Petaurista philippensis ( Elliot, 1839 )

Koli, Vijay Kumar, 2022, Petaurista philippensis (Rodentia: Sciuridae), Mammalian Species 54 (1019), pp. 1-10 : 1-5

Petaurista philippensis ( Elliot, 1839)

Indian Giant Flying Squirrel

Pteromys philippensis Elliot, 1839:217 . Type locality “Mahratta of the Ghats,” India.

Pteromys oral Tickell, 1842:401. Type locality “Jungle Mehals and Singhbhum,” Jharkhand, India.

Pteromys griseiventer Gray, 1843:133 . Type locality “ India.”

Pt. petaurista (?) var. cineraceus Blyth, 1847:865 . Type locality “Arracan and Tenasserim provinces;” Burma.

Pteromys grandis Swinhoe, 1862:358 . Type locality “Island of Formosa [= Taiwan];” China.

Pteromys yunanensis Anderson, 1875:282 . Type locality “Neighbourhood of Zeugyechen, Yunnan,” China.

Pteromys lylei Bonhote, 1900:192 . Type locality “Doi Sritepe, Chingmai, Siam [= Thailand].”

Pataurista philippensis : Wroughton, 1911:1015. First use of current name combination; incorrect subsequent spelling of Petaurista Link, 1795 .

Petaurista philippensis : Wroughton, 1911:xxxi. Corrected spelling for Pataurista philippensis : Wroughton, 1911:1015.

Petaurista lanka Wroughton, 1911:1017 . Type locality “ Ceylon [= Sri Lanka].”

Petaurista cinderella Wroughton, 1911:1018 . Type locality “Dangs, Surat District, Bombay Presidency;” India.

Petaurista lylei venningi Thomas, 1914a:26 . Type locality “Kalaw, west of Taunggyi, alt. 4,700’;” Burma.

Petaurista mergulus Thomas, 1922:1067 . Type locality “Ross Island, Mergui Archipelago;” Burma.

Petaurista lylei badiatus Thomas, 1925:501 . Type locality “Ngai-Tio, Central Tonkin;” Vietnam.

Petaurista petaurista rufipes Allen, 1925:13 . Type locality “Yungan, Fukian Province, China.”

Petaurista hainana Allen, 1925: 14 . Type locality “Nam Fong, Island of Hainan, China.”

Petaurista mergulus reguli Thomas, 1926:22 . Type locality “King Island, Mergui Archipelago,” Burma.

Petaurista rubicundus Howell, 1927:82 . Type locality “Mapientung, Szechwan, China.”

Petaurista cineraceus stockleyi Carter, 1933:1 . Type locality “Melamoong, northwestern Siam [= Thailand], 2000 feet.”

Petaurista lylei miloni Bourret, 1942:28 . Type locality “Milon at Diem-her, Lang-son Province,” Tonkin, Vietnam.

Petaurista petaurista nigra Pang and Wang, 1981:169 . Type locality “Chiching (alt 1,900m) of Gaoligong Mountains, Gongshan Xian, northwestern Yunan,” China.

CONTEXT AND CONTENT. Order Rodentia , suborder Sciuromorpha , family Sciuridae , subfamily Sciurinae , tribe Pteromyini , genus Petaurista . Five subspecies are currently recognized ( Wilson and Mittermeier 2019; Burgin et al. 2020):

P. p. annamensis Thomas, 1914b:204. See above.

P. p. cineraceus ( Blyth, 1847) : 865. See above.

P. p. lylei ( Bonhote, 1900) :192. See above.

P. p. mergulus Thomas, 1922:1067 . See above.

P. p. philippensis ( Elliot, 1839) :217. See above.

NOMENCLATURAL NOTES. Common names associated with Petaurista philippensis are the Indian giant flying squirrel and large brown flying squirrel ( Fig. 1 ). It was originally assigned to the genus Pteromys based on the first holotype ( Elliot 1839). Following that, different specimens of large flying squirrels from various locations in southeastern Asia were described as distinct species of Petaurista due to variation in pelage coloration ( Wroughton 1911; Thomas 1914a, 1914b, 1922, 1925, 1926; Allen 1925; Howell 1927; Carter 1933; Bourret 1942). Some authors ( Swinhoe 1862; Allen 1925; Pang and Wang 1981) recognized P. philippensis as a subspecies of Petaurista petaurista , the red giant flying squirrel, before Corbet and Hill (1991, 1992) separated P. philippensis as a distinct species, which was further supported by morphological and genetic studies ( Corbet and Hill 1992; Oshida et al. 2000a, 2000b, 2004; Yu et al. 2006; Song et al. 2012). The genus Petaurista diverged from the genus Pteromys about 16 million years ago in the Miocene epoch ( Mercer and Roth 2003). Petaurista philippensis belongs to an older lineage that split about 5 million years ago from Hainan giant flying squirrel, P. hainana , and 4.3 million years ago from the red and white giant flying squirrel, P. alborufus , and shares similar cladistic features with P. petaurista ( Yu et al. 2006) .

