TROPICS Vol. 10 (1): 63-7L Issued May 30, 2000

Biogeography of Living in the

Masahanr MoToKAwA The University Museum, Sakyo, Kyoto 606-8501,

ABSTRACT The faunas of the living non-volant mammals in the Ryukyu Islands are geographically different among northem, central and southem islands, and the Senkaku Group. The Tokara Gap and the Kerama Gap are recognized as important borders ofdistributional ranges, The northem Ryukyu species are the same as those on the main-islands ofJapan; probably they have been isolated only since the late Pleistocene. The central Ryukyu species include endemic elements that are considered as Miocene immigrants, The southern Ryukyu Islands has one endemic species, Prionailurus iriomotensis, which was possibly derived from the ancestral form ofP. bengalensis in the middle Pleistocene. The Senkaku Group has two species, of which lVesosc aptor uchidai is endemic to this island group at the generic level. This may be closely related to Mogera insularis in Taiwan. The second species, agrarius, is a continental species and probably immigrated in the late Pleistocene,

Key words: phylogeny / distribution / biogeography / Pleistocene / Miocene

The Ryukyu Islands is a long archipelago, about 1200 km in length ranging between Kyushu and Taiwan (Fig. 1). It consists of approximately 150 islands (Mezaki, 1980). Seven island groups are usually recognized for this archipelago: osumi, Tokara, Amami, okinawa, Miyako, Yaeyama and Senkaku Groups (Fig. 1). In the Ryukyu Islands, several endemic species of mammals occur, making this archipelago an interesting and important region for the studies of evolution and conservation of mamrnals (Abe et al., 1994). Nevertheless, the origin and biogeography have been discussed for some remarkable species only (Kizaki & Oshiro, 1977). Herc,I discuss the distributional patterns of the Ryukyu living non- volant mammals and their biogeographical implications through a review of published data. The specific names follow Wilson & Reeder (1993) unless otherwise stated. Distribution data are taken from Abe et al. (1994), Motokawa (1996) and Funakoshi (1993). Five species, the house rut Rottus norvegicus, the black nt tanezurni, the house mouse Mzs musculus and the house musk murinus in the Ryukyus, and the Japanese deer Cervus nippon in ttre Okinawa Group, are excluded from the present discussion, because they were possibly introduced with human activities (Kuroda, 1924; l+be et al.,1994). Distributions of the Ryukyu mammals are shown in Table 1. A total of 18 non-volant mammals are known from the Ryukyus, eight of which are endemic to this region. Based on distributional patterns, the Tokara Gap between northern and southern and the Kerama Gap between the Okinawa and the Miyako Groups are recognized as important barriers to dispersals for most Ryukyu mammals (see below). The fauna of the Senkaku Group is different from those in 64 M. MOTOKAWA

Fig. 1. The map of the Ryukyu Islands.

the rest of the Ryukyus. Thus, the Ryukyu Islands is divided into four regions for the following discussion: northern, central and southern islands as divided by the Tokara and Kerama Gaps, and the Senkaku Group. Among the Ryukyu non-volant mammals, the wild boar Szs scrofa is widely distributed in the Palaearctic and Oriental regions including the Ryukyu Islands, the main-islands of Japan, Taiwan and continental China (Corbet & Hill, L992; Abe et al., 1994). In the Ryukyus, this species is recorded from Amamioshima and of the Amami Group, Okinawajima of the Okinawa Group, and Ishigakijima and kiomotejima of the Yaeyama Group (Abe et al., 1994\. Such a distribution of this species is exceptional in that it includes both sides of the Kerama Gap. The Ryukyu populations of this species are characterized by smaller overall size and some unique morphological characters (Kuroda, 1924; Semba, 1964; Imaizumi, 1973). As a result, these populations are sometimes considered as a relict form deserving a distinct subspecies (as S. scrola riukiuana [see Kuroda, L924; Ellerman & Morrison-Scott, 19511) or even a full species status (as S. riukiuana [see Imaizumi, L9731). On the other hand, Semba (1964) supposed that the Ryukyu populations had originated from introduced domestic of ancient people in the Ryukyus. It is also possible that the hybridization occurred between the Ryukyu relic form and the inhoduced boar. As such, problems regarding the origin and taxonomic status of the Ryukyu wild boar are highly complicated and definitely need further intensive studies.

