Systematic Study of Flying Squirrels (Mammalia, Sciuridae) in Title Lao PDR( Dissertation_全文 )

Author(s) Daosavanh, SANAMXAY

Citation 京都大学

Issue Date 2020-03-23

URL https://doi.org/10.14989/doctor.r13320

Right

Type Thesis or Dissertation

Textversion ETD

Kyoto University Systematic Study of Flying Squirrels (Mammalia, Sciuridae) in Lao PDR

Daosavanh SANAMXAY

Graduate School of Science Kyoto University

March 2020

CONTENTS

Page Chapter 1 Introduction 1 Chapter 2 Second species of the genus Biswamoyopterus from 20 Lao PDR, with the comparison on morphology to other similar species Chapter 3 First record of the red giant flying squirrel, 34 Petaurista petaurista from Lao PDR, and the taxonomic and distribution summary in mainland Southeast Asia Chapter 4 First record of Temminck’s flying squirrel, 49 Petinomys setosus from Lao PDR Chapter 5 General discussion 59 Conclusion 64 Acknowledgements 65 References 66

CHAPTER 1

Introduction

1.1 General introduction to flying squirrel The family Sciuridae is the second largest group of the order Rodentia consisting of 292 species and 60 genera. The tribe Pteromyini (flying squirrels) currently involves 52 species that are placed in 15 genera, and a number of fossil species have also been described in 13 additional extinct genera (Jackson and Schouten 2012; Jackson and Thorington 2012; Koprowski et al. 2016). Flying squirrels are a diverse group of nocturnal, arboreal rodents that are highly adapted for gliding locomotion which resulted of the presence of a membrane between their wrists and ankles (a patagium) that they extend when gliding. Moreover, because of the strictly arboreal habit and high sensitivity to climate changes, flying squirrels are thought to be good indicators of the vicissitude of forests and also ideal study objects for investigating habitat changes and species diversification in the context of global environmental change (Arbogast 2007). They range in size from the pygmy flying squirrel Petaurillus (13 grams), to the giant flying squirrel Petaurista (3 kilograms) (Thorington and Heaney 1981; Koprowski et al. 2016). They live in trees and feed on nuts, fruit, or other plant material, and insect (Lee and Liao 1998). The degree of herbivory varies with their body size; the smaller size species tend to be less herbivorous and the largest are the most herbivorous (Muul and Lim 1978). The origination of flying squirrels therefore appears to be relatively recent, approximately 18–20 million years ago (early Miocene), and flying squirrels are monophyletic group and it’s a sister group of one lineage of tree squirrels, the Sciurini with consisting of the American and the northern Eurasian tree squirrels (Mercer and Roth 2003; Steppan et al. 2004). On the evolutionary study, flying squirrels separated into two large groups (Black 1972), one is New World flying squirrels (Glaucomys) which occurred in North America and second is Old World or Eurasian flying squirrels which found in Eurasia which New World flying squirrels diverged from Asian flying squirrels is estimated to have followed 4–6 million years later (Mercer and Roth 2003). Flying squirrels occur in North America and Eurasia, ranging from northern coniferous forest to the tropical lowlands, but absent from the Australian region, South America, Africa, and the polar regions (Hoffmann et al. 1993; Thorington et al. 2002). According to

1 number of species, the species richness hotspot of flying squirrel occurs in the Oriental region; however, the research effort is disproportionate to this pattern (Lee and Liao 1998).

1.2 Taxonomic history of flying squirrel The taxonomic history of flying squirrels is convoluted. Linnaeus described two flying squirrels in 1758: the European flying squirrel as Sciurus volans and the North American flying squirrel as Mus volans. Because he gave them both the species name volans, and both were soon considered to belong to the genus Sciurus, another species name, volucella, was given to the North American squirrel by Pallas in 1778 and was used for 137 years, until 1915. An additional four flying squirrels were described during the rest of the 18th century, three of them being placed in the genus Sciurus. The fourth was placed in a new genus, Petaurista, by Link in 1795. In 1800, George Cuvier introduced the name Pteromys for flying squirrels, separating them from the non-gliding squirrels placed in the genus Sciurus, and placed two species in Pteromys, the European flying squirrel and one of the giant flying squirrels from Southern Asia. In 1825, Frederic Cuvier introduced a second generic name, Sciuropterus. These two generic names were used for all but one of the 77 species, initially, Pteromys was used for the large flying squirrels of Southern Asia, and Sciuropterus for the small to medium-size squirrels. The one species not included in these two genera was the distinctive woolly flying squirrel, Eupetaurus cinereus Thomas, 1888. Thus, in Major’s (1893) classification of squirrels, only three genera—Pteromys, Sciuropterus, and Eupetaurus—were listed. At that time, Pteromys included the large flying squirrels. Subsequently, Thomas (1896) resurrected the name Petaurista for these large flying squirrels, and Sciuropterus included all the other, mostly smaller, and flying squirrels. The generic subdivision of the flying squirrels was furthered by Heude (1898), who placed the complex-toothed flying squirrel Pteromys xanthipes in a new genus Trogopterus. Then Thomas (1908) reexamined the Sciuropterus group and divided it into six genera: Trogopterus, Belomys, Pteromyscus, Sciuropterus, Petaurillus, and Iomys, based on characters of teeth and cranium. Furthermore, divided the genus Sciuropterus F. Cuvier, 1825, into four subgenera: Sciuropterus (the small North Eurasian flying squirrels), Glaucomys (the Himalayan and the North American flying squirrels), and Hylopetes and Petinomys (small to medium-size flying squirrels of Southern Asia). Howell (1915) named the Himalayan flying squirrel, Eoglaucomys,

2 and separated it from Glaucomys, recognizing both as full genera. Pocock (1923) elevated Hylopetes and Petinomys to full genera, based on differences between their bacula and the baculum of Glaucomys volans. Subsequently, Ellerman (1947) combined Eoglaucomys with Hylopetes, but Thorington et al. (1996) reported anatomical evidence that demonstrated this was inappropriate. When Thomas (1896) resurrected the name Petaurista Link, 1795, for the large Asian flying squirrels, he considered the name Pteromys G. Cuvier, 1800, to be a junior synonym, but Miller (1914) subsequently noted that Pteromys should be used for the small Eurasian flying squirrel, with Sciuropterus F. Cuvier, 1825, as a junior synonym. The name Sciuropterus was still used by Simpson (1945), but Ellerman and Morrison-Scott (1951) affirmed Miller’s (1914) conclusion that the name Pteromys should be used for the North Eurasian flying squirrel, based on Cuvier’s (1800) original description and a subsequent clarification by Fleming (1822). With the delineation of three additional genera, Aeromys Robinson and Kloss, 1915, Aeretes Allen, 1940 and Biswamoyopterus Saha, 1981, the current taxonomic arrangement was reached of approximately 52 species of flying squirrels allocated to 15 genera (Koprowski et al. 2016). The taxonomic name of the group, at the family level, expresses how closely related flying squirrels are thought to be to other squirrels. Brandt (1855) separated them from other squirrels, naming them the subfamily Pteromyinae, but he kept them in the squirrel family Sciuridae. Major (1893) suggested that flying squirrels are not closely related to other squirrels, but he did not formally recognize this idea, including both in the subfamily Sciurinae. Because Miller (1912) considered Pteromys to be a junior synonym of Petaurista, he gave the flying squirrels the new name Petauristidae, and raised them a family separate from the Sciuridae. When the name Pteromys was accepted as a senior synonym for Sciuropterus, the name Pteromyinae became the valid family-level name again (Corbet and Hill 1992; Hoffmann et al. 1993).

1.3 Phylogenetic history of flying squirrel From a review of the taxonomic history, a number of phylogenetic hypotheses become evident. First, those who have carefully reviewed the flying squirrels have considered them to be a monophyletic group (Major 1893; Thomas 1908; Ellerman 1940). This was questioned by Black (1963) and by Hight et al. (1974), but supported by Thorington (1984). Second, the relationship of the flying squirrels to the other squirrels is ambiguous (Emry and Korth 1996),

3 whether they evolved from an Oligocene tree squirrel or are more distantly related, having been derived independently from Eocene paramyids. More explicit phylogenetic hypotheses were presented by McKenna (1962), which grouped the genera of flying squirrels in two different ways. He combined boxes to provide a supra-generic grouping of flying squirrels into five groups, which could take to be hypotheses of monophyly: 1) The Glaucomys group, consisting of Glaucomys, Eoglaucomys, Pteromys, Olisthomys (= Petinomys setosus), and Petaurillus; 2) The Iomys group consisting of only Iomys; 3) The Petinomys group including Aeromys, Petinomys (exclusive of P. setosus), “Petinomys” vordermanni, and Hylopetes; 4) The Trogopterus group including the three genera Trogopterus, Pteromyscus, and Belomys; 5) The Petaurista group consisting of Petaurista, Aeretes, and Eupetaurus. Mein (1970) reviewed McKenna’s characters and came to different conclusions about the supra-generic groupings of flying squirrels, listing the three groups: 1) The Glaucomys group consisting of Glaucomys, Eoglaucomys, and Iomys; 2) The Petaurista group, including Pteromys, Trogopterus, Pteromyscus, Belomys, Aeretes, Petaurista, and Eupetaurus; 3) The Petinomys group, including Petinomys, Hylopetes, and Aeromys. Thorington and Darrow (2000) noted that flying squirrels could be divided into two groups: 1) The Glaucomys group includes Glaucomys, Eoglaucomys, Iomys, Petinomys, Hylopetes, and Petaurillus; 2) The Petaurista group includes Pteromys, Trogopterus, Pteromyscus, Belomys, Aeretes, Petaurista, Eupetaurus, and Aeromys. The hypothesis was based on differences in detail of the wrist articulations and the insertion of the tibiocarpalis muscle at the ankle. They hypothesized that the gliding membrane evolved very early in the history of the subfamily (Thorington et al. 1998), followed shortly by the evolution of these modifications at wrist and ankle. Later, flying squirrels adapted to various feeding niches, with concomitant evolution of the teeth and skulls. Therefore, they hypothesized that these postcranial features are primary and diagnose two basal clades, while the cranial and dental characters diagnose subsequent clades. Thorington et al. (2002) combined cranium, post cranium, and muscle characters in the analysis, with results of three groups: 1) The Glaucomys group, consist of Glaucomys, Eoglaucomys, Petaurillus, Iomys, Hylopetes, and Petinomys; 2) The Petaurista group includes

4 Pteromys, Aeretes, Petaurista, and Eupetaurus; 3) The Trogopterus group including Trogopterus, Pteromyscus, Belomys, and Aeromys. Mercer and Roth (2003) using interphotoreceptor retinoid-binding protein (IRBP), and mitochondrial 12S and 16S ribosomal DNA in the phylogenetic study of flying squirrel in genus level. They suggested that flying squirrel is monophyletic group, with two main clades: 1) Clade 1 consists of Pteromys, Trogopterus, Pteromyscus, Belomys, Aeretes, Petaurista, Eupetaurus, and Aeromys; 2) Clade 2 comprises of Glaucomys, Eoglaucomys, Iomys, Petinomys, Hylopetes, and Petaurillus. This result is perfectly congruence with the study of Thorington and Darrow (2000). Steppan et al. (2004) present a revised classification of squirrels based on two nuclear genes, which are C-myc and RAG1. They classified five subfamilies in family Sciuridae, of which all flying squirrels were classified as a tribe Pteromiyini with sister to tribe Sciurini (Holarctic and Neotropical tree squirrels) in subfamily Sciurinae.

1.4 Diversity of flying squirrel Koprowski et al. (2016) reported 52 species in 15 genera are widely distributed in the world. Later on, a new species was described from Yunnan Province, Biswamoyopterus gaoligongensis (Li et al. 2019). The most diversity of flying squirrels are found in Southeast Asia, consists of nine genera (60% of total genera), 32 species (60.4% of total species). Recently, in mainland Southeast Asia there are nine genera, 19 species (Koprowski et al. 2016), including Petaurista alborufus, P. caniceps, P. elegans, P. pataurista, P. philippensis, P. yunanensis, Biswamoyopterus laoensis, Aeromys tephromelas, Belomys pearsonii, Pteromyscus pulverulentus, Iomys horsfieldii, Hylopetes alboniger, H. phayrei, H. spadiceus, H. platyurus, Petinomys setosus, P. genibarbis, P. vordermanni, Petaurillus kinlochii; meanwhile 36 nominal taxa were included either in synonym or subspecies. Most of controversial taxa were included in P. philippensis, P. petaurista, P. elegans, I. horsfieldii and H. phayrei through their geographic range. The geographic variation in pelage colour is considerable but there is no comprehensive description or revision. Recently, flying squirrels in Asia continue to suffer strong pressure of habitat destruction, mainly clear cutting of primary forests, especially in Southeast Asia (Muul and Lim 1978). Moreover, it is also suffered by strong pressure of hunting and trade (Duckworth et al. 1999).