DIAGNOSIS

Petaurista philippensis is the second largest member of the genus Petaurista , the largest member of the genus is P. nobilis , the Bhutan giant flying squirrel. Petaurista nobilis has a distinct bright orange-buff area on the forehead which is absent in P. philippensis and they do not occur in sympatry. Petaurista philippensis differs from the sympatric species, P. petaurista , P. yunanensis , and P. hainan primarily by having a longer skull (mean greatest length of skull 79.10 ± 2.01 SD mm versus <77.16 ± 2.73) and condylobasal region (mean condylobasal length = 73.93 ± 2.14 SD mm versus <71.55 ± 2.51— Song et al. 2012). There are also coloration differences. Petaurista philippensis has a uniformly dark gray or black coat that is grizzled with white, whereas P. petaurista has a reddish brown coat with less extensive grizzling. The pelage of the ventral surface of P. philippensis is gray to buff, with brown or dark gray margins on the ears. The color of the head matches the rest of the body. In mature P. philippensis the tail is dark brown, black, or gray, sometimes with a black tip. The tail in P. petaturista is yellow to orange with a dark tip ( Thorington et al. 2012; Menon 2014). The anterior one-half of the ear is white in P. petaurista but brownish-orange to gray in P. philippensis ( Sanamxay et al. 2015) . Petaurista philippensis has thinner hair on the venter (29.5 ± 0.15 μm) and head (43.6 ± 0.50 μm) than P. petaurista (50.0 ± 0.0 μm and 60.0 ± 0.1 μm, respectively— Bahuguna 2011). Petaurista philippensis has longer skull than P. petaurista and all cranial measurements show a significant difference between these two species ( Song et al. 2012).

GENERAL CHARACTERS

Depending on geographical location and seasonal changes, the pelage color of Petaurista philippensis ranges from brownish-grizzled white or dark gray to black. The underparts are white, but rufescent in Taiwan. The eyes are round and black, and the vibrissae are dark and prominent. The tail is brown or gray to black, except the ventral surface of the tail base, which is gray. The tail tip is sometimes black ( Thorington et al. 2012). The ears are almost hairless. The body color of P. philippensis varies as it ages ( Hutton 1949). Its tail and feet are jet black during its juvenile stage with a black band over its shoulders and a white and light-gray underside ( Hutton 1949). The fur thickens during the monsoon season, and thins during the dry season ( Hutton 1949). Ramakrishnan et al. (2016) reported a melanistic specimen from Sathyamangalam Tiger Reserve, India. External sexual dimorphism is lacking; hence, sex identification is possible only by carefully examining the genitalia ( Koli and Bhatnagar 2014).

The front foot has three toes and two subequal metacarpal pads. The hind foot has four toe pads, a large metatarsal pad, and one small supplementary pad behind the outer toe pad. The length of the hind foot is 83.42 ± 7.74 (mean ± SD) mm (range 65–100), and the length of the ear is 49.21 ± 4.20 (mean ± SD) mm (range 42–58— Thorington and Heaney 1981). The tail is bushy and longer than the length of the head–body. Females have two pectoral and four inguinal mammae ( Jerdon 1867; Blanford 1891; Wroughton 1911; Xavier et al. 1998). The gliding membrane is made up of three parts: the propatagium (between the head and wrist), the plagiopatagium (between the forelimb and hind limb), and the uropatagium (between the hind limbs and tail). The uropatagium of this genus is proportionately larger than that of the other gliding squirrel genera ( Glaucomys Thomas, 1908 , Petinomys Thomas, 1908 , and Pteromys G. Cuvier, 1800 — Johnson-Murray 1977).

The mean body mass (g) of adult females is greater and more variable (1,335 ± 135 SD g) than that of adult males (1,260 ± 122 SD g), but other body measurements, such as body length (combined mean 378 mm), tail (combined mean 459 mm), ear (combined mean 73 mm), hind foot (combined mean 47 mm), and styliform cartilage (combined mean 88 mm), did not differ ( Lee et al. 1993a).

