Collected Papers in Honor of Professor Emeritus Banri Endo: Commemoration of His Seventieth Birthday Hideo Takahashi, corresponding author. e-mail: htak@dokkyomed.ac.jp phone: +81-282-87-2123; fax: +81-282-86-6229

Published online 1 June 2006 in J-STAGE (www.jstage.jst.go.jp) DOI: 10.1537/ase.051201


Index
Introduction
Materials
Methods
Results and Discussion
Contents of MCPA2
Cranial websites
Conclusions
Acknowledgments
References

Introduction

Photographic atlases of human or other vertebrate bones are not designed merely as a collection of skeletal images. In such atlases, photos are selected to complement text information so that the illustrated contents can be used for educational purposes in primatology and physical anthropology (White and Folkens, 1991; Alexander, 1994; Whitehead et al., 2005). However, the Mammalian Crania Photographic Archive Second Edition (MCPA2), which we introduce here, is intended simply as a research resource, and was initially inspired by a voluminous data book on skeletal growth (Eto and Ashizawa, 1992). The latter reference book contains 600 radiographs of children’s growing hands, and spurred us to digitize a number of photographs at an early stage of our mammalian cranial image database project.

The primary purpose of this database project was to develop an efficient and accurate method of recording images of mammalian crania displayed in anatomical standard planes (Department of Anatomy DUSM, 2000a). A digital camera with sufficient CCD resolution, equipped with a telephoto or telemacro lens, was used to shoot more than 10,000 cranial pictures in any of six anatomically fixed directions. This system was found to be the most easy-to-use and economical device for capturing and digitizing images as of 1997. Prior to this, we started a preparatory study of the database project in 1990. Thus, the project itself has continued for 15 years and is still in progress, sometimes being revised on the web (Takahashi et al., 2004). For the morphometrics of cranial profiles or contours, which have interested us the most due to their use in skeletal morphology and biomechanics, numerical data are provided, based on the photographic measurement of the images on a computer monitor.

To provide an overview of the history of our database project, we start by pointing out that a much longer period was required to prepare the skeletal materials we used for our database product, MCPA2 (Shigehara et al., 2005). During a research career of almost 40 years, one of the authors (N.S.) has tried every means of collecting vertebrate bodies, from zoos to pet shops. After cleaning and maceration, more than 7000 animal skeletons have been housed and registered at different Japanese institutions in Sendai, Mibu, and Inuyama. The skeletal materials in Mibu, which include nearly 3000 vertebrates, all accessible to anyone regardless of academic or non-academic affiliation, were initially compiled in the Vertebrate Skeletal Collection Catalogue of the Dokkyo University School of Medicine (DUSM) (Department of Anatomy DUSM, 1992) This catalog accelerated the use of the materials in skeletal biology.

An image database that could aid skeletal research seemed impossible in 1990, when we initailly launched a preparatory study of video imaging. Video camcorders, not digital cameras, were then the most advanced image input tools with a recording function. In measuring video-captured images of crania on a computer screen, mensural errors were estimated and evaluated (Takahashi et al., 1995). From 1996 to 1998, basic techniques in taking pictures, image capturing, and database creation were developed by our project. The accomplishments of such technical research were applied to all mammalian crania housed at the Department of Anatomy, DUSM in Mibu. In 1999, nearly 8000 captured images were uploaded to our “Mammalian Crania Picture Archive” website database (http://taxa.soken.ac.jp/MCPA/en/mammal.html). Sample CDs compiled from the web images were distributed to the participants of our image database symposium, held at the annual meeting of the Anthropological Society of Nippon in Sapporo (Shigehara, 1999; Takahashi, 1999; Yamashita, 1999). In 2000, abridged CDs, containing the images and text on our database, were released along with a revised vertebrate skeletal catalog (Department of Anatomy DUSM, 2000a, b). The contents of our website and CDs were presented at another symposium of biological image databases at the National Science Museum, Tokyo (Shigehara et al., 2000).

