FULL PAPER Anatomy

Proportion and Cluster Analyses of the Skull in Various Species of the Tree Shrews

Hideki ENDO1), Tsutomu HIKIDA2), Loke Ming CHOU3), Katsuhiro FUKUTA4) and Brian J. STAFFORD5,6)

1)Department of Zoology, National Science Museum, Tokyo, 3–23–1 Hyakunin-cho, Shinjuku-ku, Tokyo 169–0073, 2)Department of Zoology, Faculty of Science, Kyoto University, Kyoto 606–8501, Japan, 3)Raffles Museum of Biodiversity Research, National University of Singapore, Singapore, 4)Laboratory of Morphology and Function, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Aichi 464–8601, Japan, 5) Division, National Museum of Natural History, Smithsonian Institution, Washington DC and 6)Department of Anatomy, Howard University College of Medicine, Washington DC, U.S.A.

(Received 18 April 2003/Accepted 20 August 2003)

ABSTRACT. The skull adaptation was functional-morphologically examined in 14 species of the tree shrews. From the data of the propor- tion indices, the similarities were confirmed between T. minor and T. gracilis, T. tana and T. dorsalis, and T. longipes and T. glis. We demonstrated that the splanchnocranium was elongated in terrestrial T. tana and T. dorsalis and shortened in arboreal T. minor and T. gracilis from the proportion data. In both dendrogram from the matrix of the Q-mode correlation coefficients and scattergram from the canonical discriminant analysis, the morphological similarities in the skull shape suggested the terrestrial-insectivorous adaptation of T. tana and T. dorsalis, and the arboreal adaptation of T. minor and T. gracilis. Since the osteometrical skull similarities were indicated among the three species of Tupaia by cluster and canonical discriminant analyses, the arbo-terrestrial behavior and its functional-mor- phological adaptation may be commonly established in T. montana, T. longipes and T. glis. KEY WORDS: canonical discriminant analysis, proportion, Q-mode, skull, tree shrew. J. Vet. Med. Sci. 66(1): 1–7, 2004

The arboreal and terrestrial tendencies and the patterns of sia). Since T. mulleri has been considered as a subspecies of behavior have been shown in various species of the tree T. splendidula [10], we included T. mulleri to T. splendidula shrews [1, 2, 4, 5, 9, 11]. Since the skulls have been func- in the statistical analyses. Sex determination was dependent tional-morphologically adapted to each style of locomotion, on the biological data of specimens. We used adult skull we previously examined the 4 species of Tupaia, and sug- specimens with fully erupted molars. gested that T. tana, T. javanica and T. minor have evolved Species composition, origin, and sex are shown in Table different behaviors [7]. Using the skull specimens of 14 1. Skull measurements were obtained with vernier calipers species of Scandentia, we compared the skull size and shape to the nearest 0.05 mm. Measurements are defined in Table among the species to confirm the relationships between the 2, and were based on Driesch [3]. In the present analysis we skull characteristics and the locomotion strategies [8]. used the same osteometrical data as those in the previous Although we compared the measurement data among the study [8]. The mean measurement values were shown in species and applied the principal component analysis to the each species [8]. The skull proportion indices were obtained osteometrical data to discuss the adaptational patterns of as quotients of each measurement value divided by the geo- skull form [8], the skull proportion indices should be actu- metric mean of all measurement values. The significant dif- ally obtained and the similarities of skull shape among tree ferences of proportion indices were examined among shrews should be quantitatively examined to elucidate the various species by nonparametric U-test using software Sta- morphological adaptation in various types of skull form in tistica (Statsoft Inc., Tokyo, Japan). these tree shrews. The clustering was performed by UPGMA method for the distance matrix converted from the matrix of the Q-mode MATERIALS AND METHODS correlation coefficients to avoid loss of information [12]. We did not use the measurement raw data but the proportion We examined 337 skulls of 14 species of the tree shrew indices in this cluster analysis. The distance matrix and the (Tupaia montana, T. picta, T. splendidula, T. mulleri, T. lon- dendrogram between species were obtained using the soft- gipes, T. glis, T. javanica, T. minor, T. gracilis, T. dorsalis, ware Statistica. The canonical discriminant analysis was T. tana, melanura, D. murina, and Ptilocercus also undertaken in each species using the proportion indices. lowii) [8]. The specimens have been stored in Muséum The first two canonical discriminant functions were calcu- National d'Histoire Naturelle (Paris, France), the Mammal lated and their scores were plotted using the software Statis- Division of the Smithsonian Institution (Washington DC, tica. We also applied another canonical discriminant U.S.A.), The University Museum, Kyoto University (Kyoto, analysis to the osteometrical data of the species excluding Japan), the Raffles Museum of Biodiversity Research, D. melanura, D. murina, P. lowii, T. tana and T. dorsalis to National University of Singapore (Singapore), the Depart- detail the morphological similarities among the typical ment of Wildlife and National Parks (Kuala Lumpur, arbo-terrestrial Tupaia species. List of measurements and Malaysia), and Bogor Zoological Museum (Bogor, Indone- their abbreviations are summarized in Table 2. 2 H. ENDO ET AL.

