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Volume 79, Issue 2 (May 2015)

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First records of Murina lorelieae (Chiroptera: Vespertilionidae) from Vietnam

Vuong Tan Tu
  • MNHN, ISYEB UMR 7205, CP51, 55 rue Buffon, 75005 Paris, France
  • MNHN, UMS 2700, CP26, 43, rue Cuvier, 75005 Paris, France
  • Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, 18, Hoang Quoc Viet road, Cau Giay district, Hanoi, Vietnam
/ Raphaël Cornette
  • MNHN, ISYEB UMR 7205, CP51, 55 rue Buffon, 75005 Paris, France
  • MNHN, UMS 2700, CP26, 43, rue Cuvier, 75005 Paris, France
/ José Utge
  • MNHN, UMS 2700, CP26, 43, rue Cuvier, 75005 Paris, France
/ Alexandre Hassanin
  • Corresponding author
  • MNHN, ISYEB UMR 7205, CP51, 55 rue Buffon, 75005 Paris, France
  • MNHN, UMS 2700, CP26, 43, rue Cuvier, 75005 Paris, France
  • Sorbonne Universités, UPMC Univ Paris 06, UFR927, 75005 Paris, France
  • Email:
Published Online: 2014-06-07 | DOI: https://doi.org/10.1515/mammalia-2013-0101

Abstract

In 2011, three specimens from an unknown species of tube-nosed bat (genus Murina) were collected in montane moist forest at altitudes between 1117 and 1682 m in the Ngoc Linh Nature Reserve of Vietnam. We sequenced the mitochondrial COI gene from Ngoc Linh bats and performed comparisons with Murina sequences available in the nucleotide databases. The results suggested that the three unidentified specimens belong to Murina lorelieae, a species recently described from a single specimen collected in southern China. Nucleotide distances between specimens from Ngoc Linh and southern China are exceptionally low for M. lorelieae (1.25%) in comparison with three other Murina species, i.e., Murina cyclotis, Murina feae, and Murina huttoni (3.9–5.5%). We suggest that M. lorelieae is adapted to montane forests, which may have facilitated long-distance dispersal events between southern China and Vietnam during glacial periods of the Pleistocene. Morphological comparisons based on body-size measurements and geometric morphometric analyses of the skulls showed differences between Vietnamese specimens and the Chinese holotype of M. lorelieae. We proposed that the Vietnamese specimens belong to a distinct subspecies, M. lorelieae ngoclinhensis.

This article offers supplementary material which is provided at the end of the article.

Keywords: DNA barcode; morphology; Murininae; Southeast Asia; subspecies

Introduction

The subfamily Murininae includes the tube-nosed bats and hairy-winged bats of the three genera Murina, Harpiocephalus, and Harpiola (Kuo et al. 2006). The systematics of the genus Murina is regularly renewed since half of the species have been described in the past 10 years: Murina harrisoni (Csorba and Bates 2005), Murina tiensa (Csorba et al. 2007), Murina harpioloides (Kruskop and Eger 2008), Murina eleryi (Furey et al. 2009), Murina bicolor, Murina gracilis, Murina recondita (Kuo et al. 2009), Murina beelzebub, Murina cineracea, Murina walstoni (Csorba et al. 2011), Murina jaintiana, Murina pluviallis (Ruedi et al. 2012), Murina chrysochaetes, Murina lorelieae, Murina shuipuensis (Eger and Lim 2011), Murina annamitica, and Murina fionae (Francis and Eger 2012). However, the taxonomic status and geographical distribution of some species are highly controversial. For instance, Csorba et al. (2011) considered that Southeast Asian bats previously identified as Murina tubinaris should be split into two distinct species, Murina belzeebub or Murina cineracea, whereas Francis and Eger (2012) treated M. cineracea as a junior synonym of Murina feae.