The skull morphometry ( Fig. 2 ) of P. philippensis differs from other Petaurista , primarily by being longer in skull and condylobasal lengths ( Song et al. 2012). Cranial dimensions (mm, mean ± SD; range) in 21 adult specimens were: maximum length of skull 79.10 ± 2.01 (75.35–82.71); condylobasal length 73.93 ± 2.14 (69.10–77.75); basal length 68.60 ± 2.09 (64.44–72.39); occipitonasal length 78.70 ± 2.08 (74.96– 82.77); palatal length 41.82 ± 1.47 (39.11–43.80); length of palatal bridge 28.10 ± 1.32 (26.13–30.64); length of upper toothrow 38.94 ± 1.13 (37.27–40.77); length of upper molars 12.46 ± 0.47 (11.67–13.29); maximum breadth of upper molars 20.43 ± 0.79 (19.07–22.57); rostral length 17.63 ± 0.81(16.05– 18.93); rostral breadth 16.56 ± 0.72 (15.36–18.11); length of auditory bulla 14.81 ± 0.67 (13.73–15.76); breadth of auditory bulla 11.18 ± 0.48 (10.50–12.41); breadth of zygomatic plate 11.18 ± 0.48 (10.50–12.41); breadth of occipital condyles 18.58 ± 0.88 (17.48–20.22); height of occipital 8.53 ± 0.57 (7.47–9.57); zygomatic breadth 51.42 ± 1.72 (46.48–54.73); mastoid breadth 30.05 ± 1.31 (27.71–32.11); nasal length 24.34 ± 1.46 (21.98–27.34); nasal breadth 15.30 ± 0.96 (13.53– 17.40); mandible length 54.82 ± 1.33 (52.31–57.68); height of mandible 32.23 ± 1.23 (29.61–34.64); length of lower diastema 10.82 ± 0.65 (9.42–11.94); length of lower molar row 14.03 ± 0.56 (13.16–15.37); length of lower toothrow 36.99 ± 1.18 (34.98–39.89); mandibular height 12.31 ± 0.52 (11.02–12.95— Song et al. 2012).

Cranial measurements (mean ± SD mm) for nine P. philippensis of unknown sex from Yunnan, China were: cranial length 77.21 ± 2.13; braincase length 56.30 ± 1.76; cranial width 37.64 ± 1.30; zygomatic arch width 52.02 ± 2.61; postorbital constriction 19.34 ± 1.07; distance between base of the anterior surface of post-glenoid process and M3 32.04 ± 1.38; nasal length 24.86 ± 1.38; length of tympanic bullae 14.7 ± 0.73; diastema length 17.07 ± 0.89; length of maxillary toothrow 18.09 ± 0.74; width of maxillary toothrow at M 2 20.55 ± 1.05; maximum mandible length 50.71 ± 1.70; maximum height of mandible 32.76 ± 0.59; length of mandibular toothrow 17.82 ± 2.91 ( Yu et al. 2006).

DISTRIBUTION

Petaurista philippensis is distributed in southern China, Taiwan, India, Sri Lanka, Myanmar, Thailand, Laos, and Vietnam, and has the most widespread geographic range of any flying squirrel in the tropical and subtropical zones of southeastern Asia ( Fig. 3 ; Wilson and Mittermeier 2019). It is found at high densities between 50 and 500 m of elevation and in habitats ranging from lowland forests to mountains, but has never been recorded above 2,200 m ( Nandini 2001a; Yu et al. 2006; Koli et al. 2013a).

In India, P. philippensis is found in large forests (evergreen, semi-evergreen, tropical deciduous, tropical rainforest or subtropical rainforest, subtropical dry deciduous, subtropical moist deciduous forests, temperate mixed forest, and plantations near forest areas) of the Peninsula and south of the Ganges River ( Ashraf et al. 1993; Umapathy and Kumar 2000; Nandini 2001a, 2001b; Molur et al. 2005; Prater 2005; Koli et al. 2013a; Sharma and Sharma 2013; Koli 2016). It has a patchy distribution in western and central India ( Molur et al. 2005; Sharma 2007; Das 2012; Koli 2012; Koli et al. 2013a; Singh and Dharaiya 2021), and it is found in and around Madhuca indica (oil nut or butter nut) groves and belts ( Sharma 2007; Koli et al. 2013a; Sharma and Sharma 2013). In the southern peninsula it is present in the Western Ghats Mountains and a few localities in the Eastern Ghats ( Ashraf et al. 1993; Umapathy and Kumar 2000; Nandini 2001a, 2001b; Molur et al. 2005; Kumara and Singh 2006; Polimati and Aditya 2021). The key factors affecting its regional scale distribution include tree density, large trunk girth, canopy height, and canopy cover ( Babu et al. 2015). It is found in highly disturbed and degraded forests of Andhra Pradesh ( Sreekar et al. 2012), and in forest edges of the Western Ghats ( Nandini and Parthasarathy 2008).