During two periods, from 1997 to 1999 and from 2000 to 2002, we participated in the Sokendai (The Graduate University for Advanced Studies) project for developing Biological Image Databases (http://taxa.soken.ac.jp/), presided over by Hirotami T. Imai (Japanese Ant Database Group, 2003; http://ant.edb.miyakyo-u.ac.jp/E/index.html). Since the second period, our goal has shifted from recording all mammalian crania in Mibu to increasing the number of species; therefore, new and rare skeletal materials were borrowed from institutions outside Mibu, which resulted in the Mammalian Crania Photographic Archive 2nd Edition (MCPA2).

Throughout the MCPA and MCPA2 projects, the methods of taking standard view anatomical photographs with low distortion were kept consistent, because these digital images are intended for various kinds of observations, comparisons, and measurements. In this report, we first outline the making of MCPA2. Thereafter, the specifications of MCPA2 are summarized in comparison with several related databases available on the web.


Materials

We photographed mammalian crania, without the mandibles and hyoid bones, that had been macerated in Japan and were housed in five institutions (Table 1). We excluded severely fractured and very young specimens. Nearly all the mammalian materials from DUSM were included in the first release (Department of Anatomy DUSM, 2000a). Thus, the number of specimens exceeded 50 for several species, such as the American mink, rhesus monkey, crab-eating macaque, foxes, the Japanese marten, raccoon-dog, domestic dogs, and the squirrel monkey. In the current release (MCPA2), crania were chosen and added from the other four institutions listed in Table 1, concentrating mainly on species unavailable at DUSM. The total number of specimens photographed amounted to 1825.



All mammalian skeletons from Tohoku University in Sendai, which had been macerated and prepared mostly by Shigehara (N.S.), were added. Monkeys and apes were selected from the collections of the Primate Research Institute, Kyoto University and the Japan Monkey Centre, Inuyama. A number of rare mammals from the Institute for Live Fossils (private laboratory of Tomoyuki Inaba) significantly contributed to increasing the number of species in the collection.


Methods

Every cranium was photographed from six angles, including the anterior, posterior, right, left, superior, and inferior anatomical views. A horizontal plate was placed on a tripod platform that could rotate around the vertical axis. Each cranium was set on this plate and could be rotated by pitch, yaw, and roll systems similar to defining an airplane’s attitude. The tripod platform was rotated for yaw. For all the views, except the inferior view, wooden or rubber wedges were inserted under the occipital region and beneath the teeth for pitch and roll, respectively, to orient the orbitomeatal (Frankfort horizontal) plane horizontally (Martin and Saller, 1957). In the inferior view, the palatine plane was set horizontally, corresponding to the occlusal plane formed by the maxillary molar and premolar tips. For specimens that could not have their orbitomeatal plane adequately oriented or defined, the palatine plane was adopted for all views.

Superior and inferior views of crania were photographed through a front-reflective surface mirror, which was installed at an angle of 45° over the specimens. Using the mirror permitted a long-distance shot of the two views, by moving the optical axis through 90° from vertical to horizontal; thus, a sufficient distance could be maintained between the object and the camera, which was capable of moving freely on the ground and holding itself in the same direction as in the other four views. A custom-made surface mirror was used to decrease scattering and suppress ghost images, which inevitably appear in normal mirrors.

We selected a Kodak DCS460c with a CCD (27.6 × 18.4 mm) of 6 megapixels (3060 × 2036), the highest resolution available for consumer use in 1996. The digital camera had been assembled on a Nikon N90 body, to which we mounted a 200 or 500 mm Nikkor lens. Either of these focal lengths decreases perspective distortion. Crania size dictated which lens was selected. The 500 mm lens (f/4 Nikkor IF-ED AF-S) was used for crania exceeding 8 cm in maximum length at fixed distances of 5, 7, 10, 15 and 20 m, approximately, depending on cranial size. The 200 mm lens (f/4 Micro-Nikkor IF Ai-S) was utilized for smaller crania (less than 8 cm in maximum length) at a distance of 1.2 m. Four globe-shaped fluorescent lamps were used to light the crania. Exposure time was 1/5 second at f8 for every image.