Table 1. Behavioral character, origin and sex composition of the specimens in each species Species Behavior Origin of Specimes Male Female Tupaia montana Arbo-terrestrial 52 54 Tupaia picta Arbo-terrestrial Borneo 3 0 Tupaia splendidula Arbo-terrestrial Borneo 2 2 Tupaia mulleri Arbo-terrestrial Borneo 1 1 Tupaia longipes Arbo-terrestrial Borneo 9 3 Tupaia glis Arbo-terrestrial Malayan Peninsula 22 38 Tupaia javanica Arbo-terrestrial 9 6 Tupaia minor Arboreal Borneo, Sumatra 5 4 Tupaia gracilis Arboreal Borneo 14 6 Tupaia tana Terrestrial Borneo, Sumatra 24 26 Tupaia dorsalis Terrestrial Borneo 2 3 Dendrogale melanura Arboreal Borneo 10 5 Dendrogale murina Arboreal Thailand, Vietnam 2 4 Ptilocercus lowii Arboreal Malayan Peninsula 13 17 Total 168 169

The index of LBO was larger in T. minor, T. gracilis, D. Table 2. List of measurements and their abbreviations melanura and D. murina, and smaller in T. tana and T. dor- 1.Cranium salis. Profile length PL The dendrogram and the distance matrix are shown (Fig. Condylobasal length CL 2, Table 5). The dendrogram of male was fundamentally Short lateral facial length SL Zygomatic width ZW similar to that of female. We confirmed the two large clus- Least breadth between the orbits LBO ters as follows: 1) T. montana, T. picta, T. longipes, T. glis, Greatest neurocranium breadth BNB T. tana and T. dorsalis, and 2) T. javanica, T. minor, T. gra- Median palatal length MPL cilis, D. melanura, D. murina, and P. lowii. Only T. splen- Length from Basion to Staphylion LBS didula was present in the different cluster between sexes. Dental length DL The results of the discriminant analysis were visualized Greatest palatal breadth GPB (Fig. 3, Table 6). The pattern of plots was not demonstrably Greatest mastoid breadth GMB Height from Akrokranion to Basion HAB different between sexes. The plots of T. tana and T. dorsalis 2.Mandible and those of T. minor and T. gracilis were concentrated. P. Length from the condyle LC lowii was separated from the other species in plot distribu- Length from the angle LA tion. Length from Infradentale LIA We also showed the plots of the individual discriminant to aboral border of the alveolus scores and the discriminant functions using the osteometri- Height of the vertical ramus HR cal data in each species except D. melanura, D. murina, P. Height of the mandible at M1 HM lowii, T. tana and T. dorsalis (Fig. 4, Table 7), since we The measurement items were based on Driesch [3]. could not clarify the plot distribution in the typical arbo-ter- restrial species at the chart scale of Fig. 3. The plot distribu- RESULTS tion of T. montana, T. glis and T. longipes showed the species-specific tendency at the higher scale of chart (Fig. The proportion indices are arranged in Table 3, and the 4), although the plot areas were adjacently located among relationships of the proportion indices between PL and SL the three species. The plots of T. minor, T. gracilis and T. are shown in Fig. 1. The significant differences are shown javanica were concentrated into the three groups separated among species in Table 4. The significant differences were from the other species (Fig. 4), although the plot areas of the not found in many measurements between T. minor and T. three species were partially overlapped in male. gracilis, T. tana and T. dorsalis, and T. longipes and T. glis (Tables 3 and 4). The indices in the two species of Dendro- DISCUSSION gale were similar in many measurements. The index of SL clearly demonstrated that the face and splanchnocranium We pointed out that the five groups of skull adaptation were rostro-caudally elongated in terrestrial T. tana and T. pattern have been established in these tree shrews [8]. In dorsalis and shortened in arboreal T. minor, T. gracilis and addition, the separation of eight groups was obviously visu- P. lowii (Fig. 1). The PL and CL in the two arboreal species, alized in the principal component charts [8], and it was con- T. minor and T. gracilis, were relatively smaller (Fig. 1), sistent with the locomotion strategies in these species. In although the significant differences were not clearly shown this study we demonstrated that the proportional similarities between the arboreal and arbo-terrestrial Tupaia species. without size factor were confirmed between the arboreal SKULL PROPORTION IN TREE SHREWS 3