5 1.5 Diversity and study of flying squirrel in Lao PDR In Lao PDR, Osgood (1932) reported four flying squirrels which he referred to these following name forms: Petaurista lylei badiatus and Petaurista marica from Xiengkhouang Province (northeast of the country); Pteromys (Hylopetes) alboniger from Pakse District, Champasak Province (South of the country); and Pteromys (Hylopetes) spadiceus from Thateng District, Xekong Province (South of the country). Later, Delacour (1940) reported similar result, but P. l. badiatus was also found in Bolaven plateau, Champasak Province (South of the country). Then, Bourret (1944) reported one flying squirrel, Pteromys (Hylopetes) phayrei, collected from Savannakhet Province (South of the country). In 1972, Deuve wrote a series of notes on mammals of Lao PDR with included five different flying squirrels that he assigned to these following names: Petaurista petaurista lylei, P. elegans marica, Hylopetes alboniger alboniger, H. phayrei phayrei and Hylopetes spadiceus spadiceus, but only two species have found by him which are Petaurista petaurista lylei from Houayxai District in Bokeo Province (northwest of the country), Paksan District in Bolikhamxai Province (Central of the country), Xaiyabouly Province (northwest of the country), Xe Banghiang in Savannakhet Province (South of the country), and Thakhek District in Khammouan Province (Central of the country); Hylopetes alboniger alboniger from Vientiane Capital. His assigning of P. p. lylei and P. e. marica may followed taxonomic classification of Ellerman and Morrison-Scott (1951) who considered P. lylei as subspecies of P. petaurista and P. marica as a subspecies of P. elegans. Two decades later, Srikosamatara et al. (1992) observed two different flying squirrels in the fresh food market of Vientiane Capital, and they assigned to Petaurista petaurista and Hylopetes alboniger. However, the authors most likely followed the taxonomic interpretation of Askins (1977) who considered the range of P. petaurista to include all of Lao PDR, but this supposition was based on a different interpretation of the taxonomy, one which included P. philippensis and allied forms as synonyms. Therefore, the latest species list of flying squirrels was summarized by Duckworth et al. (1999) which included six recognized species: Petaurista philippensis, it was found throughout the country from Mekong plains to almost 1000 m in elevation; P. elegans from Nam Phui National Protected Area in Xaiyabouly Province, Phonsavan village in Xiengkhouang Province, and Nakai Namtheun National Park in Khammouan Province; Belomys pearsonii, it was known from the remains of two individuals found in owl pellets collected in Khammouan Limestone National Protected Area, Khammouan Province; Hylopetes

6 alboniger from Nam Xam National Protected Area in Huaphan Province (northeast of the country), and Nam Phui National Protected Area in Xaiyabouly Province; H. phayrei from Nam Phui National Protected Area in Xaiyabouly Province, Lak Sao village in Bolikhamxai Province, Khammouan Limestone National Protected Area in Khammouan Province, Dong Ampham National Protected Area in Attapeu Province (South of the country); H. spadiceus from Nam Ha National Protected Area in Louang Namtha Province (northwest of the country), and Khammouan Limestone National Protected Area in Khammouan Province. Corbet and Hill (1992) mapped distribution of six flying squirrel species in Lao PDR, including P. philippensis, P. petaurista, P. elegans, B. pearsonii, H. phayrei, and H. alboniger. However, P. petaurista is no confirmed record of specimen from Lao PDR. Moreover, there is no recorded of B. pearsonii from previous reports in the country, but it was mapped to occur in northeastern. The result of mapping may consider the similar of habitat to North Vietnam where Osgood (1932) described a new subspecies, B. pearsonii blandus, collected in Muong Moum, South of Lai Chau, Tonkin, Vietnam which approximately 90 km to nearest border of Lao PDR. The B. p. blandus is similar to B. pearsonii of Sikkim (holotype), but smaller, with decidedly smaller teeth and shorter, broader nasals. The only known of this species in Lao PDR is from remained of two individuals in owl pellets collected in Khammouan Limestone National Protected Area, Khammouan Province (Duckworth et al. 1999). Then, Francis (2008) re- mapped and concluded similar results, but with exclusion of P. petaurista, and inclusion of Petaurista yunanensis and H. spadiceus. But there is now particular record of specimen of P. yunanensis. Consequently, Thorington et al. (2012) summarized six species of flying squirrel distribute in the country as same list in Duckworth et al. (1999). In 2013, a new species, Biswamoyopterus laoensis, was described from Bolikhamxai Province, Central of the country by Sanamxay et al. (2013). Soon after, two species were confirmed to occur in Lao PDR, which are P. petaurista and Petinomys setosus (Sanamxay et al. 2015; Sanamxay et al. 2019). Recently, Koprowski et al. (2016) considered P. yunanensis as valid species, and included it to northern part of Lao PDR; however, there is no specific record specimen of P. yunanensis in the country. In summary, it is fundamentally recognized nine species of five genera distribute in Lao PDR, including Petaurista philippensis, P. petaurista, P. elegans, Biswamoyopterus laoensis, Belomys pearsonii, Hylopetes alboniger, H. phayrei, H. spadiceus, and Petinomys setosus. The collection site of each species is summarized in Table 1-2.

7 1.6 Taxonomic note of some flying squirrel species The giant flying squirrel Petaurista (Rodentia: Sciuridae) contains many recognized species, with each intricately divided into several forms or subspecies. Petaurista inhabits forests in lowlands and mountains up to 4000 m in elevation across Asia from Pakistan and Kashmir eastward to East and Southeast Asia. More than 18 Petaurista forms have been described as valid species in different taxonomic revisions on the basis of dental and cranial characteristics and external structures (Allen 1940; Ellerman 1940; Corbet and Hill 1992; Thorington and Hoffmann 2005). Currently, 16 Petaurista forms considered as valid species, including P. albiventer, P. alborufus, P. caniceps, P. elegans, P. hainana, P. lena, P. leucogenys, P. magnificus, P. mechukaensis, P. mishmiensis, P. nobilis, P. petaurista, P. philippensis, P. siangensis, P. xanthotis, P. yunanensis (Koprowski et al. 2016). Most of the controversial remain forms were included either in the P. petaurista complex or in the P. philippensis complex which have had a complicated taxonomic history due to intraspecific geographic variation across their distribution in Asia. A number of disagreements and uncertainties about the phylogeny and taxonomy of this polymorphic genus remain. Delimitation of the species has been unstable. The group badly needs a comprehensive revision to clarify the relationship between these forms, especially in southern China and Southeast Asia (Corbet and Hill 1992). The Red giant flying squirrel, P. petaurista, is considered a species complex and should be revised as new taxonomic data becomes available (Koprowski et al. 2016). This species is first described as Sciurus petaurista Pallas, 1766 from West Java. In 1795, Link proposed name Petaurista to be generic name of on flying squirrel, then Thomas (1896) resurrected the name Petaurista for the large Asian flying squirrels. Ellerman (1940) was inclined provisionally to divide four groups (albiventer, alborufus, petaurista, sulcatus), 61 forms were recognized. The form petaurista was included in petaurista group and he named it as Petaurista petaurista petaurista. Later on, Ellerman and Morrison-Scott (1951) considered petaurista as a valid species (Petaurista petaurista), with 24 taxa considered as either subspecies or synonym, which are albiventer, annamensis, badiatus, birrelli, cinderella, cineraceus, fulvinus, grandis, griseiventer, hainana, inornatus, lanka, lylei, mergulus, miloni, oral, philippensis, primrosei, reguli, rubicundus, rufipes, stockleyi, venningi, yunanensis. Then, Corbet and Hill (1992) also classified petaurista as distinct species, with 14 taxa (albiventer, barroni, batuana, birrelli, candidula, fulvinus, inornatus, melanotus, mimicus, nitida, nitidula, taguan, taylori, terutaus)

8 and 11 taxa (cicur, interceotio, lumholtzi, marchio, nigrescens, nigricaudatus, penangensis, rajah, rufipes, sodyi, stellaris) considered as synonym and nominal subspecies, respectively. Because Corbet and Hill (1992) also classified philippensis to be a valid species, then some taxa of Petaurista petaurista in Ellerman and Morrison-Scott (1951) were included in Petaurista philippensis. Later, Thorington and Hoffmann (2005) reclassified taxa included in P. petaurista of Corbet and Hill (1992) by considering sodyi to synonym, and proving seven synonym taxa to valid subspecies, including albiventer, batuana, candidula, melanotus, nitidula, taylori, and terutaus. Then, Thorington et al. (2012) were summarized similar result of Thorington and Hoffmann (2005). However, the molecular data is strongly supported that albiventer is a valid species of genus Petaurista, and grandis is closely related to P. petaurista then P. philippensis (Oshida et al. 2004; Yu et al. 2006). Therefore, in the recent summary of P. petaurista by Koprowski et al. (2016) there are 16 taxa were considered as valid subspecies through the geographic range, comprising of P. p. batuana, P. p. cicur, P. p. grandis, P. p. interceotio, P. p. lumholtzi, P. p. marchio, P. p. melanotus, P. p. nigricaudatus, P. p. nigrescens, P. p. nitidula, P. p. penangensis, P. p. petaurista, P. p. rajah, P. p. rufipes, P. p. stellaris, P. p. terutaus. They are distributing in South China (Sichuan, Guangxi, Guangdong, Fujian), Taiwan, Thailand (West side), Myanmar, Malaysia, Sumatra, Java, Borneo (including some adjacent small islands). In mainland Southeast Asia and some adjacent islands, seven taxa were recognized either synonym or subspecies, including melanotus from Selangor, Malay Peninsula; terutaus from Tarutau Island, straits of Malacca; candidula from Kindat (now Mindat), West Myanmar; taylori from Bankasun, South Tenasserim, Myanmar; barroni from Sriracha, southeast Thailand; cicur from Ban Kok Klap, Bandon, northeast Malaya (now southern Thailand); penangensis from Penang Island, Malaysia. However, Sanamxay et al. (2015) record P. petaurista from South of Lao PDR, and it was assigned to barroni and proposed as a valid subspecies of P. petaurista which separated from subspecies in Myanmar and western Thailand by Chao Pharya River and its basin, and separated from subspecies in southern Thailand and Malay Peninsular by the Isthmus of Kra (Fig. 1-1). In 1839, Elliot described a new flying squirrel named Pteromys philippensis from Madras, India. Ellerman (1940) included P. philippensis in albiventer group and he named it as Petaurista philippensis philippensis, and included griseiventer form as a synonym. However, Ellerman and Morrison-Scott (1951) included the Petaurista philippensis philippensis to

9 Petaurista petaurista, and the name was changed to Petaurista petaurista philippensis, with three taxa were listed as synonym (cinderella griseiventer, oral). It was ranked as a valid species because it is clearly separable from P. petaurista by external structures (Corbet and Hill 1992). They included 14 taxa (annamensis, cinderella, cineraceus, grandis, griseiventer, hainana, lanka, lylei, mergulus, nigra, oral, rubicundus, rufipes, yunanensis) and six taxa (badiatus, miloni, primrosei, reguli, stockleyi, venningi) to be synonym and subspecies, respectively. However, Thorington and Hoffmann (2005) considered six taxa in synonym list of Corbet and Hill (1992) should be valid subspecies due to long geographic distance between each type locality. They are included annamensis, cineraceus, grandis, lylei, mergulus, and yunanensis. Thorington et al. (2012) kept all subspecies list of Thorington and Hoffmann (2005), and proved three taxa to valid subspecies, including hainana, nigra, and rubicundus because their genetic distances and type localities. However, based on molecular data its suggested that grandis is considered as subspecies of P. petaurista (Oshida et al. 2000a, b), and hainana and yunanensis could be elevated to valid species (Yu et al. 2006). Therefore, Koprowski et al. (2016) summarized four taxa to be subspecies of P. philippensis, which are P. p. annamensis, P. p. cineraceus, P. p. lylei, P. p. mergulus. Petaurista philippensis is distributing in India, Sri Lanka, Central and South China, Myanmar (also some islands), Lao PDR, Vietnam, Thailand, and Cambodia. In mainland Southeast Asia and some adjacent islands, 10 taxa were described either synonym and subspecies which are annamensis from Nhatrang, South Annam, Vietnam; badiatus from Ngai-tio, Tonkin, Vietnam; cineraceus from Arakan, Myanmar; lylei from Doi Sritepe, Chiengmai, Thailand; mergulus from Ross island, Mergui islands, Myanmar; miloni from Diem-her, Lang-son province, Vietnam; primrosei from Sullivan island, Mergui islands, Myanmar; reguli from King island, Mergui islands, Myanmar; stockleyi from Melamoong, northwest Thailand; venningi from Kalaw, South Shan state, Myanmar (Fig. 1-1). Since the genus Biswamoyopterus have described by Saha (1981) until nowadays the phylogenetic relationships of this genus to other flying squirrels have not been explored. As well, based on the intensive survey the species has not been sighted where it was discovered since its discovery in 1981 (Krishna et al. 2016). Meanwhile, the recent articles on flying squirrels’ phylogeny were published by Thorington et al. (2002) based on morphological characters and Mercer and Roth (2003) and Steppan et al. (2004) based on molecular data; however, Biswamoyopterus was excluded in these studies because of specimen scarcity.

10 Consequently, its phylogenetic position and the relationship to other flying squirrel species are unknown. In 1908, Thomas named genus Petinomys for small to medium-size flying squirrels of Southern Asia. It is one of genus that containing greatest number of species, including P. crinitus, P. fuscocapillus, P. genibarbis, P. hageni, P. lugens, P. mindanensis, P. setosus, P. vordermanni. They are all restricted to Southeast Asia (Myanmar, Thailand, Malay Peninsula, Java, Sumatra, Borneo, Philippines), excepted P. fuscocapillus found in western Ghats of South India and the Central and South regions of Sri Lanka (Thorington et al. 2012; Koprowski et al. 2016). Recently, Sanamxay at al. (2019) includes P. setosus into Central of Lao PDR. This later species was described from Padang, Sumatra, Indonesia by Temminck in 1844 as Pteromys (Sciuropterus) setosus. Ellerman (1940) recognized four well marked groups: fuscocapillus, genibarbis, hageni, setosus. He included Pteromys setosus to setosus group and changed name to Petinomys setosus. Later, Ellerman and Morrison-Scott (1951) included taxa phipsoni as subspecies of P. setosus; however, it was allocated to Petinomys vordermanni by Hill (1961). Later, Carter (1942) described a new species, Pteromys (Olisthomys) morrisi, from northern Myanmar; however, Muul and Thonglongya (1971) re-examined specimens that refer to P. setosus from Sumatra (Padang, Deli, Lampong), West Malaysia (Selangor, Johore), East Malaysia, southern Thailand (lower Isthmus of Kara), northern Thailand, and northern Myanmar. They suggested that the specimens from Sumatra, East and West Malaysia, and the one from southern Thailand be considered as a subspecies, Petinomys setosus setosus; the specimens from northern Thailand and the one from northern Myanmar appear to larger than those South of the Isthmus of Kra and the consistent presence of a white tip on the tail, therefore, they be assigned to a separate subspecies, Petinomys setosus morrisi. Contradictory, Corbet and Hill (1992), Thorington and Hoffmann (2005), Thorington et al. (2012) and Koprowski et al. (2016) considered P. s. morrisi as a synonym of P. setosus.

