Eight specimens of Sphenodus have been collected from the Upper Cretaceous, Coniacian of Nakagawa Town in Hokkaido, northern Japan. They are referred to as S. cf. lundgreni and Sphenodus spp. 1 and 2, and described in detail. Nearly complete specimens of Sphenodus were previously unknown from the Cretaceous in the Pacific region, and the Nakagawa specimens are the first to exhibit distinct root morphologies, which allow comparison at the species level. A review of the occurrences of this genus reveals that their distribution concentrates in the mid- to high palaeolatitude regions. This distributional pattern of Sphenodus may represent its preference for colder water and possibly explains the extinction of this genus across the Paleocene—Eocene boundary, when the thermal maximum began.
Introduction
The Late Cretaceous saw various lineages of fish and tetrapods in marine environments prospers at a global scale (e.g. Underwood, 2006; Benson and Butler, 2011; Friedman and Sallan, 2012). The Neoselachii (Compagno, 1977) include modem sharks, rays and their close relatives and their rapid diversification during the Cretaceous has been documented in the fossil record (Underwood, 2006). For example, in the Smoky Hills Chalk, the famous Late Cretaceous Lagerstätte in Kansas, Shimada and Fielitsz (2006) recorded at least 10 neoselachian species. However, most fossil species of sharks are represented by teeth only due to their cartilaginous skeletons.
A large number of macroinvertebrates and reptilian fossils have been reported from the Upper Cretaceous of Nakagawa Town in Hokkaido, northern Japan (e.g. Nagao and Matsumoto, 1939; Matsumoto, 1943; Noda, 1983; Takahashi et al., 2003; Hirayama and Hikida, 1998, 2006; Ogawa and Nakaya, 1998; Mochizuki et al., 2006; Murakami et al., 2008), but scientific publications on its shark fossils are quite limited. To our knowledge, Research Group for Mesozoic Fossil Shark (1977) is the only publication on the shark fossils from the Upper Cretaceous in the town, but their geological setting in the studied area is hardly mentioned and the described specimens are mostly fragmentary. In fact, for the Upper Cretaceous of Hokkaido as a whole there are only a handful of publications concerned with selachians and a few known selachian taxa (e.g. Yabe, 1902; Tan, 1950; Uyeno, 1972; Kuga, 1985; Uyeno and Matsui, 1993; Tomita and Kurihara, 2011). Considering that various taxa are known from the Upper Cretaceous of other parts of the world (e.g. Cappetta, 1987; Welton and Farrish, 1993) and that Hokkaido is practically the only place in the northwestern Pacific where a continuous marine succession of the Upper Cretaceous with a well established biostratigraphic framework is available, the fossil shark fauna of Nakagawa Town deserves more intensive systematic study.
Our recent field work in Nakagawa Town revealed the presence of a rich fossil selachian fauna in the Upper Cretaceous. In this short contribution, we describe eight specimens referred to Sphenodus, an orthacodontid selachian genus. Occurrences of this genus have been reported from the Upper Cretaceous of Japan (Research Group for Mesozoic Fossil Sharks, 1977; Uyeno et al., 1981; Uyeno and Matsui, 1993; Kitamura, 1997), but the collection from Nakagawa is important because of its good preservation including the root. In addition, the Sphenodus specimens include ones not referable to any existing species of this genus. We also review the geographic and stratigraphic occurrences of the fossil record of the genus based on the literature.
Geological setting
The Sphenodus specimens came from the Nishichirashinai Formation exposed at a riverside cliff of the Abeshinai River in Nakagawa Town, Nakagawa County, Kamikawa Subprefecture, Hokkaido, Japan (44°38′24.0″N, 142°03′38.6″E, Figure 1). The Nishichirashinai Formation spans an interval from the Coniacian to the lower Santonian, and is characterised by well bioturbated greyish siltstone and sandy siltstone (Takahashi et al., 2003; Takahashi et al., 2007).