Table 3. The proportion indices in each measurement of various species

PL CL SL ZW LBO GNB MPL LBS DL GPB GMB HAB LC LA LIA HR HM Tupaia montana M 2.465 2.119 1.069 1.289 0.703 0.948 1.287 0.840 1.266 0.792 0.982 0.582 1.662 1.667 1.020 0.676 0.178 0.029 0.026 0.026 0.035 0.024 0.029 0.033 0.022 0.027 0.023 0.045 0.016 0.026 0.029 0.027 0.029 0.011 F 2.470 2.130 1.071 1.274 0.695 0.956 1.298 0.843 1.273 0.800 0.980 0.580 1.659 1.664 1.026 0.681 0.173 0.029 0.024 0.026 0.032 0.020 0.031 0.024 0.019 0.023 0.018 0.046 0.021 0.018 0.024 0.022 0.025 0.010 Tupaia picta M 2.416 2.100 1.057 1.244 0.700 0.941 1.292 0.819 1.277 0.783 1.006 0.581 1.667 1.677 1.027 0.701 0.183 0.027 0.033 0.044 0.038 0.015 0.014 0.017 0.039 0.013 0.016 0.026 0.010 0.024 0.045 0.034 0.004 0.012 Tupaia splendidula M 2.424 2.089 1.007 1.287 0.701 0.960 1.252 0.854 1.245 0.768 1.010 0.603 1.650 1.668 1.002 0.715 0.186 0.041 0.034 0.032 0.017 0.007 0.027 0.027 0.038 0.026 0.020 0.016 0.032 0.003 0.003 0.023 0.013 0.019 F 2.451 2.135 1.041 1.266 0.668 0.963 1.292 0.852 1.262 0.791 1.006 0.590 1.663 1.659 1.034 0.695 0.175 0.012 0.004 0.012 0.018 0.013 0.037 0.008 0.010 0.016 0.018 0.017 0.018 0.018 0.027 0.004 0.033 0.005 Tupaia longipes M 2.447 2.123 1.049 1.195 0.677 0.928 1.325 0.805 1.307 0.826 1.002 0.594 1.676 1.670 1.057 0.664 0.183 0.028 0.015 0.018 0.066 0.027 0.028 0.010 0.011 0.017 0.017 0.024 0.015 0.012 0.018 0.014 0.023 0.012 F 2.403 2.073 1.049 1.222 0.685 0.967 1.302 0.791 1.280 0.824 1.006 0.604 1.651 1.639 1.039 0.675 0.189 0.007 0.023 0.020 0.006 0.007 0.045 0.020 0.019 0.020 0.019 0.010 0.015 0.017 0.031 0.006 0.023 0.010 Tupaia glis M 2.457 2.131 1.076 1.231 0.694 0.920 1.317 0.828 1.292 0.766 0.982 0.585 1.683 1.689 1.057 0.670 0.183 0.027 0.029 0.031 0.023 0.024 0.023 0.025 0.025 0.021 0.020 0.029 0.021 0.021 0.028 0.028 0.032 0.016 F 2.471 2.145 1.072 1.209 0.686 0.940 1.320 0.837 1.303 0.781 0.989 0.583 1.674 1.679 1.060 0.659 0.178 0.027 0.023 0.022 0.031 0.025 0.022 0.020 0.021 0.021 0.021 0.019 0.013 0.020 0.026 0.026 0.022 0.010 Tupaia javanica M 2.458 2.143 0.983 1.286 0.735 1.019 1.281 0.872 1.243 0.777 0.935 0.598 1.647 1.647 0.992 0.688 0.180 0.040 0.013 0.016 0.024 0.024 0.033 0.020 0.018 0.022 0.021 0.047 0.020 0.029 0.030 0.008 0.030 0.012 F 2.469 2.140 0.982 1.260 0.725 1.022 1.280 0.865 1.242 0.787 0.922 0.606 1.626 1.654 1.008 0.685 0.185 0.024 0.044 0.020 0.031 0.020 0.014 0.023 0.036 0.031 0.026 0.030 0.016 0.019 0.055 0.014 0.035 0.013 Tupaia minor M 2.420 2.068 0.889 1.351 0.795 1.085 1.161 0.897 1.176 0.794 1.000 0.624 1.612 1.599 0.963 0.703 0.184 0.027 0.021 0.019 0.029 0.039 0.019 0.034 0.029 0.015 0.014 0.022 0.020 0.025 0.036 0.044 0.019 0.013 F 2.447 2.063 0.906 1.312 0.780 1.092 1.177 0.876 1.189 0.795 1.008 0.630 1.630 1.605 0.964 