Bull. Kitakyushu Mus. Nat. Hist. Hum. Hist., Ser. A, 3: 123-133, March 31, 2005

Depositional environments and taphonomy of the bone-bearing beds of the Lower Cretaceous Kuwajima Formation, Tetori Group, Japan

Shinji Isaji1 Hiroko Okazaki1 Ren Hirayama2 Hiroshige Matsuoka3 Paul M. Barrett4 Takehisa Tsubamoto5 Mikiko Yamaguchi6 Ichio Yamaguchi6 Tatsuya Sakumoto6 INatural History Museum and Institute, Chiba, 955-2 Aoba-cho, Chuo-ku, Chiba 260-8682, Japan 2School of International Liberal Studies, Waseda University, 1-17-14 Nishiwaseda Shinjuku-ku, Tokyo 169-0051, Japan 3Department of Geology and Mineralogy, Faculty of Science, Kyoto University, Kitashirakawa-oiwake-cho, Sakyo-ku, Kyoto 606-8224, Japan ^Department of Palaeontology, The Natural History Museum, London, Cromwell Road, London SW 7 5BD, UK 5Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan 6Shiramine Institute of Paleontology, 10-1-20 Kuwajima, Hakusan, Ishikawa 920-2502, Japan

(Received August 21, 2004; accepted September 12, 2004)

ABSTRACT—The bone-bearing beds of the Lower Cretaceous Kuwajima Formation (Tetori Group) are described. Three facies of bone-bearing beds (Facies I: carbonaceous sandstones; Facies II: dark grey fine-grained silty sandstones; Facies III: dark greenish-grey mudstones) are present in inter-channel deposits that originated on a floodplain. The grain size of the sediments, and plant and molluscan fossils occurring in each bone-bearing bed, indicate that Facies I was deposited in a peat marsh, Facies II in a shallow lake, and Facies III in a vegetated swamp. Isolated small bones and teeth are the most abundant vertebrate fossils. Common elements in Facies II are aquatic vertebratessuch as fishes and turtles. Facies III is characterized by the occurrence of terrestrial lizards, tritylodontid synapsids and mammals. Vertebrate fossil assemblages in Facies II and III are not mixed with each other even though they both represent parautochthonous assemblages. In contrast, Facies I is allochthonous, and is composed mostly of reworked sediments from Facies II. Depositional environments of the bone-bearing beds are strongly correlated with the composition of their fossil assemblages, indicating that different facies preserve the original faunal differences that existed between the shallow lake and vegetated swamp environments.

INTRODUCTION Ishikawa Prefecture, has been a famous fossil locality (Figure 1) since the first discovery of dinosaur remains in During the past two decades, a large number of 1985. However, until recently, only a handful of speci- vertebrate fossils have been recovered from the Mesozoic mens were collected from Kaseki-Kabe, because the thin non-marine formations of Japan. The LowerCretaceous fossiliferous beds, which crop out several metres above Kuwajima Formation has yielded vertebrate fossils from ground level in an almost vertical cliff section, were not several localities. "Kaseki-Kabe", which means literally suitable for large-scale excavations. "Fossil Bluff' in Japanese, in Kuwajima, Hakusan City, In 1997, a road tunnel was driven through the cliff

This paper is one of those given at the Symposium of Early Creteceous Terrestrial Biota held in the Kitakyushu Museum of Natural History and Human History on the 1st and 2nd of September in 2003. 121 Shinji Isaji et at.

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V" tunnel H

10m """"-"-" ~~ "^~^~" ~~ :?v&& In-channels

•10m Inter-channels

in situ tree trunk

north Tedori Lake south Figure I. A: Location of Kaseki-Kabe (marked with *. 36 I2*N. 136 38'E). Kuwajima. Hakusan City, Ishikawa Prefecture. Japan. \i: Photograph of Kaseki-Kabe. view from the North West. C: Sketch of Kaseki-Kabe. showing inter-channel and in-channel deposits. Small arrows show the position of an in situ tree trunk. Modilied from Masuda et al.. (1991). section (Figure IB. C) permitting us to observe the fos- mals such as lizards, trilylodontid synapsids and mammals siliferous horizons in detail. So far. three facies of bone- have been newly discovered from several fossiliferous bearing rocks have been identified and numerous verte horizons, which had not been recognized in the cliff brate fossils have been found. The vertebrate fossil section prior to the tunnelling operation. These discov assemblages from Kaseki-Kabe include fishes, anurans. eries revealed that the compositions of the vertebrate fossil turtles, choristoderes. lizards, pterosaurs, sauropods. ther- assemblages are strongly related to the bone-bearing opods, hypsi lophodontian-gradc ornithopods. facies. Such modes of occurrence are noteworthy from a iguanodontians. birds, tritylodonlid synapsids and mam taphonomic point of view. mals (for references, see Figure 2). These materials have The purpose of this study is to describe the modes of been under study by a multi-institutional research team occurrence of vertebrate fossils from the Kuwajima For sponsored by the Shiramine Board of Education and by an mation of Kaseki-Kabe. This paper also discusses the Anglo-Japanese team under the leadership of Susan E. depositional environments and taphonomic processes that Evans (University College London) and Makoto controlled the composition of the small vertebrate fossil Manabe (National Science Museum. Tokyo). assemblages. Among the taxa listed above, small terrestrial ani Institutional abbreviation: SBEI-Shiramine Institute Bone-bearing beds of the Lower Cretaceous Kuwajima Formation 125

