Introduction

Paleoecological studies of Upper Cretaceous shark fauna have been based on the many fossil shark teeth deposited in tropical and warm temperate shallow-marine environments including the Western Interior Sea (e.g. Shimada et al., 2006), Europe (e.g. Vullo et al., 2007), the Middle East area (e.g. Davis, 1887), North Africa (e.g. Rage and Cappetta, 2002), Australia (e.g. Siverson, 1996), and Antarctica (e.g. Kriwet et al., 2006). Regionally, studies of the Upper Cretaceous shark fauna have concentrated on the Western Interior Sea, Europe, and Australia, and in geological terms the origin of these faunas was the late Early Cretaceous to early Late Cretaceous periods (Albian to Turonian: Siverson, 1996, 1997; Cumbaa et al., 2010), and the remainder of the Late Cretaceous (Campanian to Maastrichtian: Siverson, 1992; Case and Cappetta, 1997; Beavan and Russell, 1999). However, reports of shark faunas from the Santonian are rare, particularly from the North Pacific region, leaving this fauna less well understood. Records of Cretaceous fossil shark teeth from Japan (northwestern Pacific region) have been sporadic, and restricted mainly to descriptions of specimens. Consequently, there is insufficient information to assess the taxonomic composition and paleoecological significance of the Cretaceous shark fauna from Japan and worldwide. In the present study, the Japanese Cretaceous shark fauna was investigated, primarily using shark teeth from the Hinoshima Formation (Santonian Age), and features of the Upper Cretaceous shark fauna in the western Pacific Ocean (mid-latitudes in the Northern Hemisphere) were studied.

Stratigraphy and age of the Himenoura Group

The Hinoshima Formation belongs to the Upper Cretaceous Himenoura Group (named by Nagao, 1930) and is distributed primarily from the Uto Peninsula to the east coast of Amakusa Kamishima Island, and south of Amakusa Shimoshima in Kumamoto Prefecture and Koshikishima Islands in Kagoshima Prefecture, Japan. Tashiro and Noda (1973) separated the Himenoura Group into the Lower Himenoura Subgroup (Santonian to lower Campanian) and the Upper Himenoura Subgroup (Campanian to Maastrichtian), and separated the Lower Himenoura Subgroup, which is distributed on the east coast of Amakusa Kamishima Island, into the Hinoshima Formation (mainly Santonian Stage) and the Amura Formation (mainly Campanian Stage). They also subdivided the Hinoshima Formation into the lower, middle, and upper members, and the Amura Formation into the lower and upper members (Tashiro et al., 1986). Kojo et al. (2011) stated that the Upper and Lower Himenoura subgroups were deposited in almost the same period, and also revised the stratigraphic division of the Himenoura Group. The present study follows the framework of Kojo et al. (2011). The Himenoura Group, which is distributed on Amakusa Kamishima and Goshoura islands, unconformably overlies the Higo metamorphic rocks on Amakusa Kamishima Island, and is unconformably overlain by the Paleogene Miroku Group (e.g. Komatsu et al., 2009; Kojo et al., 2011). Studies of the depositional environmental of the Himenoura Group on Kamiamakusa Island (Tashiro et al., 1986; Fujino, 2003; Sato et al., 2005) indicate a rapid transgression and a transition to a deep-sea setting. Numerous paleontological studies of mollusks in the Himenoura Group have been reported (e.g. Kobayashi and Amano, 1955; Amano, 1956; Tashiro, 1971, 1972, 1976). This study follows Kojo et al. (2011) with respect to the geological age of the Hinoshima Formation of the Himenoura Group, which is assigned to the Santonian based on the presence of Inoceramus amakusensis. Previous studies have reported on (e.g. Kitamura et al., 1995; Kitamura, 1997; Goto and the Japanese Club for Fossil Shark Tooth Research, 2004; Kitamura, 2013) and reviewed (Yabumoto and Uyeno, 1994; Goto et al., 1996; Kitamura, 2008) the fossil shark teeth in the Himenoura Group.

Material and methods

Fossil shark teeth (168 specimens) were collected from outcrops and float rocks near outcrops at five localities in Kamiamakusa City (Kumamoto, Japan): Himedo Park (64 specimens), Kugushima (38 specimens), Wadanohana (63 specimens), Higashiura (two specimens), and Kotorigoe (one specimen) (Table 1, Appendix 1). Some of these specimens had been studied by Kitamura et al. (1995) and Kitamura (1997, 2013), but private collections were excluded. The specimens are held in the Kumamoto City Museum (KCM) and the Goshoura Cretaceous Museum (GCM). The classification of specimens followed Cappetta (2012).

