Discovery and description of a mysterious Asian flying squirrel (Rodentia, Sciuridae, Biswamoyopterus) from Mount Gaoligong, southwest China

Abstract 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.gaoligongensissp. 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.


Introduction
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 (Jackson and Thorington 2012;Jackson and Schouten 2012;Koprowski et al. 2016). The genus Biswamoyopterus Saha, 1981 is the most recently described in the tribe and initially only included Biswamoyopterus biswasi Saha, 1981 based on a single specimen collected in Namdapha National Park, northeast India (Saha 1981). Biswamoyopterus biswasi was placed in its own genus by Saha (1981) as it was considered to exhibit a unique combination of characters that distinguish it from other genera including: 1) large body size, cylindrical tail, and well-developed uropatagium (tail membrane or interfemoral membrane) similar to Petaurista, Aeretes and Aeromys; 2) the presence of ear tufts similar to Belomys and Trogopterus; and 3) cuspidate brachyodont dentition similar to Hylopetes and Aeromys. In addition to these characters, Biswamoyopterus was recognised to have pale-yellow incisors similar to Aeromys and Eupetaurus (Corbet and Hill 1992). In reference to these characters, Sanamxay et al. (2013) described a second species of Biswamoyopterus (B. laoensis) based on a single specimen collected from central Lao PDR. So far, all knowledge of Biswamoyopterus comes from the morphological description of these two holotypes. As a result, the International Union for Conservation of Nature (IUCN) listed Biswamoyopterus biswasi as critically endangered due to hunting and habitat loss from logging (Molur 2016) and Biswamoyopterus laoensis as data deficient (Kennerley 2017).
There is a gap of 1,250 km between the type localities of the two described Biswamoyopterus species (Sanamxay et al. 2013). Western Yunnan, southwest China occurs between the two type localities of Biswamoyopterus (Fig. 1). In 2017 and 2018, two specimens of Biswamoyopterus sp. were collected in Mount Gaoligong (the watershed of the Irrawaddy River and the Nu River [Salween River]), west Yunnan ( Fig. 1) that appeared to have different pelage and cranial characters from the two described species of Biswamoyopterus. Therefore, the aim of this study was to: 1) undertake a detailed comparison of the specimens collected in Yunnan province, China with the two described species; and 2) if these Yunnan specimens proved to be distinct, formally describe and name a new species of Biswamoyopterus.

Ethics statement
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).

Morphological techniques
The external and craniodental measurements of type specimen of Biswamoyopterus biswasi and Biswamoyopterus laoensis were employed from the literature (Saha 1981;Sanamxay et al. 2013). External measurements of Biswamoyopterus sp. nov. were copied from the label tied on the specimen, included body mass, head and body length, tail length, hind feet length, and ear length. Craniodental measurements of Biswamoyopterus sp. nov. were taken with digital caliper to the nearest 0.01 mm; the mensural points follow Saha (1981) and Sanamxay et al. (2013) to facilitate the subsequent comparison (Fig. 2). A total of 28 craniodental measurements were used, including: Molars; Superscript (P X , M X ) upper premolars and upper molars, and Subscript (P X , M X ) lower premolars and lower molars.
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. Holotype. Specimen KIZ: 034924 (field number bs1628), an adult male, skull, dried skin, baculum, and remaining body part in alcohol deposited in the Kunming  Etymology. The specific name is derived from Mount Gaoligong, the type locality of the new species and -ensis, Latin for belonging to.