Facies I II III carbonaceous sandstones dark grey fine-grained silty sandstones dark greenish-grey mudstones Gastropoda Gastropoda Gastropoda Viviparus onogoensis - (va) Viviparus onogoensis - (va) Viviparus onogoensis - (r)

c Si, Micromelania sp. - (r) Micromelania sp. - (r) « ^ Pleuroceridae - (r) Pleuroceridae - (r) |1 Pupilloidea family indet.- (r) s 1 Physidae- (c) Bivalvia Bivalvia Bivalvia Unio ogamigoensis - (va) Unio ogamigoensis - (va) Unio ogamigoensis - (r) Sphaerium sp.- (r) Sphaerium sp.- (r)

Plant fragmented & dispersed completely fragmented & accumulated in situ rootlet fossils charophytan zygotes Environ ment peat marsh shallow lake vegetated swamp

Bone articulated (< 1%) articulated (< 5%) articu all isolated associated + dispersed (< 1%) associated + dispersed (< 5%) lation isolated + dispersed (> 98%) isolated + dispersed (> 90%) Neopterygii Neopterygii Neopterygii Semionotidae Semionotidae Semionotidae Lepidotes sp. ft Lepidotessp. • Lepidotes sp. ft Sinamiidae Sinamiidae Sinamiidae Sinamia up. Ar'Ar^A' Sinamia sp. ^A"'A"A' Sinamia sp. *** Pachycormidae ft Ostcoglossidae ft Lower Teleostei **• Lower Teleostei * • * Lower Teleostei * Anura Arachaeobatrachia ft Testudines Testudines Testudines Testudinoidea "A" "A" Tcstudinoidea "kit*k-k Testudinoidea * Trionychoidea 'A'"A" Trionychoidea "A"A"A"A' Trionychoidea * Sinemiidae ft Sinemiidae ** family indet. * family indet. "A"^ Squamata Squamata Squamata Anguimorpha ft Sakurasaurus sp. *•*• Paramacellodidae "A"A"A" Amphisbaenia ** Long-bodied animals ••* family indet. * family indet. * family indet. 60 gen. A (herbivore) * J2 gen. B (bicuspid) • gen. C (striated) • E gen. D (amphicoelous) ft gen. E (very small) * C3 gen. F (deep jaw, small teeth)ft

M Choristodera Choristodera Choristodera L. IShokawa -si- family indet. * family indet. * family indet. * t: Pterosauria Pterosauria Pterosauria > Type A ft Type A ft TypeB • TypcC • Type D t!r Theropoda Theropoda Theropoda Dromaeosauridae • Dromaeosauridae * Dromaeosauridae * Oviraptorosauria+Therizinosauridae Tyrannosauridae ft ft Theropoda family indet. • Sauropoda Titanosaurlformes *• Omithopoda Omithopoda Omithopoda Iguanodontidae ** Iguanodontidae •• Iguanodontidae -*-* Hypsilophodontian-grade ft Hypsilophodontian-grade * Omithischia indet. ft Aves ?Enantiornithiformes ft Synapsida Synapsida Synapsida Tritylodontidae * Tritylodontidae ft Tritylodontidae 'A"A"A"A' Mammalia Triconodonta ** Multituberculata *