Shark teeth horizons and sedimentary facies of the Upper Cretaceous in the Hinoshima Formation

Himedo Park.—The lower part of the Hinoshima Formation is exposed at Himedo Park (Figure 1), and three fossil layers are evident: a bottom fine sandstone bed (105 cm thick) containing bivalves (Nippononectes tamurai tamurai, N. t. immodesta, and oyster fragments), a medium–coarse sand bed (80 cm thick) containing an abundance of fossil shark teeth, and an upper fine sand bed (280 cm thick) containing ammonoids (Polyptychoceras sp. and Protexanites sp.). All the shark teeth in the coarse sand bed layer are small. The bivalves in the fine sandstone bed layer include articulated shells and oyster (Crassostrea sp.) fragments. Hummocky cross-stratified (HCS) sandstone beds occur in the southern part of Himedo Park (Figure 1).

Kugushima.—At Kugushima Island the two main beds that contain fossil shark teeth belong to the lower part of the Hinoshima Formation (Figure 1). The first of these (horizon a) is a black shale layer (70 cm thick) located 132–133 m above the boundary between the lower part of the Hinoshima Formation and the basal Higo metamorphic rocks. The fossil shark teeth are associated with bivalves including Fenestricardita ezonuculana, Glycymeris (Glycymeris) amakusensis, Apiotrigonia sp., and Inoceramus sp., and are scattered irregularly throughout the beds. The second bed (horizon b) is a fine sandstone layer (1 m thick) located 167–168 m above the boundary. The fossil shark teeth in this layer are associated with bivalves including G. (G.) amakusensis. Fossil shark teeth were also evident in three other horizons: a mudstone layer immediately below horizon a; a mudstone layer approximately 4 m above horizon a; and a sandstone bed layer containing gravel and Apiotrigonia minor and G. (G.) amakusensis, located ∼4 m above horizon b. Fossil shark teeth were also obtained from float stones of mudstone to fine sandstone, which also contained G. (G.) amakusensis.

Wadanohana.—The shark teeth beds of Wadanohana belong to the lower part of the Hinoshima Formation. Many fossil shark teeth were obtained from the black shale layer (50 cm thick) located 38.5–38 m below the boundary between the lower and middle parts of the Hinoshima Formation (Figure 1). Here the fossil shark teeth are associated with bivalves including Nucula (Nucula) amanoi, Acila (Truncacila) hokkaidoensis, and Ezonuculana mactraeformis mactraeformis. Gastropods (Buscyconidae) and ammonoids (Eupachydiscus haradai, Eupachydiscus sp., and Polyptychoceras sp.) are also present (Kitamura et al., 1995; Kitamura, 1997, 2008, 2013).

Table 1.

The Hinoshima Formation fossil shark teeth: taxa and number of specimens. Him, Himedo Park; Kug, Kugushima; Wad, Wadanohana; Hig, Higashiura; Kot, Kotorigoe.

Higashiura.—The Higashiura region ranges from the head of Cape Matsugahana to southern Ryugatake, and consists of the Higo metamorphic rocks and the lower and middle parts of the Hinoshima Formation. The lower part is composed of fine sandstone overlying the basement Higo metamorphic rocks, and is conformably overlain by the middle part, which is composed of black mudstone (> 100 m thick; Figure 1) containing ammonoids (Polyptychoceras sp., Gaudryceras sp., and Eupachydiscus sp. in nodules) and bivalves including Inoceramus (Inoceramus) amakusensis and Parvamussium yubarense. The sedimentary structures of the lower part are indeterminable. Fossil shark teeth have been obtained from 30 cm below a fossiliferous horizon (∼20 cm thick) in the middle part of this mudstone layer (Figure 1), where they are associated with the disarticulated bivalve Acila (Truncacila) sp. (Kitamura, 2008) (Table 1). The mudstone of the shark teeth horizon does not contain slump debris, but adult ammonoids and inoceramids are present in the horizons above and below.

Figure 1.

Study area (localities) and comparison of columnar sections containing horizons with fossil shark teeth.

Kotorigoe.—The shark teeth bed of Kotorigoe belongs to the middle part of the Hinoshima Formation and is composed of black mudstone (Figure 1). This mudstone has yielded fossil shark teeth and the ammonoid Gaudryceras sp. (Kitamura et al., 1995).

Features and paleoecological significance of the shark fauna from the Upper Cretaceous Himenoura Group of the Hinoshima Formation

Himedo Park.—Crassostrea sp. is known to inhabit tidal flats (Kumagae and Komatsu, 2004), and the presence of HCS indicates a shallow water (shoreface) depositional environment (Saito, 1989). These factors indicate the presence of a coastal shallow-water environment and the para-autochthonous occurrence of bivalves. Similar findings have been reported by Komatsu et al. (2008). The depositional environment of Himedo Park suggests a distributary channel and sand bar developed on a delta at the head of a bay. The coarse sand bed containing many shark teeth is considered to have formed the sand body at the bay mouth (Komatsu et al., 2008, 2009), as inferred from features including a coarse sand bed, HCS sandstone beds, and the presence of brackish water bivalves (Crassostrea sp.) and marine bivalves (e.g. Nippononectes tamurai). The fossil shark taxa include Notorynchus sp., Ptychodus mammillaris, and Cretalamna appendiculata, which appear to have inhabited the waters of inner coastal bays. The presence of highly worn fossil shark teeth (C. appendiculata), teeth having cusps, and the roots of shark teeth suggests deposition in fast-moving currents. This active circulation of marine water is thought to have resulted from the effects of the transgression (Komatsu et al., 2008).