NORTHERN RYUKYUS

Seven species of mammals, the Japanese white-toothed shrew dsinezumi, the Japanese Mogera wogura (specific name following Motokawa & Abe [1996]), the Japanese monkey Macaca fuscata, the Japanese weasel Mustela itatsi, the Japanese deer Cerws nippon, the Japanese Biogeography of mammals in the Ryukyus 65

Table 1. Distribution of the non-volant terrestrial mammals in the Ryukyu Islands. Species Island groups and regions MI OS NT ST AM OK MY YY SK TW Soricidae Crocidura dsinezumi +++ Crocidura orii I + Crocidura watasei l'2 ++ Mogera wogura 3 ++ Nesoscaptor uclidai I Cercopithecidae Macaca fuscata ++ Felidae P r ion ailur us ir iomo tens is 1'4 Mustelidae Mustela itatsi ++ Suidae Sus scrofa + ++++ Cervidae Ceraus nWon ++ Apodemus argenteus ++ Apodemus speciosus +++ Apodemus agrarius Diplothrix legata I ++ osimensis t + Tokudaia muenninki 7 + Mrts caroli + Leporidae Pentalagus furnessi 1 + Abbreviatio:rs for island groupj and rggions, MJ: main-islands of Japan; OS: Osumi Group; NT and ST: Tokara islands north and south of the Tokara Gap, respectively; AM: Amami Group; OK: Okina*a Group; MY: Miyako Group; W: Yaeyarna Group; SK: Senkaki Groirp; TW: Taiwan. 1, Endemic species of the Ryukyus; Specific names follow: 2, Motokawa ef al. (L996),3, Motokawa & Abe (19%) and {, Corbet & Hill (1992). small field mortse Apodemus argentew and the Japanese large field motse Apodemus speciosus, are recorded from the Osumi Group. Of these species, C. dsinezutni and A. speciosus are also recorded from the northern Tokara Group. All of these seven species in the northern Ryukyus are also distributed in the rnain-islands of Japan. Their distributional ranges in the Ryukyus are restricted to the north of the Tokara Gap. This strait is usually considered a border between the Palaearctic and Oriental faunal realms in the Ryukyus, and is often referred to as the "Watase's line" (Watas6, t9l2; Okada,1927).

CENTRAL RYUKYUS

The genera Diplothrix and Tohtdaia are endemic to Amamioshima and Tokunoshima of the Amami Group and Okinawajima of the Okinawa Group. The former genus is comprised of a single species D. legata and is often divided into two subspecies: D. l. legata for the Amami populations and D. l. M. MOTOKAWA okinavensis for the Okinawajima population. The latter genus includes three karyologically divergent species (Musser & Carleton, L993): T osimensis from Amamioshima, an undescribed species from Tokunoshima, and Z muennincki from Okinawajima. The leporid genus Pentalagas, consisting of one species P furnessi, and the soricid species Crocidura orii, are endemic to Amamioshima and Tokunoshima of the Amami Group. Pentalagus is considered to have diverged from the extinct genus Pliopentalagus; its extant closest relative may be the African genus Pronolagas (see Tomida, [1997]). Crocidura orii was originally described by Kuroda (L924) as a subspecies of C. dsinezumi, which is widely distributed in the main-islands of Japan. Later, Imaizumi (1961) gave it a separate species status C. orii, on the basis of a few morphological features. Most subsequent scientists still regarded C. orii as the closest relative to or a local variant of. C. dsineatmi (Abe et al., 1994), but recently Motokawa (1998a) demonstrated that a number of important morphological characters discriminate C. orii from C. dsinezumi. He suggested that the former is rather distant from the latter phylogenetically. Crocidura watasei is endemic to the Amami and the Okinawa Groups, occurring on 14 islands (Motokawa, 199Sb). This species was considered a subspecies of the Southeast Asian C. horsfieldii by many authors (e.g., Ellerman & Morrison-Scott, 1951; Abe et al., 1994). However, because it's chromosomal number Qn=26, Harada et al., L985) is distinct from that of C. horsfteldii (2n=38, Krishna Rao & Aswathanarayana, 1978), it is obvious that C. watasei is actually a separate species endemic to the central Ryukyus (Motokawa et al., 1996). Mus caroli is known only from Okinawajima of the Okinawa Group within Japan, though it is widely distributed in Southeast Asia and Taiwan (Musser & Carleton, 1993). The reason for such a range restriction of this species in Japan remains uncertain. Because this species is associated with cultivated fields (Abe et al., L994), it is probable that this mouse was introduced to the Ryukyus with human activities.