0.674 0.187 0.027 0.031 0.015 0.029 0.028 0.047 0.017 0.027 0.013 0.022 0.035 0.024 0.039 0.032 0.024 0.016 0.013 Tupaia gracilis M 2.447 2.070 0.945 1.293 0.767 1.081 1.197 0.872 1.202 0.805 1.060 0.646 1.594 1.590 0.966 0.677 0.171 0.025 0.020 0.019 0.020 0.021 0.033 0.039 0.016 0.016 0.016 0.026 0.037 0.020 0.029 0.018 0.022 0.011 F 2.457 2.061 0.946 1.299 0.755 1.086 1.211 0.867 1.205 0.810 1.066 0.637 1.588 1.588 0.969 0.667 0.174 0.018 0.026 0.035 0.022 0.012 0.023 0.023 0.019 0.018 0.017 0.046 0.030 0.022 0.021 0.026 0.025 0.007 Tupaia tana M 2.595 2.257 1.291 1.142 0.657 0.881 1.454 0.823 1.369 0.681 0.918 0.574 1.758 1.747 1.111 0.589 0.171 0.049 0.042 0.037 0.026 0.019 0.026 0.038 0.028 0.023 0.026 0.029 0.015 0.027 0.041 0.031 0.032 0.013 F 2.581 2.242 1.264 1.135 0.651 0.881 1.438 0.820 1.370 0.696 0.923 0.575 1.762 1.759 1.115 0.600 0.171 0.044 0.034 0.042 0.029 0.022 0.030 0.033 0.014 0.032 0.021 0.043 0.020 0.027 0.037 0.031 0.031 0.010 Tupaia dorsalis M 2.571 2.190 1.251 1.147 0.685 0.985 1.427 0.781 1.352 0.743 0.951 0.597 1.707 1.684 1.111 0.560 0.162 0.032 0.037 0.005 0.017 0.000 0.040 0.011 0.044 0.010 0.017 0.016 0.058 0.013 0.017 0.047 0.012 0.004 F 2.542 2.229 1.257 1.159 0.673 0.933 1.432 0.790 1.355 0.718 0.931 0.586 1.729 1.713 1.117 0.573 0.170 0.015 0.037 0.013 0.021 0.020 0.004 0.029 0.023 0.028 0.011 0.037 0.013 0.031 0.027 0.038 0.038 0.006 Dendrogale M 2.559 2.158 1.062 1.269 0.742 1.115 1.288 0.879 1.242 0.721 1.037 0.646 1.564 1.527 0.974 0.667 0.155 melanura 0.028 0.021 0.025 0.024 0.021 0.025 0.023 0.024 0.017 0.017 0.030 0.027 0.022 0.025 0.023 0.015 0.009 F 2.555 2.147 1.059 1.244 0.734 1.153 1.272 0.887 1.255 0.734 1.045 0.649 1.555 1.533 0.980 0.640 0.156 0.017 0.030 0.027 0.029 0.014 0.043 0.022 0.021 0.012 0.025 0.023 0.030 0.015 0.011 0.040 0.025 0.006 Dendrogale murina M 2.486 2.151 1.003 1.288 0.754 1.005 1.311 0.859 1.287 0.745 0.962 0.619 1.622 1.556 1.034 0.671 0.170 0.035 0.025 0.021 0.083 0.017 0.014 0.027 0.005 0.022 0.005 0.023 0.009 0.003 0.058 0.007 0.030 0.011 F 2.465 2.125 0.963 1.256 0.744 1.074 1.259 0.865 1.265 0.777 1.002 0.643 1.579 1.571 1.006 0.648 0.178 0.027 0.019 0.034 0.022 0.018 0.022 0.040 0.020 0.019 0.014 0.023 0.020 0.030 0.029 0.031 0.018 0.003 Ptilocercus lowii M 2.489 2.225 0.809 1.446 0.553 0.976 1.165 1.065 1.157 0.761 1.085 0.564 1.668 1.739 0.985 0.776 0.193 0.022 0.022 0.017 0.020 0.013 0.024 0.024 0.016 0.012 0.013 0.013 0.014 0.019 0.024 0.014 0.011 0.010 F 2.493 2.228 0.812 1.430 0.541 0.971 1.166 1.071 1.154 0.759 1.083 0.557 1.676 1.747 0.981 0.767 0.204 0.024 0.025 0.025 0.035 0.013 0.028 0.016 0.018 0.015 0.019 0.013 0.020 0.021 0.026 0.023 0.025 0.009 The mean values of proportion indices are arranged in the upper row, while the standard deviations in the lower row.