1.7 The country profile Lao People’s Democratic Republic (Lao PDR) is a landlocked country with an area of 236,800 km2 and located at Central Indo-Chinese sub region, is surrounded by China, Vietnam, Cambodia, Thailand and Myanmar. According to a recent national survey carried out in 2015, forests in the Lao PDR cover approximately 11.06 million hectares, or 46.72% of the total land

11 area of the country (Ministry of Agriculture and Forestry 2015). There are currently 24 National Protected Areas, covering almost 3.7 million hectares, or more than 15 % of the country’s land area (Ministry of Natural Resources and Environment 2016). The major river of the country is the Mekong, which rises in Tibet to North of Lao PDR and flows through the country into Cambodia. Tributaries within Lao PDR contribute 35% of flow in the Mekong. Lao PDR is classified into three physiographic units which are Northern Highlands—rugged mountainous topography, the Annamite Range—mountainous topography, and Mekong Plain—the river plain lies South of the Northern Highlands and West of the Annamite Range (Duckworth et al. 1999) (Fig. 1-2). Lao PDR consist of eight forest types were classified by its ecosystems, their structure, function and biodiversity. 1) Northern Indochina subtropical forests; 2) Northern Thailand- Laos moist deciduous forests; 3) Louang Prabang montane rain forests; 4) Northern Khorat Plateau moist deciduous forests; 5) Central Indochina dry forests; 6) Northern Annamites rain forests; 7) Southern Annamites montane rain forests; 8) Southeastern Indochina dry evergreen forests (Mekong River Commission 2015).

12

Figure 1-1. The localities of species, subspecies and synonym of flying squirrel in mainland Southeast Asia (sensu Corbet and Hill 1992; Koprowski et al. 2016), and species record in Lao PDR (sensu Osgood 1932; Delacour 1940; Bourret 1944; Deuve 1972; Duckworth et al. 1999). Open squares are localities of Petaurista philippensis: the 4 subspecies include number 1. P. p. cineraceus, 3. P. p. lylei, 14. P. p. annamensis, 16. P. p. mergulus; the six synonymies include

13 number 2. P. lylei venningi, 4. P. cineraceus stockleyi, 5. P. lylei badiatus, 6. P. lylei miloni, 15. P. mergulus reguli, 17. P. mergulus primrosei; and number 7 to 13 are P. philippensis record from Lao PDR. Open circles are localities of Petaurista petaurista: the 4 subspecies include number 24. P. p. cicur, 25. P. p. tarutaus, 26. P. p. penangensis, 27. P. p. melanotus; the 3 synonymies include number 18. P. candidula, 22. P. annamensis barroni, 23. P. taylori; number 19. P. petaurista record from Lao PDR; and number 20 and 21 are P. petaurista record from Thailand. Black hexagons are localities of Petaurista elegans: the 2 subspecies are number 28. P. e. marica, 34. P. e. punctatus; number 29 to 33 are P. elegans record from Lao PDR. Open diamonds are localities of Hylopetes phayrei: the type locality is number 36. H. phayrei; the 2 synonymies include number 35. Sciuropterus phayrei probus, 37. Pteromys phayrei anchises; number 38 to 42 are H. phayrei record from Lao PDR. Open triangles are localities of Hylopetes spadiceus: the type locality is number 43. H. spadiceus; the synonym is number 48. Sciuropterus (Hylopetes) belone; number 44 to 47 are H. spadiceus record from Lao PDR. Black circles are localities of Hylopetes alboniger: the synonym is number 49. H. leonardi; number 50 and 51 are H. alboniger record from Lao PDR. Black triangles are localities of Petinomys setosus: the synonym is number 52. Pteromys (Olisthomys) morrisi; number 53 is P. setosus record from Lao PDR. Black pentagons are localities of Belomys pearsonii: the subspecies is number 54. B. pearsonii blandus; number 55 is B. pearsonii record from Lao PDR. Black star number 56 is type locality of Biswamoyopterus laoensis. Black square number 57 is type locality of Petaurista yunanensis.

14

Figure 1-2. Physiographic units of Lao PDR. Adapted from Duckworth et al. (1999)

1.8 Outline of the thesis In this study, I pay attention on flying squirrels taxonomy, diversity, and distribution based on specimens from Lao PDR, with the comparison to other species distributed in Southeast Asia. For these purposes, I first made detailed examination of their external and skull morphologies, and then made comparison with type specimens and museum specimens. The surveys were conducted in 15 local markets and 14 forest sites between 2011-2019 (Fig. 1-3; Table 1-1). In the Chapter 1, I introduced general information of flying squirrels, taxonomy, phylogeny, diversity and distribution. Moreover, the country profile of Lao PDR, and diversity and taxonomic studies on flying squirrels in the country were also included. In the Chapter 2, I reported the second species of the genus Biswamoyopterus from Lao PDR, with the comparison on morphology to other similar species. In the Chapter 3, I reported first record of the red giant flying squirrel, Petaurista petaurista from Lao PDR, and the taxonomic and distribution summary in mainland Southeast Asia. In the Chapter 4, I reported first record of Temminck’s flying squirrel, Petinomys setosus from Lao PDR. The Chapter 5, I summarize my findings on Lao flying squirrel and discussion.

15 Table 1-1. Survey sites in this present study. No. Name of point District Province Local market survey site 1 Thongsengchan Huay Xai Bokeo 2 Xum Neua Xum Neua Houa Phan 3 Phou Khoun Phou Khoun Louangprabang 4 Nam Ngam Pek Xiengkhouang 5 Thongnami Pak Kading Bolikhamxai 6 Chout Song Tha Kek Khammouan 7 Kok Mahaxay 8 Dong Xayphouthong 9 Phalanxay Tha Phalanxay Savannakhet 10 Dong Phou Vieng Phine 11 Lak Sip See Phathomphone Champasak 12 Tha Teng Tha Teng 13 Sekong La Mam Xekong 14 Dak Cheung Dak Cheung 15 Samakkhixay Samakkhixay Attapeu Forest survey site 1 Nam Ha 1 Sing Louang Namtha 2 Nam Ha 2 Vieng Phoukha 3 Phousabot Poungchong Kham Xiengkhouang 4 Tham Ang Louang Vangvieng Vientiane 5 Nam Kading 1 Bolikhanh 6 Nam Kading 2 Pak Kading Bolikhamxai 7 Ban Chomthong Viengthong 8 Ban Tha Khankeo Na Kai Khammouan 9 Ban Dang Mahaxay 10 Ban Na Khouang Sanasomboon Champasak 11 Ban Houy Kong Paksong 12 Ban La Vee 13 Ban Mo Lamam Xekong 14 Sekong Forest

16 Table 1-2. The summarize of collecting species in each survey sites of this study. Number in parentheses is represented number show in Fig. 1-3 for the local market sites. Number in brackets is represented number show in Fig. 1-3 for the forest sites. Species List of collecting site (2) Xum Neua (3) Phou Khoun (5) Thongnami (7) Kok Petaurista philippensis (15) Samakkhixay [1] Nam Ha 1 [7] Ban Chomthong [12] Ban La Vee Petaurista petaurista (13) Sekong (3) Phou Khoun Petaurista elegans (5) Thongnami [3] Phousabot Poungchong Biswamoyopterus laoensis (5) Thongnami (2) Xum Neua (3) Phou Khoun (4) Nam Ngam (6) Chout Song Belomys pearsonii (8) Dong (10) Dong Phou Vieng (14) Dak Cheung [1] Nam Ha 1 (12) Tha Teng Hylopetes alboniger [1] Nam Ha 1 (1) Thongsengchan (3) Phou Khoun (4) Nam Ngam (5) Thongnami Hylopetes phayrei (6) Chout Song (7) Kok (8) Dong (9) Phalanxay (13) Sekong

17 (14) Dak Cheung (15) Samakkhixay [1] Nam Ha 1 [13] Ban Mo [14] Sekong Forest (3) Phou Khoun (11) Lak Sip See (15) Samakkhixay Hylopetes spadiceus [8] Ban Tha Khankeo [10] Ban Na Khouang [11] Ban Houy Kong Petinomys setosus [4] Tham Ang Louang

18

Figure 1-3. The study sites in Lao PDR. Black triangular represents local market sites. Black circle represents forest sites. The black and red number above each point represents number of market sites and forest sites, respectively, which presented in Table 1-1. The blue line represents the Mekong River.

19 CHAPTER 2

Second species of the genus Biswamoyopterus from Lao PDR, with the comparison on morphology to other similar species

2.1 Introduction A unique flying squirrel from a proposed biosphere reserve in Namdapha, Tirap District, Arunachal Pradesh, India in 1981 by Dr. Shyamrup Biswas of the Zoological Survey India. It was subsequently described as a new genus and species, Biswamoyopterus biswasi Saha, 1981, the Namdapha flying squirrel. Information about this taxon was summarized in a series of publications including Corbet and Hill (1992), Thorington and Hoffmann (2005), Thorington et al. (2012), and the species was listed as Critically Endangered in the IUCN Red List (Molur 2008). However, the genus was only known from the holotype specimen (Reg. No. 20705) which resides in the Zoological Collection of the Zoological Survey of India, Kolkata [Calcutta], India. In September 2012, a team from the National University of Laos undertook a survey of flying squirrels in the informal food markets of Lao PDR. In the market at Ban (village) Thongnami, Pak Kading District, Bolikhamxai Province, Central Lao PDR (Fig. 2-1), I observed several species of Pteromyini including Hylopetes phayrei Blyth, Petaurista elegans Müller, and P. philippensis Elliot for sale as ‘bush-meat’. In addition, there was a female specimen of a large flying squirrel, which superficially resembled P. philippensis but differed in a number of external characters. On subsequent examination in the university museum, this individual was also found to have cranial and dental characters that clearly differentiated it not just from P. philippensis but from the genus Petaurista itself. A review of the literature confirmed that it was referable to the elusive genus Biswamoyopterus but that it differed specifically from B. biswasi. Therefore, it was described as a new species to science, Biswamoyopterus laoensis, is the second record of the genus, and the first record of the genus from Lao PDR and Southeast Asia (Sanamxay et al. 2013).

20 2.2 Materials and Methods An adult female was collected in Central Lao PDR and is held in the zoological collection of the Faculty of Environmental Sciences (FES), National University of Laos, Lao PDR. For morphometric record and comparison, I took measurements (in mm) where relevant followed Hayashida et al. (2006), Helgen et al. (2009) and Koyabu et al. (2009). They include: M: body mass; HB: head and body length—from tip of the nose to the anus, ventrally; T: tail length—from anus to tip of the tail, not including hairs; HF: hindfoot length—from the extremity of the heel behind the os calcis to the extremity of the longest digit, not including the claw or the hair; E: Ear length—from the intertragal notch to the tip; ONL: occipitonasal length (= greatest length of skull)—from the tip of nasals to the supraoccipital; CBL: condylobasal length—from the tip of gnathion to the occipital condyle; MB: mastoid breadth—taken across the mastoid bone, on a line perpendicular to the long axis of the skull; ZB: zygomatic breadth— the greatest breadth across the zygomatic arches; ZH: zygomatic height—from the bottom edge of the jugal to the tip of the superior process of the jugal; BB: breadth of braincase—the greatest breadth of the braincase at the posterior roots of the zygomatic arches; BH: braincase height— from the basioccipital plane to the crown of the braincase; RB: rostrum breadth—the greatest breadth across the rostrum, including the bony capsules enclosing the nasolacrimal canals; NL: nasal length—from the anterior tip of the nasal bones to the most posterior suture between the nasal and frontal bones; MWN: maximum width of nasals bone—the maximum width towards the tip of nasal bones; IOB: interorbital breadth—taken across the supraorbital notch; POB: postorbital breadth—the narrowest width across the constriction posterior to the orbits; LIF: length of the incisive foramina—from the anterior border to the posterior border of the incisive foramina; LBP: length of bony palate—from the posterior edge of the incisive foramen to the staphylion; PPL: postpalatal length—the distance from the posterior margins of the palatal bridge to the posterior border of the occipital bone (the ventral lip of the foramen magnum); LAB: length of auditory bulla—taken across the longitudinal length of the bulla, not including the bony eustachian tube; WAAM: width of auditory bullae across the external auditory meati— from the tip of the left external acoustic meatus to the tip of the right external acoustic meatus; IBG: inter bullae gap—taken across the narrowest width of the basisphenoid between the bullae; P3–M3: upper toothrow length—from the front of the third upper premolar to the back of the crown of the third upper molar; M2–M2: greatest palatal breadth—from the labial wall of the

21 left second upper molar to labial wall of the right second upper molar, across the palate; M1– M1: width of the bony palate at the first upper molar—from lingual wall of left first upper molar to the lingual wall of right first upper molar; P4–M3: lower toothrow length—from the front of the fourth lower premolar to the back of the crown of the third lower molar; ML: mandible length—from the most posterior part of the condyle to the most anterior part of the body of mandible, not including the lower incisors; MH: mandible height—from bottom margin of angular process to tip of the coronoid process.

2.3 Systematics

Biswamoyopterus laoensis Sanamxay, Douangboubpha, Bumrungsri, Xayavong, Xayaphet, Satasook, and Bates, 2013

Holotype FES.MM.12.163 (Field No. DS20120925.11), adult female, skull extracted, dry skin, captured by a hunter, collected from the market by Daosavanh Sanamxay, Sysouphanh Xayavong, and Vilakhan Xayaphet on 25 September, 2012.