Figure 2. Faunal and floral list of three bone-bearing facies found at Kaseki-Kabe and interpretation of their depositional environments. The total number of specimens found during 1997 to 2002 is based on the occurrence of isolated skeletal remains such as a tooth, a scale and a bone fragment. Associated or articulated specimens are counted as one specimen. Vertebrate fossils (•&: known only by one specimen; *: 50). Molluscan fossils (va; very abundant, c; common, r; rare). Sources of information on the fauna are summarized as follows: fishes (Yahumoto, 2000a, 2000b, 2000c, 2002), anurans (Matsuoka, 2000), turtles (Hirayama, 1996, 1997, 1999, 2000), choristoderes (Evans and Matsumoto, personal communication), lizards (Evans and Manabe, 2000), pterosaurs (Unwin and Matsuoka, 2000), sauropods (Barrett et al., 2002), theropods (Manabe et al., 1989, Manabe et al., 200o! Manabe and Barrett, 2000), hypsilophodontian-grade ornithopods (Manabe and Barrett, 2000, Ohashi et al. 2003), iguanodontids (Hasegawa et al. 1995, Manabe and Barrett, 2000), birds (Unwin and Matsuoka. 2000), tritylodontid synapsids (Setoguchi et al., 1999, Matsuoka and Setoguchi, 2000) and mammals (Rougier et al., 1999, Takaim et al., 2001). 126 Shinji Isaji et al. of Paleontology, Hakusan City, Ishikawa Prefecture, Geological Age Japan. The precise age of the Kuwajima Formation is un known because this non-marine formation is barren of reliable index fossils and is not interbedded with marine GEOLOGICAL SETTING strata containing ammonites or other index fossils. The Tetori Group is widely distributed in central However, circumstantial evidence indicates that the Honshu (Figure 1A) and is traditionally divided into Kuwajima Formation may be assigned to the Valanginian three subgroups: the Kuzuryu, Itoshiro and Akaiwa Sub stage of the Lower Cretaceous. groups in upward sequence (Maeda, 1961). In the Shir- The Mitarai Formation ( = Mitarashi Formation in amine area, the Itoshiro and Akaiwa Subgroups crop out Sato et al., 2003) of the Kuzuryu Subgroup in the Shok- and are subdivided into four formations; the Gomijima, awa area, which is distributed about 30 kilometers south Kuwajima, Akaiwa and Kitadani Formations in ascend east from Kaseki-Kabe (Figure 1A) yields ammonites. ing order (Maeda, 1961). The Gomijima Formation The age of this ammonite fauna is suggested to be Latest consists mostly of conglomerates containing gravels der Jurassic—Earliest Cretaceous (Tithonian—Berriasian) ived from the Hida basement metamorphic rocks. The (Sato et al., 2003). Although the Mitarai Formation Kuwajima Formation is composed of lower muddy sand does not crop out in the Shiramine area, it is regarded as stones deposited under brackish conditions and upper older than the Gomijima Formation, which is the basal alternating beds of sandstones and mudstones that were conglomerate of the Tetori Group in the Shiramine area deposited in freshwater. The Akaiwa Formation consists (Maeda, 1961). mostly of coarse-grained sandstones and contains inter The Kitadani Formation of the uppermost Tetori bedded conglomerates composed of orthoquartzites. The Group is regarded as late Hauterivian to Aptian in age Kitadani Formation consists of alternating beds of mud- based on non-marine trigonioidid bivalves (Matsumoto stones and sandstones. The latter two formations also et al, 1982, Matsukawa, 1983, Tashiro and Okuhira, represent a variety of freshwater depositional environ 1993, Isaji, 1993, Matsukawa et al, 1997, for review see ments. Tsubamoto et al, 2004). In addition, the spore and The section at Kaseki-Kabe is assigned stratigra- pollen assemblages from the Akaiwa Subgroup can be phically to the uppermost part of the Kuwajima Forma correlated to Hauterivian to Aptian assemblage from the tion. Kaseki-Kabe is composed of alternating beds of Songliao Basin, China (Umetsu and Matsuoka, 2003). fine-grained sandstones, mudstones and thick coarse Based on this palaeontological and stratigraphical evi grained sandstones (Figure IB, C). Alternating beds of dence, the Kuwajima Formation is considered to be fine-grained sandstones and mudstones contain numerous younger than basal Cretaceous and older than Hauter plant and animal fossils. In situ tree trunks (ca. 50-300 ivian: thus, it is tentatively assigned to the Valanginian. cm in height and 10-100 cm in diameter, Figure IC), At present, there is no radiometric date for the rootlets and occasional coals indicate that subaerial depo Kuwajima Formation. The Gifu-Ken Dinosaur sition of sediment continued long enough to allow devel Research Committee (1993) attempted to date the Okur- opment of a well-vegetated floodplain. Well-preserved odani Formation in the Shokawa area (the lateral equiva plant leaves in coarse-grained sandstones appear to have lent of the Kuwajima Formation: Maeda, 1961), by been deposited in the lake under high-energy conditions. fission track and potassium-argon analyses using tuff and Numerous remains of aquatic animals, including mol very fine-grained mud layers. As a result, they concluded luscs, ostracods and vertebrates, indicate that subaqueous that the Okurodani Formation was deposited somewhere deposition of sediment also occurred on the floodplain. in the period ranging from 140 to 120 Ma (i.e. sometime Thus, the alternating beds of fine-grained sandstones and in the Early Cretaceous). mudstones represent inter-channel sediments deposited on a floodplain (Figure IC). DESCRIPTION Thick coarse-grained sandstones within the section often show a channel-like distribution, being intercalated Bone-bearing rocks from the inter-channel deposits with the alternating beds of fine-grained sandstones and were collected as a result ofthe tunnelling at Kaseki-Kabe mudstones. Such coarse-grained sandstones contain (Figure IC). They can be divided into three principal numerous pebbles to cobbles of orthoquarzite, mud facies (Facies I: carbonaceous sandstones; Facies II: dark gravels and driftwood, especially in the basal part. grey fine-grained silty sandstones; Facies III: dark Therefore, the thick coarse-grained sandstones are regard greenish-grey mudstones) although intermediate facies are ed as channel deposits (Figure IC). also present. Their detailed stratigraphical arrangement Bone-bearing beds of the Lower Cretaceous Kuwajima Formation 127 of the three facies is currently unknown, as they have not dermal bones of turtles have been discovered. Occa been studied in situ in the tunnel boring. sional associated or articulated skeletons of turtles are Vertebrate fossils are generally rare, but the assem also present. Terrestrial animals such as lizards, blages that have been recovered are remarkably diverse in tritylodontid synapsids and mammals, which are common terms of the number of taxa represented. The fossil elements in Facies III, are extremely rare or absent (Figure assemblages obtained from each facies are listed in Figure 2, Table 1). 2. Facies III: Dark greenish-grey mudstones Facies I: Carbonaceous sandstones This facies is observed in large boulders that reach This facies is represented in large boulders with a approximately 100 cm in maximum diameter. The sedi maximum thickness of approximately 50 cm. The rocks ments are generally massive with occasional thin bedding. are usually massive and coarse-grained. They also often They consist of well-sorted silty mud and occasional show well-developed parallel bedding marked by thin angular very fine-grained quartz sands. The mud is accumulations of numerous plant remains. The coarse normally dark greenish-grey in colour, and frequently has grained sandstones tend to grade into organic-rich fine a blue-ish tint. This facies is extremely friable and crum grained sandstones or coals. bly following weathering. Plant remains consist mainly of compressed stems Plant remains, such as leaves and stems are rare, but and completely fractured leaves, which often show align numerous in situ rootlets have been observed (Figure 3C). ment in the same direction, indicating the direction of Individual rootlets often attain lengths exceeding 200 mm water flow. In situ plant remains are not observed. and reach diameters of approximately 3 mm. The stems Molluscan fossils, including unionid bivalves and vivipar- of the rootlets are present, extend perpendicularly to the id gastropods, are poorly preserved, due to post-burial bedding plane, and have some branches running obliquely diagenesis. Trace fossils are not found. downward. Some branches extend parallel to the bed All vertebrate fossils found in this facies are preserved ding plane. as isolated bones and teeth. The size of each fossil is Unionid bivalves and viviparid gastropods are generally less than 5 cm. They have been abraded to extremely rare. In particular, bivalve shells are always varying degrees and are commonly fragmented and occa disarticulated and fragmented when they occur. In con sionally heavily weathered. The most abundant elements trast, tiny gastropods, including sinistral pulmonates and are aquatic vertebrate remains, such as fish scales and terrestrial pupilloidids, which have never been discovered dermal bones of turtles (Figure 2). in Facies I and II, are common (Figure 2). Molluscan shells are occasionally coated with pyrite. Many bur Facies II: Dark grey fine-grained silty sandstones rows (10-20 mm in diameter) are also present. Microfos This facies is observed in large boulders that reach sils such as charophytan zygotes and ostracods are approximately 100 cm in maximum diameter. The sedi extremely rare. ments are generally massive and poorly stratified. They Vertebrate fossils are small and mostly isolated. In comprise silty matrix mixed with angular fine-grained general, small bones tend to be better preserved than those quartz sands. recovered from Facies I and II, but considerable variation Plant remains are preserved as fractured leaves and in preservation still occurs. Figures 3A and 3B show stems, but are not found accumulated in layers. In situ examples of articulated skeletal remains. In contrast, rootlets are rare. Microfossils such as charophytan Figure 3D shows disarticulated, but associated and well- zygotes and ostracods tend to be common in the slightly preserved, remains. Sometimes heavily modified (i.e. stratified part of this facies. Trace fossils are rare. abraded, fragmented and weathered) bones occur in asso Numerous viviparid gastropods and unionid bivalves ciation (Figure 3E, F). occur. The unionid bivalves are commonly articulated The fossil assemblage is characterized by the common and often found in life position. Isolated opercula of occurrence of terrestrial lizards, tritylodontid synapsids viviparids are often found. and mammals (Figure 2). Lizards are usually found as Vertebrate fossils are generally small and isolated, isolated dermal bones, vertebrae or jaws, but some but well preserved. Large bones (more than 10 cm in articulated specimens have also been found (Figure 3A, size) are extremely rare and heavily fractured and weather B). Hundreds of tritylodont teeth have been found so far ed where present. The fossil assemblage is characterized (Figure 2, Table 1) despite the loss of other skeletal by numerous occurrences of aquatic vertebrate remains elements. Tritylodont teeth are also usually found in (Figure 2). So far, hundreds of isolated fish scales and isolation. Generally, these isolated teeth have abraded 128 Shinji Isaji et al.