Cranial orientation on each image were evaluated on computer monitors with a checklist including items such as exposure, focus, and camera rotation for all views, in addition to those features for each relevant view like symmetry, teeth overlap, and orbitomeatal plane. Rejected images were retaken and were assessed a maximum of four times. Poor images were caused mostly by technical difficulties in alignment. The natural asymmetry of the specimens, however, cannot be ignored.

The background of the crania was covered with black velvet into which the canine tips may sink while supporting the cranium’s weight. To prevent this, canines were set on a black, rigid rubber plate. A scale for image measurement was placed at the mid-depth of the object between the front and back. The cumulative number of shots, which was indispensable when creating the database, was located in a corner of the frame.

Our database contains four caliper measurements for each specimen. Nasion–basion length, zygomatic breadth, posterior cranial breadth (width of braincase especially the neurocranium), and maximum length (prosthion–opisthocranion length) of all specimens were measured with calipers; however, the data were sometimes missing due to unidentifiable points. Zygomatic breadth in our measurement was defined as the width of the cranium around the zygomatic region, which usually was obtained by measuring bizygomatic width, but sometimes by measuring biorbital width if larger. All measurements, except nasion–basion length, can be used to crosscheck measurements digitized from bone images on a computer screen.

Finally, we googled several websites containing skull photographs of mammals. These related sites were compared with MCPA2 in terms of such aspects as the number of images, the number of species, and image size.


Results and Discussion

Contents of MCPA2

The numbers of families, genera, and species contained in our mammalian database are summarized by order in Table 2, where the percentage shows the proportion of our final content to the total in each taxonomic category. The Order Primates included the largest number of specimens;. the Order Carnivora was the second largest in this respect. It is noted that the primate species exceeded 50% (93/181) of the total number of species within the order, while the number of all mammalian species photographed in our project represents only 7% (308/4282) of the grand total. This bias of bone selection arises from the preference for primate skeletons. In general, the scientific names and common names are based on Corbet and Hill (1991), while the taxonomy of Japanese mammals and their Japanese names are derived from Imaizumi (1988). For the other species not included in the above references, we consulted two Smithsonian Institute publications (Wilson and Reeder, 1992; Wilson and Cole, 2000). Domestic species are placed in independent categories, since they are different from their ancestors. For noncommercial purposes, in the meantime, no restriction is imposed on the use of these skeletal images.



The ranges in maximum length and breadth of all crania in MCPA2 are shown in Figure 1. The cephalic index is defined by the ratio of maximum cranial breadth to maximum length; usually its percentage terms have been used (Martin and Saller, 1957). The largest specimen was an Indian elephant (754 × 585 mm, DKY-0853). The smallest was a greater Japanese shrew-mole (25.8 × 12.7 mm, ILF-0152). Three human crania with no documented population background, which were selected from medical education osteological collections, were medium-sized and had cephalic indices ranging from 0.7 to 0.8. The average modern Japanese would be the most circular (brachycephalic, 0.86) (Kouchi, 2000) amongst the variation of this index in our cranial database. The lowest index (0.20) was calculated for a giant anteater (DKY-2186). The Grevy’s zebra (DKY-1764) has a large-sized and long cranium.


View Details
Figure 1.
Ranges in maximum length and breadth of crania of MCPA2. Three cephalic indices (1.0, 0.5, 0.2) are shown as lines. Several eccentric specimens are indicated.


Cranial websites

Very few websites containing cranial images of mammals could be found on the internet. Six institutional and three private databases were discovered using image search engines. Table 3 compares our site (MCPA2) with these other sites in terms of several criteria.