At the Abeshinai locality, the outcrop is mainly composed of dark grey silt and is approximately 10 m high. In the lower part of the outcrop, a lens (approximately 0.5 m thick and 9 m wide) of matrix-supported, poorly sorted pebble conglomerate is inserted and the shark fossils were recovered therein. The upper margin of the lens is nearly flat whereas the lower margin is wavy. Within this conglomerate lens, rip-up clasts are abundant and many pebbles are rounded. Associated fossils are also found from this conglomerate, including the ammonite Gaudryceras denseplicatum, bivalves Nanonavis, Glycymeris and Acila, ichthyoliths and plant remains, as well as fragments of solidified trace fossils. The lithological characteristics of the conglomerate lens suggest that it is composed of channel-fill sediment (Takahashi et al., 2007). The shark fossils from the conglomerate are dated as Coniacian based on the age of the Nishichirashinai Formation determined by Takahashi et al. (2003) and on the occurrence of G. denseplicatum.
Material and methods
Of the eight shark teeth described here, five were collected in August, 2005 by one of us (YN), and the rest during our fieldwork at the same locality in September, 2014. All specimens are housed in Nakagawa Museum of Natural History of Nakagawa Town.
All shark teeth were prepared physically with air scribers and an air grinder and their images were processed with Adobe Photoshop and Adobe Illustrator. Close-up photos were taken with a Leica DFC290 HD microscope using Leica Application Suite V3.1.0. Descriptive tooth terminology largely follows that of Cappetta (1987).
Institutional Abbreviations.—KCM, Kumamoto City Museum, Kumamoto, Japan; NJSM, New Jersey State Museum, Trenton, NJ, USA; NMV, Nakagawa Museum of Natural History, Hokkaido, Japan.
Systematic palaeontology
Class Chondrichthyes Huxley, 1880
Subclass Elasmobranchii Bonaparte, 1838
Cohort Euselachii Hay, 1902
Subcohort Neoselachii Compagno, 1977
Order Synechodontiformes Duffin and Ward, 1993
Family Orthacodontidae Glükman, 1957
Genus Sphenodus Agassiz, 1843
Type species.—Sphenodus longidens Agassiz, 1843.
Remarks.—The phylogenetic relationships of Sphenodus to other sharks have been debated (e.g. Woodward, 1889; Herman, 1977; Cappetta, 1987; Duffin and Ward, 1993; Maisey et al., 2004), but Klug (2010) demonstrated the monophyly of the order Synechodontiformes, and Sphenodus belongs to this order. The present study follows her view.
Classification within this genus, especially that of the Cretaceous species, has been controversial; Duffin and Ward (1993) listed 29 species in this genus, several of which have later been regarded as synonymous and/or dubious (see Kriwet et al., 2006; Adolfssen and Ward, 2014). There are three species known from the Jurassic, Sphenodus macer (Quenstedt, 1851), S. nitidus Wagner, 1862 and S. longidens Agassiz, 1843 (Böttcher and Duffin, 2000), whereas S. lundgreni (Davis, 1890) is the only species from the Cretaceous recognised as valid (Adolfssen and Ward, 2014). The differences among the species described here and the four species known from the Jurassic and the Cretaceous are summarised in Table 1 based on Böttcher and Duffin, (2000), Kriwet et al. (2006), Rees (2010), and Adolfssen and Ward (2014).
Table 1.
Distinguishing characters of Sphenodus. “1”, “0”, and “?” indicate presence, absence, and unknown state of the character, respectively. Parentheses refer to the features in the separate cusp in NMV 86 (see text). Data compiled from Böttcher and Duffin (2000), Kriwet et al. (2006), Rees (2010) and Adolfssen and Ward (2014).
Sphenodus cf. lundgreni
Figure 2A–C
Material.—NMV 86 (cusp and root) and NMV 87 (root missing much of the cusp)
Description.—NMV 86 consists of a cusp and a root not connected but found together in a small block. Their broken surfaces do not match exactly and the slight size discrepancy suggests that they might actually represent two separate teeth. NMV 87 retains the base of the cusp.
The root is flat and short mesiodistally. The exact height/width ratio of the tooth is not available, because the middle part that connects the root and the cusp is missing in NMV 86; the ratio of the broken cusp height to the width of the root is 1.3. Numerous short ridges are present on the lower part of the labial and lingual surfaces of the root and the upper surface of the labial face. The root is elliptical and there are five grooves running labiolingually on the basal surface. Pores on the root are rare.
The cusp of NMV 86 is slender and inclined lingually, but not sigmoidal. The labial face is nearly flat and the lingual face is convex. Both faces are smooth but several short folds are present on the base of the labial surface. The cutting edges are quite sharp, but they are barely traced on the root.
