterior to the auditory bullae (BCH), least interorbital width (IOW), zygomatic width (ZW), rostral width at the level of the preorbital foramina (WR), rostral length from the preorbital foramen to the alveolus of the inner incisor (LR), C­M3 length (CM3), length of interval between cingulum of upper canine and large premolar (`pseudodiastema', PD), molariform tooth row length (P4M3), width of M3 (WM3), length of M3 (LM3), crown measured width between outer margins of upper canines (CC), crown measured width between outer margins of M3 (M3M3), lower jaw length from alveolus of I1 to the

S

YSTEMATIC

D

ESCRIPTION

Myotis badius sp. nov. Holotype IBSS u-88, adult , body in 75% alcohol, skull and baculum extracted, collected by Li Zhenxin and M. P. Tiunov on June 16, 2006. Paratypes IBSS (Field No. u-06-8), adult , body in alcohol, skull extracted, collected by Li Zhenxin and M. P. Tiunov on June 13, 2006 from Longxu Cave; (Field No. u-06-80) adult , body in alcohol, skull extracted, collected by Li Zhenxin and M. P. Tiunov on June 16, 2006 from Dashi Cave; 10 adult (Field Nos.: u-06-13, u-06-14, u-06-15, u-06-16, u06-20, u-06-22, u-06-28, u-06-35, u-06-34, u-0634a), all bodies in alcohol with skulls extracted, collected by Li Zhenxin and M. P. Tiunov on June 13, 2006 from Longxu Cave. ZMMU S-186520 (Field No. u-06-9), adult , body in alcohol, skull extracted, collected by Li Zhenxin and M.P. Tiunov on June 13, 2006 from Longxu Cave; S-186521 (Field No. u-06-16), adult , body in alcohol, skull extracted, collected by Li Zhenxin and M. P. Tiunov on June 13, 2006 from Longxu Cave. Etymology The species name `badius' is connected to colouration of the fur ( `badius' (Lat.) = `chestnut'). We suggest Chestnut Myotis as an appropriate English vernacular name. Type locality Dashi Cave, near Shicaohe village, Shuanghe Town, Yunnan Province, China (24°29'N, 102°22'E). Diagnosis A species of Myotis of small size belonging to the `siligorensis' species group: forearm length = 36.8 mm (35.0­38.5 mm, n = 20), condylobasal length of skull = 12.2 mm (11.8­12.6 mm, n = 20). Margin of


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plagiopatagium attached to the metatarsus of first toe. Foot, including claw, 44% (37­51, n = 20) of tibia. Frontal part of skull distinctly elevated above the low rostrum, as in M. siligorensis, M. csorbai and M. annamiticus. Both small upper premolars (P2 and P3) present in the tooth row and clearly visible in lateral view. Lower molars belong to seminyctalodon type, as in M. siligorensis, M. phanluongi and M. annamiticus. New form could be clearly distinguished from all the latter species by the shape of baculum. Measurements of the holotype (in mm) are as follows: body length -- 42, tail length -- 37, length of free tail tip -- 0.5, ear length -- 12.5, tragus length -- 5.6, tibia length -- 15.7, foot length with claws -- 6.7, forearm length -- 35.7, length of the first digit (without claws/with claws) -- 4.7/5.7, Mc2 -- 29.2, Mc3 -- 32.4, Ph3.1 -- 8.5, Ph3.2 -- 8.0, Ph3.3 -- 6.5, Mc4 -- 32.4, Ph4.1 -- 8.0, Ph4.2 -- 7.5, Mc5 -- 31.2, Ph5.1 -- 7.5, Ph5.2 -- 7.0; and CBL -- 12.1, CCL -- 11.4, W -- 7.0, BCW -- 6.5, BCH -- 5.0, IOW -- 3.25, ZW -- 8.2, WR -- 4.1, LR -- 2.35, CM3 -- 4.25, PD -- 0.75, P4M3 -- 3.45, WM3 -- 1.2, LM3 -- 0.65, CC -- 3.2, M3M3 -- 5.25, LMD -- 8.9, HMD -- 2.6, MCM3 -- 4.9. Description External characters: The hairs of the dorsal pelage are brownish-chestnut. The fur is a uniform light-brown on the ventral surface. Ear comparatively short, not extending, when laid forward, to anterior end of muzzle. Tragus relatively short, a little less than half as high as the conch; its anterior border straight, its widest portion in the lower third. Wing membrane wide, the fifth finger comparatively long, about 82% of the third finger in length. The calcar is about 37% (33.0­44.9, n = 13) the length of the posterior border of the interfemoral membrane when measured from the foot to the tip of the tail, without keel and terminal lobe (Fig. 1). Tail relatively long, on average 85% of head and body length; about 0.45 mm of its tip is free from the membrane. The ventral surface of the interfemoral membrane is sparsely haired, the hairs are about 0.7­0.8 mm in length. Cranial and dental characters: Frontal part of the skull is distinctly elevated above the low rostrum (as in M. csorbai and M. siligorensis). Brain case height ca. 75.7% (71.4­80.7, n = 20) of skull width. Upper surface of rostrum with a visible middle groove. Interorbital constriction remarkably narrow; interorbital width about 46% of skull width. Posterior border of naris extending to the frontal margin of the upper canine. Sagittal crest is scarcely evident,