species, T. minor and T. gracilis, D. melanura and D. murina, and between the completely terrestrial species, T. tana and T. dorsalis. The similarities between T. minor and T. gracilis, and T. tana and T. dorsalis were also established in the dendro- grams from Q-mode correlation coefficients (Fig. 2) as

Fig. 1. The relationships of the proportion indices between PL (Profile length) and SL (Short lateral facial length) in various species. Horizontal axis, PL, and vertical axis, SL. Symbols indicate the species as follows: M, Tupaia montana, P, T. picta, S, T. splendidula, U, T. mulleri, L, T. longipes, G, T. glis, J, T. javanica, m, T. minor, g, T. gracilis, D, T. dorsalis, T, T. tana, 1, Dendrogale melanura, 2, D. murina, and 3, Ptilocercus lowii. The same symbols are used for both sexes. 4 H. ENDO ET AL.

Table 4. Siginificant differences of proportion indices among various species of tree shrews PL CL SL ZW LBO GNB MPL LBS DL GPB GMB HAB LC LA LIA HR HM 1.Male T. montanaXT. longipes 0.095 0.640 0.022 0.000 0.012 0.034 0.000 0.000 0.000 0.000 0.246 0.042 0.028 0.502 0.000 0.132 0.238 T. montanaXT. glis 0.298 0.052 0.493 0.000 0.133 0.000 0.000 0.100 0.000 0.000 0.653 0.256 0.000 0.001 0.000 0.369 0.108 T. montanaXT. minor 0.005 0.001 0.000 0.002 0.000 0.000 0.000 0.001 0.000 0.652 0.481 0.001 0.002 0.001 0.001 0.037 0.259 T. montanaXT. gracilis 0.030 0.000 0.000 0.638 0.000 0.000 0.000 0.000 0.000 0.036 0.000 0.000 0.000 0.000 0.000 0.838 0.062 T. montanaXT. tana 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.002 0.000 0.000 0.000 0.052 0.000 0.000 0.000 0.000 0.045 T. montanaXT. dorsalis 0.020 0.025 0.017 0.017 0.216 0.099 0.017 0.035 0.017 0.025 0.234 0.855 0.039 0.272 0.020 0.017 0.049 T. longipesXT. glis 0.408 0.223 0.019 0.074 0.090 0.433 0.602 0.005 0.033 0.000 0.117 0.408 0.459 0.037 0.931 0.602 0.794 T. longipesXT. minor 0.072 0.003 0.003 0.003 0.003 0.003 0.003 0.003 0.003 0.003 0.739 0.028 0.003 0.003 0.003 0.009 0.739 T. longipesXT. gracilis 0.900 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.017 0.001 0.000 0.000 0.000 0.000 0.147 0.038 T. longipesXT. tana 0.000 0.000 0.000 0.002 0.036 0.000 0.000 0.032 0.000 0.000 0.000 0.005 0.000 0.000 0.000 0.000 0.036 T. longipesXT. dorsalis 0.034 0.034 0.034 0.099 0.480 0.059 0.034 0.346 0.034 0.034 0.059 1.000 0.034 0.480 0.034 0.034 0.034 T. glisXT. minor 0.018 0.002 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.009 0.151 0.005 0.001 0.001 0.001 0.034 0.901 T. glisXT. gracilis 0.206 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.417 0.019 T. glisXT. tana 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.253 0.000 0.000 0.000 0.028 0.000 0.000 0.000 0.000 0.007 T. glisXT. dorsalis 0.022 0.037 0.022 0.022 0.835 0.028 0.022 0.076 0.022 0.117 0.095 0.835 0.117 0.835 0.076 0.022 0.095 T. minorXT. gracilis 0.064 0.711 0.001 0.003 0.139 0.711 0.021 0.096 0.012 0.308 0.003 0.267 0.195 0.579 0.459 0.042 0.052 T. minorXT. tana 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.073 T. minorXT. dorsalis 0.053 0.053 0.053 0.053 0.053 0.053 0.053 0.053 0.053 0.053 0.053 0.699 0.053 0.053 0.053 0.053 0.053 T. gracilisXT. tana 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 1.000 T. gracilisXT. dorsalis 0.026 0.026 0.026 0.026 0.026 0.039 0.026 0.026 0.026 0.026 0.026 0.266 0.026 0.026 0.026 0.026 0.266 T. tanaXT. dorsalis 0.336 0.043 0.083 0.700 0.054 0.021 0.211 0.124 0.336 0.027 0.068 0.773 0.027 0.027 1.000 0.102 0.248 D. melanuraXD. murina 0.053 0.667 0.032 1.000 0.519 0.032 0.283 0.133 0.032 0.086 0.032 0.086 0.032 0.519 0.032 0.667 0.053 D. melanuraXP. Lowii 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.002 0.000 0.000 0.000 0.107 0.000 0.000 D. murinaXP. Lowii 0.734 0.027 0.027 0.027 0.027 0.089 0.027 0.027 0.027 0.062 0.027 0.027 0.027 0.027 0.027 0.027 0.027