Animal Diversity Web

(Museum of Zoology, University of Michigan)

http://animaldiversity.ummz.umich.edu/site/index.html

Four hundred species with 2000 images can be accessed from the classification table. Encyclopedic text information accounts for all animals in detail, with more than 1200 photographs of living mammals. Cranial images photographed from, more or less, three different directions are medium-sized and appropriate for an XGA monitor. Some skulls can be rotated 3-dimensionally using QuickTime-VR.

Skull Gallery

(Anthropology Department, Glendale Community College)

http://www.glendale.edu/skull/

Nine hundred images are exclusively primate and include 50 species from prosimians to apes. Fossil and modern humans also are found. The medium-sized images are taken from 12 different angles including oblique views (left–front, right–front, right–back, left–back).

UMass Mammalogy Database

(University of Massachusetts Amherst, Biology Department)

http://informatics.bio.umass.edu/instruction/biol548/mammfrnt.phtml

This is a skeletal search page including approximately 200 mammalian species. The images consist mainly of skulls and partly of postcranial skeletons. These images are very large and have been photographed on a black background.

Visual Database of Primatology

(Primate Research Institute, Kyoto University)

http://www.pri.kyoto-u.ac.jp/gazodb/honemenu.shtml

This is our sister website whose images are shared with ours. Thumbnail images in a common scale are demonstrated in all six views.

The Marine Mammal Database

(Department of Zoology, National Science Museum, Tokyo)

http://svrsh2.kahaku.go.jp/skull/

This is a web content of 50 marine mammal species with more than 200 cranial images taken from six different angles. The section entitled “Illustrated Guide of Marine Mammals” provides concise morphological descriptions of the species of the Order Cetacea with body dimensions and stranding records in Japan.

DigiMorp

(National Science Foundation Digital Library at The University of Texas in Austin)

http://www.digimorph.org/index.phtml

The data have not been acquired with normal photography, but digitally reconstructed from voxel data of a high-resolution X-ray CT. The reconstructable images are theoretically innumerable, because they can be requested for any direction possible. In Table 3, however, the number of images for DigiMorph is 170, which refers to the number of thumbnails prepared for mammals and their extinct relatives. In addition to skeletal surface rendered models, slice movies for internal structure are provided for some species. This database ranges from vertebrates to some invertebrates and plants.

Skull Collection

http://www.d91.k12.id.us/skyline/teachers/robertsd/skulls.htm

A private site by DeLoy Roberts. Various vertebrates are provided with three cranial measurements and dental formulae. One hundred of the species are mammals.

Will’s Skull Page

http://www.skullsite.co.uk/index.htm

A private site by Will Higgs. The photographic quality is excellent with good focus enhanced by soft and delicate shadows with good lighting. Concise descriptions, measurements, and dental formula are provided for each species. A skull preparation guide and glossary of osteological terms may be useful.

Chunnie’s Mammal Skulls

http://www.geocities.com/chunniemonster/index.html

This is an anonymous private site with 50 mammalian images of medium size. Twenty crania of mammals are supplied with four measurements and dental formulae. Skull cleaning methods are explained in the page.


Conclusions

Compared to the skeletal databases cited above, our website (MCPA2) has the following features: (1) The largest number of cranial images for mammals so far. (2) The second largest number of species after the Animal Diversity Web. (3) The most abundant primate contents. (4) In addition to a representative specimen, the other non-representative specimens of the species (sometimes more than 50) serve to recognize variation in bone form within the same species. (5) Extremely large image size. (6) Six different views in standard anatomical planes are precisely and constantly provided for every specimen. (7) Maxillary dentition is obtained from the inferior view. (8) A scale is recorded on each image, from which the size of cranium can be estimated in millimeters on a computer screen. (9) Four caliper measurements are provided to crosscheck image measurement. (10) Full use of images for noncommercial purposes is possible without having to obtain permission.