SOUTHERN RYUKYUS

In the Miyako Group, no native living mammals have been known. In the Yaeyama Group, two species, the Iriomote cat Prionailurus iriomotensis (specific name following Corbet & Hill [1992D from Iriomotejima, and the wild boar Szs scrofa from Iriomotejima and Ishigakijima are recorded' The former was originally described by Imaizumi (1967) as an endemic genus and species Mayailurus iriomotensis on the morphological basis. This cat was often considered as a relic of the Miocene immigrant (Kizaki & Oshiro, L977),butrecent genetic studies indicated that P. iriomotensr's is closely related to P. bengalensis (Suzuki et al., 1994; Masuda et al., 1994), a species distributed in the continental part of East Asia, Taiwan, and Tsushima of Japan (Corbet & Hill, 1992).

SENKAKU GROUP

In the Senkaku Group, two native mammals, the striped field mouse Apodemus agrarius and the Senkaku mole Nesoscaptor uchidai have been recorded from Uotsurijima. Apodemus agrarius is widely distributed from Europe to East Asia including Taiwan and continental China (C-orbet & Hill, L992; Musser & Carleton,1993\, but is not found elsewhere in Japan (Abe et al., L994).The Biogeography of mammals in the Ryukyus 67

E 2.0 E g

(D 1.8

I C) E c 1.6 Cd b I 1.4 oc o ,t3 1.2 (l) .cl ()o c (l) 1.0 l- rho l}- 6 0.8 27.O 29.0 31.0 33.0 35.0 37.0 39.0 41.0 43.0 45.0

Greatest length of skull (in mm) Fig.2. The relationships between the greatest length ofskull and the difference between I1-M3 and C-M3 in the Asian moles of the gents Mogem (modified fiom Abers [195] tigure). The plot of the Senkaku mole, Nesoscaptor uchidai, is added based on the measurements ofAbe et al. (L99I).

Uotsurijima population differs slightly from the Taiwanese population (2n=48) by having larger molar width and a B-chromosome (?n=49) (Shiraishi & Arai, 1980). Nesoscaptor uchidai was described by Abe et al, (199L) as a new genus and species endemic to Uotsurijima on the basis of a unique specimen. This species differs from other moles mostly by having fewer teeth (38, vs 40-44 in other mole species; Abe et a1.,1991). Phylogenetic position of this mole remains uncertain, and its generic status definitely needs verification on the basis of additional data. Moles, extinct or extant, have not been recorded from the central and southern Ryukyus. Considering the close paleogeographic relationship of the Senkaku Group with Taiwan and the continental China (Ota et al., 1993), it is likely that N. uchidai has closest relatives in these regions. Nesoscaptor uchidai has relatively large difference between Il-M3 and C-M3 (=1.78), a good indicator of the rostrum shape which is one of the most important taxonomic characters (Abe, 1995). The scatter plot between this value and the greatest length of skull places N. uchidai closest to the Taiwanese population of Mogera insularis (Fig. 2). Furthermore, N. uchidai has head and body length and greatest length of skull of 129.9 and 31.82 (in mm; Abe et aI., L991), respectively, that are similar to values for corresponding measurements in the Taiwanese M. insularis (120.5 + 10.5 and 32.81 + 0.85 [mean tS.D.]: Abe, 1995). The major differences between N. uchidai and, M. insularus lie in the number of teeth (42 in M. insularis) and sacral vertebral bones (7, vs 6 in M, insularis; Abe et al 1991; Abe, 1995). M. MOTOKAWA

