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Morphological Variation of Large Japanese Field Mice, Apodemus Speciosus on the Izu and Oki Islands

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Morphological Variation of Large Japanese Field Mice, Apodemus Speciosus on the Izu and Oki Islands Mammal Study 31: 29–40 (2006) © the Mammalogical Society of Japan Morphological variation of large Japanese field mice, Apodemus speciosus on the Izu and Oki Islands Yasushi Takada1,*, Eiichi Sakai1, Yasushi Uematsu1 and Takashi Tateishi2 1 Department of Anatomy, School of Dentistry, Aichi-Gakuin University, Chikusa-ku, Nagoya 464-8650, Japan 2 Tokorozawa, Japan Abstract. Morphological variation was examined in large Japanese field mice, Apodemus speciosus, of five populations from the Izu Islands (from Oshima, Shikinejima, Niijima, Kozushima and Miyakejima), four from the Oki Islands (from Dogo, Nishinoshima, Nakanoshima and Chiburijima), and four from the Japanese mainland of Honshu. Univariate and multivariate (PCA) analyses were conducted on the basis of body-, mandible-, and molar-measurements. Overall, the insular mice had a tendency toward gigantism, and also showed marked morphological differentiation among the islands. The sizes of the mandible and molar were inversely correlated to island area and temperature, thus suggesting a selective effect. Although faunal diversity might be related to the morphological variation in size, there was no clear relationship between the morphological variation and biotic factors such as predation and competition. The populations from the Izu Islands underwent marked morphological divergence, suggesting founder effects. The Izu Island are oceanic and have probably never been connected with Honshu, hence mice were likely transported from Honshu. On the other hand, the Oki Islands had been connected with Honshu in the late Pleistocene. The founders of the insular mice related to the history of the islands could have likely affected the morphological variation. Key words: Apodemus speciosus, Izu Islands, large Japanese field mice, Oki Islands, variation. Large Japanese field mice, Apodemus speciosus occur in Mice from the Izu and Oki Islands have been exam- Hokkaido, the mainland of Honshu, Kyushu, Shikoku, ined morphologically as to the size of bodies, skulls and smaller islands, in Japan (Abe et al. 2005), and are and molars (Hiraiwa et al. 1958; Imaizumi 1962, common in fields and woods (Takada et al. 1999a). 1964; Miyao et al. 1968; Miyao et al. 1969; Sakai and They are present on the Izu Islands of Oshima, Niijima, Miyao 1979, 1980; Fujii 1998). These studies found Shikinejima, Kozushima and Miyakejima (Takada et al. that mice from Oshima, Niijima, Dogo, Nishinoshima, 1999a), and on the Oki Islands of Dogo, Nishinoshima, Nakanoshima and Chiburijima have large bodies, skulls, Nakanoshima and Chiburijima (Uematsu et al. 1986). or molars, and that those from the Oki Islands have short According to the classification of the species based tails. However, more detailed morphological analyses of on morphological characters, mice from Oshima and the mice throughout both Islands have not yet been done. Niijima are designated Apodemus speciosus insperatus, On the other hand, mice from extensive regions includ- and those from the Oki Islands A. s. navigator, distin- ing the Izu and Oki Islands have been studied as to guished from A. s. speciosus on Honshu, Kyushu and genetic geographical variations in the chromosome num- Shikoku (Thomas 1905; Tokuda 1941; Imaizumi 1960). ber, the allozymes, and the gene sequences (Tsuchiya et Mice on Miyakejima were classified as a new species, al. 1973; Tsuchiya 1974; Hirai et al. 1980; Saitoh et al. A. miyakensis by Imaizumi (1969), but are an insular 1989; Suzuki et al. 2004). Suzuki et al. (2004) found form of A. speciosus. (Kobayashi 1981). Kobayashi that mice from the Japanese archipelago can be divided (1981) thought that these insular mice have been differ- into two major clades; one clade from islands such as entiated on their respective islands. Niijima, Shikinejima, Miyakejima and so on, another *To whom correspondence should be addressed. E-mail: [email protected] 30 Mammal Study 31 (2006) Fig. 1. Map showing sampling localities. from wider regions such as Oshima, the Oki Islands, and genetic differentiation. Foster (1964) clarified that Honshu and so on. insular rodents tend to become larger while insular carni- The Izu and Oki Islands have geologically different vores and artiodactyls smaller, and he pointed out the features: the former being oceanic (Taira 1990; Taira and impoverishment of predators and competitors and the Kiyokawa 1998) while the latter continental (Naruse and limit of their food supply as important factors controlling Hayashi 2004). The Izu Islands have probably never the body size changes. Further, many studies have found been connected with Honshu according to geological out morphological and genetic variations of insular mice evidence (Taira 1990), flora (Shimizu 1996), herpeto- and insectivores: Berry (1964, 1969, 1986), Berry et al. fauna (Hasegawa 1999), and mammalian fauna (Takada (1978), Davis (1983) on Apodemus sylvaticus and Mus et al. 1999a). To