B

:igure 3. Modes ofoccurrence of vertebrate fossils from Facies 111. A. Partly articulated undescribed long-bodied lizard. (SBEI-I568) B. Partly articulated undescribed paramacellodid lizard. (SBEI-I90) C. Counterpart or A. Note the insitu rootlets perpendicular to the bedding plane. D. Associated skeletal remains of Sakurasaurus sp. (SBEI-199). E, F. Associated bone fragments and teeth of a tritylodontid. (E: SBEI-1567; F: SBEl-127). Abbreviations: bt: buccal tooth; c: crack: d: dentary; I": femur: i; incisor; m: maxilla: wb: weathered bone: r: rib: ro: rootlet. \: vertebra. All scale bars: 10 mm. Hone-bearing beds of the Lower Cretaceous Kuwajima Formation 129

Table I. Number of turtle and tritylodontid specimens collected from Facies I. II and 111 during the period 1997 to 1999. The number of specimens is based on the occurrenceof isolated remains as in Figure 2. 'marks indicate that the number of specimens has increased in these categories from the figures shown here since the time of initial data collection, though exact figures are not currently available.

Facies I Facies II Facies III

Turtle remains 55* 588' 5 Tritvlodont remains 3 197' crowns and corroded roots. In contrast, associated teeth lake sediments containing vertebrate remains and mollus do not usually suffer any significant abrasion of their can shells. This may have resulted in the deposition of crowns and roots. Such teeth are often found in associa carbonaceous sandy sediments (Facies I). tion with heavily weathered bones (Figure 3E. F). //; situ rootlets, and the well-sorted mudstones. in Mammals have been discovered only from this facies: they Facies III suggest that these sediments represent a vegetat are usually represented by isolated jaw elements. ed subaerial swamp. Greenish-grey mud. well-preserved Remains of fishes and turtles are extremely rare (Figure 2. rootlets, and a pyrite coating on molluscan shells seem to Table I), but they are sometimes associated with each be indicative of anoxic conditions in the interstitial spaces other when they do occur. in silty sediment: this may be due to a high groundwater Eggshells are found only in Facies III. They are level. The well-sorted mud appears to come from the usually fragmented and concentrated in small areas of the suspended fine-grained sediments in overbank Hows, fol bedding plane. Round and slightly compressed eggs lowing the deposition of coarser sediments on levees and have also been discovered and are occasionally associated crevasse splays. The surface was probably inundated for with each other. short periods only, as water-dependent unionid bivalves

are rare. As is well known, a variety of depositional environ DISCUSSION ments including channel, lake, swamp, marsh and forest Depositional Environments of the bone-bearing rocks are locally distributed and scattered throughout the flood- The alternating beds of fine-grained sandstones and plain in recent river systems. In such fioodplains. sedi mudstones at Kaseki-Kabe appear to represent a variety of mentary deposits must grade laterally and vertically into depositional environments on a floodplain. The bone- each other. In the case of Kaseki-Kabe. gradations bearing rocks (Facies I, II and III) treated in this paper are among the three facies are observed. This indicates that the key to reconstructing the nature of the terrestrial and three depositional environments, in which each bone- freshwater ecosystem. bearing facies has been deposited, were present and occur Abundant remains of aquatic organisms in Facies II red simultaneously on the floodplain. as illustrated in suggest that subaqueous depositional environments, such Fig tire 4. as those o\~ a shallow lake (backswamp pond), were In addition, it may be inferred that calcareous skele present. It is presumed that plant remains, which were tons such as those of charophytan zygotes, ostracods. supplied from the surrounding swamps and forests, ac molluscs and vertebrate remains were protected chemi cumulated in the old shallow lake together with reworked cally from pre-fossilization dissolution. As discussed by