2.Female T. montanaXT. longipes 0.004 0.007 0.108 0.011 0.335 0.858 0.775 0.004 0.592 0.063 0.284 0.038 0.391 0.211 0.253 0.642 0.032 T. montanaXT. glis 0.899 0.009 0.745 0.000 0.080 0.010 0.000 0.193 0.000 0.000 0.651 0.495 0.001 0.010 0.000 0.000 0.026 T. montanaXT. minor 0.091 0.001 0.001 0.034 0.001 0.001 0.001 0.018 0.001 0.602 0.374 0.003 0.080 0.002 0.001 0.461 0.032 T. montanaXT. gracilis 0.175 0.000 0.000 0.049 0.000 0.000 0.000 0.013 0.000 0.160 0.001 0.000 0.000 0.000 0.000 0.175 0.805 T. montanaXT. tana 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.491 0.000 0.000 0.000 0.000 0.350 T. montanaXT. dorsalis 0.004 0.004 0.004 0.004 0.086 0.100 0.004 0.004 0.004 0.004 0.093 0.567 0.004 0.011 0.004 0.004 0.453 T. longipesXT. glis 0.008 0.005 0.057 0.293 0.764 0.230 0.133 0.006 0.064 0.009 0.099 0.036 0.051 0.040 0.072 0.211 0.133 T. longipesXT. minor 0.034 0.724 0.034 0.034 0.034 0.034 0.034 0.034 0.034 0.077 0.480 0.077 0.480 0.289 0.034 1.000 0.724 T. longipesXT. gracilis 0.020 0.439 0.020 0.020 0.020 0.020 0.020 0.020 0.020 0.439 0.071 0.197 0.020 0.039 0.020 0.606 0.020 T. longipesXT. tana 0.005 0.005 0.005 0.005 0.026 0.007 0.005 0.015 0.005 0.005 0.005 0.026 0.005 0.005 0.005 0.008 0.022 T. longipesXT. dorsalis 0.050 0.050 0.050 0.050 0.513 0.127 0.050 0.827 0.050 0.050 0.050 0.127 0.050 0.050 0.050 0.050 0.050 T. glisXT. minor 0.087 0.002 0.001 0.001 0.001 0.001 0.001 0.013 0.001 0.324 0.324 0.002 0.036 0.001 0.001 0.170 0.214 T. glisXT. gracilis 0.101 0.000 0.000 0.000 0.000 0.000 0.000 0.006 0.000 0.004 0.000 0.001 0.000 0.000 0.000 0.356 0.259 T. glisXT. tana 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.002 0.000 0.000 0.000 0.185 0.000 0.000 0.000 0.000 0.011 T. glisXT. dorsalis 0.004 0.004 0.004 0.011 0.250 0.652 0.004 0.012 0.008 0.004 0.007 0.652 0.008 0.057 0.011 0.004 0.133 T. minorXT. gracilis 0.670 0.831 0.033 0.670 0.136 0.831 0.055 0.522 0.201 0.286 0.055 0.670 0.055 0.286 1.000 0.670 0.088 T. minorXT. tana 0.002 0.002 0.002 0.002 0.002 0.002 0.002 0.002 0.002 0.002 0.002 0.002 0.002 0.002 0.002 0.002 0.033 T. minorXT. dorsalis 0.034 0.034 0.034 0.034 0.034 0.034 0.034 0.034 0.034 0.034 0.034 0.034 0.034 0.034 0.034 0.034 0.077 T. gracilisXT. tana 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.001 0.000 0.000 0.000 0.001 0.595 T. gracilisXT. dorsalis 0.020 0.020 0.020 0.020 0.020 0.020 0.020 0.020 0.020 0.020 0.020 0.039 0.020 0.020 0.020 0.020 0.302 T. tanaXT. dorsalis 0.115 0.474 0.943 0.174 0.073 0.010 0.830 0.026 0.616 0.086 0.830 0.390 0.086 0.045 0.943 0.197 0.943 D. melanuraXD.murina 0.014 0.142 0.014 0.462 0.221 0.014 0.327 0.221 0.462 0.027 0.050 0.806 0.221 0.142 0.221 0.806 0.014 D. melanuraXP. Lowii 0.001 0.002 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.066 0.002 0.001 0.001 0.001 0.667 0.001 0.001 D. murinaXP. Lowii 0.128 0.002 0.002 0.002 0.002 0.002 0.002 0.002 0.002 0.107 0.002 0.002 0.002 0.002 0.107 0.002 0.002 Each value indicates the limit percentage in which the significant differences are confirmed between the two species. shown in description data and photographs [1, 7]. The insta- row to search insects by using their long nose. We also sug- ble results on T. splendidula may be due to the small sample gest that the elongated nose area may contribute to the olfac- size in this species. The small cluster that consisted of T. tory function in the two terrestrial species. In addition, the minor and T. gracilis was present in the large cluster includ- index of LBO is fundamentally related to binocular visual ing Dendrogale and Ptilocercus. Although the genetic dis- sense in arboreal behavior [6] and becomes generally tance has not been reported among these species, we noticed smaller in arboreal species than in terrestrial T. tana and T. that the adaptational similarities were confirmed among T. dorsalis. However, in the tree shrews, the LBO index was minor, T. gracilis, D. melanura, D. murina and P. lowii as larger in T. minor, T. gracilis, D. melanura and D. murina, suggested in the previous works [1, 2, 11]. than in the terrestrial species. Since the terrestrial life T. tana and T. dorsalis were similar in the indices of requires the insect-searching behavior and rostro-caudal many measurements (Tables 3 and 4). We suggest that the elongation of the skull in case of tree shrews [5, 8], we sug- two species showed the adaptational convergence, since gest that, as a result, the proportion index of LBO has not both species are dependent on termites and on the soil become smaller in the arboreal species than in T. tana and T. surface [5], and extended the splanchnocranium and dental dorsalis with long face. SKULL PROPORTION IN TREE SHREWS 5