In China, P. philippensis is present in southern and central provinces, including Hainan, Yunnan, Sichun, and Shaanxi ( Yu 2002; Smith and Xie 2008). In Taiwan, it is found in broadleaf hardwood forests and secondary conifer plantations at elevations ranging from 300 to 2,200 m ( Lee et al. 1986, 1993b). According to Lee et al. (1986), P. philippensis can acclimate to changing habitats. Petaurista philippensis is also found in some locations within Thailand, including Bangkok, and Huai Ko Mong (Mae Salieng district, Mae Hongson Province— Jackson 2012). No fossils are known.

FORM AND FUNCTION

Form. —The vertebral formula of Petaurista philippensis is 7 C, 12 T, 7 L, 3 S and 27 Ca, total 56. The foramen transversarium is present in all cervical vertebrae except C 7. The length and width of the centrum increase from 1 L to 7 L, respectively. Hemal arches are found on caudal vertebrae 4 through 9 and hemal processes on caudal vertebrae 10 through 19 ( Thippan et al. 2019).

Bahuguna (2011) examined primary guard hairs (mean ± SD) of dried specimens of P. philippensis collected from random locations within each region. Dorsal (60.0 ± 0.0 μm) and tail hairs (59.09 ± 0.2 μm) are thickest, those of the head are of intermediate thickness (43.6 ± 0.50 μm), and hairs of the venter are thinnest (29.5 ± 0.15 μm). Cross-section examination shows the medullae of dorsal (50.0 ± 0.0 μm) and tail hairs (49.09 ± 0.2 μm) are thickest, head hairs are of intermediate thickness (33.6 ± 0.5 μm) and ventral hairs are thinnest (24.5 ± 0.15 μm). Head, ventral, and tail hairs are smooth due to having smoother scale margins than dorsal hairs, which have irregular scale patterns. The medullary configuration of dorsal, head, and ventral hairs is of the multiserial oblong ladder type, whereas in tail hairs it is in the wide lattice form.

The baculum of P. philippensis is small, complex in form, and similar morphologically to that of P. petaurista . The fanshaped proximal end protrudes from the shaft at an angle of 45.3–48.3° ( Fig. 4 ). A groove is present on the right side. The base is concave and connects with a ligament before splitting into two bundles. A tooth-like projection is found at the curve between the shaft and the proximal end. Bacular measurements (mm: mean ± SE) were: length, 81.74 ± 0.41; height at base, 36.42 ± 0.32; height of proximal end, 50.02 ± 0.28; width, 12.0 ± 0.12; and weight, 5.52 g ( Day et al. 1992). Pocock (1923) found no proximal end in the baculum of a juvenile specimen.

Function. —Shoulder, arm, and forearm muscles are adapted for arboreal living and gliding, distinguishing Petaurista from nongliding tree squirrels. The absence of cranial fibers of the trapezius restricts craniad movements. The lateral head of the triceps has an extensive muscular origin, which leads to an increase in the number of long muscle fibers, which reduces induced drag ( Thorington et al. 1998). Various forelimb muscles aid in secure landing ( Thorington et al. 1997).

helps in safe landing after a glide. The impact is absorbed by the triceps. Compared to nongliding tree squirrels, the radius and ulna are elongated and mobility between the distal ends of radius and ulna has been greatly reduced ( Thorington et al. 1997). The scapula plays an important role in gliding by providing sites for attachment of a large number of muscles. The scapula of P. philippensis has larger acromion processes than North American squirrels ( Glaucomys and Sciurus ) but lacks the expanded supraspinous region present in P. petaurista ( Essner and Scheibe 2000) .

