Mammal Study 31: 29–40 (2006) © the Mammalogical Society of

Morphological variation of large Japanese field mice, Apodemus speciosus on the Izu and

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, , and ), and four from the Japanese mainland of . 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. Samples from the Izu and Oki mandibular (LM1–LM3) molars. We used molars with Islands tended to have longer HFLs as compared to slightly worn cusps (molar wear stages II–V), and those from Honshu, and those from Niijima, Shikinejima analyzed the mean value of the two measurements for and the Oki Islands had proportionately short tails. each molar. Morphological analyses were conducted by univariate Mandible and molar measurements and multivariate statistics using the STATISTICA 03J Multivariate analyses of variance using a two-way package (StatSoft. Inc. 2003). Principal component design revealed a significant difference among samples analyses (PCA) using a correlation matrix of pooled but not between sexes both as to mandible variables samples were employed to examine variations among (Wilks’ lambda = 0.033, P < 0.0001, among samples; samples on the basis of ten mandibular and six molar and Wilks’ lambda = 0.958, P = 0.49, between sexes), variables. Mahalanobis’ distance (D2), a morphological and as to molar variables (Wilks’ lambda = 0.068, P < distance, was calculated as an indication of morpho- 0.0001, among samples; and Wilks’ lambda = 0.977, P = logical divergence between samples using ten mandible 0.46, between sexes). Data from both sexes were there- and six molar variables. fore pooled for the following analyses. The mandibular 32 Mammal Study 31 (2006)

Table 1. Measurements for male body size.

BW (g)1) HBL (mm)1) TL (mm)1) HFL (mm)1) TL/HBL (%)2) Oshima Mean 40.0 112.6 107.0 25.5 92.0 SD 10.1 9.5 10.2 0.8 4.2 n 998925 Shikinejima Mean 47.4 114.7 93.1 25.4 81.5 SD 9.78.94.80.83.3 n 16 16 14 16 27 Niijima Mean 48.0 115.6 93.1 25.8 81.6 SD 2.60.73.80.63.0 n 333313 Kozushima Mean 36.6 106.9 97.1 25.2 91.4 SD 9.09.28.60.75.7 n 57 58 55 59 67 Miyakejima Mean 29.5 103.7 92.5 25.1 89.2 SD 3.76.05.70.64.6 n 36 36 36 36 38 Boso Pen. Mean 32.6 104.1 92.8 24.3 88.7 SD 4.66.77.50.85.9 n 13 13 12 13 15 Miura Pen. Mean 37.9 108.4 95.8 24.2 89.1 SD 7.78.76.80.75.2 n 40 40 33 40 34 Izu Pen. Mean 33.4 105.6 97.1 24.3 92.5 SD 8.19.09.70.77.0 n 17 17 16 17 20 Nagoya Mean 37.3 107.7 97.3 23.9 90.0 SD 7.79.09.10.74.6 n 24 29 25 29 28 Dogo Mean 37.3 107.9 83.5 24.8 77.4 SD 12.6 13.0 11.8 1.0 4.4 n 24 25 23 25 27 Nishinoshima Mean 35.2 99.8 79.2 25.6 79.7 SD 11.3 13.1 5.3 0.8 7.2 n 88787 Nakanoshima Mean 41.1 106.3 85.4 25.6 80.6 SD 17.1 13.4 11.0 0.7 4.8 n 41 41 41 41 42 Chiburijima Mean 48.1 111.6 86.2 25.7 77.4 SD 14.7 13.8 10.3 0.7 4.7 n 31 31 28 31 28 1) In adults, 2) in all ages after weaning. and molar measurements were shown in Tables 2 and 3. molars (UM1, LM1, LM2; negative ones). The results of PCA were shown in Tables 4 and 5, and The samples from the islands tended to have larger the plots of the sample means of the first (PC1), versus mandibles and wider molars than those from Honshu. the second (PC2) component in Fig. 3A, B, using man- When comparing two groups (i.e. islands vs. Honshu) dibular and molar measurements. The first component in sample means of scores of PC1 for mandibles and (PC1), where all the variables being negative vectors, molars, there were significant differences; the t-test indi- expressed the overall size of the mandibles and molars. cated t = 3.99, df = 11, P = 0.002 as to mandibles, and t = The second component (PC2) expressed the shape or the 4.51, df = 11, P = 0.001 as to molars, and the Mann- relative size, i.e. the relative height of the posterior (M3, Whitney U-test Z = 2.78, n = 9 for the island, n = 4 for M4, M5; positive vectors) to the anterior parts (M1, M2; Honshu, P = 0.005 as to mandibles and molars. When negative ones) for the mandible, and the relative size of comparing the individual samples, it was indicated that the upper and lower third molars (UM3, LM3; positive the samples from Shikinejima, Niijima, Nishinoshima, vectors) to the upper first and the lower first and second Nakanoshima and Chiburijima have large mandibles, Takada et al., Morphological variation of insular field mice 33

