We describe the tooth of a fossil beaver (Castoridae, Rodentia) discovered in the lower Miocene Koura Formation of Shimane Prefecture, western Japan. The specimen is an isolated, unworn left lower third molar that can be assigned to a large castorid, Youngofiber. To determine the taxonomic classification based on the internal enamel patterns of the tooth, we reconstructed those patterns using a three-dimensional image by X-ray peripheral quantitative computed tomography (pQCT). The obtained enamel patterns indicate that the M3 of Youngofiber is characterized by a transversely elongated proparafossettid and simple synclinids running obliquely and parallel. Moreover, the present specimen retains a well developed mesostriid extending up to half the lingual height of the crown. This characteristic is shared with another castorid specimen from the lower Miocene Nojima Group in Nagasaki Prefecture, suggesting a close relationship between Koura and Nojima beavers.
Introduction
The lower Miocene Koura Formation is distributed in Mihonoseki Town, Matsue City, Shimane Prefecture, western Japan (Figure 1) and consists mainly of nonmarine sediments, including five acidic tuff beds (lower t1 to upper t5 as defined by Kano and Nakano, 1985). Although the fission track dates of these tuff beds were not calculated by the IUGS recommended zeta calibration, it was approximately 26–23 Ma and 22 Ma for the range and the uppermost part of the Koura Formation, respectively (Kano and Yoshida, 1984). In addition, the upper Koura Formation is estimated to represent the early stage of the opening of the Japan Sea based on the chemical analysis of its sediments (Kogane et al., 1994). The Koura Formation yields brackish to freshwater mollusks, terrestrial plants of the Daijima flora, and pharyngeal teeth of cyprinid fish (e.g., Suzuki, 1949; Kano and Yoshida, 1985; Yasuno, 1991). Recently, terrestrial vertebrate fossils were discovered in the same horizon of the Sai and Karubi coasts in the area (Figure 1); these fossils included turtles, crocodiles, carnivores, artiodactyls, rodents, and footprints of quadrupeds (Kawano et al., 2010). This paper presents the systematic description of a castorid rodent tooth that was first discovered from the upper Koura Formation.
Fossil beavers have been found in North America, Europe, and Asia, ranging from the latest Eocene to the Holocene. Most recently, Korth (2001, 2007a) reviewed the classification of the family, recognizing five subfamilies (Agnotocastorinae, Anchitheriomyinae, Palaeocastorinae, Castoroidinae, and Castorinae). Within the Castoroidinae, he included two tribes (Trogontheriini and Castoroidini). Among them, Anchitheriomyinae and Trogontheriini are dominant in the Miocene of East Asia, and Xu (1994) proposed the “Asiacastor tooth pattern clade” for the two groups based on their dental morphology.
In Japan, castorid fossils have been found from the upper Oligocene Sasebo Group and the lower Miocene Nojima and Mizunami Groups (Tomida and Setoguchi, 1994; Kato and Otsuka, 1995; Tomida et al., 1995; Matsuhashi, 2007). Kato and Otsuka (1995) described a fragmentary tooth of Steneofiber sp. from the late Oligocene of Ohashi Kannon in Nagasaki Prefecture, indicating that it represented the earliest occurrence of this genus in Asia. On the other hand, Tomida and Setoguchi (1994) described three castorids (Youngofiber sinensis and two unidentified species) from the lower Miocene Mizunami Group, central Japan, and suggested that the diversity of beavers in Far East Asia is more expansive than previously thought. Kato and Otsuka (1995) also described fossil beavers from the lower Miocene Nojima Group in Nagasaki Prefecture. Morphologically, they referred to it as a large species with the “Asiacastor tooth pattern.” Thus, most of the beavers from Japan have been classified uncertainly because the teeth examined were fragmentary, unerupted, or isolated. Although the specimen from the Koura Formation is also an isolated, unworn tooth, we successfully observed the dental pattern by using X-ray computed tomography and identified the taxonomical position of the specimen.
Figure 1.
A. Location map of castorid fossils in Japan. B. Geologic map and geographical position of the fossil locality in the Shimane Peninsula (modified after Kano and Nakano, 1985).
Figure 2.
Left lower third molar of Youngofiber sp. (NMNS-PV 22052) from the lower Miocene Koura Formation. A. Sketch in occlusal view with terminology and measuring points; B. occlusal view, stereophotograph; C. buccal view; D. lingual view; E. radical view. Abbreviations: propaf, proparafossettid; paf, paraflexid; msf, mesoflexid; mtf, metaflexid; hyf, hypoflexid; pas, parastriid; hys, hypostriid; mss, mesostriid; L, length; W, width.