Kugushima.—The presence of fossil shark teeth in horizon a is thought to be an autochthonous occurrence because sedimentary structures and gravels are not visible in the massive mudstone layer (Komatsu et al., 2008), which is intensively bioturbated. In contrast, the fossil shark teeth in horizon b are thought to be a result of gravity flow, perhaps a submarine debris flow, because the fine sandstone contains sandstone gravels, indicating an allochthonous occurrence. Horizon a contains shallow-water bivalves including Apiotrigonia minor, Ezonuculana mactraeformis mactraeformis, and Glycymeris (Glycymeris) amakusensis, while horizon b also contains G. (G.) amakusensis and non-articulated shells. As noted above, horizon a contains teeth of a number of shark species thought to have inhabited the bottom and surface layers offshore, while horizon b contains teeth of shark species thought to have inhabited shallow to offshore waters. These fossil shark teeth are better preserved than those from Himedo Park.

Wadanohana.—Fossil shark teeth were also obtained from a black massive mudstone bed containing slump debris and many bivalves. This bed is thought to have been formed by a gravity flow (i.e., a submarine debris flow) because the presence of mudstone containing bivalves, and non-articulated and irregularly scattered shells, indicates an allochthonous occurrence. The bivalves comprise shallow-water taxa including Apiotrigonia minor, Ezonuculana mactraeformis mactraeformis, Glycymeris (Glycymeris) amakusensis, and Eriphyla sp., as well as deep-water taxa including Nucula (Nucula) amanoi, Nanonavis sachalinensis, Myrtea (Myrtea) ezoensis, and Thayasira (Thayasira) himedoensis (Tashiro et al., 1986; Aberhan, 1994; Tashiro, 1994). This bed also contains offshore taxa including E. mactraeformis mactraeformis and G. (G.) amakusensis, and continental shelf taxa including Inoceramus sp. and Nanonavis sachalinensis (Kumagae and Komatsu, 2004). This assemblage indicates that shallow and continental shelf bivalves were deposited together in the deep sea by a submarine debris flow. It is thought that teeth from shallow-water to offshore shark species were also deposited there. These teeth are better preserved than those from Himedo Park. For example, multicuspid teeth (such as those from Hexanchus) and labio-lingually compressed teeth (such as those from Echinorhinus) are well preserved, indicating a shorter transport distance than the teeth at Himedo Park.

Higashiura.—Fossil shark teeth were obtained from < 30 cm below a fossiliferous horizon (∼20 cm thick) in the middle part of this mudstone layer (Figure 1). The fossil shark taxa detected were Chlamydoselachus sp. B and Hexanchidae gen. et sp. indet., associated with the disarticulated bivalve Acila (Truncacila) sp. The mudstone of the shark teeth horizon does not contain slump debris, but adult ammonoids and inoceramids are present in the horizons above and below. This indicates that the depositional facies were deeper-water than those of Kugushima or Wadanohana, and indicate an autochthonous occurrence.

Kotorigoe.—The mudstone yielded one fossil shark taxon (Squalicorax sp.) and ammonoids (Gaudryceras sp.). The depositional facies, which are similar to those of Higashiura, are thought to have been deeper than those of Kugushima or Wadanohana, and indicate an autochthonous occurrence.

Composition of the shark fauna from the Hinoshima Formation

The shark fauna from the Hinoshima Formation consists of 23 species, 15 genera, 11 families, and six orders (Table 1). In order of abundance the taxa include Lamniformes and Hexanchiformes (nine species), each comprising 39%; Hybodontiformes (two species: 9%); and Echinorhiniformes, Squaliformes, and Synechodontiformes (single species: each 4%). The number of specimens collected from the Hinoshima Formation included 129 Lamniformes, among which Cretalamna appendiculata (Cretoxyrhinidae) was the dominant species (116); 22 Hexanchiformes; seven Hybodontiformes; five Echinorhiniformes; two Squaliformes; and three Synechodontiformes. The Lamniformes included five families, six genera, and nine species (Figures 2–5). The teeth designated KCM 12-000378 and KCM 12-000272 were identified as Notorynchus sp. based on the following criteria. Cretaceous specimens of Notorynchus have been described as Notorynchus aptiensis (Pictet, 1865) or indeterminate species (Underwood et al., 2011; Cappetta, 2012). Underwood et al. (2011) erected the genus Gladioserratus based on Early and “Middle” Cretaceous specimens (including N. aptiensis), which were distinguished from Notorynchus. Notorynchus specimens (lower jaw teeth) obtained from the Hinoshima Formation (KCM 12-000378, Figure 3-22; KCM 12-000272, Figure 3-23) are distinguished from congeners of the genus Gladioserratus by having a rectangular root profile, gracile cusps, and a gradual increase in the size of the serrations on the mesial edge of the teeth.