Table 2. Measurements for mandibles (×100, in mm) and sample means of ages.

AgeM1M2M3M4M5M6M7M8M9M10 Oshima Mean 6.41) 245.9 322.8 639.5 675.6 777.7 1241.7 1310.8 1396.7 1583.5 1725.7 SD 2.6 12.3 14.9 40.2 44.7 43.8 49.1 55.4 48.8 58.1 67.2 n 15 15 15 15 15 13 15 13 15 15 15 Shikinejima Mean 4.11) 273.7 352.7 625.1 666.1 781.3 1265.2 1376.4 1445.9 1643.4 1752.3 SD 1.9 17.7 17.2 53.4 50.0 63.3 59.3 76.4 63.6 86.7 71.5 n 20 20 20 20 20 15 20 15 20 20 20 Niijima Mean 4.51) 275.8 355.0 636.1 686.6 800.7 1288.6 1402.1 1468.6 1675.8 1788.3 SD 2.9 10.6 13.6 36.8 42.0 38.5 35.8 37.8 39.4 45.2 44.4 n 11 11 11 11 11 10 11 10 11 11 11 Kozushima Mean 5.01) 247.4 330.4 602.9 643.5 746.3 1205.7 1288.1 1327.2 1507.9 1661.6 SD 2.6 14.4 17.1 43.1 51.7 52.0 61.9 74.3 66.2 80.0 85.8 n 51 51 51 51 51 51 51 51 51 51 51 Miyakejima Mean 4.41) 238.9 309.7 610.1 659.3 754.9 1185.5 1272.2 1343.2 1510.5 1639.1 SD 1.7 9.6 10.2 30.9 33.8 39.0 35.0 43.2 45.6 59.9 54.0 n 34 34 34 34 34 34 34 34 34 34 34 Boso Pen. Mean 4.81) 226.3 301.1 594.4 641.3 728.0 1158.4 1228.4 1309.6 1470.3 1613.6 SD 2.8 15.9 27.0 45.2 36.0 48.9 88.9 103.0 69.6 93.7 104.6 n 7 7777777777 Miura Pen. Mean 7.81) 234.8 327.1 596.8 629.6 721.0 1169.6 1254.3 1316.0 1489.0 1600.8 SD 2.8 12.7 11.7 26.0 30.0 32.4 45.9 55.5 42.3 59.2 59.8 n 11 11 11 11 11 11 11 11 11 11 11 Izu Pen. Mean 7.01) 234.4 309.4 623.0 662.0 747.9 1177.1 1250.3 1333.5 1504.8 1637.4 SD 2.2 7.9 10.4 34.3 35.1 36.8 58.1 74.2 43.2 58.7 62.6 n 14 14 14 14 14 11 14 11 14 14 14 Nagoya Mean 6.41) 232.9 312.6 609.0 654.6 746.4 1190.2 1271.4 1335.7 1499.5 1637.2 SD 2.2 11.6 17.5 31.8 31.7 33.4 50.1 54.8 46.0 54.8 62.8 n 27 27 27 27 27 27 27 27 27 27 27 Dogo Mean 3.72) 246.9 331.7 656.6 703.1 787.3 1265.3 1341.8 1429.9 1584.0 1739.7 SD 1.2 16.0 14.1 45.9 47.1 56.1 52.5 64.7 67.2 85.2 75.3 n 20 20 20 20 20 20 20 20 20 20 20 Nishinoshima Mean 2.92) 255.9 351.1 656.4 704.9 785.9 1299.0 1365.1 1446.1 1619.3 1786.4 SD 1.5 18.1 20.3 40.8 41.2 44.3 72.9 77.5 81.4 98.6 105.8 n 7 7777777777 Nakanoshima Mean 3.52) 258.4 353.9 664.4 716.2 800.1 1267.3 1340.6 1411.8 1608.5 1759.6 SD 1.5 18.3 20.5 49.5 54.0 59.0 77.9 86.6 84.1 107.7 108.4 n 27 27 27 27 27 27 27 27 27 27 27 Chiburijima Mean 4.82) 264.6 353.0 668.9 709.6 809.6 1282.0 1369.4 1454.7 1645.5 1757.8 SD 1.2 18.4 22.8 58.5 60.1 66.3 77.8 92.0 89.7 116.0 106.5 n 22 22 22 22 22 22 22 22 22 22 22 1) Months. 2) Tooth wear stages (after Hikida and Murakami (1980)) converted Roman to Arabic numerals. while those from Miyakejima, Kozushima and Honshu (unadjusted R2 value) of the variation found in mandibles have small ones (Fig. 3A). Similarly, those from (with island area contributing 61.6%, and temperature Niijima, Nishinoshima, Nakanoshima and Chiburijima 13.9%), and 80.3% of the variation in molars (with had wide molars, while those from Honshu had narrow island area 66.0%, and temperature 14.3%). There were ones (Fig. 3B). however no significant effects of island area and temper- Stepwise multiple regression analyses were conducted ature, when testing the small-island samples excluding to examine the relationships between sample means of Honshu ones (Table 6). the score of PC1 for mandibles and molars both with log The Mahalanobis’ distance (D2) between the samples transformed island area and with the annual mean of was set out in Table 7. The relationship among the sam- mean monthly temperature of recent 22 or 30 years. The ples was shown by the cluster analysis of unweighted regression was significant, when all the samples were pair-group method using arithmetric average based on included; the score of PC1 was correlated with island the distance (Fig. 4). The Dogo, Nishinoshima, and area and temperature (Table 6). It explained 75.5% Nakanoshima samples formed one cluster, and the 34 Mammal Study 31 (2006)