In the Fig. 4 we suggest that the similar arbo-terrestrial adaptation may be shown among T. montana, T. longipes and T. glis. However, we conclude that the three species also indicated the morphological identity as an independent species in skull proportion from the charts. Its functional- morphological and adaptational factors have remained unclear, although the similarities among T. javanica and T. minor-T. gracilis were shown in the skull shape at chart scale of Fig. 4. We think that T. javanica may be highly adapted to arboreal life in comparison with the arbo-terres- trial species, T. montana, T. longipes and T. glis. The molecular genetic works will be carried out to clarify the phylogenetic relationships among the tree shrew species and will contribute to the functional-morphological expla- nations of the adapatational characters in the skull of various species.

ACKNOWLEDGEMENTS. We thank Dr. J. Cuisin, Muséum National d'Histoire Naturelle (Paris, France), Dr. J. Mead and G. Linda and staffs of the Smithsonian Institution (Washington DC, U.S.A.) and Dr. Masaharu Motokawa, The University Museum, Kyoto University (Kyoto, Japan) for their kind helps in our examinations of Museum speci- Fig. 2. Dendrograms of morphological similarities mens. We are also grateful to the curatorial staff of the Raf- among species based on the skull shape calculated fles Museum of Biodiversity Research, National University by the use of Q-mode correlation coefficients. of Singapore (Singapore), of the Department of Wildlife and Clustering was carried out by UPGMA method. National Parks (Kuala Lumpur, Malaysia), and of Bogor M) Male. F) Female. The distance matrices are Zoological Museum (Bogor, Indonesia). This study was shown in Table 5. Symbols are explained in the legend of Fig. 1. financially supported by Grant-in-Aids for Scientific Research nos. 13640705, 13575027, 14405030 and

Table 5. Lower half distance matrix transformed from Q-mode correlation coefficients male Tupaia Tupaia Tupaia Tupaia Tupaia Tupaia Tupaia Tupaia Tupaia Tupaia Dendrogale Dendrogale montana picta splendidula longipes glis javanica minor gracilis tana dorsalis melanura murina Tupaia picta 0.240 Tupaia splendidula 0.720 0.460 Tupaia longipes 0.420 0.260 0.930 Tupaia glis 0.330 0.230 0.970 0.210 Tupaia javanica 1.290 1.260 0.690 1.430 1.600 Tupaia minor 1.340 1.270 0.490 1.520 1.740 0.200 Tupaia gracilis 1.400 1.310 0.620 1.420 1.770 0.400 0.080 Tupaia tana 0.730 0.840 1.600 0.640 0.300 1.720 1.940 1.890 Tupaia dorsalis 0.750 0.850 1.680 0.560 0.400 1.720 1.850 1.690 0.090 Dendrogale melanura 1.630 1.710 1.390 1.630 1.740 0.870 0.700 0.500 1.220 1.040 Dendrogale murina 1.490 1.460 1.250 1.340 1.460 0.670 0.660 0.620 1.280 1.140 0.370 Ptilocercus lowii 1.270 1.320 0.670 1.430 1.420 0.620 0.630 0.840 1.460 1.710 1.160 1.230

female Tupaia Tupaia Tupaia Tupaia Tupaia Tupaia Tupaia Tupaia Tupaia Dendrogale Dendrogale montana splendidula longipes glis javanica minor gracilis tana dorsalis melanura murina Tupaia splendidula 0.258 Tupaia longipes 0.405 0.425 Tupaia glis 0.358 0.470 0.490 Tupaia javanica 1.202 1.255 1.025 1.503 Tupaia minor 1.369 1.348 1.057 1.758 0.306 Tupaia gracilis 1.328 1.339 0.967 1.768 0.405 0.079 Tupaia tana 0.673 0.838 0.983 0.208 1.677 1.890 1.925 Tupaia dorsalis 0.666 0.894 0.885 0.219 1.662 1.860 1.850 0.029 Dendrogale melanura 1.574 1.727 1.405 1.656 0.874 0.671 0.473 1.363 1.262 Dendrogale murina 1.541 1.592 1.072 1.673 0.424 0.305 0.183 1.737 1.618 0.262 Ptilocercus lowii 1.288 0.835 1.486 1.427 0.825 0.784 0.920 1.379 1.548 1.220 1.135 6 H. ENDO ET AL.