Class
Diagnosis. 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 postorbital 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 M 3 . 3) M 1 and M 2 are sub-square in outline, and as large as P 4 . The hypoconid of P 4 -M 2 are very developed, strongly pointed towards posterior buccal side.
Description. 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. 4). The back and upper surface of patagium are predominantly reddish brown, while the back between the shoulder and uropatagium is speckled with numerous white-tip furs that are absent from the head, shoulder, plagiopatagium, outer edge of uropatagium, limbs, and tail (Fig. 4). Similar to the shoulder, the head is reddish brown, but showing some yellowish grey in the crown. The ear is naked, with two bunches of long hairs (i.e., ear tufts) at the ear base, the anterior tufts are black, and the posterior tufts are basally white and terminal black. The back of each manus is reddish brown and the digits are black, while the whole pes and digits are black. The tail is cylindrical, the part beyond the uropatagium is black, and the part within the uropatagium is the same colour as the uropatagium. Throat, belly, and ventral surface of patagium are yellowish white. However, the scrotum is dark brown which strongly contrasts with the abdominal pelage.
Skull is large with a short muzzle and an expanded outward zygomatic arch, making the outline of skull short and wide (Fig. 5). The frontal depression is deep and postorbital processes are large and well developed. 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 auditory bullae are relatively large, with a honeycomb pattern of complex septae. The interpremaxillary foramen is well opened, which is not common in most flying squirrel genera. The mandible is generally similar to that of other flying squirrels. The coronoid process is less developed, only slightly higher than condylar process when the mandible is placed on a plane.
The anterior surface of incisors is pale yellow. Cheek teeth are strongly cuspidate brachyodont, with slightly pitted enamel.
Maxillary teeth: P 3 is strong and unicuspid. Parastyle is prominent on P 4 and dwindle on the following molars in an anterior to posterior gradient. Paracone is prominent on P 4 , M 1 , M 2 , and M 3 . Metacone is prominent on P 4 , M 1 , and M 2 , and indistinct on M 3 . Between protocone and metacone, at the exit of the middle valley of P 4 , M 1 , M 2 , and M 3 , there are two mesostyles form a projecting gutter. Protocone is prominent on P 4 , M 1 , M 2 , and M 3 . Hypocone is small, separated from protocone by a notch, distinct on M 1 and M 2 , small on P 4 , and absent on M 3 . The anteroloph and posteroloph are indistinct on P 4 and M 3 ; distinct on M 1 and M 2 , but they do not develop into a ridge as high as the protoloph and metaloph. A protoloph connecting the protocone with the paracone on M 1 , M 2 , and M 3 , and notched on P 4 . A metaloph connecting the protocone with the metacone on M 2 , interrupted by one big or two small metaconules on P 4 and M 1 , and absent on M 3 . Mandibular teeth: Four main cusps (protoconid, hypoconid, metaconid, and entoconid) are all distinct on P 4 , M 1 , M 2 , and M 3 . Mesoconid is present on the buccal side of P 4 , M 1 , M 2 , and M 3 , 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 P 4 and M 1 , indistinct on M 2 and M 3 .
Comparison. Body size, B. gaoligongensis sp. nov. is similar to B. biswasi but clearly smaller than B. laoensis (Table 1). Pelage colour becomes dark gradually from B. biswasi to B. gaoligongensis sp. nov. and to B. laoensis. The back, B. biswasi is morocco-red speckled with white, B. gaoligongensis sp. nov. is reddish brown speckled with white, and B. laoensis is dark reddish brown speckled with white. The belly, B. biswasi is white, B. gaoligongensis sp. nov. is yellowish-white, and B. laoensis is pale orange. The tail beyond uropatagium, B. biswasi is pale smoky grey, with a dark tip, both B. gaoligongensis sp. nov. and B. laoensis are black (Fig. 4). The ear tufts, B. biswasi are white, B. gaoligongensis sp. nov. are bicolour (the anterior tufts are black, and the posterior tufts are basally white and terminal black), and B. laoensis are black (Fig. 6).
The muzzle of B. gaoligongensis sp. nov. is very short, B. biswasi is intermediate, and B. laoensis is much longer (Fig. 5, Table 1). As a result, the outline of skull of B. gaoligongensis sp. nov. is short and wide, B. biswasi is relatively short, and B. laoensis appears    (Fig. 7). The metacone and hypocone of M 1 and M 2 of B. gaoligongensis sp. nov. are most developed among three species, followed by B. laoensis, again B. biswasi. As a result, M 1 and M 2 of B. gaoligongensis sp. nov. are almost equal to P 4 , while those of B. laoensis and B. biswasi are smaller than P 4 . In addition, the outline of M 1 and M 2 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. 5).  Distribution. 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. 1). Although these three localities cover the east and west slopes of Mount Gaoligong (the watershed of the Irrawaddy River and the Nu River [Salween River]), they are all restricted in a small area of southern Mount Gaoligong. Natural history. 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.
Conservation status. 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.

Discussion
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 bis-wasi and Biswamoyopterus laoensis in pelage colour and craniodental traits (Figs 4, 5; Table 2). Within the distribution of Biswamoyopterus and adjacent areas (Fig. 1), they occur sympatrically with a number of flying squirrels including Belomys pearsonii, Eupetaurus sp., Hylopetes alboniger, H. phayrei, Petaurista alborufus, P. caniceps, P. elegans, P. petaurista, P. philippensis, P. yunanensis and Trogopterus xanthipes (Jackson and Thorington 2012;Jackson and Schouten 2012). This high diversity of both genera and species may be the result of the region acted both as refugia and diversification centre since the late Miocene (Lu et al. 2013;Mercer and Roth 2003).