Figure 4. Reconslruction of the depositional environmenls for the three bone-bearing facies (Facies 1. II and 111), a: fish: b: lurile: c: lizard; d: tritylodont teeth: e: gastropod: f: bivalve: g: bone fragment: h: burrow: i: charophyte: j: conifer: k: fern, (illustrated by S. MABUCHl) 130 Shinji Isaji et al. parautochthonous

shallow lake (Facies II)

peat marsh (Facies I) allochthonous Figure 5. Transportation of skeletal remains between the three depositional envi ronments. Arrow indicates the flow direction and quantity of transported skeletal remains.

Retallack (1984), chemical factors such as high pH and/or Vertebrate fossil assemblages anoxic conditions may have protected the calcareous The major differences in the vertebrate fossil assem skeleton. blages from each bone-bearing facies are best illustrated The molluscan shells are the key to knowing the pH by the modes of occurrence ofskeletal remains from small conditions of their habitats. In general, extant unionid animals, including fishes, turtles, lizards and tritylodontid bivalves and viviparid gastropods suffer shell corrosion at synapsids. In contrast to other, larger, vertebrate taxa their umbonal and apical regions (i.e. the older parts of from Kaseki-Kabe (such as dinosaurs), the remains of the shell) during life because the pH of freshwater is such animals are abundant, with thousands of elements generally low (ranging from pH 5.6 in rainwater saturated available for study. The large sample size suggests that with C02) to pH 6-8 (world average of inland water, potential collection biases in the environmental distribu Hutchinson, 1957). Even in neutral pH conditions, tion of these remains can be ignored. In addition, sam shell corrosion occurs due to physical abrasion against the pling of the remains from each facies was essentially substratum and biological factors, such boring by algae random, as the collection procedure relied upon the seren and bacteria (e.g. Isaji, 1995). In the case of the mollus dipitous recovery of material from the rocks removed from can fossils from Facies II of Kaseki-Kabe, they have Kaseki-Kabe during the tunnelling operation, which ex suffered no corrosion to the older part of the shell. cavated several different stratigraphical levels. Therefore, the paleo-pH conditions of the surface water in So far, thousands of dermal bones of turtles and fish floodplain environment appear to have been higher than scales have been recovered from Facies II, but they are neutral. rare in Facies III. In contrast, hundreds of vertebrae and In addition to the higher pH values in the surface dermal bones of lizards and tritylodont teeth have been waters of the floodplain, the anoxic conditions found in recovered from Facies III, but they are extremely rare in the interstitial spaces of the muddy sediments were also an Facies II. As well-preserved bone occurs in both facies, important factor in preserving the calcareous remains it is unlikely that selective dissolution of vertebrate from decay. Well-preserved rootlets in Facies III should remains took place, so this factor cannot account for the be attributable to the lower activity of bacteria under faunal difference observed. anoxic conditions. In such circumstances, the inter- and This demonstrates simply that the subaqueous intra-crystalline organic matrices decay slowly, with the deposits preferentially yield aquatic animals while the result that the calcareous skeletons keep their shapes for subaerial deposits generally yield terrestrial animals. the long time. This idea may be supported by the abun This suggests in turn that vertebrate skeletons were not dant occurrence of biological carbonates, such as tiny transported from another community, even though they thin-shelled gastropods and amniote eggshells, which have been transported from their original position. In contain a high level of organic matter. other words, both fossil assemblages consist of parauto- Bone-bearing beds of the Lower Cretaceous Kuwajima Formation 131 chthonous remains (Figure 5). Therefore, it seems rea specimen (i.e. the more resistant teeth have kept their sonable to assume that the original faunal differences original shape, while the softer bone has been more between the shallow lakes and the vegetated swamps are extensively damaged). preserved in the fossil assemblages. In contrast to Facies II and III, vertebrate remains of CONCLUDING REMARKS Facies I are completely isolated and comprise mostly aquatic animals with rare terrestrial forms, which seem to Major biological changes occurred during the Late be reworked from the shallow lake (Facies II) and vegetat Jurassic to Early Cretaceous transition (Unwin, 1999, ed swamp (Facies III) facies, respectively. It seems that Hedges et al., 1996, Evans and Manabe, 1999, Evans et the vertebrate fossil assemblages of Facies I are allochth al, 1998, Manabe et al., 2000). However, most of the onous (Figure 5). events that have been recognized are based mainly on the Remains of large animals, such as iguanodontian fossil record of large animals. In contrast, the fossils of dinosaurs, are noteworthy. Although they are also small terrestrial tetrapods have often been overlooked. preserved as isolated teeth, and other large skeletal Therefore, little has been discovered regarding historical remains have not been found (as