Table 3. Buccolingual crown diameters of the molars (×1000, in mm).

UM1 UM2 UM3 LM1 LM2 LM3 Oshima Mean 1414.4 1384.1 1056.3 1240.7 1271.8 1047.5 SD 23.3 24.6 52.8 27.2 18.1 22.3 n 18 18 18 18 18 18 Shikinejima Mean 1431.3 1366.6 1046.3 1265.7 1301.1 1047.6 SD 24.6 23.5 24.0 28.0 22.7 25.0 n 17 17 17 17 17 17 Niijima Mean 1443.6 1391.0 1106.5 1257.6 1325.9 1102.9 SD 28.1 31.2 35.2 29.7 27.4 25.4 n 24 24 24 24 24 24 Kozushima Mean 1371.7 1343.6 1034.0 1211.4 1256.0 1047.4 SD 45.8 48.3 59.5 44.1 45.8 34.8 n 31 31 31 31 31 31 Miyakejima Mean 1427.6 1372.0 1058.5 1219.3 1274.9 1046.4 SD 34.8 32.4 37.1 35.0 30.0 29.9 n 24 24 24 24 24 24 Boso Pen. Mean 1361.5 1333.2 1012.1 1196.9 1233.1 1025.2 SD 43.8 40.0 49.5 38.5 36.5 30.2 n 27 27 27 27 27 27 Miura Pen. Mean 1321.0 1272.9 965.5 1166.8 1198.1 996.8 SD 44.4 34.0 57.0 28.4 29.6 34.6 n 10 10 10 10 10 10 Izu Pen. Mean 1353.4 1323.2 1019.5 1194.5 1231.5 1011.7 SD 43.5 48.6 50.2 31.0 37.9 26.4 n 13 13 13 13 13 13 Nagoya Mean 1314.1 1283.7 1006.0 1146.5 1186.4 1003.0 SD 34.3 37.0 50.3 32.1 28.0 26.7 n 22 22 22 22 22 22 Dogo Mean 1396.8 1368.6 1040.8 1249.2 1290.7 1031.7 SD 32.2 43.6 50.4 47.0 38.7 31.3 n 32 32 32 32 32 32 Nishinoshima Mean 1462.7 1421.0 1086.4 1297.9 1345.1 1112.6 SD 31.7 39.2 39.7 45.0 37.7 27.3 n 17 17 17 17 17 17 Nakanoshima Mean 1478.0 1407.1 1034.0 1307.6 1354.5 1091.4 SD 39.1 41.4 42.5 36.9 36.6 38.5 n 24 24 24 24 24 24 Chiburijima Mean 1522.9 1440.4 1004.0 1358.5 1404.2 1098.7 SD 34.6 33.5 46.0 36.2 35.6 31.5 n 16 16 13 16 16 16

Table 4. Factor loadings of PCA of ten mandible measurements Table 5. Factor loadings of PCA of six molar measurements based based on pooled samples. on pooled samples.

Variable Factor 1 Factor 2 Variable Factor 1 Factor 2 M1 –0.894 –0.329 UM1 –0.939 –0.183 M2 –0.821 –0.477 UM2 –0.943 –0.044 M3 –0.917 0.338 UM3 –0.600 0.771 M4 –0.895 0.383 LM1 –0.894 –0.312 M5 –0.946 0.252 LM2 –0.948 –0.170 M6 –0.968 –0.051 LM3 –0.869 0.220 M7 –0.948 –0.114 Eigenvalue 4.585 0.805 M8 –0.964 0.001 Variance (%) 76.4 13.4 M9 –0.975 –0.024 M10 –0.977 –0.026 Eigenvalue 8.68 0.68 Variance (%) 86.8 6.8 Takada et al., Morphological variation of insular field mice 35

Table 6. Result of multiple regression analysis, sample means of scores of PC1 (for mandibles and molars) dependent on log island area (km2) and annual mean temperature (°C).

Locality and character β1) P adjusted R2 n All islands including Honshu For mandible Regression 0.0009 0.71 13 Island area 0.87 0.0003 Temperature 0.38 0.038 For molar Regression 0.0003 0.76 13 Island area 0.90 0.0001 Temperature 0.39 0.023 Izu and Oki Islands For mandible Regression 0.15 0.30 9 Island area 0.59 0.13 Temperature 0.72 0.074 For molar Regression 0.085 0.41 9 Island area 0.60 0.097 Temperature 0.81 0.038 1) Standardized regression coefficient.

Fig. 3. Plots of sample means of the first two principal components, based on mandible (A) and molar (B) measurements. Numerals indi- cate sample nos. as in Table 7.

Shikinejima and Niijima samples diverged from the other samples as to mandible traits (Fig. 4A). On the other hand, the Chiburijima sample showed marked differentiation with regard to molars (Table 7, Fig. 4B).