In the end of the year 2011, a joint bat expedition between the Institute of Ecology and Biological Resources (IEBR) and Muséum national d’Histoire naturelle, (MNHN, Paris) took place in the Ngoc Linh Nature reserve in the Kon Tum province of Central Vietnam (Figure 1). During the expedition, three adult tube-nosed bats, one male and two females, were collected and identified as the same morphospecies. At first sight, their general appearance was similar to that of Murina cyclotis. However, external measurements and the detailed examination of both dorsal and ventral pelages suggested that these specimens belong to a species of Murina not recorded from Vietnam.

Figure 1

Geographic location of Ngoc Linh Nature Reserve (Kon Tum province, Vietnam) and photograph of the live specimen of Murina lorelieae ngoclinhensis ssp. nov. (holotype MNHN 2013-1078, ♂). The map was created using Online Map Creation (http://www.planiglobe.com).

Playing the important part of recent studies on bats, DNA barcoding was recognized as a useful taxonomic method to accelerate the discovery of new species (Francis et al. 2010). This approach is based on the comparisons of DNA sequences of the 5′ fragment of the mitochondrial cytochrome c oxidase subunit I (COI) gene. Fortunately, the COI sequences of almost all Indochinese species of Murina are available in the international nucleotide databases (EMBL/GenBank/DDBJ and BOLD). These data allow the rapid species identification of unknown specimens collected in this region.

Therefore, we sequenced the COI barcode fragment from tube-nosed bats collected in the Ngoc Linh Nature Reserve in order to make rapid comparisons with all COI sequences previously generated for Murina species. Then, we performed morphological comparisons among the four Murina species collected during our expedition in Ngoc Linh.

Materials and methods

Field survey

The Ngoc Linh (Kon Tum) Nature Reserve (geographic coordinates: 14°45′–15°15′N and 107°21′–108°20′E) covers an area of 41.42 km2 in the Kon Tum Plateau of the Central Highlands of Vietnam (Figure 1). Topologically, the region is composed mostly of mountainous and hilly terrain, including the second highest mountain in Vietnam, Mount Ngoc Linh (2598 m). The complex topology and climate of the region support a variety of vegetation types including lowland tropical rainforest at elevations <1000 m and montane tropical rainforest above an altitude of 1000 m. Despite the conversion of forest to agriculture in parts of the low altitude range of the nature reserve, Ngoc Linh retains a large area of undisturbed primary forest, mostly found at high elevations (Trai et al. 1999). These habitats contain high levels of biodiversity and endemism, many of those were recently described or are to be discovered (Bain and Nguyen 2004, Abramov et al. 2006, Kruskop et al. 2006, Jenkins et al. 2007, Orlov 2009).

Bats were captured in the field using four-bank harp traps in combination with several Ecotone mist nets. Bats were then measured, photographed, and initially identified following the field guides (Borissenko and Kruskop 2003, Francis 2008). All captured bats were adults as confirmed by the presence of fully ossified metacarpal-phalangeal joints.

DNA barcoding analyses

Total genomic DNA was extracted from muscle samples using QIAGEN DNeasy Tissue Kit (Qiagen, Hilden, Germany) following the manufacturer’s protocol with the final volume of 200 μl eluted DNA in AE buffer.

For this study, the 5′ fragment of the mitochondrial COI gene was amplified and sequenced with two primers: UTyr and C1L705 (Hassanin et al. 2012). The polymerase chain reactions (PCR) were carried out in a volume of 20 μl containing 3 μl of PCR buffer 10× with MgCl2, 2 μl of dNTPs (6.6 mm), 1 μl of each of two primers (10 μm), and 0.1 μl of Taq polymerase (2.5 U, Qiagen, Hilden, Germany). The PCR was run using the C1000 Touch thermal cycler (BIO-RAD) as follows: 4 min at 94°C; the denaturation/annealing/elongation process was set with 5 cycles of 30 s at 94°C, 60 s at 60°C, and 60 s at 72°C, followed by 30 cycles of 30 s at 94°C, 60 s at 50°C, and 60 s at 72°C. Final elongation followed for 5 min at 72°C. PCR products were purified using ExoSAP Kit (GE Healthcare, Buckinghamshire, UK) and then sequenced in both directions using an automated DNA Sequencer (Applied Biosystems 3100). These two last steps were performed at the Centre National de Séquençage (Genoscope) in Evry (France). Sequences were edited and assembled using Codoncode Alignment Version 3.7.1 (CodonCode Corporation).

