Research Article |
Corresponding author: Xue-Long Jiang ( 13669718061@163.com ) Academic editor: Raquel López-Antoñanzas
© 2019 Quan Li, Xue-You Li, Stephen M. Jackson, Fei Li, Ming Jiang, Wei Zhao, Wen-Yu Song, Xue-Long Jiang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Li Q, Li X-Y, Jackson SM, Li F, Jiang M, Zhao W, Song W-Y, Jiang X-L (2019) Discovery and description of a mysterious Asian flying squirrel (Rodentia, Sciuridae, Biswamoyopterus) from Mount Gaoligong, southwest China. ZooKeys 864: 147-160. https://doi.org/10.3897/zookeys.864.33678
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The flying squirrels of the tribe Pteromyini (Family Sciuridae) currently include 15 genera of which the genus Biswamoyopterus comprises two recognized species, B. biswasi Saha, 1981 and B. laoensis Sanamxay et al., 2013. These two species were each described from only one specimen that are separated from each other by 1,250 kilometres in southern Asia, where they occur in northeast India and central Lao PDR respectively. In 2017 and 2018, two specimens of Biswamoyopterus were discovered from Mount Gaoligong, west Yunnan province, southwest China (between the type locality of the two recognized species). This study aimed to evaluate the taxonomic status of these two newly acquired specimens of Biswamoyopterus by comparing their morphology with the two described species of the genus. The results of this study showed that the specimens from Yunnan province (China) differed from both B. laoensis and B. biswasi in both pelage colour and craniology, and should be recognised as a distinct species, B. gaoligongensis sp. nov., which is formally described here. This study contributes to the understanding of the flying squirrels of southern Asia and identifies an additional species that appears to be endemic to southwest China; however, more research is required to provide details of its ecology, distribution, and conservation status.
Biodiversity, conservation, mammal, Pteromyini, systematics, taxonomy, threatened, wildlife, Yunnan
The flying squirrels of the tribe Pteromyini (Family Sciuridae) currently comprise 52 species of recent mammals that are placed in 15 genera. A number of fossil species have also been described and includes in several of the genera containing extant species as well as 13 additional extinct genera (
There is a gap of 1,250 km between the type localities of the two described Biswamoyopterus species (
Animals used for this study were approved by the Animal Ethics Committee of the Kunming Institute of Zoology, Chinese Academy of Sciences (approval ID: SMKX2018021).
ZSI Zoological Collection of the Zoological Survey of India, Kolkata [Calcutta], India.
NUoL Zoological collection of the Faculty of Environmental Sciences, National University of Laos, Vientiane, Lao PDR.
KIZ Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
Holotype
CHINA • 1♂, holotype of Biswamoyopterus gaoligongensis sp. nov., skin and skull available; Yunnan province, Baoshan city, Longyang county, Lujiang township, Baihualin village; 25.298N, 98.785E; 2040 m a.s.l.; Jan. 2017; Quan Li leg.; Broad-leaved evergreen forests; KIZ 034924 (field No. bs1628).
INDIA • 1♂, holotype of Biswamoyopterus biswasi, skin and skull available; Tirap District, Namdapha, 26 km east of Miao, Deban; ca. 350 m a.s.l.; Apr. 1981; Shyamrup Biswas leg.; collected from a tall Nahar tree (Mesua ferrea) at 20:15 pm; ZSI 20705.
LAO PDR • 1♀, holotype of Biswamoyopterus laoensis, skin and skull available; Bolikhamxai Province, Pak Kading District, Ban (village) Thongnami, Thongnami market (Purchased from the market by the collectors. The collectors speculated that the original collection site might be Nam Kading National Biodiversity Conservation Areas or Khammouan Limestone National Biodiversity Conservation Areas (NBCA), which is about 5 km Northeast of Thongnami and Khammouan Limestone NBCA, and about 25 km Southeast of Ban village); 18.172N, 104.24E; Sep. 2012; Daosavanh Sanamxay, Sysouphanh Xayavong, and Vilakhan Xayaphet leg.; NUoL FES.MM.12.163.
Paratype
CHINA • 1 sex unknown, paratype of Biswamoyopterus gaoligongensis sp. nov., skin of head and skull available; same locality as for KIZ 034924; Dec. 2018; a native of the area leg.; KIZ 035622 (field No. 201812001).