Discussion

Firstly, we examined the relationship between the morphological variations found in the insular field mice and environmental factors. Island area and temperature Fig. 4. Similarity relationship by UPGMA cluster analysis of have likely significant effects on the mandibular- and Mahalanobis’ distance based on mandible (A) and molar (B) measure- molar-sizes of the mice (Table 6), although temperature ments. 36 Mammal Study 31 (2006)

Table 7. Mahalanobis’ distances (D2) between samples using ten mandibles and six molar variables. For each pair-samples, the values from mandibles and molars are given below and above diagonal respectively.

Sample no. [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12] [13] [1] Oshima 4.20 6.82 2.18* 2.00* 2.38 8.98 3.31 9.25 2.99 7.85 13.63 33.31 [2] Shikinejima 23.35 4.43 5.70 3.67 7.58 11.63 7.68 16.67 3.37 5.22 5.43 19.74 [3] Niijima 19.09 1.42* 6.84 5.47 11.22 18.01 12.69 20.10 8.72 2.34* 7.29 24.75 [4] Kozushima 7.05 19.50 17.56 4.34 0.79* 4.20 1.65* 4.88 3.59 9.25 15.76 38.48 [5] Miyakejima 5.83 19.00 16.19 7.14 4.65 10.22 5.38 10.91 5.45 9.07 12.55 31.35 [6] Boso Pen. 3.56* 30.42 26.34 8.19 3.03* 2.65* 0.66* 2.90 4.43 13.92 20.03 43.57 [7] Miura Pen. 11.33 22.87 23.17 10.62 10.72 10.57 2.63* 2.20* 9.50 22.48 26.32 51.85 [8] Izu Pen. 3.42* 29.02 26.40 8.20 3.84* 1.07* 7.97 2.58* 3.54 16.62 22.62 46.99 [9] Nagoya 4.37 25.62 22.02 6.48 2.02* 1.50* 6.73 1.99* 11.97 26.89 35.53 66.32 [10] Dogo 8.92 31.88 26.89 16.97 11.59 9.84 15.25 9.63 7.29 9.51 12.87 30.00 [11] Nishinoshima 12.30 33.36 27.55 16.19 21.02 17.49 18.30 17.55 14.40 5.13* 3.48 16.10 [12] Nakanoshima 10.18 30.96 27.03 9.18 16.75 13.47 11.08 11.28 10.97 10.58 5.78* 5.77 [13] Chiburijima 10.35 13.65 12.20 12.88 11.46 15.62 7.27 13.11 10.06 9.12 10.59 9.29 * not significant (P > 0.05: adjusted probability which multiplied by the number of pairs tested). The other values are significantly different from zero (P < 0.05). contributed to the variation much less as compared with Faunal diversity might be therefore an important factor island area. We cannot however evaluate too much these contributing to the size variation of the mice. In contrast, environmental effects, because they were not found sig- a mammalian fauna in the Izu Islands is impoverished nificant when confining to only the small-island samples. throughout, where no dominant competitor is likely Millien and Damuth (2004) found significant but very present (Takada et al. 1999a), and the only mammalian weak effects (that is, low contribution) of island area and predator, introduced weasels occur on Oshima and latitude on the incisor size of their samples of Japanese Miyakejima but not on Shikinejima, Niijima and field mice, although they inappropriately analyzed it Kozushima (Hasegawa 1999). Apodemus argenteus and using individual measurements of specimens instead of shrew-moles likely compete with A. speciosus for food sample means. There are however no significant effects resources and habitats (Miyao 1970; Uemastu 1993); of island area and latitude, when reanalyzing their data A. argenteus occurs on Dogo and Nishinoshima, while using the sample means (adjusted R2 = 0.34, P = 0.08, n shrew-moles on Nakanoshima in addition to the former = 11). The samples from the Izu and Oki Islands tended two islands. Nevertheless, there was no clear relation- to have longer hindfeet, proportionately shorter tails, ship between the size variation in A. speciosus and the larger mandibles and wider molars than the Honshu