Type locality Collected from Thongnami market, Ban (village) Thongnami, Pak Kading District, Bolikhamxai Province, Lao PDR, 18°10.302'N, 104°14.115'E (Fig. 2-1). Its actual place of origin is not known. However, most of the ‘bush-meat’ sold in this market is sourced from two NBCAs (National Biodiversity Conservation Area) namely Nam Kading NBCA, which is about 5 km northeast of Thongnami and Khammouan Limestone NBCA, which is about 25 km Southeast of the village.

Etymology The name is derived from Lao PDR, the country where the type specimen was collected and ensis (Latin for ‘belonging to’). Its proposed English name ‘Laotian giant flying squirrel’.

22 Diagnosis This is a large flying squirrel (a head and body length of 455 mm, a tail length of 620 mm, and a body mass of 1,800 grams). The tail is cylindrical, not distichous and is entirely black from its tip to the outer border of the well-developed interfemoral membrane, with the exception of a small patch of grey hairs adjacent to the membrane on the under-surface (Fig. 2-2). The dorsal pelage is an admixture of dark reddish brown and black hairs, variably grizzled with whitish-grey. The ventral pelage is orange intermixed with grey. The upper surface of each patagium is thickly haired, comparable in color to the upper body but with significantly less grizzling; the underside is sparsely covered in orange hairs and with numerous, clearly defined, discontinuous black lines; these lines are also present on the underside of the interfemoral membrane (Fig. 2-2). The ears are dark grey/black, virtually naked but with tufts of long black hairs at the base of the anterior and posterior margins; a small tuft of hairs is also present beneath the mid-part of the ear, posterior to the posterior margin of the eye. The skull is large with an occipital nasal length (ONL) of 74.4 mm. The tympanic bullae are large and closely aligned to one another, with a narrow basiocciput (Fig. 2-3); their internal structure includes numerous (12) septae in a complex honeycomb pattern. The anterior tips of the nasals are virtually straight, not rounded. The upper and lower incisors are yellow on their anterior surface. In the cheekteeth, P3 is relatively well developed and P4 slightly exceeds M1 in size. Both M1 and M2 have two well developed cusps on the labial side and one large and one smaller cusp on the lingual side; an additional smaller cusp is present on the posterior transverse ridge.

Description This is a large flying squirrel (Table 2-1), the upper surface of which is predominantly an admixture of dark reddish brown and black hairs, variably grizzled with whitish-grey. Individual hairs are variable in color but usually comprise the following components: metallic-ash at the base for up to 20 mm, reddish brown in the mid-part for about 15 mm, and a black tip of about 3 mm. A distinctive whitish-grey band, some 6 mm in length, is present in hairs that reside in areas of the upper surface that are extensively grizzled. These areas of extensive grizzling include the crown of the head, on the upper back, and on the rump extending on to the base of the tail—that part of the tail which is contained within the interfemoral membrane. There is also some grizzling on the upper forearms.

23 The upper surface of each patagium, which is thickly haired, is comparable in color to the body but has little or no grizzling. The upper surface of the interfemoral membrane is also well haired, especially adjacent to the tail; except in the region of the tail, it is covered in deep reddish-brown hairs. The fore- and hind-feet are covered in black hairs on their upper surface and dark pads on their under surface. The claws form a half circle with very sharp tips. The ventral pelage is pale orange (peanut butter color) with white tips to some hairs. On the midline of the body and chest it is dark orange with metallic-ash bases and white tips. The throat is grey and the chin has a dark metallic-ash colored patch. The anterior margin of the forearms is black, the color extending to the forefeet, wrist, pro-patagium and styliform cartilage. The undersides of the patagia are more sparsely covered in orange hairs and are marked with numerous, clearly defined, discontinuous black lines (Fig. 2-2). These lines are stronger and even more clearly defined on the underside of the interfemoral membrane. The lateral margins of the patagia and the interfemoral membrane have a well-developed fringe of dark, blackish hairs, above and below. These hairs are metallic-ash at their bases, gradually darkening towards the tip. The interfemoral membrane is relatively large; it is connected to about one third of the basal part of the tail. The tail is cylindrical, not distichous, and is entirely black from its tip to the outer border of the interfemoral membrane, with the exception of a small patch of grey on the underside, adjacent to the membrane. The individual hairs are black at the tip and grey basally. On the head, the ears are predominantly black and denuded of hairs. Small tufts of long black hairs are present at the base of the anterior and posterior margins of each ear and at the base of the ear. The eyes are ringed with a narrow band of black hairs, which extends posteriorly to the anterior base of the ear and anteriorly on to the nose. There is a patch of reddish brown above each eye. The cheeks are a variable black, deep red and grizzled whitish- grey in color. The upper surface of the head is strongly grizzled in silver-grey. Three pairs of mammae occur on the distal part of the belly. The skull is large with an occipito-nasal length of 74.4 mm. When viewed in lateral profile, it is relatively flat with a low braincase. The orbital regions are large. In lateral view, the zygomatic arches are low and the jugal bone is not greatly expanded anteriorly; when viewed from above, the zygomata are broad, especially posteriorly (Fig. 2-3). The rostrum is short and wide and the anterior borders of the nasals are nearly straight, not strongly rounded. The

24 interorbital region is narrower than the postorbital region and the frontal depression is deep and well developed anteriorly; there is a pair of large swellings near the midline at the posterior end of the frontal. The postorbital processes are large but relatively short, with a mean length of 7.9 mm. Temporal ridges are present but do not connect to each other. The squamosal is in broad contact with the anterior, upper part of each bulla, where it forms a broad shelf roofing the dorsal region of the bulla. The mastoid regions are very small and mastoid process is undeveloped. The tympanic (auditory) bullae are very large, thick and opaque. Within each bulla, the septae form a complex, honeycomb pattern. The anterior palatine foramina are well developed. The anterior border of the pterygoid fossa is posterior to the posterior borders of M3-M3. The pterygoids are large, robust, and curve towards the anterior base of the bullae. The basioccipital is relatively narrow with a prominent ridge in the midline. In the dentition, the upper incisors are almost proodont. The anterior surface of each tooth is yellow, not pigmented with orange, and there is a deep groove on the inner margin. The small upper premolar (P3) is relatively well developed and is situated in a notch in the anterior border of the second upper premolar (P4). This latter tooth is large and slightly exceeds M1 in size. P4 has three well defined cusps on the labial side and one large cusp on the lingual side; there is an additional small cusp present in the mid-part of the posterior transverse ridge. Both the first and second upper molars (M1 and M2) have two well-developed cusps on the labial side and one large and one smaller cusp on the lingual side; they also have an additional smaller cusp on the posterior transverse ridge. The third upper molar (M3) has one cusp on the labial side and a well- developed cusp on the lingual; the posterior part of the tooth is sharply laminated. In the lower dentition, the incisor is yellow (similar to the upper incisor). The first premolar (P4) is subequal in size to the first molar (M1). It has two cusps on both the labial and lingual sides; the anterior lingual cusp is the largest and there is an indistinct cusplet attached to it posteriorly; there is also a small cusplet on the labial side set between, and slightly internal to, the anterior and posterior cusps. The first and second lower molars (M1 and M2) are essentially similar to P4 but are larger and M2 has a less well developed posterior lingual cusp. The third lower molar (M3) is more elongated and larger than M1 and M2 and without a posterior cusp on the lingual side.

25 Comparison Biswamoyopterus laoensis Sanamxay et al., 2013 is the second species described for the genus. It is distinguished from all other flying squirrels, with the exception of B. biswasi, by its distinct combination of generic characters. Superficially, it is most similar in size, coloration and morphology to Petaurista and particularly P. philippensis in Lao PDR. However, externally it differs (inter alia) by having ears denuded of long hairs and the ventral surface of the patagium being marked with numerous, clearly defined, discontinuous black lines. In the skull, it has relatively much larger tympanic bullae and a distinctly narrower basiocciput compared to all species of Petaurista. The internal structure of the bullae is also different. In B. laoensis, the septae within the bullae form a complex honeycomb pattern whilst those in Petaurista have four or fewer septae. In the dentition, the upper and lower incisors are yellow rather than the typical orange-red found in Petaurista and the cheekteeth are simplified and strongly cuspidate, not wrinkled and sculptured as in Petaurista. However, in order to rule out any possibility that this species had been described before under a name applied incorrectly to Petaurista, the characters of B. laoensis were compared with the type descriptions of the sixteen taxa currently referred to P. petaurista and P. philippensis (Corbet and Hill 1992; Thorington and Hoffmann 2005), which were named from the Indochinese Division (sensu Corbet and Hill 1992, page 4). P. petaurista and P. philippensis were selected as they are essentially similar in size to B. laoensis; a third species, P. elegans was omitted since it is significantly smaller. For P. petaurista, descriptions of the following taxa were compared with B. laoensis: barroni Kloss from Thailand; candidula Wroughton and taylori Thomas from Myanmar. For P. philippensis, the taxa included: hainana Allen, rufipes Allen and yunanensis Anderson from China; cineraceus Blyth, mergulus Thomas, primrosei Thomas, reguli Thomas, and venningi Thomas from Myanmar; lylei Bonhote and stockleyi Carter from Thailand; and annamensis Thomas, badiatus Thomas and miloni Bourret from Vietnam. In all cases, B. laoensis could be distinguished by one or more characters. The structure of the cheekteeth of Biswamoyopterus also differentiates the genus from Trogopterus Heude, which has a highly complex cusp pattern as well as a greatly enlarged P4; this later character is shared with the genus Eupetaurus Thomas, the pelage of which is extraordinarily woolly. The genus Pteromyscus Thomas shares with Biswamoyopterus the character of larger tympanic bullae but the cusp pattern of the cheekteeth is once again more

26 complex, P3 is small or sometimes absent, the tail is distichous and not cylindrical, and there is no interfemoral membrane. These later two characters are shared with the genus Aeretes Allen, which additionally has upper incisors that are orange, cheekteeth that are complex, and tympanic bullae with three septae, not numerous septae in a honeycomb pattern as observed in B. laoensis. The tails of Iomys Thomas, Hylopetes Thomas, Petinomys Thomas, and Petaurillus Thomas are distinctly distichous and there is no interfemoral membrane. However, the cheekteeth are more cuspidate and share some of the characters observed in Biswamoyopterus. The tympanic bullae of Iomys and Hylopetes in particular are significantly smaller than those of Biswamoyopterus, a character shared with Aeromys Robinson and Kloss, which like the other two genera has a significantly broader basiocciput than that seen in Biswamoyopterus and a much less complex structure of septae within the bullae. However, Aeromys, like Biswamoyopterus, has yellow, not orange incisors. In comparison to Biswamoyopterus biswasi, the only other species known within the genus, B. laoensis is essentially similar in size externally (HB: 455 mm, Tail: 620 mm, and Ear: 52 mm in B. laoensis versus HB: 405, Tail: 605 mm and Ear: 46 mm in B. biswasi) (Table 2-1) but differs in most aspects of pelage color. This is most apparent in a comparison of the ventral pelage, which is illustrated and described in Saha (1981, p. 333 and Plate VI B). According to Saha (1981), the underside of the body of B. biswasi is white with the hairs having pearly grey bases. Each patagium is also white below but washed with a faint orange-rufous; the underside of the interfemoral membrane is white with a band of pale Morocco red near the margin; the margin is grizzled with grey and white, more so near the tail root. This compares to the essentially orange, intermixed with white/greyish hairs found on the ventral surface of B. laoensis, which also has a very well-developed fringe of dark/black hairs on the border of the interfemoral membrane. In addition, the patagia and interfemoral membranes of B. laoensis are marked with numerous, black, discontinuous lines, which are not apparent in B. biswasi. The tail of B. biswasi is cylindrical and on the ventral side is pale grey-white for most of its length, darkening towards a dark brown/black tip. In B. laoensis, it is also cylindrical but black throughout its length on the ventral side except for a small patch of grey near the border of the interfemoral membrane and orange-grey for that portion of the tail that lies within the interfemoral membrane. On the dorsal surface in B. laoensis, the tail is also black for its entire length except at its base where it is covered in dark reddish-brown hairs, grizzled with whitish-

27 grey. However, in B. biswasi, the tail beyond the interfemoral base is initially pale smoky grey changing to rufous red, then russet and finally to dark brown near the tip; within the interfemoral membrane the tail is grey washed with red. The upper body of B. biswasi is Morocco red grizzled with white. This is similar to B. laoensis but a little paler. The patagia in B. biswasi also appear a little paler than those of B. laoensis. The crown of the head in both B. biswasi and B. laoensis is characteristically pale but this is more extreme in B. biswasi. Both species have ears denuded of long hairs. However, B. biswasi has a well-developed tuft of pale hairs at the posterior base of each ear; in B. laoensis this is black. In the skull and teeth, the occipitonasal length and zygomatic breadth of 74.4 mm and 47.7 mm respectively in B. laoensis are essentially similar to those reported by Saha (1981) for B. biswasi, which were 72.4 mm and 47.5 mm. However, the length of the tympanic bullae and upper cheekteeth of B. laoensis is 17.3 mm and 16.3 mm respectively, considerably exceed those of B. biswasi, 15.5 mm and 15.5 mm respectively. Both species have a deeply depressed frontal, a relatively short palate, well developed palatal foramina, and tympanic bullae with a honeycomb pattern of septae. The structure of the teeth is also similar.

Habitat Although the exact habitat of Biswamoyopterus laoensis is not known, the village market at Thongnami, where the holotype was found, is approximately 5 km southwest of Nam Kading NBCA and it is reported that extensive hunting occurs within at least some of this NBCA (Evans et al. 2000). The area comprises limestone karst with mostly pristine dry evergreen forest or semi-evergreen forest with an elevation of 160–1,600 m. The village of Thongnami is also approximately 25 km northwest of Khammouan Limestone NBCA, which is also a karst area with a dry open xerophytic flora on the limestone and small pockets of semi-evergreen forest in the valleys and low-lying areas (Thewlis et al. 1998). It is possible that B. laoensis may be present in at least one or possibly both of these NBCAs.