Acknowledgments

We are grateful to the following specimen contributors: Tohoku University School of Dentistry (Masayoshi Kikuchi); the Japan Monkey Centre (Mitsuo Iwamoto); Tomoyuki Inaba; and Mitsuru Aimi. Several animal snapshots were provided, courtesy of Hirohisa Hirai, Minoru Kinoshita, Juichi Yamagiwa, Kunio Watanabe, Tetsuro Matsuzawa, Yoshi Kawamoto, Hiroyuki Tanaka, Mikiko Tanaka, Naoki Koyama, Mitsuru Aimi, and Yasuhiro Go. Special thanks for technical advice on web design go to Hirotami Imai, Akira Kihara, and Yoshihiro Ugawa. This project was supported by Grants-in-Aid from the Japan Society for the Promotion of Science (#08554036) and Sokendai Collaborative Research (1997–1999, 2000–2002).


References
Alexander R.M. (1994) Bones: The Unity of Form and Function. Peter N. Nevraumont Books, Macmillan, New York.
Corbet G.B. and Hill J.E. (1991) A world list of mammalian species. British Museum, London.
Department of Anatomy DUSM. (1992) Vertebrate Specimen Catalogue. Matsui PTO, Tochigi (in Japanese).
Department of Anatomy DUSM. (2000a) Mammalian Crania Picture Archive 2000 (CD-ROM). Matsui PTO, Tochigi.
Department of Anatomy DUSM. (2000b) Vertebrate Specimen Catalogue. Matsui PTO, Tochigi (in Japanese).
Eto M. and Ashizawa K. (1992) Longitudinal observations on physical growth and TW2 skeletal maturation of girls in Tokyo: Radiographic atlas of hand wrist. Therapeia, Tokyo.
Imaizumi Y. (1988) A World List of Mammals with Japanese Names. Heibon-sha, Tokyo (in Japanese).
Japanese Ant Database Group (2003) Ants of Japan. Gakken, Tokyo.
Kouchi M. (2000) Brachycephalization in Japan has ceased. American Journal of Physical Anthropology, 112: 339–347.
Martin R. and Saller K. (1957) 1. Methodik (Becken). Lehrbuch der Anthropologie, Band I. Gustav Fischer Verlag, Stuttgart.
Shigehara N. (1999) Cranial measurements of the human skeletal remain on the image data. Anthropological Science, 107: 89.
Shigehara N., Takahashi H., and Yamashita M. (2000) Image database for mammalian crania. The 6th Symposium of the Union of Japanese Societies for Natural History. Topri, Tokyo (in Japanese).
Shigehara N., Takahashi H., and Yamashita M. (2005) What skulls prove?—Skull database on the web. Newton, 25: 90–97 (in Japanese).
Takahashi H. (1999) Digital image capturing and processing system for mammalian crania. Anthropological Science, 107: 89.
Takahashi H., Yamashita M., and Shigehara N. (1995) Measurement of primate crania and mandibles derived from video image data. Anthropological Science, 103: 168.
Takahashi H., Yamashita M., and Shigehara N. (2004) Mammalian Crania Photographic Archive—From the Mouse to the Elephant (DVD-ROM with a leaflet). Therapeia, Tokyo.
White T.D. and Folkens P.A. (1991) Human Osteology. Academic Press, San Diego.
Whitehead P.F., Sacco W.K., and Hochgraf S.B. (2005) A Photographic Atlas for Physical Anthropology. Morton Publishihng, Englewood, Colorado.
Wilson D.E. and Cole F.R. (2000) Common Names of Mammals of the World. Smithsonian Institution Press, Washington and London.
Wilson D.E. and Reeder D.M. (1993) Mammal Species of the World: A Taxonomic and Geographic Reference. Smithsonian Institution Press, Washington and London.
Yamashita M. (1999) Construction of the image database of the mammalian crania collection of Dokkyo University School of Medicine. Anthropological Science, 107: 90.