FIG. 1. Calcar of M. badius. Scale bar is 10 mm

lambdoid crest is visible laterally, but lacking in the central portion. Outer upper incisor (I3) trifid, equal or slightly less than internal incisor (I2). Upper canine is short; it scarcely exceeds the posterior premolar (P4) in height and has a smaller crown area (Fig. 2). Anterior premolar (P2) is in contact with the canine and is 1/2 its height. Middle premolar (P3) small, about two thirds of P2 in height and half to two-thirds the crown area. Both small upper premolars are situated in the tooth row and are visible when the skull is viewed laterally. Posterior premolar (P4) is low, with an antero-internal cusp. Upper molars with well-developed protoconules. In the lower dentition, the first (I1) and second lower incisors (I2) are three- or four-lobed when viewed from the front. The inner two incisors are imbricated; there is usually a small gap between I2 and the third incisor (I3). The canine is small, its height less than that of the posterior lower premolar (P4). The first lower premolar (P2) scarcely exceeds half the height of the canine. The second lower premolar (P3) is about half to two-thirds of P2 in height and lies within the tooth-row. The lower first molar is always nyctalodont (the postcristid is connected to the hypoconulid). The second molar is nyctalodont or seminyctalodont dental type (where the postcristid may connect to both entoconid and hypoconulid, or to neither). The third molar is usually myotodont or more rarely nyctalodont (Fig. 3). A similar tooth structure was revealed earlier in Lasionycteris noctivagans (Legendre, 1984). Recently nyctalodontia, which is common to the tribe Pipistrellini, was described in other Vespertilionidae lineages


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M. P. Tiunov, S. V. Kruskop, and J. Feng

FIG. 2. Dorsal, ventral and lateral views on the cranium and mandible of M. badius sp. nov. (holotype)


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200 µm

Comparison with Similar Species Morphometric comparisons In a two-dimensional projection of the first two principal components the newly described taxon is clearly segregated without overlap from M. siligorensis samples, including similar sized M. phanluongi (Fig. 5), and even more so from other Myotis species used as comparative material. PC1 is highly correlated with overall skull size and upper and lower tooth rows; while PC2 has high positive correlation with rostral width and length (Table 1), suggesting that corresponding measurements are of particular identification value. The only specimen not well separated from the new species sample is a M. cf. annamiticus specimen from Laos, which, nonetheless, can be differentiated from M. badius by the same physical features as M. annamiticus. Physical comparisons The newly described Myotis is most similar to M. siligorensis, which is widely distributed from northern India to Vietnam and south to Malaysia and Borneo (Simmons, 2005) and also in south China

FIG. 3. Lower molar structure of M. badius sp. nov. (holotype)

including the genus Myotis (Kruskop, 2007). However, in the genus Myotis this dentition type is still known only in the `siligorensis' species group (Borisenko et al., 2008). Baculum: The baculum of M. badius is in general similar to that of other species in this species group. It is very small, straight, narrow, bluntly pointed on the distal tip and slightly widened gradually to the proximal base (Fig. 4A). A reduced urethral groove is present on the bottom of the proximal half as an oval-shaped depression. Greatest length is ca. 0.45 mm, greatest width ca. 0.15 mm (n = 4 adults).

A

B

C

D

E

FIG. 4. Camera lucida tracings of bacula of selected Asiatic Myotis spp.: A -- M. badius sp. nov. (dorsal, ventral, lateral, ventro-lateral views); B -- M. siligorensis from Central Vietnam (ventral and left lateral views); C -- M. phanluongi (dorsal and left lateral views); D -- M. csorbai from Nepal (ventral and left lateral views); E -- M. muricola from Southern Vietnam (dorsal, ventro-lateral and left lateral views). Scale bar = 0.5 mm


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PC 1 FIG. 5. Bivariate scatterplot of the first two principal components, calculated on the basis of 16 cranial measurements for 64 specimens of Myotis. See Table 1 for eigenvalues and component loadings

(Wang, 2003). However, these two species differ in several features. The new species is a little larger than M. siligorensis: mean forearm length 36.8, condylo-canine length 11.3; vs. 33.9 and 10.5 mm in M. s. alticraniatus (our data) or 30.8 and 11.2 mm, in M. s. siligorensis (Bates and Harrison, 1997), respectively. Unfortunately, we have no available material from Thailand. However, according to original description (Shamel, 1942), M. s. thaianus is much smaller then M. badius (forearm 31.6 mm, CBL 11.0 mm) and with considerably narrower rostrum (M3M3 4.2 mm). Amongst named forms terra typica of M. s. sowerbi is closest to that of M. badius. Myotis s. sowerbi is of similar size, but based on Howell's (1926) original description it differs from the new species by darker coloration, lacking brown, and by distinctly longer tragi. Available specimens from Fujian have considerably longer rostral portions of the skull and the two males are smaller than males of M. badius in overall skull dimensions. The new species has shorter ears than M. siligorensis, not extending, when laid forward, to the anterior end of the muzzle. Average length of the calcar in the new species is about 13.0 mm (12.0­14.0, n = 14), while only 4­5 mm in M. siligorensis (Bates et al., 1999). The baculum of M. badius is generally similar to that of M. siligorensis but about half as wide in the proximal part and with a less pronounced depression on the ventral side. The new species differs from the similar-sized and recently described M. phanluongi in the shape of the baculum (Fig. 4) and in rostrum shape. Myotis phanluongi has a quite slender rostrum (Borisenko et al., 2008), while that of M. badius is distinctly wider and more robust.