in the case of changes in the small vertebrate fauna despite their impor tritylodontid synapsids), their modes of occurrence are tance as basal components for terrestrial vertebrate eco different from those of the small animals. These larger systems. fossils are obtained from all three facies (Figure 2). Most Our knowledge of the diversity of Early Cretaceous of the iguanodontian teeth are terminally resorbed terrestrial vertebrate fauna has expanded rapidly with the (Hasegawa et al., 1995): this indicates that the teeth were finding of new Lagerstatten such as the Jehol Group of shed by living animals . The occurrence of such teeth in Liaoning, China (e.g. Luo, 1999, Ji et al, 1999, 2001, all three facies indicates that these dinosaurs were not 2002, Zhou and Zhang, 2002, Zhou et al, 2003). In the restricted to a single habitat, but ranged across the whole Tetori Group, the bone-bearing Facies III contains impor floodplain. tant small vertebrate fossil assemblages including terres trial lizards, tritylodontid synapsids and mammals that Agents of disarticulation complement those of the slightly younger Jehol Group. Post mortem disarticulation of an animal skeleton is At present, Facies III is found nowhere else in the Tetori the result of combined physical, chemical and biological Group, occurring only at Kaseki-Kabe. Even here, it has processes. For example, scavenging and fluvial transpor been overlooked for many years, even though the first tation are both important factors in subaqueous de discovery of a dinosaur was made at the locality in 1985. positional environments (Cook et al., 1998). In addi Another vertebrate fossil assemblage similar to those tion, weathering is also important in subaerial de recovered from Facies I and II of Kaseki-Kabe has been positional environments. reported from the Okurodani Formation of the Shokawa Some specimens from Facies III demonstrate that area in neighbouring Gifu Prefecture (Cook et al, 1998). scavenging and weathering played an important ta Depositional environments of the Okurodani Formation phonomic role at Kaseki-Kabe. Figure 3D shows an are similar to those of the Kuwajima Formation, suggest association of skeletal remains scattered on a narrow slab. ing horizons of Facies 111 sediments may be present at All of these elements are believed to pertain to one indi Shokawa, which have not yet been discovered. vidual of the lizard Sakurasaurus sp. (Evans and Finally, the co-occurrence of aquatic (Facies I and II) Manabe, 1999). All of the small bones are well preser and terrestrial (Facies III) vertebrate fossil assemblages at ved and do not appear to show any signs of abrasion or Kaseki-Kabe also suggests that different types of fossil weathering. In this case, scavenging by small animals, assemblages are generally present in the floodplain such as insects and worms, may have caused disarticula deposits, representing different habitats in the same small tion of the skeleton, as water transport was probably not region. Moreover, these findings remind us that we must an important factor in this swamp facies. In the case of look more carefully into the composition of oft-ignored other specimens (Figure 3E, F), however, subaerial weath "hidden" microvertebrate assemblages for a fuller under ering may be the most important factor. In these slabs, a standing of Early Cretaceous terrestrial biotas. few teeth are associated with heavily weathered small bone fragments. The teeth are also weathered, but have kept much of their original shape. This mode of occur ACKNOWLEDGMENTS rence suggests that a part of a jaw, including teeth, was We are grateful to the Shiramine Board of Education, slowly weathered, resulting in selective preservation of the Hakusan City, Ishikawa Prefecture for financial assistance 132 Shinji Isaji et al. and for their interest in this research. We wish to thank nal of Vertebrate Paleontology, 17 (Supplement to 3): 52-53A. K. Baba, S. Hayashi, N. Honda, Y. Kakegawa, C. Hirayama, R. 1999. Testudinoid turtles from the Early Cretaceous (Neocomian) of Central Japan. Abstracts of papers, 59'h Kawai, Y. Kitamura, Y. Kobayashi, S. Koike, C. Annual Meeting, Society of Vertebrate Paleontology, Journal of Matsui, R. Matsumoto, A. Matsushita, A. Obata, T. Vertebrate Paleontology, 19 (Supplement to 3): 51-52A. Oda, T. Ohashi, M. Okura, K. Shimizu, S. Shimojima, Hirayama, R. 2000. Fossil turtles. In, Matsuoka, H. ed.. Fossil of the Kuwajima "Kaseki-Kabe" (Fossil-bluff), Scientific report on K. Takahashi, J. Tokoro, S. Yamaguchi for their assis a Neocomian (Early Cretaceous) fossil assemblage from the tance in collecting the materials and preparation, and also Kuwajima Formation, Tetori Group, Shiramine, Ishikawa, to E. Cook, C. J. Nicholas, S. Sherlock for support Japan, p. 75-92, pis. 28-37. Shiramine Village Board of Educa tion, Ishikawa Prefecture, Japan, (in Japanese) during the fieldwork. We thank Makoto Manabe Hutchinson, G. E. 1957. A treatise on limnology: vol. I, Geography, (National Science Museum, Tokyo), Susan E. Evans physics, chemistry. John Wiley & Sons, New York. 1015pp. (University College London), Guillermo W. Rougier Isaji, S. 1993. Nippononaia ryosekiana (Bivalvia, Mollusca) from the (University of Louisville), Yoshitaka Yabumoto (Kita Tetori Group in Central Japan. Bulletin of the National Sci ence Museum, Series C, 19: 65-71. kyushu Museum of Natural History and Human History) Isaji, S. 1995. Defensive strategies against shell dissolution on and Michael Benton (University of Bristol) for helpful bivalves inhabiting acidic environments: The case of Geloina suggestions. This research was supported by the Grant- (Corbiculidae) in mangrove swamps. The Veliger, 38: 235-246. Ji, Q., Z. Luo and S.