The external and craniodental measurements of type specimen of Biswamoyopterus biswasi and Biswamoyopterus laoensis were employed from the literature (
BB Breadth of braincase,
BH Braincase height,
CBL Condylobasal length,
DL Diastema length,
FL Frontal length,
GPB Greatest palatal breadth,
IBG Inter bullae gap,
IOB Interorbital breadth,
LAB Length of auditory bulla,
LBP Length of bony palate,
LIF Length of the incisive foramina,
MB Mastoid breadth,
MH Mandible height,
ML Mandible length,
MRTL Mandibular tooth row length,
MWN Maximum width of nasals,
MYTL Maxillary tooth row length,
NL Nasal length,
OB Orbit breadth,
ONL Occipitonasal length,
PL Palate length,
POB Postorbital breadth,
PPL Postpalatal length,
RB Rostrum breadth,
WAAM Width of auditory bullae across the external auditory meati,
WPFM Width of the bony palate at the first upper molar,
ZB Zygomatic breadth,
ZH Zygomatic height.
P Premolars,
M Molars;
Superscript (PX, MX) upper premolars and upper molars, and
Subscript (PX, MX) lower premolars and lower molars.
The nomenclature of cheek teeth structures followed
Pelage colour comparisons were made among all four available specimens. Skull and teeth were studied using a stereo binocular microscope. As only four skull specimens were available, statistical analysis was not possible.
Mount Gaoligong Flying Squirrel. Chinese common name "高黎贡比氏鼯鼠".
Specimen KIZ: 034924 (field number bs1628), an adult male, skull, dried skin, baculum, and remaining body part in alcohol deposited in the Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Science (KIZ).
Baihualin village [25.298167N, 98.784683E], Lujiang township, Longyang County, Baoshan City, Yunnan, China. The locality is located on the eastern slope of the southern Mount Gaoligong.
The specific name is derived from Mount Gaoligong, the type locality of the new species and –ensis, Latin for belonging to.
Biswamoyopterus gaoligongensis sp. nov. can be distinguished from the other two described species of Biswamoyopterus by the following combination of traits: 1) The ear tufts at the base of the posterior margins of ears are bicolored, basally white and terminal black. The scrotum is dark brown which strongly contrasts with the yellowish-white abdominal pelage. 2) The muzzle is very short, and the zygomatic arch is distinctly expanding outward, making the outline of the skull short and wide. The outer margin of the nasal bone, the orbital margin of the frontal bone, and the post-orbital margin of the frontal bone are almost parallel to the midline of skull on the dorsal view. The central point of the posterior margin of the palatal bones lies in front of the posterior margin of M3. 3) M1 and M2 are sub-square in outline, and as large as P4. The hypoconid of P4-M2 are very developed, strongly pointed towards posterior buccal side.
Biswamoyopterus gaoligongensis sp. nov. is a large flying squirrel (head and body length: 440 mm, tail length: 520 mm, and body mass: 1370 g) with a very developed uropatagium that extends approximately one-third of the proximal tail length in fresh specimen (Fig.
Skull is large with a short muzzle and an expanded outward zygomatic arch, making the outline of skull short and wide (Fig.
Skulls, left maxillary (above) and left mandibular (below) tooth rows of the three known Biswamoyopterus species. A (ZSI 20705, holotype) Biswamoyopterus biswasi B (KIZ 034924, holotype) Biswamoyopterus gaoligongensis sp. nov. C (NUoL FES.MM.12.163, holotype) Biswamoyopterus laoensis. The images of C were derived from
The anterior surface of incisors is pale yellow. Cheek teeth are strongly cuspidate brachyodont, with slightly pitted enamel.
Maxillary teeth: P3 is strong and unicuspid. Parastyle is prominent on P4 and dwindle on the following molars in an anterior to posterior gradient. Paracone is prominent on P4, M1, M2, and M3. Metacone is prominent on P4, M1, and M2, and indistinct on M3. Between protocone and metacone, at the exit of the middle valley of P4, M1, M2, and M3, there are two mesostyles form a projecting gutter. Protocone is prominent on P4, M1, M2, and M3. Hypocone is small, separated from protocone by a notch, distinct on M1 and M2, small on P4, and absent on M3. The anteroloph and posteroloph are indistinct on P4 and M3; distinct on M1 and M2, but they do not develop into a ridge as high as the protoloph and metaloph. A protoloph connecting the protocone with the paracone on M1, M2, and M3, and notched on P4. A metaloph connecting the protocone with the metacone on M2, interrupted by one big or two small metaconules on P4 and M1, and absent on M3.
Mandibular teeth: Four main cusps (protoconid, hypoconid, metaconid, and entoconid) are all distinct on P4, M1, M2, and M3. Mesoconid is present on the buccal side of P4, M1, M2, and M3, the notch between mesoconid and hypoconid is distinct, seems to be formed by the intense wear and tear. Mesostylid is small and fused with metaconid on P4 and M1, indistinct on M2 and M3.