PC 2

sp. nov. s. alticraniatus s. sowerbi phanluongi laniger annamiticus csorbai taiwanensis

Myotis badius differs from M. muricola in overall size, a less robust skull with a prominently concave frontal profile, distinctly smaller canine teeth and by the shape of its baculum. The baculum in M. muricola is much larger, wide, and saddleshaped, with a rounded tip and well developed

TABLE 1. Component loadings and other indices derived from the principal component analysis of 16 cranial measurements of 64 Myotis specimens. See text for measurement abbreviations Character CBL CCL W BCW BCH IOW WR LR CM3 PD P4M3 CC M3M3 LMD HMD MCM3 CBL CCL W BCW BCH IOW Eigenvalue % of total variance Principal component 2 0.001 0.057 -0.216 -0.044 -0.043 -0.050 0.938 0.877 -0.093 0.032 0.006 0.001 -0.118 0.023 -0.260 0.007 0.001 0.057 -0.216 -0.044 -0.043 -0.050 1.860 11.63

1 0.850 0.851 0.465 0.598 0.623 0.417 0.016 -0.066 0.900 0.081 0.808 0.688 0.461 0.485 0.662 0.815 0.850 0.851 0.465 0.598 0.623 0.417 10.190 63.72

3 0.106 0.161 0.007 0.148 0.048 -0.011 -0.209 0.341 0.095 0.973 -0.171 -0.136 -0.065 0.070 -0.169 0.123 0.106 0.161 0.007 0.148 0.048 -0.011 1.230 7.71


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urethral groove (Fig. 4E). The upper canine of M. muricola is proportionally longer and exceeds the third premolar (P4) in height (Bates et al., 1999; Borisenko and Kruskop, 2003). The newly described Myotis differs from M. annamiticus and M. csorbai by the location of attachment of the wing membrane and by the distinct shape of the baculum (Kruskop and Tsytsulina, 2001). The new species can be easily distinguished from M. csorbai, as well as from M. longipes and M. laniger, by the semi-nyctalodont lower molars. Unfortunately, we could not compare our specimens directly to another Chinese Myotis of similar size, M. davidi. According to available descriptions, the latter species also has a long calcar, as in M. badius. Myotis davidi appears to be distinct from the new species in having P3 reduced and displaced inward in the tooth-row and by a low, flattened braincase, as well as by smaller external size (Allen, 1938; Smith and Yan Xie, 2008). We have yet to provide any molecular-based comparison of the new species with its relatives. As can be seen from recent publications (Borisenko et al., 2008; Francis et al., 2010) genetic markers do not always segregate morphologically distinct forms within the `siligorensis' species group. Further investigation into the molecular characteristics of M. badius should be undertaken, using acceptable comparative sequences with selection of an adequate genetic marker. Habitat Myotis badius was captured in limestone caves at about 2,000 m a.s.l. These caves are situated at the edge of a limestone range, surrounded and partly covered with heavily disturbed semi-evergreen subtropical forest and scrubs. Other bat species found in association with M. badius in these caves include Rhinolophus sinicus, R. pusillus, Hipposideros armiger and M. laniger. A
CKNOWLEDGEMENTS

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LLEN,

We would like to express our thanks to Li Zhenxin, Jiang Tinglei and Shi Limin (College of Urban and Enviromental Sciences, Northeast Normal University, Changchun, China), T. A. Makarikova and V. E. Panasenko (Institute of Biology and Soil Science, FEB of the RAS, Vladivostok, Russia) for their assistance in the field. We are grateful to Dr. J. E. Eger (Royal Ontario Museum, Toronto, Canada), Dr. A. V. Borisenko and Dr. N. V. Ivanova (Biodiversity Institute of Ontario, Guelph, Canada) for permitting and shipment of some ROM collection materials used as comparison. Morphometric and morphological studies were undertaken with the support of RFBR grants 0904-00283-a and 10-04-00683-.


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M. P. Tiunov, S. V. Kruskop, and J. Feng ZHANG, Z., X. TAN, K. SUN, S. LIU, L. XU, and J. FENG. 2009. Molecular systematics of the Chinese Myotis (Chiroptera, Vespertilionidae) inferred from cytochrome-b sequences. Mammalia, 73: 323­330. Received 18 October 2010, accepted 07 December 2010

WANG, Y. X. 2003. A complete checklist of mammal species and subspecies in China: a taxonomic and geographic reference. China Forestry Publishing House, Beijing, 394 pp. [In Chinese].