presence or absence of the predators and/or competitors samples, representing gigantism of the insular samples. on the islands (Fig. 3). To understand the nature of size Large body size is likely more efficient metabolically, variation in island mice, as Angerbjörn (1986) pointed thereby likely having longer survival, especially so in out, it may be needed to look for other biotic mecha- cold environment, and a short tail indicative of slow nisms, e.g. life history variables such as age-specific activity; and it has been explained that the absence of survival and reproduction. predators and/or competitors on a small island contrib- As discussed above, the morphological variation of utes to the above changes (Foster 1964; Miyao 1970; the mice cannot be explained fully by selective force Angerbjörn 1986). Thus mice from small islands and alone such as climate and biotic factors. It is therefore cold regions are expected to have large body size. useful to argue in favor of the possible relevance of sto- Faunal difference might have an effect on the size chastic effects, such as founder effects on morphological variation found in the mice from Izu and Oki Islands. A variation. The Izu Islands are an oceanic island arc and mammalian fauna in the Oki Islands become rich in have probably never been connected with Honshu (Taira accordance with area from Chiburijima, the smallest, to 1990; Taira and Kiyokawa 1998), the mice had been Dogo, the largest island (Uematsu et al. 1986), although therefore likely transported to the islands from Honshu in the only mammalian predators are likely-introduced some ways such as a human agency or a natural rafting Japanese weasels which occur all the islands, and intro- event. Mice, Apodemus speciosus generally inhabit fal- duced raccoon dogs on the Chiburijima (Uematsu 1993). low grounds in agricultural land (Takada 1983; Takada Takada et al., Morphological variation of insular field mice 37 et al. 1999a), and sometimes actively invade houses Hirai et al. (1980) found that the mice in the Oki Islands (Tateishi 1999), thus it seems likely that they could have (from Dogo and Dozen whose name was not written in been accidentally transported on watercraft with cargoes the paper but may be Nishinoshima) were more closely such as crops (see Sakai and Miyao 1980; Takada et al. related to each other than to the Honshu samples, accord- 1999a, for detailed discussion). If human introduction of ing to the allozymic differentiation. Suzuki et al. (2004) mice in the Izu Islands was true, then it should date found, on the basis of the mitochondrial gene sequences, back at most to the Paleolithic- (some 20,000 B. P.) or that the mice from the Izu Islands of Shikinejima, the early Jomon-era when early human activities on the Niijima, and Miyakejima had a close relationship, but islands were ascertained (Hashiguchi 1988; Niijima- markedly diverged from the Oshima mice which were mura 1996). To the contrary, Suzuki et al. (2004) clari- closely related to the mice from Dogo and Nishinoshima. fied a marked sequence divergence of mitochondrial The present morphological analysis however showed a DNA genotype of mice between the islands (Shikine- slight disagreement; the mice from Oshima, Miyakejima, jima, Niijima, and Miyakejima) and Honshu; they used a and Kozushima had a close relationship apart from those molecular clock and presented a hypothesis that mice of Shikinejima and Niijima (Fig. 4A). Both the morpho- colonized the islands 0.2–0.3 million years ago