Body size, B. gaoligongensis sp. nov. is similar to B. biswasi but clearly smaller than B. laoensis (Table
Body Mass (in grams), external and skull measurements (in mm) of four specimens of genus Biswamoyopterus.
Measurements | B. biswasi (ZSI 20705) | B. gaoligongensis sp. nov. (KIZ 034924) | B. gaoligongensis sp. nov. (KIZ 035622) | B. laoensis (NUoL FES.MM.12.163) |
---|---|---|---|---|
Body Mass | – | 1370.0 | – | 1800.0 |
Head and body length | 405.0 | 440.0 | – | 455.0 |
Tail length | 605.0 | 520.0 | – | 620.0 |
Hind feet length | 78.0 | 75.0 | – | 74.5 |
Ear length | 46.0 | 47.0 | 46.0 | 52.0 |
Occipitonasal length (ONL) | 72.40 | 69.75 | 71.11 | 74.39 |
Condylobasal length (CBL) | 70.10 | 66.37 | 67.73 | 70.99 |
Mastoid breadth (MB) | – | 30.72 | 33.50 | 30.79 |
Zygomatic breadth (ZB) | 47.50 | 48.41 | 48.30 | 47.72 |
Zygomatic height (ZH) | – | 4.61 | 4.58 | 4.86 |
Breadth of braincase (BB) | – | 33.86 | 34.46 | 32.84 |
Braincase height (BH) | – | 22.90 | 24.15 | 22.55 |
Rostrum breadth (RB) | – | 19.61 | 19.62 | 17.04 |
Nasal length (NL) | 20.90 | 19.35 | 20.70 | 22.57 |
Maximum width of nasals (MWN) | – | 13.15 | 12.51 | 13.37 |
Interorbital breadth (IOB) | 19.00 | 15.75 | 16.38 | 14.06 |
Postorbital breadth (POB) | – | 18.87 | 20.55 | 17.19 |
Length of the incisive foramina (LIF) | 6.40 | 5.65 | 5.86 | 5.85 |
Length of bony palate (LBP) | – | 20.08 | 22.01 | 23.83 |
Post palatal length (PPL) | – | 28.72 | 29.68 | 28.77 |
Length of auditory bulla (LAB) | 15.50 | 14.68 | 14.57 | 17.33 |
Width of auditory bullae across the external auditory meati (WAAM) | – | 35.88 | 36.76 | 35.96 |
Inter bullae gap (IBG) | – | 6.52 | 6.76 | 5.01 |
Maxillary tooth row length (MYTL) | 15.50 | 15.92 | 16.23 | 16.33 |
Greatest palatal breadth (GPB) | – | 18.26 | 18.61 | 19.37 |
Width of the bony palate at the first upper molar (WPFM) | – | 8.58 | 8.03 | 8.05 |
Mandibular tooth row length (MRTL) | – | 15.24 | 15.41 | 15.33 |
Mandible length (ML) | – | 44.44 | 46.53 | 45.36 |
Mandible height (MH) | – | 27.10 | 27.37 | 29.78 |
Palate length (PL) | 34.70 | 32.60 | 32.87 | – |
Diastema length (DL) | 15.70 | 13.70 | 15.03 | – |
Orbit breadth (OB) | 24.60 | 26.17 | 26.50 | – |
Frontal length (FL) | 28.60 | 27.66 | 30.63 | – |
Ear tufts of the three Biswamoyopterus species, the red arrow indicates the anterior tufts, and the yellow arrow indicates the posterior tufts A (ZSI 20705, holotype) Biswamoyopterus biswasi B (KIZ 034924, holotype) Biswamoyopterus gaoligongensis sp. nov. C (NUoL FES.MM.12.163, holotype) Biswamoyopterus laoensis. The image C was derived from
The muzzle of B. gaoligongensis sp. nov. is very short, B. biswasi is intermediate, and B. laoensis is much longer (Fig.
The posterior margin of the palatal bones relative to the posterior margin of M3 (dotted line) and shape of the preglenoid process (arrow) of the three Biswamoyopterus species A (ZSI 20705, holotype) Biswamoyopterus biswasi B (KIZ 034924, holotype) Biswamoyopterus gaoligongensis sp. nov., C (NUoL FES.MM.12.163, holotype) Biswamoyopterus laoensis. The image C was derived from
The metacone and hypocone of M1 and M2 of B. gaoligongensis sp. nov. are most developed among three species, followed by B. laoensis, again B. biswasi. As a result, M1 and M2 of B. gaoligongensis sp. nov. are almost equal to P4, while those of B. laoensis and B. biswasi are smaller than P4. In addition, the outline of M1 and M2 of B. gaoligongensis sp. nov. is sub-square, B. laoensis is sub-rectangle, and B. biswasi is sub-triangular. The hypoconid of B. gaoligongensis sp. nov. is strongest among three species, followed by B. biswasi, again B. laoensis (Fig.