Remarks.—The roots of NMV 86 and NMV 87 are similar to Sphenodus lundgreni in several points: the root is ornamented with numerous grooves; strong short folds are present on the lower part of the lingual face of the crown. However, there is no guarantee that the cusp of NMV 86 belongs to the root or even to the same individual, and the morphology of the cusp in these Nakagawa specimens cannot be confirmed. Therefore they are identified as Sphenodus cf. lundgreni.
Figure 2.
Sphenodus from the Coniacian in Nakagawa Town, Hokkaido. A, labial view; B, lingual view; C, basal view of the cusp and root of Sphenodus cf. lundgreni (NMV 86); D, labial view; E, lingual view; F, lateral view; G, top view of Sphenodus sp.1 (NMV 88); H, labial view; I, lingual view; J, top view (NMV 90); K, labial ;view; L, lingual view M, basal view of Sphenodus sp.2 (NMV 91). Scale = 10 mm.
Sphenodus sp. 1
Figure 2D–G
Material.—Two complete teeth (NMV 88, 89).
Description.—In both teeth, the cusp and a nonbilobed root that extends horizontally are present. The cusp is slightly sigmoidal from side view and considerably slender. The lingual face is convex and the labial face is slightly so. Both faces are nearly smooth, although many vertical folds are present at the base of the cusp; these folds are very short but pronounced. The cutting edges are well developed and extend to the upper part of the root. The root is elongatedly oval in apical view and apicobasally flattened considerably and the apical surface gradually slants toward the edge. The height/width ratio of the tooth is 0.81 (NMV 88) and 0.86 (NMV 89). The surface of the root is rough; there are many short grooves that extend from the centre toward the edge and several pores on the upper surface of the root.
Remarks.—Sphenodus sp. 1 is distinguished from all of the previously known species of Sphenodus, because the quite small ratio of height/width of the tooth and the ornamentation of the root are so characteristic. The roots of NMV 88 and NMV 89 are similar to the specimens RT-6 and KCM 12-000359 of Kitamura (2014), but both of Kitamura's specimens do not bear complete crowns. The specimen identified as S. lundgreni in Callahan et al. (2014: NJSM GP 23223) could be conspecific with S. sp. 1 in this study, yet more detailed information on its characteristics is required for precise comparison.
Sphenodus sp. 2
Figure 2H–M
Material.—Four incomplete teeth (NMV 90, NMV91, NMV 92, NMV 93).
Description.—The cusp is long and relatively stout, and the labial and lingual faces are equally rounded. The cutting edges are moderately developed and they continue to the upper part of the root but gradually become weak. The crown face is quite smooth and weak folds are present on the base of the cusp only in NMV 93. The cusp inclines lingually, and is sigmoidal in profile in NMV 91. The root is relatively narrow, trapezoidal and moderately flat and expands lingually. The edge of the root bulges slightly. On the root surface, numerous pores are present, particularly on the distal edges. On the lingual surface of the neck on the root, where the root meets the cusp, and on the edge of the root, there are numerous short ridges running apico-basally. The height/width ratio of the tooth is 1.56 in NMV 90.
Remarks.—Sphenodus sp. 2 is separated from known species including Sphenodus sp. 1 by several characters: the more rounded robust crown on both sides; the weakness of the cutting edges on the upper surface; the bulge of the root edges; numerous pores on the root surface; the narrow root compared to the tooth height. NMV 91 is similar to Sphenodus sp. 1 in the shape of the sigmoidal crown, but based on the characters of the remaining part of the root, NMV 91 is referred to as Sphenodus sp. 2.
Discussion
Significance of the Sphenodus specimens from Nakagawa.—Most Cretaceous specimens referred to this genus lack the root (e.g. Agassiz, 1843; Davis, 1890; Research Group for Mesozoic Fossil Shark, 1977; Uyeno et al., 1981; Uyeno and Matsui, 1993; Kriwet et al., 2006), so their identification at species level has been questioned. The nearly complete specimens in this study, NMV 88 and NMV 89, in which both the root and the crown are preserved, are quite rare and they are important to confirm the taxonomic identification of Sphenodus, in particular, this genus from the Cretaceous.