ORIGIN OF THE RYUKYU MAMMAI-S

Recently, Ota (1998), after reviewing previously published hypotheses on the paleogeography of the Ryukyus, proposed a new hypothesis on the basis ofbiological data ofamphibians and reptiles in this region. Here, I use Ota's (1998) hypothesis and paleogeographical map to discuss the origin of the Ryukyu mammals. In the middle and late Miocene, the land bridge connected areas ranging from eastern China to Kyushu of Japan. This is the most recent connection between the continent and the central Ryukyus. The Tokara Gap between northern and central Ryukyus and the Kerama Gap between central and southern Ryukyus were formed during the Pliocene by partial submergence of the large Miocene landbridge. Consequently, several separate land masses, including two super-islands, existed during the Pliocene: one extending from curent wsstern Yaeyama to the northern Miyako Groups, and the other from current Kumejima of the Okinawa Group to Amamioshima of the Amami Group (Ota, 19e8). Therefore, all central Ryukyu endemic mammals can be considered as of Miocene immigrants. This explains the high endemisms of these mammals. For example, Pentalagus furnessi, Tohtdaia ositnensis, T muennincki, Diplothrix legata are endemic to the central Ryukyus at the generic level. The remaining two endemic species, Crocidura watasei and C. orii, have congeners in the Palaearctic and Oriental regions, but are remarkably different from other East Asian species. The former has a remarkably reduced number of chromosomes (2r=26) as compared to the others (2n=40; Maddalena & Ruedi, 1.994), whereas the latter is divergent morphologically with its closest relative remaining undetected (Imaizumi, 1961; Motokawa, 1998a: see above). The extensive divergences observed in these two species may be also the consequence of long term isolation in the central Ryukyus. In the early Pleistocene, the landbridge from eastern China to the southern Ryukyu super-island was formed. A portion of this landbridge, coresponding to the current Miyako Group, was first isolated. The current Yaeyama Group was then separated from the continent in the middle Pleistocene (Ota, 1998). Prianailurus iriomotensis, the endemic species in the Yaeyama Group appears to have speciated from the ancestral form of the continental and Taiwanese P bengalensis at the time when the landbridge was restricted from oastern China to the current Yaeyama Group, because P iriomotensis does not occur in the Miyako Group. This is concordant with results of the genetic study of Suzuki et al. (1994) which suggested that P. iriomotensis migrated during the middle or late Pleistocene. Masuda et al. (1994) estimated divergence time of P iriomotensis from the continental P bengalensis as 0.2 million years. This value seems to be smaller than that expected by the above mentioned scenario, but Masuda et al. (1994) did not indicate its confidence limits' In the late Pleistocene, land areas expanded to form several super-islands as a result of a sea level drop, but the southern Ryukyus seem to have remained isolated from the continent. The continental area extended eastward to the current Taiwan and the Senkaku Group at this time (Ota, 1998). Thereforc, Apodemus agrarius and Nesoscaptor uchidai are likely to have migrated to Uotsurijima in the late Pleistocene. Abe et al. (L99t) supposed that N. uchidai is the relic of the Miocene immigrant, being isolated on the island for a long time. However, the morphological and paleogeographical data do not support this view. The Osumi and northern Tokara Groups probably have been isolated from Kyushu since the late Pleistocene (Ota, 1998). This can explain the high similarity between faunas of Biogeography of mammals in the Ryukyus

the northern Ryukyus and Kyushu. At present, the Tokara Gap and the Kerama Gap are considered as important borders of mammalian distribution in the Ryukyus, although the distribution of Sus scrofa offers an exception (see above). of this species is confused and further analysis of its morphological and genetic properties are desired. Future studies on the phylogenetic relationships and the divergence times of the Ryukyu endemics, including the poorly known Nesoscaptor uchidai in the Senkaku Group, are also desired for more detailed discussion of the origin and biogeography of the Ryukyu mammals.

ACKNOWIJDGMENTS I wish to express my sincere thanks to Tbutomu Hikida, Liang-Kong Lin, Cara Lin Bridgman, Junko Motokawa and annonymous reviewer for providing critical comments on the early version of this manuscript. This research was supported in part by a grant from the Fujiwara Natural History Foundation, and a Grant-in-Aid for Encouragement of Young Scientists from the Japan Society for the Promotion of Science (No.IL7M72\.

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