Method
The dental terminology of castorids used herein (Figure 2A) follows that of Stirton (1935) and also that of Crusafont et al. (1948) for primitive or additional structures on occlusal surfaces, where “sub-” is added to the name of the preceding fiexid or fossettid if there is an additional synclinid posterior to a main synclinid, and “pro-” is added to the following fiexid or fossettid if nothing precedes it. Measuring points are based on the anteroposterior length and buccolingual width of the occlusal surface (Figure 2A).
Internal enamel pattern images of the present specimen were reconstructed from four sections (S0 to S3) by using X-ray peripheral quantitative computed tomography (pQCT) (XCT Research SA+, Type 922011, by Stratec Medizintechnik GmbH) with a pixel size of 0.04 × 0.04 mm and a slice interval of 0.10 mm. The sections were sliced on a plane constructed from three points on the anterobuccal, anterolingual, and posterolingual edges, respectively (Figure 3). Sections S1 and S2 are defined as the trisection of the angle between the occlusal (section S0) and crown base surfaces (section S3) because the occlusal surface prospectively changes with tooth growth of the individual (see also Stirton, 1935). S1 is one-third of the internal surface away from So, and S2 is two-thirds of the internal surface away from S0. The measuring method of each surface is the same as that of the present occlusal surface in Figure 2A. The higher taxonomical classification of castorids follows Korth (2001, 2007a).
Abbreviations: NMNS-PV, National Museum of Nature and Science, Tokyo-Paleontology Vertebrate; IVPP, Institute of Vertebrate Paleontology and Paleoanthropology, Beijing; SILS, School of International Liberal Studies, Waseda University, Tokyo.
Systematic paleontology
Order Rodentia Bowdich, 1821
Family Castoridae Hemprich, 1820
Subfamily Castoroidinae Allen, 1877
Genus
Youngofiber
Chow and Li, 1978
Youngofiber sp.
Figure 2
Material.— NMNS-PV 22052, left lower third molar (M3).
Locality.—Eastern Karubi Coast, Mihonoseki Town, Matsue City, Shimane Prefecture, western Japan (GPS: 35°57′20″N, 133°30′3″E).
Horizon.—The bed between tuff t4 and t5 in the lower Miocene Koura Formation.
Measurements.—The crown size increases posterobuccally from the occlusal surface to the base. The measurements of each slicing surface are given in Table 1.
Description.—The referred material, NMNS-PV 22052, is an unworn M3 without roots. The crown base is surrounded by a cervical line. The enamel surface is rough. There is an interstitial wear facet on the anterior aspect. The occlusal outline is almost trapezoidal. The lophs of the tooth form five transversely elongated loops that are connected by the main cusps. There are five flexids and/or fossettids between the lophs.
Anteriorly, there is a small, transversely elongated fossettid (proparafossettid). Between the second and third lophs is a transversely elongated paraflexid, opening on the buccal side. The parastriid on this side is relatively shorter than the other striae. The mesoflexid is similar in shape and size to the paraflexid, and develops into a mesostriid on the lingual side. This stria extends half the lingual height of the crown. The hypoflexid is transversely shallow in the unworn state, while the hypostriid is dorsoventrally deep on the buccal side. This stria is twice as long as the mesostriid, extending nearly to the crown base. The posterior metaflexid is also similar in shape and size to the mesoflexid, and its lingual end slightly opens. These lophs and fiexids (fossettids) run nearly parallel in the anterobuccal to posterolingual direction.
Internal enamel pattern detected from X-ray pQCT scans.—We obtained the basic enamel pattern of the present specimen from four sections (S1 to S3) by using pQCT (Figure 4). Although the occlusal surface shows a complicated zigzag pattern, none of the internal enamel patterns are zigzag; they are all simple. This suggests that the observed zigzag pattern is just a juvenile feature. As observed in all sections, a large crack runs anteroposteriorly on the buccal side of the tooth, but the basic structure is observable in all images. There are five main synclinids and a small additional fossettid on the crown top (So). These main synclinids are similar to those of the external occlusal surface, obliquely extending in parallel. The accessory fossettid, which was termed the lingual subparafossettid by Crusafont et al. (1948), is positioned between the lingual ends of the para- and mesoflexids.
In the S1 and S2 sections, five main synclinids but no additional fossettids are present on the lingual side. The synclinids of S1 and S2 are slightly simpler than those of S0. The lingual end of the hypoflexid is transversely elongated and positioned between the buccal ends of the meso- and metafossettids. The outline of the sections is trapezoidal in S1 but nearly rectangular in S2 due to the posterobuccally increased crown size. The angle of the posterolingual corner is more acute in S1 than in S2. In S2, all of the fiexids excluding the hypoflexid have changed into fossettids, isolated from the outside enamel. The basic structure and enamel pattern is virtually identical between S2 and S3, but a subparafossettid appears on the buccal side of the latter section. This accessory fossettid is separated from the buccal end of the mesofossettid in S2. The smallest proparafossettid does not disappear regardless of wearing.