Petaurista philippensis is capable of both quadrupedal and gliding locomotion. The patagium is used for gliding between trees ( Koli et al. 2011; Sharma and Sharma 2013), whereas the tail acts as a steering mechanism ( Hutton 1949) and to maintain balance while in motion ( Xavier et al. 1998). Petaurista philippensis has a gliding surface area of 1,069 cm 2 after excluding the tail area, an aspect ratio of 1.42, and wing loading of 104 N/m 2 ( Thorington and Heaney 1981). Koli et al. (2011) recorded means of gliding ratio (2.32), ground speed (6.96 m /s), air speed (7.51 m /s), and gliding angle (25.53°) of P. philippensis in a tropical teak forest. Average gliding distances of 11–20 m are more common than those greater than 30 m ( Koli et al. 2011; Lian-Xian and Harding 2013). Blanford (1891) recorded the longest glide to be about 73 m. In India’s tropical deciduous forests, gliding activity is higher in summer than in the monsoon and winter seasons, whereas the early period of night (between 1930 and 2330 h) is the most active time for gliding ( Koli et al. 2011).

During gliding, the position of the propatagium determines the patterns of airflow over the airfoil, while the uropatagium forms the trailing edge of the airfoil and is often used to modify the relative amounts of lift and drag. The plagiopatagium is responsible for the majority of the lift. The position of the wingtip

ONTOGENY AND REPRODUCTION

Young are born in nest cavities ( Lin et al. 2011). At birth, they weigh more than 56 g ( Lee et al. 1993a) and measure 178–390 mm in length. In subtropical areas, female Petaurista philippensis have litters of one or two young once a year; the average is 1.04 young/year (range 1–2— Lee et al. 1993a). After examining 100 necropsied females and finding a mean (± SD) of 1.13 ± 0.34 corpora lutea, Lee et al. (1993a) concluded that embryo mortality is low after implantation and total prenatal mortality is about 7.4%. Young are weaned at about 90 days of age. At about 4–5 months, the ear, tail, hind foot, and styliform cartilage mature ( Lee et al. 1992). Young reach 20% of average adult male weight in 3 months, 50% in 4 months, 75% in 7 months, 90% in 10 months, and 100% in 10–12 months, but adult length is achieved at about 6 months ( Lee et al. 1992). The growth rate of young born during the winter and summer breeding seasons did not differ significantly. In peninsular Malaysia, a young required 90–120 days to complete physical development ( Muul and Lim 1978).

Because males have larger home ranges than females ( Kuo and Lee 2012), P. philippensis is likely to have a polygynous or promiscuous mating system, despite having little or reverse sexual dimorphism in size ( Kuo and Lee 2012). Breeding patterns may vary depending on geographical location. Lee et al. (1993a) identified two breeding seasons in subtropical Taiwan, the first in May–July and the second in October–November. According to ovary development, the two most sexually active periods for females are late November–late February (winter breeding season), and late May–early September (summer breeding season), but male reproductive organs were functional throughout year except February, when no spermatogenesis was detected ( Lee et al. 1993a). Thus, Lee et al. (1993a) suggested that females control the breeding pattern in P. philippensis .

During the mating season, the male spends more time looking for a mate and less time foraging. Males call more frequently from March to June, and from October to November than in other months ( Koli and Bhatnagar 2014). Lee et al. (1986) observed mating in December, January, and June. Females mate with 3– 5 males during the breeding season before the first pregnancy ( Lin et al. 2011), and have at least a 45-day gestation period ( Lee et al. 1993a). February and August are the months of birth in Taiwan ( Lee et al. 1993a).

Petaurista philippensis breeds in early summer in India and mates in January and February ( Zacharias and Bhardwaj 1997). Breeding occurs in tree holes; however, only the female occupies the nest ( Blanford 1891). After a birth, the mother and her offspring occupy the nest hole exclusively ( Prater 2005). Hutton (1947) examined an infant, rescued from its nest, and provides the only description of a juvenile P. philippensis . Its head was disproportionate to the rest of its body and the flat tail was about 127 mm long. The patagium was undeveloped. Wing flags extended to the elbow rather than the wrist. It had a jet black tail and feet, and white and light-gray underparts. A black band extended across its shoulders ( Hutton 1947).

Figures

Fig. 1.—An adult Indian giant flying squirrel Petaurista philippensis in gliding, October 2016. Photograph by Sharad Agarwal used with permission.

Fig. 2.—Dorsal, ventral, and lateral views of the skull and lateral view of mandible of an adult Petaurista philippensis, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, August 2014. Photograph by Dr. Song Li used with permission.

Fig. 3.—Geographical distribution of Petaurista philippensis. Map redrawn from International Union of Conservation of Nature Red List of Threatened Species. Sighting records are represented by squares.

Fig. 4.—Right lateral and left lateral view of baculum of Petaurista philippensis (redrawn from Day et al. 1992).