-A. Ji. 1999. Chinese triconodont mammal and in-Aid for Specially Promoted Research (awarded to MM: mosaic evolution of the mammalian skeleton. Nature, 398: grant no. 12800018) from the Japanese Ministry of Educa 326-330. tion and Science. Ji, Q., Z. Luo, C. Yuan, J. Wible, J. Zhang and J. Georgi. 2002. The earliest known eutherian mammal. Nature, 416: 816-822. Ji, Q., M. Norell, K. Gao, S.-A. Ji and D. Ren. 2001. The distribu tion of integumentary structures in a feathered dinosaur. Nature, REFERENCES 410: 1084-1088. Luo, Z. 1999. Refugium for relicts. Nature, 400: 23-25. Barrett, P. M., Y. Hasegawa, M. Manabe, S. Isaji and H. Maeda, S. 1961. On the geological history of the Mesozoic Tetori Matsuoka. 2002. Sauropod dinosaurs from the Lower Group in Japan. Japanese Journal of Geology and Geography. Cretaceous ofeastern Asia: taxonomic and biogeographical impli 32: 375-396. cations. Palaeontology, 45: 1197-1217. Manabe, M. and P. M. Barrett. 2000. Dinosaurs. In, Matsuoka, Cook, E., S. Isaji and M. Manabe. 1998. Preliminary results of a H. ed., Fossil of the Kuwajima "Kaseki-Kabe" (Fossil-bluff), taphonomic study of a vertebrate accumulation from the Tetori Scientific report on a Neocomian (Early Cretaceous) fossil Group (Lower Cretaceous) of Japan. Paleontological Research, assemblage from the Kuwajima Formation, Tetori Group, Shir 2: 47-52. amine, Ishikawa, Japan, p. 93-98, pis. 38-50. Shiramine Village Evans, S. E. and M. Manabe. 1999. Early Cretaceous lizards from Board of Education, Ishikawa Prefecture, Japan, (in Japanese) the Okurodani Formation of Japan. Geobios, 32: 889-899. Manabe, M., P. M. Barrett and S. Isaji. 2000. A refugium for Evans, S. E. and M. Manabe. 2000. Fossil lizards. In, Matsuoka, H. relicts? Nature, 404: 953. ed.. Fossil of the Kuwajima "Kaseki-Kabe" (Fossil-bluff), Manaue, M., Y. Hasegawa and Y. Azuma. 1989. Two new dinosaur Scientific report on a Neocomian (Early Cretaceous) fossil footprints from the Early Cretaceous Tetori Group of Japan. In, assemblage from the Kuwajima Formation, Tetori Group, Shir Gillette, D. and Lockley, M. G. eds., Dinosaur Tracks and amine, Ishikawa, Japan, p. 105-106, pis. 55-60. Shiramine Vil Traces, p. 309-312. Cambridge University Press, Cambridge. lage Board of Education, Ishikawa Prefecture, Japan, (in Masuda, F., M. Ito, M. Matsukawa, M. Yokokawa and Y. Makino. Japanese) 1991. Depositional environments. In Matsukawa, M. ed., Evans, S. E., M. Manabe, E. Cook, R. Hirayama, S. Isaji, C. J. Lower Cretaceous nonmarine and marine deposits in Tetori and Nicholas, D. Unwin and Y. Yabumoto. 1998. An Early Sanchu, Honshu, p. 11-17. IGCP-245 Field Trip Guide Book, Cretaceous tetrapod assemblage from Japan. Lower and middle 1991 Fukuoka International Symposium. Cretaceous terrestrial ecosystems: Filling the gap. New Mexico Matsukawa, M. 1983. Stratigraphy and sedimentary environments Museum of Natural History and Science Bulletin, 14: 183-186. of the Sanchu Cretaceous, Japan. Memoirs of the Ehime Gifu-Ken Dinosaur Research Committee, 1993: Report on the dino University, Natural Science, Series D (Earth Science), 9: 1-50. saur fossil excavation in Gifu Prefecture, Japan, 46pp. (in Matsukawa, M.. O. Takahashi, K. Hayashi, M. Ito and V. P. Japanese) Konovalov. 1997: Early Cretaceous paleogeography of Japan, Hasegawa, Y., M. Manabe, S. Isaji, M. Ohkura, I. Shibata and I. based on tectonic and faunal data. Memoirs of the Geological Yamaguchi. 1995. Terminally resorbed iguanodontid teeth from Society of Japan, 48: 29-42. the Neocomian Tetori Group, Ishikawa and Gifu Prefecture, Matsumoto, T., I. Obata, M. Tashiro, Y. Ohta, M. Tamura, M. Japan. Bulletin of the National Science Museum, Tokyo, Series Matsukawa and H. Tanaka. 1982. Correlation of marine and C, 21: 35-49. non-marine formations in the Cretaceous Japan. Fossils, 31: Hedges, S. B., P. H. Parker, C. G. Sibley and S. Kumar. 1996. 1-26. (in Japanese with English abstract) Continental breakup and the ordinal diversification of birds and Matsuoka, H. 2000. A frog fossil. In, Matsuoka, H. ed., Fossil of mammals. Nature, 381: 226-229. the Kuwajima "Kaseki-Kabe" (Fossil-bluff), Scientific report on Hirayama, R. 1996. Fossil land turtles from the Early Cretaceous of a Neocomian (Early Cretaceous) fossil assemblage from the Central Japan. Abstracts of papers, 56'* Annual Meeting, Kuwajima Formation, Tetori Group, Shiramine, Ishikawa. Society of Vertebrate Paleontology, Journal of Vertebrate Japan, p. 50-52. Shiramine Village Board of Education, Ishik Paleontology, 16 (Supplement to 3): 41A. awa Prefecture, Japan, (in Japanese) Hirayama, R. 1997. Paleobiogeography of Cretaceous land turtles Matsuoka, H. and T. Setoguchi. 2000. Significance of Chinese and the origin of "modern" cryptodires. Abstracts of papers, tritylodonts (Synapsida, Cynodontia) for the systematic study of 57th Annual Meeting, Society of Vertebrate Paleontology, Jour Bone-bearing beds of the Lower Cretaceous Kuwajima Formation 133

