FULL PAPER Anatomy Morphological Adaptation of the Skull for Various Behaviors in the Tree Shrews Hideki ENDO1), Tsutomu HIKIDA2), Masaharu MOTOKAWA3), Loke Ming CHOU4), Katsuhiro FUKUTA5) and Brian J. STAFFORD6,7) 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, 3)The University Museum, Kyoto University, Kyoto 606–8501, Japan, 4)Raffles Museum of Biodiversity Research, National University of Singapore, Singapore, 5)Laboratory of Animal Morphology and Function, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Aichi 464–8601, Japan, 6)Mammal Division, National Museum of Natural History, Smithsonian Institution, Washington D.C. and 7)Department of Anatomy, Howard University College of Medicine, Washington D.C., U.S.A. (Received 5 February 2003/Accepted 8 April 2003) ABSTRACT. Skull size and shape were examined among 14 species of the tree shrews (Tupaia montana, T. picta, T. splendidula, T. mulleri, T. longipes, T. glis, T. javanica, T. minor, T. gracilis, T. dorsalis, T. tana, Dendrogale melanura, D. murina, and Ptilocercus lowii). The bones of face were rostro-caudally longer in T. tana and T. dorsalis, contrasting with T. minor and T. gracilis, D. melanura, D. murina and P. lowii which have smaller facial length ratios. The arbo-terrestrial species (T. longipes and T. glis) were similar to terrestrial spe- cies in length ratios of bones of face unlike the other arbo-terrestrial species (T. montana, T. picta, T. splendidula, and T. mulleri). We propose that T. longipes and T. glis have adapted to foraging for termites and ants as have T. tana and T. dorsalis. Additionally small body size in T. javanica may be the result of being isolated in Java. We separated the species into 5 groups from the measurment values of skulls: 1) Terrestrial species; T. tana and T. dorsalis, 2) Arboreal species; T. minor and T. gracilis, 3) Arbo-terrestrial species group 1: T. montana, T. splendidula, T. picta and T. mulleri, and T. javanica, 4) Arbo-terrestrial species group 2: T. glis and T. longipes, 5) Arboreal species of Dendrogale and Ptilocercus. Principal component analysis separated species into 8 clusters as follows: 1) T. tana, 2) T. dorsalis, 3) T. montana, T. splendidula, T. picta and T. mulleri, 4) T. glis and T. longipes, 5) T. javanica, 6) T. minor and T. gracilis, 7) D. melanura and D. murina, and 8) P. lowii. We suggest that these clusters correspond to behavioral strategies and peculiarities observed in foraging, feeding and locomotion in each species. KEY WORDS: adaptation, behavior, osteometry, skull, Tupaiidae. J. Vet. Med. Sci. 65(8): 873–879, 2003 Tree shrews (Order Scandentia) consist of about 18 spe- National University of Singapore, in the Department of cies [1, 2, 6, 13, 22]. Since this order shows us the evolu- Wildlife and National Parks (Kuala Lumpur, Malaysia), and tionary process of arboreal adaptation in terrestrial animals, in Bogor Zoological Museum (Bogor, Indonesia). Sex the morphological variation in locomotor and feeding mech- determination was dependent on the description of biologi- anisms is noticeable among species [1, 22]. The behavior of cal data of specimens. Only specimens with fully erupted various species has been also detailed in field works [7]. molars were considered to be adults. Species composition, Previously we functional-morphologically examined 4 spe- origin, and sex are shown in Table 1. Skull measurements cies of Tupaia, and suggested that T. tana, T. javanica and were obtained with vernier calipers to the nearest 0.05 mm. T. minor have evolved different behaviors [10]. Here we Measurements are defined in Table 2, and were based on extend this study to include most members of Scandentia Driesch [5]. All measurements were then divided by the and to quantitatively examine morphological adaptations for geometric mean of PL in each species to remove the effects various behaviors (i.e. locomotion, foraging, feeding and of size. In these measurement ratios statistical differences nesting). In this study, we use 14 species of tree shrews among species were examined in the non-parametric U-test including Dendrogale and Ptilocercus to compare interspe- by the use of the software of Statistica (StatSoft, Inc., cies variations, and to clarify the adaptation strategy in skull Tokyo, Japan). The t-test was not used, since the normal morphology. distribution is not guaranteed with measurement ratios. Principal component analysis was used with all measure- MATERIALS AND METHODS ment data to examine variation among taxa. A package soft- ware