The COI sequences newly generated (accession numbers KF772775–KF772784) were compared to those available in the EMBL/GenBank/DDBJ nucleotide databases. A phylogenetic tree of the genus Murina was reconstructed using the Bayesian method. The outgroup species were chosen on the basis of previous molecular studies on the subfamily Murininae (e.g., Ruedi et al. 2012). Accordingly, Myotis muricola and Kerivoula hardwicki were used as the most distant outgroup species to root the tree because they belong to two different subfamilies, Myotinae and Kerivoulinae, respectively. Two other species of different genera of the subfamily Murininae were also included in the analyses: Harpiocephalus harpia and Harpiola isodon (Simmons 2005, Kuo et al. 2006). DNA sequences were aligned manually on Se-Al v2.0a11 (A. Rambaut. Sequence Alignment Editor Version 2.0 alpha 11. 2002; http://evolve.zoo.ox.ac.uk/). The COI dataset represents a total alignment of 657 nucleotides and 108 taxa. The best-fitting model of sequence evolution was selected under jModelTest (Posada 2008) using the Akaike information criterion. Bayesian analyses were then conducted using the selected GTR+G model on MrBayes v3.2 (Ronquist et al. 2012). The posterior probabilities (PP) were calculated using four independent Markov chains run for 10,000,000 Metropolis-coupled MCMC generations, with tree sampling every 1000 generations, and a burn-in of 25%. Mean pairwise distances were calculated with PAUP version 4b10 (Swofford 2002) using Kimura’s two-parameter (K2P) model.

Morphological comparisons

External measurements (Table 1, Supplementary material 2) were taken from 10 living bats or museum specimens to the nearest 0.1 mm. Mass – the weight of bat in gram; all the following measurements were based primarily on Eger and Lim (2011): TL: total length – from the tip of the face/chin to the tip of the tail; FA: forearm length – from the elbow to the wrist with both joints folded; Tib: length of tibia – from the knee to the ankle; Ear: ear length – from the base of the ear, where it attaches to the head, to the tip of the pinna; Tragus: length of tragus – from the point where the proximal edge of the tragus joins the bottom of the ear to the tip of the tragus; HF: hind foot length – from the heel to the tip of the longest toe, including the claw; 3DM, 4DM, 5DM: length of third, fourth, and fifth metacarpals taken from the wrist to the end of the respective metacarpals; 3D1P, 3D2P, 4D1P, 4D2P, 5D1P, 5D2P: length of the first and second phalanges of the respective third, fourth, and fifth digits.

Table 1

External, cranial, and dental measurements (in mm, except mass in g) of the four specimens of Murina lorelieae: Murina lorelieae lorelieae from South China, Murina lorelieae ngoclinhensis from Vietnam (see Materials and methods for acronyms).

Cranial measurements (Table 1, Supplementary material 2) include GLS: greatest length of skull – from the posterior edge of the skull to the front of the incisors; CIL: condylo-incisive length – from the occipital condyles to the front of the incisors; PAL: palatal length – from the anterior palatal emargination to the midpoint of the posterior palatal emargination (with palatal spike, if present); ZB: zygomatic breadth – greatest width across the zygoma; MB: mastoid breadth – greatest breadth across the mastoids; BBC: braincase breadth – greatest breadth across the braincase; POC: postorbital constriction – the least breadth of the constriction posterior to the orbits; IC: least interorbital breadth – shortest distance between the orbits measured at the rostrum; CM3: length of maxillary toothrow – from the front of the canine to the posterior edge of the 3rd upper molar; M2M2: breadth across upper molars – greatest breadth measured across the outer edges of the second upper molars; CC: greatest breadth across the upper canines; ML: greatest length of mandible – greatest length measured from the posterior edge of the mandibular condyles to the front of the lower incisors; CM3: length of mandibular toothrow – from the front of the canine to the posterior edge of the 3rd lower molar; HCP: height of coronoid process – measured from the inferior surface of the angular process of the ramus to the tip of the coronoid process.