Japanese materials from the Lower Cretaceous Kuwajima Forma Umetsu, K. and A. Matsuoka. 2003. Early Cretaceous fossil spores tion, Tetori Group of Shiramine, Ishikawa, Japan. Asian Paleo- and pollen from the Tetori Group in the upper reaches of the primatology, 1: 161-176. Kuzuryu River, Fukui Prefecture, Central Japan. Journal of Ohashi, T., S. Isaji. I. Yamaguchi and Y. Kobayasiii. 2003. A new Geological Society of Japan, 109: 420-423. (in Japanese with ornithopod (Dinosauria) from the Early Cretaceous Kuwajima English abstract) Formation (Tetori Group) in central Japan. Abstracts with Unwin, D. M., 1999: Cretaceous fossil vertebrates. Preface. Special programs of the 152nd Regular Meeting of the Palaeontological Papers in Palaeontology, 60: 3-5. Society of Japan, p. 52. (in Japanese) Unwin, D. M. and H. Matsuoka. 2000. Pterosaurs and birds. In, Retallack, G. 1984. Completeness of the rock and fossil record: Matsuoka, H. ed., Fossil of the Kuwajima "Kaseki-Kabe" some estimates using fossil soils. Paleobiology, 10: 59-78. (Fossil-bluff), Scientific report on a Neocomian (Early Rougier, G. W., S. Isaji and M. Manabe. 1999. An Early Cretaceous Cretaceous) fossil assemblage from the Kuwajima Formation, Japanese triconodont and a revision of triconodont phytogeny. Tetori Group, Shiramine, Ishikawa, Japan, p. 99-104, pis. 51-54. Abstracts of papers, 59lh Annual Meeting, Society of Vertebrate Shiramine Village Board of Education, Ishikawa Prefecture, Paleontology, Journal of Vertebrate Paleontology. 19 (supple Japan, (in Japanese) ment to 3): 72A. Yabumoto, Y. 2000a. A revision of the genus Sinamia from the Sato. T., K. Hachiya and Y. Mizuno. 2003. Latest Jurassic-Early Tetori Group in Central Japan. Abstracts with Programs of the Cretaceous ammonites from the Tetori Group in Shokawa, Gifu 149th Regular Meeting of the Palaeontological Society of Prefecture. Bulletin of the Mizunami Fossil Museum, 30: 151- Japan, p. 37. (in Japanese) 167. (in Japanese with English abstract and systematic descrip Yabumoto, Y. 2000b. Pachycormid fish from the Early Cretaceous tions) Tetori Group in Shiramine, Ishikawa Prefecture, Japan. Setoguchi, T., H. Matsuoka and M. Matsuda. 1999. New discovery Abstracts with Programs of the 2000 Annual Meeting of the of an Early Cretaceous tritylodontid (Replilia. Therapsida) from Palaeontological Society of Japan, p. 77. (in Japanese) Japan and the phylogenetic reconstruction of Tritylodontidae Yabumoto, Y. 2000c. Fossil fishes. In, Matsuoka, H. ed., Fossil based on the dental characters. In, Wang. Y. and Deng. T. eds.. of the Kuwajima "Kaseki-Kabe" (Fossil-bluff), Scientificreport Proceedings of the Seventh Annual Meeting of the Chinese on a Neocomian (Early Cretaceous) fossil assemblage from the Society of Vertebrate Paleontology, p. 117-124. China Ocean Kuwajima Formation, Tetori Group, Shiramine, Ishikawa, Press, Beijing. Japan, p. 46-49, pis 14-15. Shiramine Village Board of Educa Takada, T.. H. Matsuoka and T. Setoguchi. 2001. The first tion, Ishikawa Prefecture, Japan, (in Japanese) multituberculate from Japan. In, Deng, T. and Wang, Y. eds., Yabumoto, Y. 2002. An Early Cretaceous osteoglossiform fish from Proceedings of the Eighth Annual Meeting of the Chinese Shiramine, Ishikawa, Japan with a comment on the origin of Society of Vertebrate Paleontology, p. 55-58. China Ocean Phareodontins. Abstracts with programs of the 2002 Annual Press, Beijing. Meeting of the Palaeontological Society of Japan, p. 60. (in Tashiro, M. and K. Okuhira. 1993. Occurrence of Trigonioides from Japanese) the Lower Cretaceous of Shikoku, and its significance. Geologi Zhou. Z.. P. M. Barrett and J. Hilton. 2003. An exceptional cal Report of Shimane University, 12: 1-9. (in Japanese with Lower Cretaceous ecosystem. Nature, 421: 807-814. English abstract) Zhou, Z. and F. Zhang. 2002. Jeholornis compared to Archaeop- Tsubamoto, T., G. W. Rougier, S. Isaji, M. Manabe and A. M. teryx, with a new understanding of the earliest avian evolution. Forasiepi. 2004. New Early Cretaceous spalacotheriid Naturwissenschaften, 90: 220-225. "symmetrodont" mammal from Japan. Acta Palaeontologica Polonica, 49: 329-346.