Apart from the locality of the holotype, there are two more localities in Yunnan, China, where the Biswamoyopterus gaoligongensis sp. nov. was photographed. These include Linjiapu (25.28693N, 98.70102E), 10 km west of the type locality; and Banchang (25.145876N, 98.796026E), 9 km south of the type locality (Fig.
Little is known about the natural history of Biswamoyopterus gaoligongensis sp. nov. The holotype was collected from evergreen broad-leaved forest at an altitude of 2,000 meters above sea level. A set of photos taken in Linjiapu showed a Biswamoyopterus gaoligongensis sp. nov. resting on the branches of Daphniphyllum sp. Petaurista yunanensis, P. elegans, and Hylopetes alboniger were also collected in the same habitat where the holotype was collected.
The limited available information suggests that Biswamoyopterus gaoligongensis sp. nov. has a relatively low abundance. Because low-altitude forests inhabited by Biswamoyopterus gaoligongensis sp. nov. are close to human settlements, they are vulnerable to human activities. The currently known threats are agricultural reclamation and poaching.
1 | Pale orange belly and marked with numerous, black, discontinuous lines; ear tufts black; long muzzle; large auditory bulla; the posterior edge of the palatal bones is flat | Biswamoyopterus laoensis |
– | Light-coloured belly; ear tufts bicolour or white; short muzzle; smaller auditory bulla; the posterior edge of the palatal bones is concave forward | 2 |
2 | Parti-coloured tail with a dark tip; ear tufts white; the central point of the posterior margin of the palatal bones just meet the posterior margin of M3; the outline of M1 and M2 is sub-triangular; smaller hypoconid | Biswamoyopterus biswasi |
– | Black tail; ear tufts bicolour; the central point of the posterior margin of the palatal bones lies in front of the posterior margin of M3; the outline of M1 and M2 is sub-square; strong hypoconid | Biswamoyopterus gaoligongensis sp. nov. |
This study describes a third species of Biswamoyopterus in the middle of the isolated ranges of two previously known species, suggesting that the distribution of Biswamoyopterus is much broader than previously known. Although the genetic analysis within Biswamoyopterus was not available in this study, the morphological comparison shows that Biswamoyopterus gaoligongensis sp. nov. markedly differs from Biswamoyopterus biswasi and Biswamoyopterus laoensis in pelage colour and craniodental traits (Figs
Species | B. biswasi | B. gaoligongensis sp. nov. | B. laoensis |
---|---|---|---|
Size | Relatively small | Relatively small | Large |
Dorsal coloration | Morocco-red speckled with white | Reddish brown speckled with white | Dark reddish brown speckled with whitish-grey |
Ventral Coloration | White | Yellowish-white | Pale orange and marked with numerous, black, discontinuous lines |
Coloration of tail beyond the uropatagium | Pale smoky grey with a dark tip | Black | Black |
Ear tufts | White | The anterior tufts are black, and the posterior tufts are basally white and terminal black | Black |
Muzzle | Short | Shorter | Long |
Outer margin of the nasal bone, orbital margin of the frontal bone, and post-orbital margin of the frontal bone vs. midline of the skull | Inclined | Almost parallel | More inclined |
Postorbital processes | Large | Large | Relatively small |
Preglenoid process | Forward protruding | Almost flat | Almost flat |
Sutures of frontal and squamosal bone | Almost flat | Bulge | Almost flat |
Auditory bulla | Relatively small | Relatively small | Large |
Posterior margin of the palatal bones | Concave forward, the central point just meets the posterior margin of M3 | Concave forward, the central point lies in front of the posterior margin of M3 | Flat, the central point lies behind the posterior margin of M3 |
M1 and M2 | Feeble metacone and hypocone, outline of M1 and M2 is sub-triangular | Most developed metacone and hypocone, outline of M1 and M2 is sub-square | Second developed metacone and hypocone, outline of M1 and M2 is sub-rectangle |
M1 and M2 | Second developed hypoconid | Most developed hypoconid | Feeble hypoconid |
We thank Mr. Dazhou Peng, Mr. Jinlin Qian, and Mr. Chunliao Qian for their assistance in the field. We are grateful to Dr. Rong Li for identification of plant species, and Dr. Qigao Jiangzuo for some morphologic terms. We appreciate Baoshan Management Bureau of Gaoligongshan National Nature Reserve for their assistance in field work. Our research is supported by National Key Research and Development Program of China (#2017YFC0505202) and the Yunnan University “Double First-Class” Construction Program (C176240107).