Landmark-based geometric morphometric analyses (Zelditch et al. 2012) were used to describe and quantify more accurately shape differences in skulls of Murina collected in Ngoc Linh. The holotype of Murina lorelieae was also included in the analyses. Two-dimensional coordinates were recorded using tpsDig2 (Rohlf 2010) on digital images of four datasets, representing lateral and ventral views of crania, and lateral and occlusal views of mandibles. The number and locations of landmarks are indicated in Supplementary materials 3–7. Morphometric analyses were computed using “Rmorph” (Baylac 2012) library in “R” (R Development Core Team 2011). Shape variations were estimated using General Procruste Analyses (GPA) (Rohlf and Slice 1990). The differences in shape were displayed using principal component analyses (PCA) and multivariate regressions along axes (Monteiro 1999). The first PCA axes obtained from each of the four datasets were extracted and then combined in a new PCA in order to synthesize our different results.

Results and discussion

Phylogenetic analyses based on COI DNA sequences

The Bayesian tree reconstructed from the nucleotide alignment of COI sequences is presented in Figure 2. The genus Murina appears as a paraphyletic group, due to the inclusive position of Harpiola, a genus sometimes considered as a subgenus of Murina (e.g., Simmons 2005). However, these deep relationships are not robust (PP<0.5), suggesting that additional molecular markers, including nuclear markers, should be sequenced for testing the monophyly of the genus Murina.

Figure 2

Bayesian tree of the subfamily Murininae reconstructed from the analysis of 108 DNA sequences of the mitochondrial cytochrome c oxidase subunit I gene. The values on the nodes indicate posterior probabilities.

All recognized species for which at least two specimens were sequenced were found to be monophyletic with maximum support values (PP=1): Murina aenea, Murina annamitica, Murina cyclotis, Murina eleryi, Murina feae, Murina fionae, Murina harrisoni, Murina hilgendorfi, Murina huttoni, Murina peninsularis, Murina suilla, Murina ussuriensis, and Murina walstoni. Maximal intraspecific distances in the species of Murina range from 0.4% in M. hilgendorfi to 6.9% in M. cyclotis. The smallest interspecific distance was found between Murina leucogaster and Murina shuipuensis, (2.6%), the species recently described in southern China (Eger and Lim 2011). However, all other distances between species of Murina range from 9% to 19.8% (see Supplementary material 1 for details). These distances are higher than those calculated in Kerivoulinae and Myotinae, two other subfamilies of Vespertilionidae (Francis et al. 2010). These comparisons suggest therefore that the mtDNA genome of Murininae is characterized by higher rates of nucleotide substitution.

Our mtDNA analyses indicate that the three unidentified specimens from Ngoc Linh are grouped into the same clade (PP=1), which is the sister group of Murina lorelieae (PP=1), a species recently described from a single male specimen collected in Diding Headwater Forest Nature Preserve in southern China (Eger and Lim 2011; hereafter referred to as Diding). The three Ngoc Linh specimens have identical COI sequences, and they differ from the Chinese holotype by only 1.25%, which is smaller than minimal intraspecific distances calculated between allopatric populations of Ngoc Linh and southern China for three other species of Murina, i.e., 4.84% for Murina cyclotis, 3.96% for Murina feae, and 3.38% for Murina huttoni(Table 2). The molecular data indicate therefore that Ngoc Linh specimens belong to Murina lorelieae. In addition, the low COI distances calculated between Vietnamese specimens and the Chinese holotype of M. lorelieae suggest that these allopatric populations were isolated from each other more recently than allopatric populations of the three other species of Murina (see below for a possible explanation).

Table 2

Nucleotide distances based on the Kimura 2-parameter (K2P) model between Murina species found in both Ngoc Linh Nature Reserve (Vietnam) and southern China.