The habitats of sharks from the Hinoshima Formation

Morphology and locomotion of sharks

Wilga and Lauder (2004) classified extant sharks in terms of four body types and four modes of locomotion (anguilliform, subcarangiform, carangiform, and thunniform) ranging from the slowest to the fastest swimming speeds. The swimming abilities of the sharks from the Hinoshima Formation were categorized based on the locomotion types described above. The genera Chlamydoselachus and Echinorhinus are comparable to anguilliform sharks (slim, with eel-like movement and generally body type 4). The genera Paranomotodon, Hexanchus, Notorynchus, and Notidanodon are comparable to subcarangiform sharks (faster than anguilliform). Paranomotodon is considered to have had body type 2, and the others body type 3. The genera Centrophoroides and Cretascymnus were carangiform (undulating movement is limited to the back half of the body). The genera Squalicorax, Dwardius, Cretodus, Cretalamna, Protolamna, and Mitsukurinidae gen. et sp. indet. are comparable to thunniform sharks (rapid undulation of the tail or tail lobes), and generally had body type 1.

Figure 2.

Proportion and total number of fossil shark tooth specimens from the Hinoshima Formation.

Behavior and habitat of shark groups

Hybodontiformes.—Members of the genus Ptychodus (Agassiz, 1835) are thought to have been sluggish swimmers using suction feeding, similar to that of extant Orectolobiformes (Shimada et al., 2009; Shimada, 2012). Its crushing type dentition is thought to have enabled Ptychodus to crush inoceramids and ammonoids (Niedźwiedzki and Kalina, 2003; Shimada, 2012).

Hexanchiformes.—Extant Hexanchiformes Buen, 1926 include Chlamydoselachidae and Hexanchidae, which live mainly in deep water and occur worldwide (Compagno, 1984). Chlamydoselachidae are primitive fish similar to the Paleozoic Symmorium. Extant species of Chlamydoselachidae live mainly in the deep sea around Japan, and their occurrence extends from the upper Turonian to the Coniacian (Goto and the Japanese Club for Fossil Shark Tooth Research, 2004). The chlamydoselachids from the Hinoshima Formation are divided into two classes: (i) Chlamydoselachus sp. A (Figure 3-8, “Chlamydoselachus sp. 3” in Goto and the Japanese Club for Fossil Shark Tooth Research, 2004), almost three times larger than the extant species C. anguineus and C. africana, and (ii) Chlamydoselachus sp. B (Figure 3-9), which is almost 1.5 times larger than the extant species. It is thought that members of the genus Chlamydoselachus lived in shallow waters during the Mesozoic and early Cenozoic, because of the associated presence of fossil inoceramids and ammonoids, and later moved to deep water (Richter and Ward, 1990; Goto and the Japanese Club for Fossil Shark Tooth Research, 2004). Hexanchid sharks from the Hinoshima Formation include Hexanchus microdon, Hexanchus sp., Notorynchus sp., and the extinct cow shark Notidanodon dentatus. Although extant Notorynchus cepedianus inhabit shallow water, most of the extant Hexanchidae species are deep-water inhabitants (Compagno, 1984). Sphenodus sp. (Orthacodontidae) from the Hinoshima Formation is thought to have been an active offshore predator (Rees, 2012).

Echinorhiniformes.—Cappetta (2012) removed the Family Echinorhinidae (including the genus Echinorhinus) from the Squaliformes of Compagno (1984). The extant genus Echinorhinus is a sluggish swimming predator inhabiting continental shelves and slopes in deep water (Compagno, 1984).

Squaliformes.—Squaliformes (dogfish sharks) include 130 species in seven families, and mainly inhabit deep waters (Compagno, 1984). Extant squaliforms are diverse and globally distributed, mainly inhabiting deep water from the Arctic to the Antarctic (Compagno, 1984). Studies of foraminifera in Sweden indicate that the squaliform sharks inhabited shallow water in the Late Cretaceous (Siverson, 1993; Siverson and Cappetta, 2001). Klug and Kriwet (2010) suggested that deep sea adaptations in Squaliformes developed in the early Late Cretaceous, based on the construction, dating, and analysis of a genus-level phylogeny of extinct and living dogfish sharks.