Table 1.
Measurements (in mm) of each internal enamel surface of NMNS-PV 22052. The So section is consistent with the occlusal surface. L. anteroposterior length; W, buccolingual width.
Figure 4.
Internal enamel patterns in each section reconstructed from the three-dimensional image by pQCT scan. Abbreviations: 1-subpaf, lingual-subparafossettid; b-subpaf, buccal-subparafossettid; also see Figure 2.
Comparison and discussion
Korth (2007a) adopted five subfamilies (Agnotocastorinae, Anchitheriomyinae, Palaeocastorinae, Castoroidinae, and Castorinae) in the family Castoridae. NMNS-PV 22052 is most similar to Castoroidinae in having a simple pentalophodont enamel pattern with a transversely elongated proparafossettid. Agnotocastorines are the most primitive lineage of the castorids (Korth and Emry, 1997; Flynn and Jacobs, 2007), and their lower molars are also pentalophodont like the Castoroidinae, although the synclinids of the former show some variations in size and shape. In Agnotocastor, the para- and metafossettids are not elongated transversely and are smaller than the mesofossettid (Figure 5A), and the proparafossettid is small or absent in M3. Anchitheriomyines retain the primitive condition; the lower cheek teeth exhibit the pentalophodont pattern, possessing transversely well de- veloped synclinids as observed in NMNS-PV 22052. However, this lineage is characterized by greater complexity of the occlusal pattern of cheek teeth than in the other castorids (Stirton, 1934; Stefen and Mörs, 2008; see also Figure 5B). NMNS-PV 22052 has a simple, laminar enamel pattern in the internal sections, which differs from that of Anchitheriomyinae.
Palaeocastorines have unique plesiomorphic features such as small-sized rooted teeth and occlusal surfaces preserving fossettids rather than flexids (Korth, 2001). Moreover, the proparafossettid is absent in M3 in most species of this lineage (Figure 5C), resembling the primitive agnotocastorines. NMNS-PV 22052 is distinguished from the palaeocastorines in having a much larger-sized tooth with a well developed proparafossettid. The most derived lineage, Castorinae, has progressively hypsodont cheek teeth that possess well developed striids on the lingual side, differing from Castoroidinae. Although some ancestral species in castorines (e.g., Steneofiber and Chalicomys) occasionally retain an oval accessory proparafossettid in M3 (Hugueney, 1999; Mörs and Stefen, 2010; see also Figure 5G), this feature generally disappears in the early wear stage.
Figure 5.
Phylogenetic relationships of fossil castorids showing M3 enamel pattern (after Hugueney, 1999; Korth, 2001; Flynn and Jacobs, 2007). (A) Agnotocastor galushai (FAM 79310 in Emry, 1972), (B) Anchitheriomys tungurensis (A.M. 26538 in Stirton, 1934), (C) Capacikala sp. (SDSM 5448 in Stefen, 2010), (D) Asiacastor major (M-2001/60-MK in Lytschev and Aubekerova, 1971), (E) Youngofiber sp. (NMNS-PV 22052 at S1 section), (F) Priusaulax browni (UNSM 119708 in Korth and Bailey, 2006), (G) Chalicomys jaegeri (fig. 28.6 in Hugueney, 1999).
Korth (2001) classified Castoroidinae into two tribes, Trogontheriini and Castoroidini, based on dental and cranial morphology. Xu (1994) also separated these two groups by tooth pattern: i.e., the “Asiacastor tooth pattern” for Trogontheriini and the “Castoroides tooth pattern” for Castoroidini. The former is a typical pentalophodont with a proparafossettid, while the latter shows an S-shaped enamel pattern with strongly developed hypo- and mesoflexids. However, some recent works suggested that early Castoroidini species retained primitive features such as no indication of the S-shaped pattern (Korth and Bailey, 2006; Korth, 2007b; Figure 5F). In addition, Korth (2007a) established a new tribe, Nothodipoidini, which was separated from Castoroidini. NMNS-PV 22052 is similar to Trogontheriini and early species of Castoroidini and Nothodipoidini in possessing the pentalophodont enamel pattern (“Asiacastor tooth pattern”). However, it is distinguished from the latter two tribes in having the following features: 1) larger-sized tooth crown base; 2) well developed proparafossettid that is elongated transversely; 3) acute angle of the posterolingual corner of the tooth in an early/moderate wear stage; 4) narrower anterior aspect than the posterobuccal one; and 5) dorsoventrally shallower mesostriid.