Morphological comparisons

In the genus Murina, dentition differences are currently used as key characters for distinguishing two groups with no phylogenetic value (Corbet and Hill 1992, Koopman 1994): the “cyclotis group,” which contains 10 species, i.e., Murina cyclotis, Murina annamitica, Murina fionae, Murina harrisoni (including Murina tiensa), Murina huttoni, Murina lorelieae, Murina peninsularis, Murina pluvialis, Murina puta, and Murina rozendaali; and the “suilla group,” which includes 21 species, i.e., Murina suilla, Murina aurata, Murina beelzebub, Murina bicolor, Murina chrysochaetes, Murina eleryi, Murina feae (including Murina cineracea), Murina fusca, Murina gracilis, Murina harpioloides, Murina hilgendorfi, Murina jaintiana, Murina leucogaster, Murina recondita, Murina ryukyuana, Murina shuipuensis, Murina silvatica, Murina tenebrosa, Murina tubinaris, Murina ussuriensis, and Murina walstoni (Csorba et al. 2011, Eger and Lim 2011, Francis and Eger 2012, Ruedi et al. 2012). The three putative Vietnamese specimens of M. lorelieae exhibit the dental characteristics of the “cyclotis group”: the crown area of the first upper premolar (P2) represents about two thirds that of the second (P4); and both upper incisors (I2 and I3) are visible in lateral view (Figures 3 and 4). These features collectively serve to distinguish the new specimens from members of the “suilla group,” in which I2 is situated more anteriorly to I3, such that it is visible in lateral view, and the crown area of P2 is half or less that of P4 (see Figures 3A, 4A of M. feae for an example).

Figure 3

Lateral views (left) and occlusal views (right) of skulls of the four Murina species collected in Ngoc Linh Nature Reserve (Vietnam). (A) Murina feae (MNHN 2013-1080, ♀); (B) Murina cyclotis (IEBR-031211.1, ♂); (C) Murina lorelieae ngoclinhensis ssp. nov. (holotype MNHN 2013-1078, ♂); and (D) Murina huttoni (MNHN 2013-1082, ♂).

Figure 4

Front view of upper incisors (left) and occlusal views of upper left toothrows (right) of the four Murina species collected in Ngoc Linh Nature Reserve (Vietnam). (A) Murina feae (MNHN 2013-1080, ♀); (B) Murina cyclotis (IEBR-031211.1, ♂); (C) Murina lorelieae ngoclinhensis ssp. nov. (holotype MNHN 2013-1078, ♂); and (D) Murina huttoni (MNHN 2013-1082, ♂).

Within the “cyclotis group,” the three new specimens mostly resemble the holotype of Murina lorelieae by sharing similarity in both external and dental features. They have long shiny hairs (8 mm ventrally and 13–15 mm dorsally) with distinct colorations on dorsal and ventral surfaces, copper reddish-brown and dirty white, respectively (Figure 5). Dorsal hairs have a tri-colored pattern: dark gray at the base, pale in the middle, and reddish brown at the tip. The ventral underfur is bicolored: dark gray in about two thirds of the length and whitish at the tip (Figure 5). Dentally, I2 and I3 are slightly equal in height in frontal view. The mesostyles of M1 and M2 are well developed. The canines (upper and lower) are longer than the second premolars (Figures 3 and 4). These features also distinguish the three specimens from other members of the “cyclotis group.” For instance, the pelage of Murina annamitica is very similar to that of the new putative materials of M. lorelieae, but in this species, P2 and P4 are equal in height, and I2 significantly exceeds I3 in height (Francis and Eger 2012).

Figure 5

Pelage and detailed pattern of hairs (scale=5 mm) on ventral (top) and dorsal (bottom) surfaces of the four Murina species collected in Ngoc Linh Nature Reserve (Vietnam). From left to right: (A) Murina feae (MNHN 2013-1080, ♀); (B) Murina cyclotis (IEBR-Tu031211.1, ♂); (C) Murina lorelieae ngoclinhensis ssp. nov. (holotype MNHN 2013-1078, ♂); and (D) Murina huttoni (MNHN 2013-1082, ♂).