via an logical and the genetic studies therefore indicated that assumed land bridge between the islands and Honshu. the populations in the Izu Islands were heterogeneous, Spradling et al. (2001) contended that molecular clocks and thus had the different origin of the founders. On the should be used cautiously because heterogeneity in evo- other hand, the populations in the Oki Islands seem to be lutionary rate is somewhat unpredictable. We may as homogenous both morphologically (as to the mandible well therefore reserve decision about when and how trait) and genetically, suggesting that they shared mice were transported to the islands and founded the common ancestors. It is however needed to clarify population, until we can have other evidence such as the genetic variation of mice from Nakanoshima and fossil records. Chiburijima of the Oki Islands, because it have not been Insular populations can undergo rapid morphological examined. and genetic differentiation in a short period. House mice The degree of morphological divergence appears to be in British isles such as the Faroe Islands and in the different among species. In the Izu Islands, field mice Izu Islands have been likely introduced comparatively did not undergo such marked morphological variations recently, but nonetheless they show marked divergence as house mice did. That is, the value of the Mahalanobis’ among the islands (Berry 1964, 1986; Berry et al. 1978; distance between the field mouse samples in the islands Davis 1983; Takada et al. 1999b). House mice on ranged from 1.4 to 23.4 (with a mean of 13.6) for the Chichijima and Hahajima in the Ogasawara Islands mandible, and from 2.0 to 6.8 (4.6) for the molar, while probably colonized there only 200 years ago at most the house mice had a value from 13.5 to 50.5 (30.4) and derived from common ancestors, but they are now for the mandible and from 4.5 to 33.7 (15.7) for the morphologically different, and the Chichijima mice molar (on Oshima, Niijima, Kozushima, Miyakejima, and underwent additional morphological change in the last Hachijojima) (Takada et al. 1999b). These values were 20 years (Takada et al. 2002). Pergams and Ashley significantly different between the species following the (1999) presented another example of rapid morphologi- Mann-Whiteny U-test (Z = 2.948, P = 0.003, n = 10, 10, cal change in deer mice, Peromyscus maniculatus from for the mandible; and Z = 3.174, P = 0.001, n = 10, 10, three California Channel Islands in some 40 years. for the molar). In addition, the divergence in white- Marked and random morphological or genetic differen- toothed shrews from Toshima, Niijima, and Shikinejima, tiation was also found in following insular mice: wood in the Izu Islands seemed to be less marked than that in mice Apodemus sylvaticus (Berry 1969), deer mice the field mice, although we did not statistically test it out P. maniculatus and P. oreas (Ashley and Wills 1987; because of the small size of the samples; the value rang- Calhoun and Greenbaum 1991). Many of these island ing from 2.0 to 8.3 for the mandible (Takada et al. 2004). mice were likely inadvertently introduced by man and House mice have a worldwide distribution (Abe et al. have been isolated, the genes of a few founders therefore 2005), making it apparent that they can be more easily must have primarily contributed to the inter-island dif- transported to islands than field mice and white-toothed ferentiation. shrews. 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Appendix 1.