Lamniformes.—Based on their skeletons, it is thought that the genera Squalicorax, Paranomotodon, Cretodus, and most of the Mitsukurinidae sharks were fast swimmers and the top offshore predators on the continental shelf (Kriwet and Benton, 2004; Tomita and Kurihara, 2011). Furthermore, Cretalamna appendiculata, which is a dominant species in the Hinoshima Formation, is thought to be similar to the extant genus Lamna in terms of the size and morphology of the jaw and teeth (see Shimada, 2007). The genus Squalicorax has teeth similar in form to the extant Galeocerdo cuvier and is thought to have been an offshore shark (Antunes and Cappetta, 2002). It is thought that Cretodus semiplicatus inhabited shallow water, as fossil remains were found in shallow-water facies of the Mikasa Formation in Hokkaido (Tomita and Kurihara, 2011).

Synechodontiformes.—The genus Synechodus is thought to have been a sluggish benthic shark, as the dentition is similar to that of extant scyliorhinids (Compagno et al., 2005; Klug, 2009).

Figure 3.

Shark fossils from the Hinoshima Formation. 1–6, Ptychodus mammillaris; 1, KCM12-000061 (Himedo Park); 2, KCM12000148 (replica, Kugushima); 3, KCM12-000149 (replica, Kugushima); 4, KCM12-00060 (Wadanohana); 5, KCM12-000144 (replica, Wadanohana); 6, KCM12-000257 (Wadanohana); 7, Ptychodus sp., KCM12-000150 (Kugushima); 8, Chlamydoselachus sp. A, GCM-VP400 (Kugushima); 9, Chlamydoselachus sp. B, KCM12-000360 (Higashiura); 10–14, Hexanchus microdon; 10, KCM 12-000039 (Wadanohana); 11, KCM 12-000042 (Wadanohana); 12, KCM 12-000044 (Wadanohana); 13, KCM 12-000263 (Wadanohana); 14, GCM-VP401 (Wadanohana); 15, 16, Hexanchus sp.; 15, KCM 12-000346 (Kugushima); 16, KCM 12-000040 (Wadanohana); 17–21, Hexanchidae gen. et sp. indet.; 17, KCM 12-000413 (Kugushima); 18, GCM-VP402 (Kugushima); 19, KCM 12-000043 (Wadanohana); 20, GCM-VP403 (Kugushima); 21, GCM-VP407 (Higashiura); 22, 23, Notorynchus sp.; 22, KCM 12-000378 (Himedo Park); 23, KCM 12-000272 (Kugushima); 24, Notidanodon dentatus; KCM 12-000365 (Wadanohana); 25–27, Notidanodon sp.; 25, GCM-VP404 (Wadanohana); 26, GCM-VP405 (replica, Wadanohana); 27, GCM-VP406 (Wadanohana); 28, 29, Sphenodus sp.; 28, GCM-VP411 (Kugushima); 29, KCM 12-000359 (Wadanohana); 30–34, Echinorhinus wadanohanaensis; 30, KCM 12-000429 (Kugushima); 31, KCM12-000064 (Wadanohana); 32, KCM 12-000266 (Wadanohana); 33, KCM12-000267 (Wadanohana); 34, KCM12-000362 (Wadanohana); 35, 36, Centrophoroides cf. latidens; 35, KCM12-000361 (Kugushima); 36, KCM12-000419 (Kugushima). 37, Mistukurinidae gen. et sp. indet.; KCM 12-000424 (Kugushima). 38–57, Cretalamna appendiculata (Himedo Park); 38, lateral tooth (KCM 12-000031); 39, lateral tooth (KCM 12-000032); 40, anterior tooth (KCM12- 000033); 41, anterior tooth (KCM 12-000034); 42, KCM 12-000035; 43, lateral tooth (KCM 12-000036); 44, lateral tooth (KCM 12-000045); 45, lateral tooth (KCM 12-000153); 46, KCM 12-000156; 47, lateral tooth (KCM 12-000180); 48, KCM 12-000211; 49, lateral tooth (KCM 12-000261); 50, anterior tooth (KCM 12-000262); 51, KCM 12-000302; 52, KCM 12-000305; 53, KCM 12-000306; 54, anterior tooth (KCM 12-000307); 55, KCM 12-000308; 56, KCM 12-000309; 57, KCM 12-000310. Scale bars are 10 mm unless labelled otherwise.

Habitat at each locality

The habitats for the Hinoshima Formation shark fauna can be separated into three types (Figure 6).