The morphological comparisons of the three Vietnamese specimens of Murina lorelieae suggest the existence of a sexual size dimorphism in favor of females, as it is generally observed in other species of Murina (data from Kuo et al. 2009, Francis and Eger 2012). The male collected in Ngoc Linh is larger than the holotype of M. lorelieae, with a bigger body mass (5 vs. 4 g), and longer forearms (33 vs. 31 mm), tibia (19 vs. 14.6 mm), and skull (GLS: 16.23 vs. 15.5 mm) (Table 1). However, such variations in body size measurements (±10–20%) were previously mentioned in a few other species of the “cyclotis group,” such as Murina cyclotis and Murina harrisoni (Francis and Eger 2012). In addition, the skull’s shape of Ngoc Linh specimens of M. lorelieae (Figure 3) differs from that of the Chinese holotype. In lateral view, it is elongate and gradually rises from the rostrum to the forehead. By contrast, the skull of the Chinese holotype is characterized by an abruptly rising profile (Eger and Lim 2011). To better characterize the differences in skull shape, we performed landmark-based geometric morphometric analyses. Figure 6 shows the PCA constructed using the first PCA axes obtained from each of the four datasets corresponding to lateral and occlusal views of mandible, and lateral and ventral views of cranium (Supplementary materials 3–7). The first PCA axis tends to separate Murina huttoni from Murina feae. The differences in shape variation are mainly explained by the lateral view of the cranium (correlation: 0.89) and the two views of the mandible (correlations of 0.92 and 0.90 for lateral and occlusal views, respectively). The second PCA axis tends to separate M. lorelieae, and especially the holotype, from other species of Murina. The differences in shape variation are mainly explained by the ventral view of cranium (correlation: 0.97). The results show therefore that the four species collected in Ngoc Linh can be distinguished on the basis of their skull shape. In addition, the three Vietnamese specimens of M. lorelieae have a very similar shape, which differs from that of the Chinese holotype of M. lorelieae.

Figure 6

Principal component analysis based on geometric morphometric analyses of the skulls of the four Murina species collected in Ngoc Linh. The Chinese holotype of Murina lorelieae was also included in the analyses.

Our morphological comparisons have therefore revealed important differences in body size and skull shape between the Vietnamese specimens and the Chinese holotype of M. lorelieae. Hence, we propose that the Ngoc Linh specimens of M. lorelieae belong to a different subspecies, hereafter named “ngoclinhensis.”

Murina lorelieae ngoclinhensis Tu and Hassanin, ssp. nov.

Holotype

MNHN 2013-1078 (Field number VN1563, tissue code VN11-1220), adult male, in alcohol skull removed, collected 3 December 2011 by Alexandre Hassanin and Vuong Tan Tu. Mass: 5 g. Measurements (in mm) for the holotype are as follows: FA: 33.00; Tib: 19.00; Ear: 14.00; Tragus: 8.08; 3DM: 30.19; 4DM: 29.03; 5DM: 29.07; 3D1P: 14.17; 3D2P: 12.81; 4D1P: 10.48; 4D2P: 9.04; 5D1P: 11.07; 5D2P: 10.80; GLS: 16.23; CIL: 14.57; ZB: 8.83; MB: 7.65; BBC: 7.40; POC: 4.30; IC: 5.20; CM3: 5.34; M2M2: 5.50; CC:3.87; ML: 10.84; CM3: 5.64; HCP: 4.23. The sequence of the mitochondrial gene COI has been deposited in the EMBL/GenBank/DDBJ nucleotide databases with accession number KF772780.

Type locality

Ngoc Linh Nature Reserve, Kon Tum province, Vietnam. 15°03.884 N, 107°49.888 E, elevation 1682 m a.s.l.

Paratypes

  • IEBR-Tu281111.1 (Field number VN1504 – tissue code VN11-1161), Ngoc Linh Nature Reserve, Kon Tum, Vietnam, 15°04.766 N; 107°49.833 E, elevation 1117 m a.s.l., adult female, in alcohol skull removed, collected 28 November 2011 by Alexandre Hassanin and Vuong Tan Tu, accession number of COI sequence: KF772779.