Shark teeth exhibit heterodonty, which is a variation of the tooth of the individual in terms of size or shape, depending on the position of the tooth in a mouth, age, or sex of an individual (Capetta, 1987). For instance, the difference in the height/width ratio of the tooth might be caused by the difference of position within the mouth and does not necessarily indicate a taxonomic difference.
In the well preserved specimen of Sphenodus macer described by Böttcher and Ward (2000), which is the only Sphenodus specimen in which heterodonty was actually demonstrated, the width of the tooth decreases distally in general (see their fig. 9). The height/width ratios in the Nakagawa specimens identified as Sphenodus spp. 1 and 2 are similar to those of S. macer, but the morphological distinctness of the Nakagawa specimens is hardly explained by the known range of morphological variations of the latter species. Therefore, S. cf. lundgreni and Sphenodus spp. 1 and 2 likely belong to different biological species from each other. However, considering that the range of heterodonty remains unknown for any Cretaceous Sphenodus species due to the lack of specimens, it is also still possible that these three tooth-based species from Nakagawa belong to only one or two biological species.
Table 2.
Geographic and stratigraphic distribution of genus Sphenodus (Neoselachii: Orthacodontidae). Parentheses refer to the features in the separate cusp in NMV 86 (see text). RGMFS stands for Research Group for Mesozoic Fossil Shark.
Palaeobiogeography.—Although well preserved spec- tries and regions, such as Europe, Antarctica, Angola, imens are rare, remains of Sphenodus have been found Tanzania, New Zealand and Japan (Figure 3, Table 2). from the Lower Jurassic to the Paleocene of several coun- During the Jurassic and the Early Cretaceous, this genus was common in Europe, especially in Germany where a partial skeleton of S. nitidus and a complete articulated specimen of S. macer were found (Wagner, 1862; Böttcher and Ward, 2000). Sphenodus survived the K/Pg mass extinction, although their fossil record is quite limited and patchy in the Paleocene.
Figure 3.
Palaeobiogeographic distribution of Sphenodus fossils. A, Jurassic to Early Cretaceous; B, Late Cretaceous; C, early Cenozoic. Refer to Table 2 for information on each occurrence indicated by arabic numerals. Palaeogeographic map modified from Scotese (1999).
The known occurrences of this genus are limited to the regions located at palaeolatitudes higher than 30° (Figure 3). We are not aware of published palaeolatitude estimations for the Coniacian in Nakagawa, but palaeomagnetic studies of nearby areas suggest a mid-latitude location; Tamaki and Itoh (2008) demonstrated that the Oyubari area in central Hokkaido was located near Sikhote Alin in eastern Russia around the present latitude (ca. 45°N) in the Cenomanian-Turonian, whereas the Upper Cretaceous sequence in Naiba, South Sakhalin is considered to have been placed at 36.6°N (Cenomanian) to 40.8°N (Campanian to Maastrichtian) (Kodama et al., 2000; Abrajevitch et al., 2012). Meanwhile, there are many low-latitude localities such as Jamaica, Chile, Senegal and Israel where various selachian taxa have been reported but not Sphenodus (e.g. Underwood and Mitchell, 2000; López-Arbarello et al., 2008; Cuny et al., 2012; Otero et al., 2013; Retzler et al., 2013). Sphenodus may have preferred mid- to highlatitude environments. Water temperature increased rapidly and reached the maximum during the late Paleocene to the Eocene, especially in high-latitude region (Zachos et al., 1994, 2003). The extinction of Sphenodus during the Paleogene could be related to this climate change amplified at high-latitude regions.
Acknowledgements
We thank Shoji Hayashi of Osaka Museum of Natural History for assisting our fieldwork, also Taketeru Tomita of Okinawa Churashima Research Center and Ryoko Matsumoto, Hiroshi Senou, Hajime Taru, and Mitsuharu Oshima of Kanagawa Prefectural Museum of Natural History for advice on shark taxonomy and access to the comparative modem specimens under their care. Review comments from Yoshitaka Yabumoto and Diogo Mayrinck were helpful to improve the manuscript. This research was financially supported by Nakagawa Town, Tokyo Gakugei University, JSPS KAKENHI Grant Number 15K05327 to T.S.) and JSPS Postdoctoral Fellowships for Research Abroad (programme no. 25.498 to Y.N.).