The first habitat type includes the coastal zone, which is evident at Himedo Park. A number of mostly small fossil teeth of Cretalamna appendiculata (62 specimens) and the genera Ptychodus (one specimen) and Notorynchus (one specimen) were found at Himedo Park (Table 1). The absence of evidence of the presence of Carcharias and Hybodus, and the abundant presence of C. appendiculata, Ptychodus, and Notorynchus, is a feature of the Hinoshima fauna. In addition, the fossil shark teeth from Kugushima and Wadanohana are much larger than those from Himedo Park. It is thought that larger sharks inhabited offshore waters, whereas smaller sharks used coastal zones as their breeding area. Similar habitat isolation is known for the extant species Sphyrna lewini, with adult individuals inhabiting offshore waters and smaller individuals inhabiting shallow inner waters (Compagno, 1984; Holland et al., 1993). Yamaguchi (2007) noted that the breeding zone for extant S. lewini is the back of Ariake Bay (Kyushu, Japan). Coastal areas provide important breeding grounds for extant shark taxa including Hexanchus griseus and Notorynchus cepedianus, and extinct taxa including Scapanorhynchus puercoensis (e.g. Yamaguchi, 2007; Quigley, 2010; Bourdon et al., 2011). Himedo Park may have been a breeding area, based on the examination of each taxon (described below).

Figure 4.

Shark fossils from the Hinoshima Formation, continued. 1–42, Cretalamna appendiculata (Himedo Park); 1, KCM 12-000311; 2, KCM 12-000312; 3, KCM 12-000313; 4, KCM 12-000314; 5, KCM 12-000315; 6, KCM 12-000316; 7, KCM 12-000317; 8, KCM 12-000318; 9, KCM 12-000319; 10, KCM 12-000320; 11, KCM 12-000321; 12, KCM 12-000322; 13, KCM 12-000324; 14, KCM 12-000325; 15, KCM 12-000326; 16, KCM 12-000327; 17, KCM 12-000328; 18, KCM 12-000329; 19, KCM 12-000330; 20, KCM 12-000331; 21, KCM 12-000332; 22, KCM 12-000333; 23, KCM 12-000334; 24, KCM 12-000335; 25, KCM 12-000336; 26, KCM 12-000337; 27, anterior tooth (KCM 12-000338); 28, lateral tooth (KCM 12-000339); 29, KCM 12-000340; 30, anterior tooth (KCM 12-000341); 31, KCM 12-000342; 32, KCM 12-000343; 33, KCM 12-0000344; 34, KCM 12-000357; 35, lateral tooth (KCM 12-000364); 36, KCM 12-000376; 37, KCM 12-000377; 38, lateral tooth (KCM 12-000383); 39, lateral tooth (KCM 12-000384); 40, lateral tooth (KCM 12-000394); 41, KCM 12-000412; 42, lateral tooth (KCM 12-000415); 43–62, Cretalamna appendiculata (Kugushima); 43, anterior tooth (KCM 12-000010); 44, anterior tooth (KCM 12-000047); 45, KCM 12-000196; 46, KCM 12-000269; 47, lateral tooth (KCM 12-000270); 48, KCM 12-000271; 49, lateral tooth (KCM 12-000279); 50, anterior tooth (KCM 12-000280); 51, KCM 12-000281; 52, KCM 12-000282; 53, lateral tooth (KCM 12-000289; 54, anterior tooth (KCM 12-000290); 55, posterior tooth (KCM 12-000345); 56, KCM 12-000347; 57, KCM 12-000350; 58, KCM 12-000358; 59, anterior tooth (KCM12- 000416); 60, posterior tooth (KCM 12-000417); 61, lateral tooth (KCM 12-000420); 62, KCM 12-000421; 63–71, Cretalamna appendiculata (Wadanohana); 63, lateral tooth (KCM 12-000003); 64, KCM 12-000004; 65, lateral tooth (KCM 12-000005); 66, anterior tooth (KCM 12-000006); 67, KCM 12-000007; 68, KCM 12-000008; 69, lateral tooth (KCM 12-000011); 70, anterior tooth (KCM 12-000012); 71, anterior tooth (KCM 12-000013). Scale bar is 10 mm.

Shimada et al. (2010) used teeth size to estimate the length of Cretalamna appendiculata from the Futaba Group. Shimada (2005) had previously shown that the crown height of shark teeth can be used to predict the length of lamniform sharks because there is a positive correlation between tooth size and body size in these sharks. Thus, Shimada (2007) estimated the total length of an individual of C. appendiculata from the Niobrara Chalk (Kansas, USA) to be 2.3–3.0 m, based on an average crown height of 15.5 mm for the anterior teeth, and a maximum crown height of 13.5 mm for lateral teeth. Shimada et al. (2010) estimated the length range for the C. appendiculata population from the Futaba Group to be 1.5–4.2 m, by comparing the crown height of anterior teeth and the tallest lateral teeth of a C. appendiculata individual from the Niobrara Chalk with those of C. appendiculata from the Futaba Group.

Figure 5.