  • MNHN 2013-1079 (Field number VN1566, tissue code VN11-1223), Ngoc Linh Nature Reserve, Kon Tum, Vietnam, 15°03.884 N, 107°49.888 E, 1682 m a.s.l., adult female, in alcohol skull removed, collected 3 December 2011 by Alexandre Hassanin and Vuong Tan Tu, accession number of COI sequence: KF772781.

Etymology

The name “ngoclinhensis” is derived from the Mount Ngoc Linh of the Ngoc Linh Nature Reserve, Kon Tum province, Vietnam, from which all specimens of this subspecies were collected.

Diagnosis

Murina lorelieae ngoclinhensis is externally similar to the typical form, M. l. lorelieae, but significantly larger in body size (Table 1). In addition, the skull shape of the new subspecies is elongate and gradually rises from the rostrum to the forehead (Figure 3), while that of the holotype is characterized by an abruptly rising profile.

Description

This is a small bat species, generally similar to Murina lorelieae lorelieae (Table 1). The pelage is characterized by long shiny hairs (8 mm ventrally and 13–15 mm dorsally), with distinct colorations on dorsal and ventral surfaces, copper reddish-brown and dirty white, respectively. Dorsal hairs are tricolored: dark gray basally, pale in the middle and reddish brown at the tip. Ventral hairs are bicolored: dark gray in about two thirds of the length and whitish at the tip (Figure 5). The skull is domed. The lateral profile of the anterior part of the skull gradually rises from the rostrum to the forehead (Figure 3). The sagittal crest is lacking; the lambdoid crests are visible. The maxillary toothrows are convergent anteriorly (Figure 3). The dentition is quite robust. The second upper incisor (I3) is situated posterior to the first (I2), and I2 is visible laterally. I2 and I3 are subequal in height (Figure 4) and are much less than half the height of the upper canine (C1). Upper (C1) and lower (C1) canines are well developed, exceed the height and subequal the basal areas of the corresponding second premolar (P4 and P4). The crown area and the height of the first upper premolar (P2) are two thirds more than those of P4 (Figures 3 and 4). The first (M1) and second (M2) upper molars have well-developed mesostyles and curved labial (outer) faces (Figure 4). The paracone, metacone, and protocone of the first (M1) and second (M2) upper molars are distinctly defined.

Distribution, ecological notes, and conservation status

All three specimens of Murina lorelieae ngoclinhensis were collected in harp traps that were set across the paths or trails in the wet montane evergreen forest at altitudes between 1117 and 1682 m. At this elevation, the climate is different from that found in elevations lower than 500 m: it is cool and humid in daytime and much colder and foggy at nighttime. At the studied site, the forest was fairly undisturbed with good vegetation coverage and abundant banana trees in some slopes nearby small streams.

The comparisons of hairs between the four Murina species found in Ngoc Linh showed that Murina lorelieae has a much longer fur, especially on the dorsum (Figure 5). Possessing long hairs might be regarded as an adaptation to mountain climate, as it has been observed in other bat species of high elevations, such as the long-haired rousette (Stenonycteris lanosus) in Africa or Blanford’s fruit bat (Sphaerias blanfordi) in South Asia (Bates et al. 2008, Mickleburgh et al. 2008). Since all specimens of M. lorelieae were collected at high elevations, 976 m in Diding (southern China) and over 1100 m in Ngoc Linh, we therefore suggest that M. lorelieae is a montane forest dweller.

The finding of Murina lorelieae in Ngoc Linh, at approximately 1000 km south from the type locality, suggests that M. lorelieae might be a widespread species. Therefore, the species is likely distributed in relatively intact montane forests of the Annamite Range, the mountain range of eastern Indochina that extends approximately 1200 km from around 20° N, along the border between Vietnam and Lao PDR, and until the Da Lat Plateau in south-central Vietnam (Sterling and Hurley 2005). In this mountain range, rainfall varies annually between 1500 and 3850 mm, and the mean annual temperature is about 20°C (http://wwf.panda.org/). These conditions are similar to those found in Diding Headwater Forest Nature Preserve in southern China, with 1660 mm of mean annual precipitation, and 23°C of annual mean temperature (Robbins et al. 2006).