the contrary, the Oki Islands had been musculus from British islands, Ashley and Wills (1987) connected with Honshu in the late Pleistocene and have on Peromyscus maniculatus from the California Channel been isolated from it some 16,000 years ago according Islands, Calhoun and Greenbaum (1991) on Peromyscus to geological evidence (Oshima 1991). Thus the Izu maniculatus and P. oreas from islands of British Islands have an impoverished mammalian fauna; there Columbia, Hiraiwa et al. (1958) and Uematsu (1993) on are field mice, introduced house mice Mus musculus, Eothenomys smithii and Urotrichus talpoides from the introduced rats Rattus norvegicus and R. rattus, likely- Oki Islands, and Takada et al. (1999b, 2002) on house introduced white-toothed shrews Crocidura dsinezumi, mice from the Izu and Ogasawara Islands. introduced Japanese weasels Mustela itatsi and intro- Examining morphological variations of field mice, duced squirrels Callosciurus erythraeus (Hasegawa A. speciosus from the Izu and Oki Islands, which have 1999; Takada et al. 1999a). On the other hand, the Oki different geological history, should give a clue to the Islands hold a rather rich mammalian fauna; in addition cause of the morphological variation. This paper de- to the above species excluding squirrels, there are pre- scribes morphometric variations of bodies, mandibles sent hares Lepus brachyurus, dormice Glirulus japoni- and molars of the mice from the Islands and Honshu, cus, small Japanese field mice Apodemus argenteus, examines the relationship between morphological varia- harvest mice Micromys minutus, Smith’s red-backed tions and environmental factors, and argues the causes voles Eothenomys smithii, moles Mogera wogura, of the variation. shrew-moles Urotrichus talpoides, and introduced raccoon dogs Nyctereutes procyonoides (Thomas 1905; Materials and methods Tokuda 1941; Hiraiwa et al. 1958; Uematsu et al. 1986; Takada et al. 1999a; Abe et al. 2005). Field mice were collected at the following localities Mammals on islands show remarkable morphological from 1985 to 2004 (as seen in Fig. 1): the Izu Islands Takada et al., Morphological variation of insular field mice 31 To examine the effects of environmental factors on morphological variations, a multiple regression analysis was conducted; a dependent variable being sample means of size statistics for mandibles and molars, and independent ones island area (Tokyo Astronomical Observatory 1979; Sugata 1995) and temperature. Cli- mate data were taken from the website of the homepage Fig. 2. Diagram of right mandible showing the 10 measurements. of the Japan Meteorological Agency: http://www.data. kishou.go.jp/etrn/index.html. If climate data were not of Oshima, Niijima, Shikinejima, Kozushima, and available, those from a climatological station nearest to a Miyakejima; the Oki Islands of Dogo, Nishinoshima, sampling locality were used (Appendix 1). Nakanoshima, and Chiburijima; Honshu of the Boso Peninsula (Misaki-cho, Ohara-cho), the Miura Peninsula Results (Yokosuka-shi, Miura-shi), the Izu Peninsula (Kawazu- cho, Shimoda-shi), and Nagoya-shi (Moriyama-ku). The Body dimensions following data were recorded: sex, body weight to the Pregnancy and lactation accelerate growth in females nearest 0.2 g (BW), head & body length (HBL; from (Takada 2002b), hence only males were analyzed. Body rostrum to anus), tail length (TL; from anus to tail tip) measurements (BW, HBL, TL, HFL) of adult males and hindfoot length exclusive of claw (HFL) to the (i.e. lens weight ≥13.2 mg, or molar wear stages ≥II) nearest 0.1 mm. were given in Table 1. The value of the tail ratios (100 The age of mouse specimens from the Oki Islands was × TL/HBL) was given from specimens after weaning. estimated using the molar wear (Hikida and Murakami BW, HBL and TL continue to grow, while HFL nearly 1980), and that from the other localities the eye lens stops growing after reaching the adult stage (Takada weight (Takada 1982). Clean skulls were prepared fol- 2002a, b). HBL and TL grow at the same tempo (i.e. lowing Takada et al.’s (1994) technique. isometric growth) after weaning, thus tail ratios become Right mandibles and right molars were measured fol- constant (Shimizu 1957). Multiple comparisons among lowing Takada et al. (1999b). Ten mandibular dimen- samples were therefore conducted as to HFL and tail sions were measured to the nearest 0.01 mm: the heights ratios. The value of the tail ratios was judged to be nor- from the inferior edge (M1–M5), and the lengths from mal in distribution (Kolmogorov-Smirnov’s d = 0.027, the anterior edge (M6–M10) (Fig. 2). We analyzed χ2 = 5.56, df = 5, P = 0.35). Analysis of variance using the mandible measurements of specimens with eye lens a one-way design for HFL and tail ratios showed sig- weights of 13.2 to 26.2 mg (estimated age 2 to 13 nificant differences among samples (F12,314 = 18.8, P < months) or those with molar wear stages II to VIII. The 0.0001 for HFL; and F12,358 = 37.9, P < 0.0001 for tail buccolingual crown diameters were measured to the ratios). Appendix 2 shows the result of Scheffe test of nearest 0.001 mm for maxillary (UM1–UM3) and multiple comparisons.
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