Shark fossils from the Hinoshima Formation, continued. 1–25, Cretalamna appendiculata (Wadanohana); 1, anterior tooth (KCM 12-000014); 2, KCM 12-000015; 3, anterior tooth (KCM 12-000016); 4, anterior tooth (KCM 12-000017); 5, anterior tooth (KCM 12-000018); 6, lateral tooth (KCM 12-000019); 7, KCM 12-000020; 8, KCM 12-000021; 9, lateral tooth (KCM 12-000022); 10, lateral tooth (KCM 12-000023); 11, KCM 12-000024; 12, KCM 12-000025; 13, lateral tooth (KCM 12-000026); 14, lateral tooth (KCM 12-000027); 15, lateral tooth (KCM 12-000028); 16, anterior tooth (KCM 12-000029); 17, posterior tooth (KCM 12-000030); 18, anterior tooth (KCM 12-000046); 19, anterior tooth (KCM 12-000048); 20, KCM 12-000049; 21, KCM 12-000050; 22, lateral tooth (KCM 12-000258); 23, anterior tooth (KCM 12-000259); 24, lateral tooth (KCM 12-000260); 25, lateral tooth (GCM-VP409); 26, Cretalamna sp.; KCM 12-000047 (Kugushima); 27, Protolamna sp., GCM-VP410 (Wadanohana); 28, Squalicorax falcatus, KCM 12-000352 (Kugushima); 29–31, Squalicorax sp.; 29, KCM 12-000052 (Wadanohana); 30, GCM-VP413 (Wadanohana); 31, KCM 12-000265 (Kotorigoe); 32, 33, Paranomotodon sp.; 32, KCM 12-000051 (Wadanohana); 33, GCM-VP408 (Wadanohana); 34–36, Dwardius sp.; 34, KCM 12-000002 (Kugushima); 35, KCM 12-000001(Wadanohana); 36, KCM 12-000009 (Wadanohana); 37, Cretodus sp., KCM 12-000278 (Kugushima); 38–40, Synechodus sp.; 38, KCM 12-000264 (Wadanohana); 39, KCM 12-000363 (Wadanohana); 40, GCM-VP412 (Wadanohana). Scale bar at bottom center is 10 mm and applies to all photographs unless stated otherwise.

The length of Cretalamna appendiculata from the Hinoshima Formation was estimated based on the method of Shimada et al. (2010). Figure 7 shows the relationship between tooth crown height (CH) and the total length (TL) of C. appendiculata at each locality (Himedo Park, Kugushima, and Wadanohana) in the study area. For the Himedo Park specimen KCM 12-000262 (Figure 3-50), the crown height for the anterior tooth is 16.0 mm, which is 107.7% of the average crown height (15.5 mm) for anterior teeth of C. appendiculata from the Niobrara Chalk. Based on this relationship the total length of the KCM 12-000262 specimen was estimated to be 2.4–3.2 m. The estimated total length of C. appendiculata from Himedo Park was 1.1–3.4 m, based on measurements of anterior teeth (2 specimens) and lateral teeth (6 specimens). For C. appendiculata from Kugushima the length range is 2.3–4.5 m, based on measurements of anterior teeth (1 specimen) and lateral teeth (2 specimens), and for C. appendiculata from Wadanohana the length range is 1.2–5.0 m, based on measurements of anterior teeth (4 specimens) and lateral teeth (5 specimens). The smallest tooth of C. appendiculata was found for a juvenile specimen from Himedo Park, and the specimens from this location were generally smaller than those from Kugushima and Wadanohana.

Figure 6.

Habitats of the Hinoshima Formation shark fauna.

The Notorynchus sp. (KCM 12-000378; Figure 3-22) from Himedo Park is represented by a small lower tooth. Adnet (2006) calculated the length of extant hexanchid sharks from the strong relationship between shark length and the width of lower teeth, as described by the following equation: length (in m) = [111 × width of tooth (in cm) + 3.9 (R = 0.97, p < 0.001; N = 243)]/100. Based on this equation, the length of the Himedo Park Notorynchus sp. specimen (KCM 12-000378; tooth width = 14.6 mm) is estimated to have been ∼1.66 m. Similarly, the length of the Notorynchus sp. (KCM 12-000272; Figure 3-23; tooth width = 18.8 mm) from Kugushima is estimated to have been ∼2.13 m. The length range for the extant N. cepedianus is 2.0–2.9 m (possibly 3–4 m) (Compagno et al., 2005). Consequently, the Notorynchus sp. (KCM 12-000378) from Himedo Park was probably a juvenile.