for multivariate analysis (Shakai-Joho Service, Tokyo, We examined 337 skulls of 14 species of tree shrews Japan) added to Microsoft Excel 98 was used for this analy- (Tupaia montana, T. picta, T. splendidula, T. mulleri, T. lon- sis. gipes, T. glis, T. javanica, T. minor, T. gracilis, T. dorsalis, T. tana, Dedrogale melamura, D. murina, and Ptilocercus RESULTS lowii). The specimens have been stored in Muséum National d’Histoire Naturelle (Paris, France), in the Smith- The species were grouped into 5 morphological types sonian Institution, in The University Museum, Kyoto Uni- according to the data of the osteometrical ratio data in each versity, in the Raffles Museum of Biodiversity Research, species (Tables 3–5). In this grouping, the pattern of behav- 874 H. ENDO ET AL. Table 1. Species, behavioral character, origin and sex composition of the specimens Species Behavior Origin of Specimens Male Female Tupaia montana Arbo-terrestrial Borneo 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 Java 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 Table 2. List of skull and mandibular measurements and restrial species (Tables 3–5). The skull was laterally wider their abbreviations in the two species, and the ratios GNB/PL and GMB/PL Cranium were much larger than those in the species of other locomo- Profile length PL tion. Condylobasal length CL Arbo-terrestrial species group 1, T. montana, T. picta, T. Short lateral facial length SL splendidula, T. mulleri and T. javanica: The strong elonga- Zygomatic width ZW tion was not confirmed in these species unlike T. tana and T. Least breadth between the orbits LBO dorsalis, although the bones of face was relatively longer Greatest neurocranium breadth GNB than that of arboreal species. Median palatal length MPL Length from Basion to Staphylion LBS Arbo-terrestrial species group 2, T. longipes and T. glis: Dental length DL The ratios SL/PL, MPL/PL, DL/PL and LIA/PL were large Greatest palatal breadth GPB (Tables 3–5). The bones of face in the two species were ros- Greatest mastoid breadth GMB tro-caudally longer than the arbo-terrestrial group 1 in many Height from Akrokranion to Basion HAB cases. Especially the ratios DL/PL and LIA/PL of T. lon- Mandible gipes and T. glis were not different from those of terrestrial Length from the condyle LC Length from the angle LA T. tana and T. dorsalis (Tables 3–5). Length from Infradentale LIA Arboreal species of Dendrogale and Ptilocercus: The to aboral border of the alveolus bones of face were not elongated in these species, and length Height of the vertical ramus HR ratio is extremely small in P. lowii. In contrast the width Height of the mandible at M1 HM ratios ZW/PL and GMB/PL were large in Ptilocercus. First and second principal components represent size and proportion factor, respectively. We could point out that ior and locomotion such as terrestrial, arbo-terrestrial and these components segregated specimens into 8 clusters of arboreal in each species was based upon the descriptions species that were similar for both sexes (Fig. 1, Table 6): and the original data of field works (Table 1) [1, 2, 6, 7, 13, Cluster 1, T. tana, Cluster 2, T. dorsalis, Cluster 3, T. mon- 22]. We also distinguished the two groups of arbo-terres- tana, T. splendidula, T. picta, and T. mulleri, Cluster 4, T. trial species from the morphological similarities. glis and T. longipes, Cluster 5, T. javanica, Cluster 6, T. Terrestrial species, T. tana and T. dorsalis: The facial minor and T. gracilis, Cluster 7, D. melanura and D. part was rostro-caudally elongated in the skull. The ratios murina, and Cluster 8, P. lowii. SL/PL, MPL/PL, DL/PL and LIA/PL were larger than those of the other species (Tables 3–5). The ratios SL/PL and DISCUSSION MPL/PL were especially large in both sexes of the two spe- cies. The elongation of the bones of face resulted in small The skull is morphologically divided into two major ratios of skull width in terrestrially-adapted species, and the functional units, bones of cranium and bones of face, to clar- ratios ZW/PL, LBO/PL, GNB/PL and GMB/PL were much ify adaptational strategy in each species and behavior pat- smaller (Tables 3–5). tern. Measurement ratios of the bones of face are Arboreal species, T. minor and T. gracilis: The bones of noteworthy (Tables 3 and 4). SL/PL, MPL/PL, DL/PL and face were obviously short, and the ratio SL/PL was statisti- LIA/PL represent rostro-caudal length ratio in the bones of cally different from that of terrestrial species and arbo-ter- face.