Latitude (°N) of sampling localities, island area (km2), and annual mean temperature (°C) at climatological station of the sampling locality.

Sampling locality Latitude Island area Climatological station Annual mean temperature Oshima 34.41 91 Oshima 15.81) Shikinejima 34.19 4 Niijima 17.42) Niijima 34.22 23 Niijima 17.42) Kozushima 34.12 18 17.453) Miyakejima 34.05 55 Miyakejima 17.51) Boso Pen. 35.17 2274004) Kamogawa 15.62) Miura Pen. 35.12 2274004) Miura 15.62) Izu Pen. 34.45 2274004) Inatori 15.62) Nagoya 35.14 2274004) Nagoya 15.41) Dogo 36.15 242 Saigo 14.01) Nishinoshima 36.06 56 Ama 14.42) Nakanoshima 36.05 32 Ama 14.42) Chiburijima 36.01 13 Ama 14.42)

1) Annual mean of mean monthly temperature of 30 years from 1971 to 2000. 2) Annual mean of mean monthly temperature of 22 years from 1979 to 2000. 3) Mean of data from Niijima and Miyakejima stations. 4) Honshu excluding small islands.

Appendix 2.

Statistical table for body dimensions indicating significant differences between pairs of samples (tested by Scheffe’s method of multuple comparisons. Above diagonal for hind foot length, below diagonal for tail ratios (P = 0.05).

Shikine- Kozu- Miyake- Boso Miura Izu Nishino- Nakano- Chiburi- Oshima Niijima Nagoya Dogo jima shima jima Pen. Pen. Pen. shima shima jima Oshima * * Shikinejima * * * Niijima * Kozushima * * * * * Miyakejima * * * * Boso Pen. ** Miura Pen. * * *** Izu Pen. * * ** Nagoya * * *** Dogo* ****** * Nishinoshima * * * * * Nakanoshima* ****** Chiburijima * ******