Trogontheriini is a highly diverse lineage in Eurasia, containing Euroxenomys, Trogontherium, Asiacastor, and Youngofiber (Korth, 2001). One of the earliest members of this group is Euroxenomys, which ranges from the early to late Miocene of Europe (Hugueney, 1999). It is characterized by comparatively high crowned cheek teeth (height being at least twice the anteroposterior length) and the absence of a proparafossettid in M3 except in young individuals. These characteristics are shared with castorines rather than with primitive pentalophodont species. Recently, Euroxenomys has been recognized as a subgenus of Trogontherium distributed from Europe to China (Hugueney, 1999). Based on the stratigraphic range of this genus, Xu (1994) suggested that it had dispersed from Europe into China during the latest Pliocene. NMNS-PV 22052 is distinguished from Trogontherium as well as Euroxenomys in having a well developed proparafossettid and a much larger size of the crown base.
Asiacastor, which is distributed in the upper Miocene of Kazakhstan in Central Asia, is characterized by obliquely running synclinids and buccolingually enlarged proparafossettids (Lytschev and Aubekerova, 1971; see also Figure 5D). Although the enamel pattern of this genus is most similar to that of NMNS-PV 22052, the crown size of the latter is threefold larger than that of Asiacastor.
Youngofiber is an early Miocene form discovered in Jiansu Province (eastern China, 20–19 Ma) and later reported from Gifu Prefecture (central Japan, 19–17 Ma) (Chow and Li, 1978; Xu, 1994; Tomida et al., 1995). Youngofiber sinensis, the largest species of the trogontheriines, has well developed proparafossettids in its lower cheek teeth. Unfortunately, NMNS-PV 22052 cannot be directly compared with the teeth of this species due to the absence of a common specimen. Comparing the present specimen with the P4 (IVPP V 5791.3 in Chow and Li, 1978) of Y. sinensis, NMNS-PV 22052 is similar in having simple synclinids running obliquely and parallel. In reference to the crown size of section S3, NMNSPV 22052 is almost identical to the M3 (IVPP V 10457) of Y. sinensis in buccolingual width.
Recently, another castorid specimen was reported from the lower Miocene Mizunami Group of Kani City, Gifu Prefecture, central Japan (Matsuhashi, 2007). Although its systematic position has not yet been established, this species possesses the pentalophodont pattern in its lower cheek teeth. The Kani specimen differs from NMNS-PV 22052 in having the parafossettid anteriorly curving at the center and buccolingually running synclinids. Additionally, the Kani specimen is clearly smaller than NMNS-PV 22052 (personal communication with Dr. T. Mörs). On the other hand, NMNS-PV 22052 is apparently similar to a castorid specimen from the lower Miocene Nojima Group of Kosaza (Sasebo City, Nagasaki Prefecture, western Japan; Figure 1A) in having a well developed mesostriid on the lingual side of a cheek tooth (Kato and Otsuka, 1995). This shared feature suggests the close relationship between the Koura and Nojima specimens.
In conclusion, the beaver fossil from the Koura Formation was assigned to the genus Youngofiber based on morphology, measurements, and the stratigraphic age. At present, it is unclear whether this is the same species as Y. sinensis from China and central Japan. It is also similar to the large castorids from the Nojima Group, Nagasaki Prefecture, suggesting a close relationship between them. Thus, the findings of this study show that Youngofiber is widely distributed in the middle early Miocene (around 20 Ma) of East China and Japan.
In the present study, analysis using X-ray pQCT for observing the internal enamel pattern of teeth was shown to be an available method for the classification of Castoridae. In addition, we need to ascertain whether the internal patterns are consistent with actual occlusal ones caused by wear in a future study.
Acknowledgments
We would like to thank the Ministry of Nature Protection Office in Matsue for granting permission for the field work in Daisen Oki National Park and the Research Center for Coastal Lagoon Environments, Shimane University for use of its Nakaumi Field Laboratory. We thank K. Shikama (undergraduate student of SILS, Waseda Univ in 2008) for discovering the present material. Y. Takakuwa (Gunma Museum of Natural History) cleaned the present material from the sediment, and N. Kohno (NMNS) advised us on the identification of the specimen. T. Nishimura (Primate Research Institute, Kyoto Univ.) assisted with the pQCT technique. T. Kato (Kurashiki Univ. of Science and the Arts) provided access to castorid specimens for the comparative work. Y. Ando (Mizunami Fossil Museum) helped with taking pictures. Moreover, we are grateful to all members of the excavation research team. We thank T. Mörs (Swedish Museum of Natural History) and C. Jin (IVPP) for a reviewing process.
Financial support was provided by the Ministry of Education, Culture, Sports, Science and Technology Grant-in Aid for the global COE to Kyoto University (A06).