Fig. 3. The visualized results of the canonical discriminant analysis among species. Scattergrams showing the individ- ual scores on the discriminant axes 1 (horizontal) and 2 (vertical). M) Male, F) Female. Symbols are explained in the legend of Fig. 1. M) The first function comprises 61.0% of the variance and the second function 8.4%. F) The first function comprises 74.5% of the variance and the second function 8.9%.

Fig. 4. The visualized results of the canonical discriminant analysis among species. Scattergrams showing the individ- ual scores on the discriminant axes 1 (horizontal) and 2 (vertical). M) Male, F) Female. Symbols are explained in the legend of Fig. 1. The analysis was carried out from the osteometrical data of the species except Dendrogale melanura, D. murina, Ptilocercus lowii, Tupaia tana and T. dorsalis. M) The first function comprises 70.0% of the variance and the second function 12.4%. F) The first function comprises 69.6% of the variance and the second function 13.9%.

Table 6. Coefficients in each discriminant function PL CL SL ZW LBO GNB MPL LBS DL GPB male CAV1 -24.82 -34.75 -17.38 -50.03 -54.12 -50.06 -35.53 -63.28 -29.93 -63.91 CAV2 -20.23 -19.45 -50.48 -35.58 -43.84 -28.96 -41.26 -60.14 -28.02 -43.16 CAV3 10.96 21.67 42.34 20.76 58.50 59.07 21.61 39.48 24.58 20.76 female CAV1 -27.26 -35.07 -38.09 -58.88 -69.13 -54.82 -36.01 -87.91 -37.40 -64.90 CAV2 11.88 0.78 34.63 21.93 20.67 13.33 28.71 34.75 13.59 17.61 CAV3 24.08 20.31 49.91 30.51 76.26 57.05 21.20 41.89 35.40 38.84 GMB HAB LC LA LIA HR HM c. t. e. v. male CAV1 -53.48 -67.73 -17.29 -38.08 -44.14 -83.14 -278.51 827.31 53.18 CAV2 -45.08 -68.98 -14.71 -30.74 -57.22 -59.97 -245.13 726.62 20.10 CAV3 39.51 62.69 15.48 3.91 44.51 58.27 192.05 -579.12 8.56 female CAV1 -63.30 -92.54 -22.96 -38.73 -57.00 -88.87 -335.37 976.34 65.64 CAV2 22.95 34.01 20.46 21.01 26.33 29.56 144.66 -405.64 13.40 CAV3 50.03 82.34 25.89 16.23 36.73 59.88 246.11 -730.62 4.95 F-values are 18.04 in male, and 17.52 in female. c.t.: constant term. e.g.: eigen values. All osteometrical data were applied to this canonical discriminant analysis. SKULL PROPORTION IN TREE SHREWS 7

Table 7. Coefficients in each discriminant function PL CL SL ZW LBO GNB MPL LBS DL GPB Male CAV1 15.10 24.70 18.90 33.50 68.73 62.11 21.35 47.55 34.05 48.09 CAV2 -6.01 -47.34 -38.52 -23.54 -83.73 -52.35 -42.72 -43.08 -52.63 -69.17 CAV3 -15.12 0.88 -48.25 -17.29 -30.06 -24.34 -16.42 -22.17 -11.47 -62.79 Female CAV1 -52.59 -76.21 -106.64 -97.40 -193.52 -140.79 -69.27 -136.92 -100.30 -154.01 CAV2 2.81 -4.75 3.83 7.12 -30.86 -28.06 -34.22 -20.23 -28.90 -19.18 CAV3 -35.59 -0.78 -94.97 -46.91 -105.01 -66.18 -49.50 -89.40 -71.20 -117.12

GMB HAB LC LA LIA HR HM c. t. e. v. Male CAV1 43.67 62.11 29.66 17.64 35.73 69.30 234.37 -692.89 11.94 CAV2 -65.92 -92.70 -47.48 -12.14 -62.94 -83.27 -325.82 905.12 2.13 CAV3 -36.84 -47.27 -2.12 -18.71 -14.77 -30.10 -116.33 411.48 1.44 Female CAV1 -126.58 -219.02 -81.73 -69.63 -113.84 -181.08 -727.58 2125.27 10.09 CAV2 -14.51 -42.10 -27.90 -11.94 -25.86 -27.87 -158.14 330.83 2.17 CAV3 -91.32 -141.11 -60.55 -38.84 -64.05 -113.00 -418.50 1262.73 1.27 F-values are 7.48 in male, and 7.70 in female. c.t.: constant term. e.g.: eigen values. The data of Dendrogale, Ptilocercus, Tupaia tana and Tupaia dorsalis were excuded.

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