In Diding, Murina lorelieae was collected with six other species of Murininae: Murina chrysochaetes, Murina cyclotis, Murina eleryi, Murina feae, Murina leucogaster, and Harpiocephalus harpia (Eger and Lim 2011). In Ngoc Linh, Murina lorelieae occurred with four other species of Murininae: M. cyclotis, M. feae, Murina huttoni, and Harpiola isodon. As indicated previously, the smaller nucleotide distance calculated between Ngoc Linh and Diding specimens of M. lorelieae shows that these allopatric populations were isolated from each other more recently than in other species Murina (M. cyclotis and M. feae). Such result suggests that M. lorelieae had a stronger ability to disperse over long distances during the Pleistocene. During the Last Glacial Maximum, from 26,500 to 19,000 years ago (Clark et al. 2009), climatic conditions became cooler and drier in Southeast Asia. As a consequence, montane forests descended to lower elevations and expanded, whereas the distribution of lowland rainforests contracted into a few glacial refugia (Cannon et al. 2009, Woodruff 2010, Turner and Cernusak 2011). Each of the glacial periods probably showed a similar pattern and caused the expansion of montane forests and the contraction of lowland forests. During glacial episodes, populations of the widespread bat species preferring lowland rainforests were affected by forest fragmentation and restricted to a few refugia. By contrast, populations of bat species adapted to montane forests, such as M. lorelieae, are thought to have expanded. This biogeographic scenario may explain a higher capacity for long-distance dispersal in M. lorelieae than in other species of the genus Murina.

This species is the 13th recently recognized Vietnamese Murininae (Hendrichsen et al. 2001, Csorba et al. 2007 Csorba et al. 2011, Kruskop and Eger 2008, Furey et al. 2009, Francis and Eger 2012). This record continually supports that the area of Mount Ngoc Linh of the Annamite Range is a regional hotspot for biodiversity and endemism (Sterling and Hurley 2005), and Indochina hosts the highest diversity of the subfamily Murniniae (Francis and Eger 2012). As a resident of montane forests, Murina lorelieae might temporarily avoid the threats affecting bats found in lowland habitats, even though the high rate of habitat loss or disturbance in Vietnam during the recent years was regarded as a major threat to the national biodiversity (Meyfroidt and Lambin 2008, Tordoff et al. 2012). In this context, efforts should be made to conserve the remaining high biodiversity areas of the country.

Acknowledgments

In Vietnam, we would like to thank Nguyen Xuan Nghia and local guides for their help in the field and Dinh Quoc Thang and other staffs of Ngoc Linh Nature Reserve for their support during the field survey. We are grateful to other colleagues of the Institute of Ecology and Biological Resources in Hanoi for administrative assistance in Vietnam. The PhD scholarship to study in France of Vuong Tan Tu was supported by the Vietnamese Ministry of Education and Training and the French government (through Campus France Agency and “CROUS de Paris”). The research was taken place under the administrative permissions of the People’s Committee of Kon Tum, Vietnam and the Vietnam Administration of Forestry of the Vietnamese Ministry of Agriculture and Rural Development. This research was supported by the “ATM Barcode” funded by the MNHN, and the network “Bibliothèque du Vivant” funded by the CNRS, the MNHN, the INRA and the CEA (Genoscope). We thank Stéphane Aulagnier and two anonymous reviewers for helpful comments on the manuscript.

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Corresponding author: Alexandre Hassanin, Muséum national d’Histoire naturelle (MNHN), Institut de Systématique, Evolution, Biodiversité (ISYEB), UMR 7205, CP51, 55, rue Buffon, 75005 Paris, France; Sorbonne Universités, UPMC Univ Paris 06, UFR927, 75005 Paris, France; and MNHN, UMS 2700, CP26, 43, rue Cuvier, 75005 Paris, France, e-mail:


Received: 2013-07-02

Accepted: 2014-04-30

Published Online: 2014-06-07

Published in Print: 2015-05-01



Citation Information: Mammalia, ISSN (Online) 1864-1547, ISSN (Print) 0025-1461, DOI: https://doi.org/10.1515/mammalia-2013-0101. Export Citation

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