28 Distribution To date, Biswamoyopterus laoensis is only known from Thongnami in Bolikhamxai Province in Central Lao PDR. From the locality of the market and the behavior of the local hunters, it is probable that the specimen was either collected in Nam Kading or Khammouan Limestone NBCAs (Fig. 2-1). Further investigations should be carried out in these areas as well as Nakai-Nam Theun and Hin Nam No NBCAs, where limestone karst and evergreen forest are also present, to determine the distribution and abundance of this new species.

2.4 Discussion The discovery of this new species extends the known range of the genus Biswamoyopterus by some 1,250 km. Biswamoyopterus biswasi was previously collected at an elevation of 350 metres in Deban (26 km east of Miao) and until now was only known from the western slope of the Patkai Range in the catchment area of the Noa Dihing River in Namdapha, India (Saha 1981). Like B. biswasi, the extent of the geographical range of B. laoensis is currently not known. This discovery further supports the views of Lee and Liao (1998), who suggested that flying squirrels in Southeast Asia are currently inadequately researched and Jenkins et al. (2005), who noted that on-going local market surveys in Lao PDR will provide an informative overview of the exploitation of animals occurring in the surrounding area and occasionally provide interesting species’ records. Currently, the major threats for the wildlife in Lao PDR are habitat loss and harvesting for food (Duckworth et al. 1999; Timmins and Duckworth 2008). In squirrels, harvesting is the most serious threat as they rank as the most commonly traded mammalian ‘bush-meat’ in local markets (Srikosamatara et al. 1992). This is a serious conservation concern for B. laoensis. It is strongly recommended that further research of this new species be carried out urgently to help determine its range, population status, and its threats.

29 Table 2-1. Body Mass (in grams) and external and skull measurements (in mm) of two species of genus Biswamoyopterus, B. laoensis from Lao PDR and B. biswasi from India (Saha 1981). Character B. laoensis (holotype) B. biswasi (holotype) M 1800 - HB 455 405 T 620 605 HF 74.5 78.0 E 52.0 46.0 ONL 74.39 72.4 CBL 70.99 70.1 MB 30.79 - ZB 47.72 47.5 ZH 4.86 - BB 32.84 - BH 22.55 - RB 17.04 - NL 22.57 20.9 MWN 13.37 - IOB 14.06 19.0 POB 17.19 - LIF 5.85 - LBP 23.83 - PPL 28.77 - LAB 17.33 15.5 WAAM 35.96 - IBG 5.01 - P3-M3 16.33 15.5 M2-M2 19.37 - M1-M1 8.05 -

P4-M3 15.33 - ML 45.36 - MH 29.78 -

30

Figure 2-1. Type localities of the two species of Biswamoyopterus; the black square represents B. biswasi from Namdapha National Park, Arunachal Pradesh, northeast India and the black circle represents B. laoensis from Pak Kading District, Bolikhamxai Province, Lao PDR. The grey areas represent (1) Nam Kading NBCA and (2) Khammouan Limestone NBCA.

31

Figure 2-2. Views of skin of the holotype, Biswamoyopterus laoensis (FES.MM.12.163). A— Dorsal view; B—Ventral view; C—Head, left lateral view; and D—Ventral view of the left patagium and interfemoral membrane to show the discontinuous black lines. Not to scale.

32

Figure 2-3. Views of skull, mandible, and dorsal views of left maxillary (above) and left mandibular (below) toothrows of Biswamoyopterus laoensis (FES.MM.12.163). White scale bar for the skull (bottom left) is 20 mm and for the teeth (bottom right) is 5 mm.

33 CHAPTER 3

First record of the red giant flying squirrel, Petaurista petaurista from Lao PDR, and the taxonomic and distribution summary in mainland Southeast Asia

3.1 Introduction Lao People’s Democratic Republic (Lao PDR) is home to a rich variety of rare and endemic species and is considered as a biodiversity hotspot (Myers et al. 2000). In recent years, the number of mammal species recorded from the country has increased with the discovery of a range of unusual taxa, including amongst the rodents, the Kha-nyou, Laonastes aenigmamus Jenkins et al. (2005); the Lao limestone rat, Saxatilomys paulinae Musser et al. (2005); and most recently, the Laotian giant flying squirrel, Biswamoyopterus laoensis Sanamxay et al. (2013). The discovery of this later taxon increased to seven the number of flying squirrels recorded from the country, the other six being Petaurista elegans (Müller), P. philippensis (Elliot), Belomys pearsonii (Gray), Hylopetes alboniger (Hodgson), Hylopetes phayrei (Blyth), and Hylopetes spadiceus (Blyth) (Thorington et al. 2012). In addition, it has been suggested that two more species may possibly occur in the North of the country, namely, P. petaurista (Francis 2008; Thorington et al. 2012) and Petinomys setosus (Temminck) (Duckworth et al. 1999). Petaurista petaurista is currently known from Afghanistan, Pakistan, India, Nepal, South China, Myanmar, Thailand, Malaysia, Sumatra, Java, and Borneo (Thorington et al. 2012). Previously, Askins (1977) had considered the range of P. petaurista to include all of Lao PDR, but this supposition was based on a different interpretation of the taxonomy, one which included philippensis and allied forms as synonyms. Subsequently, Srikosamatara et al. (1992) reported that P. petaurista had been provisionally identified in the That Louang fresh food market in the capital city, Vientiane. However, the authors most likely also followed the taxonomic interpretation of Askins (1977). Corbet and Hill (1992) mapped the distribution of Petaurista petaurista and included northwest Lao PDR but without details. This record was probably based on that of Askins (1977), who included the forms candidula and barroni (currently included in P. petaurista) in the synonymy of P. alborufus (Milne-Edward) and mapped the range of this latter taxon as including northwest Lao PDR. Oshida et al. (1992, 2004) suggested that the taxon occurred in

34 northern Lao PDR on the basis of four individuals, which they referred to P. petaurista melanotus Gray (1837). However, this latter record is not credible because this material was obtained from a pet dealer in Japan and melanotus is a distinct Sundaic form from peninsular Malaysia (Fig. 3-1). It should be noted that Timmins and Duckworth (2008) stated that Lao PDR was known to be a source of export for various Sundaic species that do not occur naturally in the country. As such, P. petaurista is omitted from the faunal list of the country by Duckworth et al. (1999), Thorington and Hoffmann (2005), Francis (2008), Timmins and Duckworth (2008), and Thorington et al. (2012). However, on the 18 April 2013 a dead, adult male Petaurista was observed for sale in a local market in Thatlouang village, Sekong Province, South Lao PDR. This specimen is referred to P. petaurista and is here considered to be the first authenticated record from the country (Sanamxay et al. 2015).

3.2 Materials and Methods An adult male was obtained from Thatlouang village, market in Sekong Province, South Lao PDR and is held in the zoological collection of the Faculty of Environmental Sciences (FES), National University of Laos, Lao PDR. Unfortunately, the skull was damaged, which restricted the number of cranial measurements that could be taken. Measurements (in mm) were taken and followed Hayashida et al. (2006), Helgen et al. (2009), and Koyabu et al. (2009). Measurements comprise the following characters: M: body mass; HB: head and body length–from tip of the nose to the anus, ventrally; T: tail length–from anus to tip of the tail, not including hairs; E: ear length–from the intertragal notch to the crown; HF: hindfoot length–from the extremity of the heel behind the os calcis to the extremity of the longest digit, not including the claw or the hair; ONL: occipitonasal length (= greatest length of skull)–from the tip of nasals to the supraoccipital; CBL: condylobasal length–from the tip of gnathion to the occipital condyle; ZB: zygomatic breadth–the greatest breadth across the zygomatic arches; ZH: zygomatic height–from the bottom edge of the jugal to the tip of the superior process of the jugal; BB: breadth of braincase– the greatest breadth of the braincase at the posterior roots of the zygomatic arches; RB: rostrum breadth–the greatest breadth across the rostrum, including the bony capsules enclosing the nasolacrimal canals; NL: nasal length–from the anterior tip of the nasal bones to the most

35 posterior suture between the nasal and frontal bones; IOB: interorbital breadth–taken across the supraorbital notch; POB: postorbital breadth–the narrowest width across the constriction posterior to the orbits; POPB: postorbital processes breadth–from tip of the right postorbital process to the tip of the left postorbital process; LIF: length of the incisive foramina–from the anterior border to the posterior border of the incisive foramina; MWN: maximum width of nasals bone–the maximum width at the anterior end of the nasal bones; P3–M3: upper toothrow length–from the front of the third upper premolar to the back of the crown of the third upper molar; M2–M2: greatest palatal breadth–from the labial wall of the left second upper molar to labial wall of the right second upper molar, across the palate; M1–M1: width of the bony palate at the first upper molar–from lingual wall of left first upper molar to the lingual wall of right first upper molar; ML: mandible length–from the most posterior part of the condyle to the most anterior part of the body of mandible, not including the lower incisors; P4–M3: lower toothrow length–from the front of the fourth lower premolar to the back of the crown of the third lower molar; BL: baculum length–from the base to the tip of the baculum.

3.3 Systematics

Petaurista petaurista Pallas, 1766

Subspecies and synonyms from mainland Southeast Asia (as illustrated in Fig. 3-1; Corbet and Hill 1992; Thorington and Hoffmann 2005; Thorington et al. 2012) Pteromys melanotus Gray, 1837: 584; Selangor; originally Nepal in error. Petaurista terutaus Lyon, 1907: 17; Terutau (= Tarutao) Island, Straits of Malacca, Thailand. Petaurista candidula Wroughton, 1911: 1014. Kindat, western Myanmar. Petaurista taylori Thomas, 1914: 205; Bankasun, southern Tennasserim, Myanmar. Petaurista annamensis barroni Kloss, 1916: 33; Hup Bon, Sriracha, southeast Thailand. Petaurista nitida cicur Robinson and Kloss, 1914: 223; Ban Kok Klap, Bandon, Thailand. Petaurista petaurista penangensis Robinson and Kloss, 1918: 224; Penang Island, Malaysia.

36 Holotype Sciurus petaurista Pallas, 1766; West Java, Indonesia. Restricted to Preanger Regencies by Robinson and Kloss (1918).

New material FES.MM.13.001, adult, skull extracted, dry skin, obtained from a vendor at Thatlouang village, Lamam District, Sekong Province, Lao PDR, approximately 15° 21′N, 106° 43′E (Fig. 3-1). According to the vendor, the specimen was obtained in the local area, probably in or adjacent to the forests of the three former “Proposed National Biodiversity Conservation Areas (PNBCAs)”, which comprise Phou Theung, Bolaven northeast, and Phou Kathong (Sanamxay et al. 2015).

Description The specimen is a large flying squirrel with a head and body length of 435 mm, a tail length of 475 mm, and a body mass of 1,500 grams (Table 3-1). The pelage of the upper surface comprises predominantly an admixture of dark rust-colored and black hairs, variably grizzled with whitish grey. These areas include the upper neck and back (except for the crown of the head), the flanks, and on the rump extending on to the base of the tail. The upper forearms are pale orange with some grizzling (Fig. 3-2A). The ventral pelage is whitish grey. The throat is white and the chin has a dark metallic- ash colored patch. The anterior margin of the forearms is deep orange, the color extending to the sides of the neck and the chin. The wrist, pro-forearm, and styliform cartilage are black. The undersides of the patagia, forearms, and hindlegs are relatively sparsely covered in brownish- orange hairs, especially in comparison to the upper surface. This brownish-orange color extends to the interfemoral membrane, except for the area of the tail, which is covered with whitish-grey hairs. The lateral margins of the patagia have hairs with whitish-grey tips and brownish-grey bases. The interfemoral membrane has a well-developed fringe of pale grey hairs above and whitish below. The tail is cylindrical, and from the outer border of the interfemoral membrane towards the tip is entirely yellowish mixed with some black hairs. The tail tip is dark brown for about 100 mm (Fig. 3-2B and 3-2D).

37 On the head, each ear is covered by short white hairs anteriorly, including the anterior margin. The posterior part of the ear is black. The base of the ear is thickly haired; these individual hairs are white at the tip and blackish basally. The eyes are ringed with black. The cheeks are whitish grey; the hair bases are brownish grey. The upper surface of the head is similar to the upper part of the body. The nose is surrounded by short dark brown hairs (Fig. 3- 2C). Unfortunately, the skull of the specimen was damaged by the hunter and, as a consequence, some cranial characters could not be observed in details. When viewed in lateral profile, it is relatively flat with a low braincase. The orbital regions are large. In lateral view, the zygomatic arches are low and the jugal bone is greatly expanded anteriorly. When viewed from above, the interorbital region is broad, exceeding the breadth of the postorbital constriction. The rostrum is short and wide. The frontal is deeply depressed. The postorbital processes are large and relatively long (Fig. 3-3A). In the dentition, the upper incisors are orthodont. The anterior surface of each tooth is pigmented with orange. The small upper premolar (P3) is relatively well developed and is situated on the anterior border of the second upper premolar (P4). This latter tooth is similar in size to the first (M1) and second upper molars (M2). The third upper molar (M3) is the smallest molar and circular in shape. In the lower dentition, the incisor is moderately long and is brownish orange on its anterior surface. The first premolar (P4) is the smallest tooth. All the molars are essentially similar in structure, but the third lower premolar (M3) is more elongated (Fig. 3-3B). The baculum of Petaurista petaurista is essentially straight and long, with the greatest length of 26.5 mm. It has a large simple base and is slightly narrower at the tip, where there is a spiral plate (Fig. 3-3C, 3-3D, and 3-3E).

