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Title Systematic Study of Flying Squirrels (Mammalia, Sciuridae) In 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
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