Comparison Petaurista petaurista is similar to P. elegans in terms of external morphology, but differs in its larger size (in P. elegans: HB: 340–365 mm and T: 350–370 mm; Francis 2008). The ears of P. elegans are predominantly black and hairless, with dark tawny hairs at the base. In P. petaurista, the ears are white anteriorly and black posteriorly. The dorsal pelage of P. elegans has prominent white spots (Fig. 3-4A). The cheek and throat of P. elegans are pale orange, but

38 are white in P. petaurista. The skull of P. petaurista (ONL: 66–73 mm) is larger than that of P. elegans (ONL: < 65 mm) (Corbet and Hill 1992). Petaurista petaurista is more similar in size to P. philippensis (HB: 400–490 mm and T: 400–550 mm; Francis 2008) but differs in pelage color. Within the Indochinese region, P. philippensis has a much darker dorsal pelage that is extensively grizzled with white (Fig. 3-4B), whereas it is paler brown in P. petaurista and the grizzling is less extensive (Fig. 3-2A). The anterior half of the ears is brownish orange in P. philippensis but white in P. petaurista. In P. philippensis, the tail is either all-dark or all-grey but in P. petaurista, it is yellowish with a prominent dark brown or black tip (Fig. 3-4B and 3-4C). The skull of the P. petaurista specimen from Lao PDR is damaged. However, it appears to be essentially similar in size to that of P. philippensis (P3–M3: 15.0–17.8 mm; Corbet and Hill 1992). The Lao specimen was compared with the holotypes and/or original descriptions of seven taxa, which are currently referred to Petaurista petaurista (sensu Corbet and Hill 1992; Thorington and Hoffmann 2005) and which originate from mainland southeast Asia (Fig. 3-1). They are listed above as synonyms of P. petaurista and comprise P. p. candidula Wroughton, 1911 from northwest Myanmar; P. p. barroni Kloss, 1916 from southeast Thailand; P. p. taylori Thomas, 1914 from peninsular Myanmar; P. p. cicur Robinson and Kloss, 1914 from peninsular Thailand; P. p. terutaus Lyon, 1907 from Terutau Island, off the West coast of peninsular Thailand; P. p. penangensis Robinson and Kloss, 1918 from Penang Island, off the West coast of peninsular Malaysia; and P. p. melanotus Gray, 1837 from peninsular Malaysia. The Lao specimen differs from all these taxa with the exception of P. p. barroni. The taxon candidula is significantly paler, with extensive grizzling on the upper surface of the body, the chestnut hairs on the back are greatly interspersed with white; the undersurface is pure white; the external surface of the ear is white anteriorly and dark reddish-brown posteriorly; the tail is buffy grey, with a well-marked black tip. The taxon taylori is essentially deep reddish brown above, with some grizzling, whereas a large patch behind the ears and the edge of the interfemoral membrane are prominently black. The taxon cicur is a rich chestnut above, without grizzling; the margin of the antebrachial membrane and the muzzle are black; the distal half of the tail except for the black tip is orange brown. The taxon terutaus is a bright cinnamon-rufous on the upper body and patagia; there is some light grizzling, especially on the nape of the neck and shoulders; the undersurface is salmon-buff tending towards dull orange-

39 rufous on the patagia; the crown of the head is a mixture of whitish and cinnamon-rufous; the distal half of the tail except for the black tip is dull orange-rufous. The taxon penangensis is a rich chestnut above, without any grizzling; the undersurface is a creamy cinnamon; the margins of the patagia are whitish grey; the forehead is a mixture of some whitish and orange brown; the tail is deep orange brown with a short black tip. The taxon melanotus has a bright reddish-brown dorsal pelage and is without grizzling; it is pale on the cheeks and the undersurface. In contrast to the other taxa, which differ in a range of characters from the new specimen from Lao PDR, barroni from eastern Thailand is essentially similar. Its dorsal fur is comparable in color; it is chestnut brown grizzled with white above. The muzzle, cheeks, and throat are also white. The ears are dull white anteriorly and black posteriorly. The fringe of each patagium is white. The undersurface of the body is light rusty brown, with a cinnamon-brown extending on to the sides of the neck and membrane. Therefore, the Lao specimen is assigned to barroni, which is also the most geographically proximate taxon. Thorington and Hoffmann (2005) did not recognize barroni as a valid subspecies. However, on the basis of the pelage color of three Thai specimens from localities 4, 5, and 6 in Fig. 3-1 (specimen data listed in the Appendix 3- 1) and the new specimen from Lao PDR, barroni is here considered to be a distinct geographical race of Petaurista petaurista. The new specimen from Lao PDR is the first record of P. petaurista (sensu Corbet and Hill 1992; Thorington and Hoffmann 2005) from east of the Mekong River. On the basis of color, barroni appears most similar to Petaurista petaurista candidula, which is recognized as a discrete subspecies by Thorington and Hoffmann (2005). Other subspecies from the study area recognized by these authors are cicur, melanotus, penangensis, taylori, and terutaus. It is possible that future studies may show that penangensis and cicur are synonyms of P. p. melanotus. The taxon terutaus, although found in the Sundaic subregion, exhibits characters, such as grizzling on the dorsal surface, more associated with specimens from Indochina. The taxon taylori in peninsular Myanmar, on the border of the Sundaic/Indochinese subregions, also shares this character trait.

3.4 Discussion Kloss (1916) described the taxon barroni from Hup Bon Village, Sriracha District, Chonburi Province, southeast Thailand, approximately 13°7′N, 101°6′E. Originally referred to

40 Petaurista annamensis (which is currently considered to be a synonym of P. philippensis), it was subsequently included in alborufus by Askins (1977). Later, it was considered to be a synonym of P. petaurista by Corbet and Hill (1992) and Thorington and Hoffmann (2005), but it was omitted from the synonymy list by Thorington et al. (2012). Both Francis (2008) and Thorington et al. (2012) in their range maps omitted P. petaurista from eastern Thailand and thereby also omitted the type locality of P. p. barroni. Recently, Koprowski et al. (2016) included P. a. barroni as a subspecies of Petaurista albiventer Gray, 1834 described from Nepal, without explanation. The new Lao specimen of P. petaurista is differed from six subspecies described from mainland Southeast Asia, including P. p. candidula, P. p. cicur, P. p. melanotus, P. p. penangensis, P. p. taylori, and P. p. terutaus (Thorington et al. 2012). However, when compared with one flying squirrel described from Chonburi province, southeast Thailand named Petaurista annamensis barroni Kloss, 1916; it was described as subspecies of Petaurista annamensis Thomas, 1914 from khanh hoa province, South Vietnam; however, P. a. barroni is considered as synonym of P. petaurista (Corbet and Hill 1992; Thorington and Hoffmann 2005). The new specimen P. petaurista from Lao PDR shared similar morphological characters. In addition to the holotype of P. a. barroni, two specimens of flying squirrel which had been collected from Chaiyaphum and Nakhon Ratchasima provinces, northeast Thailand (Fig. 3-1, locality 4) were examined, and they are essentially correspond to morphological characters of P. a. barroni. The Laos and Thai P. petaurista specimens (including type of P. a. barroni) are separated from southern Thailand and Malay Peninsula subspecies (P. p. cicur, P. p. melanotus, P. p. penangensis, P. p. terutaus) by the Isthmus of Kra, and from western Thailand and Myanmar subspecies (P. p. candidula, P. p. taylori) by Chao Phraya River and its basin. The recent discovery of P. petaurista in southern Lao PDR indicates that this species is more widespread than previously reported (Corbet and Hill 1992; Thorington and Hoffmann 2005; Francis 2008; Thorington et al. 2012). As noted above, the market from where it was obtained is near the forests of the three formerly PNBCAs, which comprise Phou Theung, Bolaven northeast, and Phou Khanthong. This area is mostly covered with mixed deciduous forest and dry dipterocarp forest. The locality of the market, the hunting behavior of the local people, together with information obtained from the vendor, and the fact that it was already dead but still fresh, suggest that most probably it was captured in this area. Other bush meat in the

41 market included local species, such as Malayan porcupine (Hystrix brachyura Linnaeus), Red cheeked squirrel (Dremomys rufigenis Blanford), and Indochinese ground squirrel (Menetes berdmorei Blyth). Further surveys in the National Biodiversity Conservation Areas (NBCAs) near to this new locality should be conducted. These include Xe Sap NBCA, Dong Ampham NBCA, and Xe Piane NBCA. In order to clarify the actual distribution range of this species, it would be also of interest to conduct research elsewhere in Lao PDR and in areas of similar habitat in Cambodia and Vietnam. Finding this species as “bush meat” in a local market supports the view of Jenkins et al. (2005), who noted that ongoing market surveys in the country will provide an informative overview of the exploitation of animals occurring in the surrounding area and occasionally provide interesting species records. It also complements the very recent discovery of the new taxon of flying squirrel, Biswamoyopterus laoensis in an informal market in Central Lao PDR (Sanamxay et al. 2013). Moreover, this finding is also consistent with the view of Duckworth et al. (1999), who considered that one of the major threats to wildlife in Lao PDR is harvesting for food and trade.

42 Table 3-1. Body mass (in grams), external, cranial, dental and bacular measurements (in mm) of a single male Petaurista petaurista specimen from Lao PDR; measurements of the comparative taxa are taken from type descriptions. P. petaurista P. p. P. p. P. p. P. p. Characters P. p. cicur (from Lao PDR) candidula barroni terutaus penangensis M 1,500 – – – 1134 – HB 435 405 – 417 385 398 T 475 610 – 486 450 492 E 43 44 – 41 – – HF 70 84 – 77 – 72 ONL – – 77 70.5 64.3 67 CBL – 60 67.2 62 – – ZB 47.9 51 49 47.9 43.2 44.3 ZH 7.27 – – – – – BB 31.73 – – – – – BH – – – – – – RB 16.3 – – – – – NL 24.53 – 24.6 20.3 – 19.1 IOB 17.87 – 19 14 12.4 15 POB 14.87 – – – 16.6 15.6 POPB 37.09 – 39 – – – LIF 4.71 – – – – – LAB – – – – – – LBP – – – – – – PPL – – – – – – MWN 13.81 – 14 – – – P3M3 15.46 – 18.2 16.2 14.2 – M2M2 17.83 – – – – – M1M1 6.65 – – – – – ML 43.28 – – – – – MH – – – – – –

P4M3 16.16 – – – 15 – IBG – – – – – – MB – – – – – – BL 26.47 – – – – –

43

Figure 3-1. The subspecies and synonyms of Petaurista petaurista in mainland Southeast Asia with a description of the dorsal and ventral pelage and tail of each taxon. Black triangle represents the new locality in Lao PDR. Black circles are type localities of the taxa that are currently referred to P. petaurista (sensu Corbet and Hill 1992; Thorington and Hoffmann 2005). Open circles are localities of P. petaurista collected from this region, which are held in the Natural History Museum, London [BM(NH)] and Natural History Museum, National Science Museum Thailand [NHM]. Numbers from 1 to 23 refer to localities listed in Appendix 3-1.

44

Figure 3-2. Views of skin of Petaurista petaurista (FES.MM.13.001) from Lao PDR. (A) Dorsal view; (B) ventral view; (C) head, left lateral view; and (D) ventral view of the left patagium and interfemoral membrane to show edge of patagium and interfemoral membrane (scale = 300 mm).

45

Figure 3-3. (A) Views of skull, mandible (scale = 50 mm) and (B) dorsal views of the left maxillary (left) and left mandibular (right) toothrows (scale = 5 mm) of Petaurista petaurista (FES.MM.13.001); (C) dorsal view, (D) lateral view, and (E) ventral view of bacula of Petaurista petaurista (FES.MM.13.001), P. philippensis, and P. elegans, from left to right, respectively (scale = 10 mm).

46

Figure 3-4. Views of skins. (A) Dorsal view of Petaurista elegans (FES. MM.12.161); and (B) dorsal and (C) ventral views of P. philippensis (FES.MM.12.152) from Lao PDR (scale = 300 mm).

47 Appendix 3-1 Specimens of Petaurista petaurista held in the Natural History Museum, London (BM[NH]) and the Natural History Museum (NHM), National Science Museum Thailand (NSM). Numbers from 1 to 23 in parentheses refer to localities included in Fig. 3-1. (1) BM(NH).10.10.19.4; Kindat, upper Myanmar, approximately 23°44′N, 94°26′E. (2) BM(NH), not registered; Mogaung, Kachin, Myanmar, approximately 25°18′N, 96°56′E. (3) BM(NH).15.5.5.40; Kin, Sagaing, Myanmar, approximately 22°45′N, 94°41′E. (4) THNHM- M-2344; Khon San, Pa Phu Khieo, Chaiyaphum, Thailand, approximately 16°31′N, 101°45′E. (5) THNHM-M-2340; Sakae Rat, Nakhon Ratchasima, Thailand, approximately 14°36′N, 102°2′E. (6) BM(NH).47.1472; Hup Bon, Sriracha, Chonburi, Thailand, approximately 13°7′N, 101°6′E. (7) BM(NH).14.12.1.5; Bankasun, Tenasserim, Myanmar, approximately 12°4′N, 99°1′E. (8) BM(NH).55.1656 and BM(NH).55.1657; Koh Lak, Prachuap Khilikhan Province, Thailand, approximately 11°47′N, 99°48′E. (9) BM(NH).49.431; Khok Klap, peninsular Thailand, approximately 8°53′N, 99°17′E. (10) BM(NH).10.10.1.79; Nong Thale Song Hong, Trang Province, approximately 7°51′N, 99°29′E. (11) BM(NH).55.1649; Koh Klang, Trang Province, Thailand, approximately 7°21′N, 99°34′E. (12) NMNH.123.934; Terutau Island, Straits of Malacca, Thailand, approximately 6°37′N, 99°40′E. (13) BM(NH).49.433; Penang Island, Malaysia, approximately 5°27′N, 100°13′E. (14) BM(NH).5.6.15.1; Larut hills, Perak, Malaysia, approximately 5°1′N, 100°53′E. (15) BM(NH).1939.2373; Perak, Malaysia, approximately 4°48′N, 100°47′E. (16) BM(NH), not registered; Selangor, Malaysia, approximately 3°38′N, 101°30′E. (17) BM(NH).28.7.20.62; Hutan Rizab Semangkok, Selangor-Pahang Boundary, Malaysia, approximately 3°39′N, 101°45′E. (18) BM(NH).61.1164; Bukit Pelindong, Kuantan, Pahang, Malaysia, approximately 3°50′N, 103°22′E. (19) BM(NH).22.8.12.2; Kuala Selangor, Malaysia, approximately 3°20′N, 101°14′E. (20) BM(NH).61.1163; Ulu Gombak Forest Reserve, Malaysia, approximately 3°18′N, 101°46′E. (21) BM(NH).8.1.25.6, BM(NH).8.1.25.7, BM(NH).55.1652, BM(NH).71.2714; Tioman Island, Mersing Johor, Malaysia, approximately 2°47′N, 104°10′E. (22) BM(NH).62.192 and BM(NH).85.8.1.118; Gunung Belumut Recreational Forest, Johor, Malaysia, approximately 2°1′N, 103°32′E. (23) BM(NH).118.8.14.2; Singapore, approximately 1°22′N, 103°48′E.

48 CHAPTER 4

First record of Temminck’s flying squirrel, Petinomys setosus from Lao PDR

4.1 Introduction The genus Petinomys (Rodentia: Sciuridae) consists of eight species that are widely distributed in southern India, Sri Lanka, northern Myanmar, northern Thailand, Malaysia, Sumatra, and the northern third of Borneo (Thorington et al. 2012; Koprowski et al. 2016). Temminck’s flying squirrel, Petinomys setosus (Temminck 1844) was originally described from Sumatra, and is widely distributed in Southeast Asia but has a disjunct range. Six distribution areas are recognized: 1) northern Myanmar, 2) eastern Myanmar and northern Thailand, 3) southern Thailand, 4) southern peninsular Malaysia, 5) Sumatra, and 6) the northern third of Borneo (Thorington et al. 2012; Koprowski et al. 2016). In northern Thailand, P. setosus occurs in deciduous forests at 1300–1700 m elevation (Muul and Thonglongya 1971). Petinomys setosus has not been recorded in Lao PDR, although Duckworth et al. (1999) suggested its potential occurrence in parts of northern Lao PDR where there is similar habitat to northern Thailand. Here, I report a single male Temminck’s flying squirrel collected from Vientiane province in Central Lao PDR that represents the first record of this species in Lao PDR (Sanamxay et al. 2019). This recent record is increased to nine the number of flying squirrels occurred in the country, the other eight being Petaurista elegans (Müller), P. philippensis (Elliot), Belomys pearsonii (Gray), Hylopetes alboniger (Hodgson), Hylopetes phayrei (Blyth), and Hylopetes spadiceus (Blyth), Biswamoyopterus laoensis (Sanamxay et al. 2013), and Petaurista petaurista (Sanamxay et al. 2015).

4.2 Materials and Methods During a bat survey in a forest near the Ang Louang cave at Na Mouang village, Vangvieng district, Vientiane province, Lao PDR (18°53'21.97"N, 102°22'50.08"E, 255 m in elevation) during August 12–19, 2017, a mature male flying squirrel was captured by a mist net that was set across a trail between an outcrop and a small patch of disturbed forest (Fig. 4-1). The net was 9 m long and was set 6 m above the ground from 18:00 until sunrise. The focal P. setosus specimen was deposited at the Faculty of Environmental Sciences, National University

49 of Laos (collection code FES.MM.17.001). The skull was extracted, the skin was dried, and tissue samples were stored in 95% ethanol. I compared this specimen to others held in the Thailand Natural History Museum (THNHM; See Appendix 4-1), which included three from Thailand (two males and one female), and four males from Peninsular Malaysia. As per Hayashida et al. (2006), Helgen et al. (2009), and Koyabu et al. (2009), five external and 23 cranial measurements were taken using digital calipers (Mitutoyo Corporation, Japan) and a digital scale (Tanita Corporation, Japan). The measurements included: body mass (M), head and body length (HB), tail length (T), ear length (E), hindfoot length (HF), occipitonasal length (ONL), condylobasal length (CBL), mastoid breadth (MB), zygomatic breadth (ZB), zygo- matic height (ZH), breadth of braincase (BB), braincase height (BH), rostrum breadth (RB), nasal length (NL), maximum width of nasal bones (MWN), interorbital breadth (IOB), postorbital breadth (POB), length of the incisive foramina (LIF), length of bony palate (LBP), postpalatal length (PPL), length of auditory bulla (LAB), interbullae gap (IBG), upper toothrow length (P3–M3), greatest palatal breadth (M2–M2), width of the bony palate at the first upper molar (M1–M1), mandible length (ML), mandible height (MH), and lower toothrow length (P4–M3).

4.3 Systematics

Petinomys setosus (Temminck, 1844)

Holotype Pteromys (Sciuropterus) setosus Temminck, 1844: 49; Padang, West Sumatra, Indonesia.

New material FES.MM.17.001, mature male, skull extracted, dry skin, tissue samples and baculum were stored in 95% ethanol; collected at Ang Louang cave, Na Mouang village, Vangvieng district, Vientiane province, Lao PDR (18°53'21.97"N, 102°22'50.08"E, 255 m in elevation). Deposited at the Faculty of Environmental Sciences, National University of Laos, Lao PDR.

50 Description The upper head and body pelage of this specimen are predominantly an admixture of brown and black hairs, variably grizzled with pale buff; upper surfaces of the membrane are black, extensively grizzled with creamy white, and its margin is creamy brown. The tail is distichous with a narrow base; its dorsal and ventral pelage is brownish black, with whitish-grey coloration at the base and creamy white at the tip of the tail. The cheeks, throat, ventral body surface, and membranes are generally creamy white. There is a black eye ring with a black streak continuing to its nose. The sides of its neck are grey. Its ears are naked, though tufts of long black hairs surround their base (Fig. 4-2). The dorsal surface of its fore and hind feet are black-brown. When viewed from above, the rostrum is short and wide (Fig. 4-3). The frontal is not depressed. The postorbital processes are tiny and short, and the postorbital constriction is relatively broader than the interorbital region. There is a pair of swellings near the midline at the posterior end of the frontal. The braincase is relatively broad. When viewed from the lateral profile, the braincase is considerably high. The orbital sockets are broad. The anterior portion of the jugal bone is not well developed. The mastoid regions are large, but not inflated. When viewed ventrally, the auditory bullae are large with a honeycomb pattern but not prominently inflated; there are at least 14 septae inside each auditory bulla. The mandibular coronoid process is well developed. The condylar process has a large dorsal articular surface, and the post-condylar process is well developed. The angular process is upwardly projecting. The upper incisor is orthodont. The anterior surface of each tooth is yellow. The third tiny upper premolar (P3) is well developed; P4 is relatively smaller than M1, M2, and M3, all of which have lightly pitted enamel. The anterior surface of the lower incisor is similar to the upper incisor.

The forth premolar (P4) is approximately half the size of the first molar (M1) with light pitted enamel. All lower molars are lightly pitted enamel. The first and second lower molars (M1 and

M2) are essentially similar to P4. The third lower molar (M3) is elongated posteriorly on the labial side, longer than M and M2, and has extremely reduced lingual cusps (Fig. 4-3).

51 Comparison This Petinomys setosus specimen from Lao PDR is similar to P. setosus specimens from northern Thailand. Specimens from both areas have an admixture of brown and black hairs on dorsal pelage, creamy white ventral pelage, a black eye ring that continues to the nose, and a white- tipped tail (Fig. 4-2). Moreover, most of their morphometric measurements overlap. However, when comparing other measurement values, P. setosus from Lao PDR has a longer tail (T), shorter ear (E), broader rostrum breath (RB), and higher braincase height (BH) and mandible height (MH) than specimens from Thailand (Table 4-1). The Laos and northern Thailand specimens differ from those collected from peninsular Malaysia which have prominent reddish-brown in dorsal pelage, a reddish-brown tail without a white tip, and narrow reddish-brown eye rings. The specimen from Lao PDR has a longer tail (T), broader braincase breath (BB) and postorbital breadth (POB), and higher braincase height (BH) when compared to Malaysian specimens (Table 4-1).

4.4 Discussion The genus Petinomys is similar to the genus Hylopetes in term of general pelage color and size, but Petinomys is diagnosed by having a tuft of long hairs at base of the ears and multiple septae in the auditory bullae (Corbet and Hill 1992). The specimen from Lao PDR has these characters of the genus Petinomys and was identified as Petinomys setosus based on its admixture of brown and black hairs on dorsal pelage, creamy white ventral pelage, black eye rings that connect to a black streak along its nose, and its white-tipped and flat feather-shaped tail (Fig. 4-2). The auditory bullae are honeycomb-patterned with at least 14 septae in each auditory bulla (Fig. 4-3). The greatest length of the skull is smaller than for other species in this genus, except Petinomys vordermanni, but P. vordermanni has a black- and rust-colored dorsal pelage, orange cheeks, black eye rings not connected to its nose, and complex septae in the auditory bullae (Corbet and Hill 1992; Francis 2008). The P. setosus capture location was on the east side of the Mekong River, which is hypothesized to serve as geographical barrier that affects the dispersal and diversification of some rodent species such as Callosciurus inornatus, Dremomys gularis, Tamiops maritimus, and Maxomys moi (Meijaard and Groves 2006). Around 1.5 million years (Myr) ago, the Mekong River flowed into the Salween River via the present Ping River of northern Thailand,

52 then shifted eastwards to its present course towards the Vientiane capital in Lao PDR (Meijaard and Groves 2006). According to molecular studies by Oshida et al. (2011, 2013), the divergence time between Callosciurus caniceps and C. inornatus, Callosciurus finlaysonii, and Callosciurus erythraeus griseimanus occurred around 1.2 Myr ago, when the Mekong River was a considerable geographical barrier between these two species. The formation of the Mekong River could also have led to genetic differences between P. setosus populations in northern Thailand and Central Lao PDR; a molecular study should be carried out to test this hypothesis. The Temminck’s flying squirrel has highly isolated distribution in Southeast Asia (Koprowski et at. 2016), with two forms P. s. setosus Temminck, 1844 and P. s. morrisi Carter, 1942, and those two forms could be recognized as populations under and upper the Isthmus of Kra—the Isthmus of Kra is considered to the barrier separated in to the North and South at the Isthmus of Kra—, respectively (Thorington et al. 2012). These two forms were also proposed as valid subspecies by Muul and Thonglongya (1971) based on these following morphological characters: the specimens from northern Thailand and the one from northern Myanmar appear to larger than those from South of the Isthmus of Kra (Sumatra, East and West Malaysia, and southern Thailand), and the consistent presence of a white tip on the tail. In this study, we also found that the Laos and northern Thailand specimens differ from those collected from Peninsular Malaysia which have prominent reddish-brown in dorsal pelage, a reddish-brown tail without a white tip, and narrow reddish-brown eye rings. As well some measurements are relatively larger. However, the statistical analysis functions that Muul and Thonglongya (1971) was not clear enough to support larger size of P. s.morrisi than P. s. setosus. Thus, recently they are considered as same species (Koprowski et al. 2016). Future analysis on their measurements and molecular data are needed to clarify their taxonomic status. According to a range map of P. setosus in the IUCN Red List (Clayton 2016), there is a population in southern Vietnam, but there has been no explanation of this distribution. There have been no reports of P. setosus occurring in Vietnam (Corbet and Hill 1992; Thorington and Hoffmann 2005; Francis 2008; Huynh et al. 2008; Jackson and Schouten 2012; Thorington et al. 2012; Koprowski et al. 2016); thus, this IUCN map may be erroneous. This record of P. setosus in Lao PDR may represent the seventh disjunct population of this species, according to a previous range map (Thorington et al. 2012; Koprowski et al. 2016).

53 Thus, additional studies of their divergence, geographic variation, population size, ecology, and distribution are necessary, and additional field surveys of flying squirrels in Lao PDR should be conducted. In Lao PDR, the record of P. setosus was collected from small patch of disturbed forest at the foothill of an isolated limestone outcrop, approximately 500 m from tourism sites, residential areas, and plantations. Similar to the southern part of its range, where this species is experiencing greater habitat loss, it is found in lowland forests (Thorington et al. 2012). But, in northern Thailand, P. setosus occurs in deciduous forests at 1300–1700 m in elevation (Muul and Thonglongya 1971).

54 Table 4-1. Body mass (in g), external, cranial, and dental measurements (in mm) of the focal male P. setosus specimen from Central Lao PDR, and specimens from northern Thailand and western Malaysia. P. setosus P. setosus P. setosus Characters (northern Thailand; n = 3) (western Malaysia; n = 4) (Lao PDR; n = 1) Min–Max Mean Min–Max Mean M 47 - - 28.60–58.00 42.40 HB 129.8 111–140 123.67 109–127 116 T 126.9 116–120 117.33 93–119 106 E 15.3 17–19 17.67 14–15 14.75 HF 24.8 18–24 21.33 22–24 23 ONL 32.12 - - - - CBL 30.46 27.91–30.50 29.31 26.98–30.56 28.93 MB 16.94 - - - - ZB 19.56 - - - - ZH 2.05 1.83–1.91 1.88 1.40–2.03 1.65 BB 16.64 16.20–16.82 16.50 15.37–15.97 15.68 BH 11.58 10.09–11.02 10.50 9.79–10.92 10.39 RB 7.09 5.75–6.46 6.06 5.86–6.59 6.31 NL 7.58 7.23–7.83 7.48 6.99–7.98 7.36 MWN 4.26 4.45–4.94 4.63 3.82–4.67 4.28 IOB 7.07 6.59–6.89 6.75 6.19–6.61 6.41 POB 10.84 10.54–11.47 11.08 8.42–9.96 9.25 LIF 2.61 2.30–2.79 2.54 1.80–2.10 1.96 LBP 9.53 8.99–9.68 9.36 9.05–10.62 9.73 PPL 12.64 10.86–12.76 11.99 - - LAB 7.51 6.69–7.73 7.05 6.55–7.47 6.86 IBG 2.06 - - - - P3–M3 5.66 5.47–5.79 5.60 5.08–5.43 5.29 M2–M2 7.65 7.24–7.51 7.38 7.27–7.89 7.53 M1–M1 4.33 4.25–4.39 4.33 4.33–5.01 4.68 ML 17.84 16.99–17.41 17.20 16.25–17.66 17.19 MH 11.83 9.68–10.89 10.37 9.49–11.63 10.88

P4–M3 5.68 5.33–5.58 5.47 5.23–5.46 5.34

55

Figure 4-1. Geographical distribution of P. setosus adapted from the IUCN Red List. The black triangle represents the new locality in Lao PDR. The shaded areas represent their range according to the IUCN Red List. The black dotted line represents the Mekong River.

56

Figure 4-2. External views of P. setosus from Lao PDR: dorsal (left), ventral (right), and a close up view of the head (bottom). The white bar represents 100 mm for the dorsal and ventral views.

57

Figure 4-3. Cranial and dental views of P. setosus from Lao PDR. The white bar represents 10 mm for the cranium; the gray bar represents 5 mm for the dentition (above, left maxillary toothrow; below, left mandibular toothrow).

Appendix 4-1 Specimens of Petinomys setosus held in the Thailand Natural History Museum (THNHM). Two males: THNHM-M-2320 and THNHM-M-2317; Doi Pui, Chaing Mai, Thailand. One female: THNHM-M-2318; Doi Inthanon, Chaing Mai, Thailand. Four males: THNHM-M-2179, THNHM-M-2263, THNHM-M-2264, and THNHM-M-2319; western Malaysia.

58 CHAPTER 5

General discussion

In mainland Southeast Asia, there are consisting of nine genera, 19 species (Koprowski et al. 2016). As in Chapter 2, a new species Biswamoyopterus laoensis from this study contributes to number of species in this region. In Lao PDR, previously reported three genera, six species include Petaurista philippensis, P. elegans, Belomys pearsonii, Hylopetes alboniger, H. phayrei, and H. spadiceus (Duckworth et al. 1999; Thorington et al. 2012). In this presence study I summarized five genera, nine species in Lao PDR by including Petaurista petaurista, Biswamoyopterus laoensis, and Petinomys setosus. Thus, the country contained 55.5% of genus, and 47.4% of species in mainland Southeast Asia. However, it should be noted that P. yunanensis was mentioned to occur in northern of Lao PDR (Francis 2008; Koprowski et al. 2016) where similar habitat of type locality in Yunnan Province, China; however, there is no certain record of specimen from the country. Also, in the survey of this study I did not find this species. Therefore, this study omitted P. yunanensis for the list of flying squirrels in Lao PDR. The most common species are Petaurista philippensis, Belomys pearsonii, and Hylopetes phayrei which found throughout the country (see Table 1-2; Fig. 1-3 in Chapter 1). These three species are widely distributed in this region (Thorington et al. 2012; Koprowski et al. 2016). Additionally, Belomys pearsonii is previously known from Central of Lao PDR (Duckworth et al. 1999; Francis 2008; Thorington et al. 2012; Koprowski et al. 2016) but this study I found that it is widely distributed in the country. Lao PDR is third rank in term of number of genera diversity with five genera compared to Malaysia has seven genera, and Thailand has six genera. In term of species diversity, Lao PDR also third rank with nine species, while the first rank is shared between Myanmar, Thailand and Malaysia with 11 species (Fig. 5-1). This diversity of flying squirrels found in Lao PDR may relates to high variety of habitat in the country which comprised of eight Ecoregions— based on forest type—, including 1) Northern Indochina subtropical forests; 2) Northern Thailand-Laos moist deciduous forests; 3) Louang Prabang montane rain forests; 4) Northern Khorat Plateau moist deciduous forests; 5) Central Indochina dry forests; 6) Northern Annamites rain forests; 7) Southern Annamites montane rain forests; 8) Southeastern Indochina

59 dry evergreen forests (Mekong River Commission 2015). This high variety of habitat is also home for other wildlife species which could be explained by recent new discovery of bat species such as Murina annamitica Francis and Eger, 2012, Hypsugo dolichodon Gorfol et al., 2014; reptile species such as Parafimbrios lao Teynie et al., 2015, Gekko aaronbaueri Tri et al., 2015; amphibian species such as Philautus nianeae Stuart et al., 2013, Tylototriton podichthys Phimmachak et al., 2015; bird species such as Phylloscopus calciatilis Alstrom et al., 2010. In total 19 species in mainland Southeast Asia, there are 15 species of flying squirrel found in the Indochinese division—Myanmar, Lao PDR, Vietnam, Cambodia, Thailand (North Isthmus of Kra)—including Petaurista alborufus, P. caniceps, P. elegans, P. pataurista, P. philippensis, P. yunanensis, Biswamoyopterus laoensis, Aeromys tephromelas, Belomys pearsonii, Pteromyscus pulverulentus, Hylopetes alboniger, H. phayrei, H. spadiceus, Petinomys setosus, and P. vordermanni. There are four species—Iomys horsfiedi, Hylopetes platyurus, Petinomys genibarbis, Petaurillus kinlochii—that restricted to Malay Peninsula which classified in the Malayan division of the Sundaic subregion (Fig. 5-1). There are many species boundaries at the Isthmus of Kra defining the southern boundary of the subregion, which also lacks many Sunda taxa and endemic genera that do not extend North of the Isthmus of Kra, e.g. Echinosorex, Sundasciurus (Corbet and Hill 1992). The separation of Indochinese and Malayan divisions by the Isthmus of Kra is also observed in other wildlife such as reptiles (Pauwels et al. 2003), and birds (Hughes et al. 2003). Discovering of B. laoensis and P. setosus from the region of limestone karsts, which is home to rare and endemic rodent species such as the Kha-nyou, Laonastes aenigmamus Jenkins et al., 2005 and the Lao limestone rat, Saxatilomys paulinae Musser et al., 2005. Furthermore, endemism is not restricted to rodents or even mammals: the area is also home to the endemic Lao langur, Trachypithecus laotum (Thomas 1921) and in birds to the recently discovered bare- faced bulbul, Pycnonotus hualon Woxvold et al. (2009). This may support the hypothesis that limestone karst serves as area for species diversification. Further study is needed to know their habitat, distribution, and natural population for sustainable conservation purpose not only flying squirrel itself but also habitat where they are living.

60

Figure 5-1. Species diversity and composition of flying squirrels of six countries in mainland Southeast Asia. Question marked (?) meant there is no specific collected of specimen.

The new locality record of 3 flying squirrels—Biswamoyopterus laoensis, Petaurista petaurista, Petinomys setosus—from Lao PDR is extended to East side of Mekong River, which is hypothesized to serve as geographical barrier that affects the dispersal and diversification of some rodent species such as Callosciurus inornatus, Dremomys gularis, Tamiops maritimus, and Maxomys moi (Meijaard and Groves 2006). According to molecular studies by Oshida et al. (2011, 2013), the divergence time between Callosciurus caniceps (West side of Mekong River) and C. inornatus (East side of Mekong River), Callosciurus finlaysonii (West side of Mekong River), and Callosciurus erythraeus griseimanus (East side of Mekong River) occurred around 1.2 Myr ago, when the Mekong River was a considerable geographical barrier between these comparing two pairs species. This genetic differentiation could also observe in other wildlife such as Big-headed field cricket, Brachytrupes portentosus (Tantrawatpan et al. 2011); Siamese mud crap, Henicorhynchus siamensis (Adamson et al. 2009); and amphibian species (Geissler et al. 2015). The formation of the Mekong River could also have led to genetic differences between the flying squirrels on West and East sides of the Mekong River. The molecular study and details morphology examination should be carried out to test this hypothesis.

61 The latest report on diversity of flying squirrels in Lao PDR provided number of species and distribution where authors did the survey in the country (Duckworth et al. 1999); however, it lacks of description/diagnostic characters of each species. Therefore, this study is provided the summary of key characters of flying squirrels occur in Lao PDR (Table 5-1).

Table 5-1. The key characters of eight flying squirrels occur in Lao PDR. Measurements in millimeter. Septae in

Characters auditory HB ONL IBG bullae Min–Max Cheeks Ears Min–Max Min–Max (number); H= (M±SD) (M±SD) (M±SD) honeycomb Species pattern brownish- dark reddish orange hairs Pe. philippensis 440–520 brown and 73.50–79.71 8.26–10.39 anteriorly and 2–4 (n = 12) (467.13±21.59) grizzled (76.87±1.74) (9.27±0.66) long black hairs whitish-grey posteriorly white hairs Pe. petaurista anteriorly and 435 whitish grey n/a n/a n/a (n = 1) long black hairs posteriorly black and pale orange hairless; Pe. elegans 330–345 mixed with posterior half 58.14–60.53 6.08–7.17 1–3 (n = 6) (337.50±6.12) some black and back base is (59.40±0.98) (6.56±0.42) hairs dark tawny patch Naked dark deep red and grey/black, tuft Bi. laoensis 400–455 70.96–74.39 5.01–6.62 grizzled of long black > 12/H (n = 5) (430.00±23.72) (72.24±1.31) (5.75±0.64) whitish-grey hairs surrounds the base

62 brown hairs creamy white with tuft of long Be. pearsonii 178.24–191.00 39.76–40.90 2.83–3.97 mixed with black hairs > 15/H (n = 3) (182.79±7.13) (40.27±0.58) (3.29±0.60) light brown surround the base White tinged Hy. alboniger 206.65 with pale n/a n/a 6.05 3 (n = 1) yellow dark brown White tinged hairs and a Hy. phayrei 149.26–199.00 39.50–43.64 3.91–7.34 with pale small pale grey 3 (n = 26) (174.46±10.33) (41.57±1.28) (4.96±1.05) yellow patch at the back base dark brown Creamy white hairs and a Hy. spadiceus 115.37–134.66 33.14–34.36 3.19–3.73 tinged with small creamy 3 (n = 5) (125.35±8.87) (33.81±0.50) (3.48±0.25) light orange white patch the at back base Naked dark grey/black, tuft Pet. Setosus 129.80 Creamy white of long black 32.12 2.06 > 14/H (n = 1) hairs surrounds the base Note: (M±SD) = (Mean±Standard diviation) n/a = not available HB = Head and body length ONL = Ocipital nasal length IBG = Inter bulla gap Pe = Petaurista Bi = Biswamoyopterus Be = Belomys Hy = Hylopetes Pet = Petinomys

63 Conclusion

This present study gains better understanding of the taxonomy, diversity, and distribution of flying squirrels in Lao PDR, also Southeast Asia by combination of external, cranio-dental, and baculum morphological characters and measurements. As the result, I could achieve the following contributions: discovery of a new species of flying squirrel, Biswamoyopterus laoensis, which is the second species of the genus Biswamoyopterus newly described from Southeast Asia. Confirmed the occurrence of Petaurista petaurista and Petinomys setosus in Lao PDR with the expansion of the species range. In addition, the specimen of P. petaurista from South of Lao PDR is assigned to P. annamensis barroni described from southeast Thailand, and considered as valid subspecies of P. petaurista. In summary, based on my research I fundamentally summarized nine species of five genera occur in Lao PDR, including Petaurista philippensis, P. petaurista, P. elegans, Biswamoyopterus laoensis, Belomys pearsonii, Hylopetes alboniger, H. phayrei, H. spadiceus, and Petinomys setosus. The key characters and distribution of each species are also provided.

64 ACKNOWLEDGEMENTS

I am grateful to Professor. Dr. Masaharu Motokawa (The Kyoto University Museum, Kyoto University) for his great support and supervision of my research in Japan. I would like to thank Professor. Dr. Tatsuo Oshida (Laboratory of Wildlife Biology, Obihiro University of Agriculture and Veterinary Medicine) who has supervised and always encouraged me throughout my study. I am most grateful to the JSPS RONPAKU Program, JSPS Core-to-Core Program B Asia Africa Science Platforms, and KAKENHI grant JP18H03602 for supporting scholarship for my study, filed survey in Lao PDR and airfare for examine specimens in many countries. I acknowledge the ‘2011 Thailand On-Place Scholarship under the ASEA-UNINET Program for Cambodia and Lao PDR’; the Systematics Association, UK; the Darwin Initiative, UK (Project No: 18002); the Institute Pasteur du Laos; the National Geographic Foundation (Grant No. Asia-53-16); Nagao Environmental Foundation; and the Kyoto University Museum for their financial support of our field work, contribution towards setting up a zoological research collection in Faculty of Environmental Sciences, National University of Laos. In Japan, I am most grateful to laboratory members in the Kyoto University Museum, including Mr. Shinya Okabe, Mr. Yugo Ikeda, Mr. Takashi Yato, Mr. Yutaka Toyama, Ms. Umi Matsushita, Mr. Jadab Kumar Biswas, Mr. Wai Min Thu, Mr. Hu Yifeng, Ms. Jingwen Shi, Ms. Lin Chaoyu who always help and encouragement during my time staying in Japan. In Lao PDR, I would like to thank the staff of the Faculty of Environmental Sciences, National University of Laos for their help, support and encouragement; Thanks to the staff of Ministry of Agriculture and Forestry, Lao PDR who involved in the field survey in Lao PDR for their help in the field and permission documents. Last and best, I would like to thanks my parents for their support and encouragement. Special thanks to my wife, Nouansy Sysompheng and my daughter, Chanthida Sanamxay who always encouragement, patients and understanding.

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