The dentition (upper and lower) of the Ptychodontidae exhibits monognathic heterodonty and forms a crushing pavement similar to that of extant Heterodontidae (e.g. Welton and Farish, 1993; Shimada, 2012). In terms of crown width, the specimens of Ptychodus mammillaris (KCM12-000061; Figure 3-1; mesial–distal crown width: 12.1 + mm) from Himedo Park are similar to the specimens of P. mammillaris KCM12-000257 (Figure 3-6; mesial–distal crown width: 15.5 mm) and KCM12000144 (Figure 3-5; mesial–distal crown width: 15.0 mm) from Wadanohana, although slightly smaller. Consequently, the P. mammillaris (KCM12-000061) specimen from Himedo Park was probably a juvenile. As noted above, although a large specimen (maximum length 3.4 m) of Cretalamna appendiculata was found at Himedo Park, most of the individuals were relatively small and were probably juveniles, suggesting that this was a breeding area. The presence of the large specimen of C. appendiculata at Himedo Park probably indicates that adult sharks entered the breeding area to deliver pups, as occurs with extant sharks. For example, adult hammerhead sharks (Sphyrna lewini) enter Ariake Bay in southwestern Japan (Yamaguchi, 2007) and bays in Hawaii (Clarke, 1971) to give birth and deliver pups.

Figure 7.

Relationship between tooth crown height and the total length of Cretalamna appendiculata at each locality (Himedo Park, Kugushima, Wadanohana). Specimen numbers reflect those in Figures 3–5. The method for estimating total length (TL) followed Shimada (2007) and Shimada et al. (2010).

The second habitat type is the coastal–offshore surface layer zone, which is the habitat of fast-swimming predators, as inferred for Kugushima, Wadanohana, and Kotorigoe. The genera Cretodus, Dwardius, Squalicorax, Cretalamna, and Protolamna (Lamniformes), and the genus Sphenodus (Synechodontiformes) are associated with this habitat.

The third habitat type is that in the vicinity of the continental shelf, and is characterized by the occurrence of sluggish bottom-dwelling predators. This habitat type can be seen at Kugushima, Wadanohana, Higashiura, and Kotorigoe, where it is associated with the genera Hexanchus, Notorynchus, Notidanodon, Chlamydoselachus, Echinorhinus, Centrophoroides, and Ptychodus. The shark teeth fossils associated with this habitat are thought to have been deposited on the continental shelf, as they lack signs of abrasion and are associated with well preserved ammonoid fossils.

Habitat shift in the genera Chlamydoselachus and Echinorhinus

Extant Chlamydoselachus anguineus and Echinorhinus brucus primarily inhabit the deep sea and prey on Cephalopoda and bottom-dwelling fishes (Compagno, 1984). Two types of fossil teeth of the genus Chlamydoselachus from the Hinoshima Formation were reported by Goto and the Japanese Club for Fossil Shark Tooth Research (2004). The first type (Chlamydoselachus sp. 3) is three times larger than those of extant species, and the second type (Chlamydoselachus sp. 2) is similar in size to those of extant species. In this study, Chlamydoselachus sp. A (GCM-VP400; Figure 3-8) is similar to the first type described above, and Chlamydoselachus sp. B (KCM12000360; Figure 3-9) is similar to the second type. The first type, comprising large and robust teeth, has also been found in Upper Cretaceous deposits of the Izumi Group in Osaka, in Antarctica, and in Angola. They are thought to have belonged to species inhabiting shallow water (Richter and Ward, 1990; Antunes and Cappetta, 2002; Goto and the Japanese Club for Fossil Shark Tooth Research, 2004). Consoli (2008) noted that following the extinction of cephalopods having a shell (such as ammonoids) after the Cretaceous-Paleogene (K-Pg) boundary, the rise of modern soft-bodied taxa resulted in a change in tooth structure. Thus, shark dentition evolved from that well suited to eating hard-shelled cephalopods to gracile cusps, and the sharks migrated into deep-sea areas. Large robust (Chlamydoselachus sp. A) and small (Chlamydoselachus sp. B) shark teeth types were found in Kugushima horizon b and from Wadanohana; these depositional environments appear to have been allochthonous. Chlamydoselachus sp. B was also found at Higashiura, which was a deeper depositional environment than those of Kugushima and Wadanohana, and is also indicative of an autochthonous occurrence. Thus, it is likely that Chlamydoselachus sp. A and B inhabited similar environments, or that Chlamydoselachus sp. B occurred in deeper waters than did Chlamydoselachus sp. A. Large and robust (C. goliath) and small (C. gracilis) shark teeth have been found associated with the ammonoid genus Eupachydiscus in Upper Cretaceous deposits (upper Campanian–Maastrichtian) in Africa (Angola), and in deep-sea environments (Antunes and Cappetta, 2002; p. 137). Tanabe (1979) also raised the possibility that desmoceratid ammonoids, including Eupachydiscus, inhabited deeper offshore environments than did collignoniceratids and heteromorphic ammonites, suggesting that the two types of Chlamydoselachus in the Hinoshima Formation also inhabited deeper offshore environments, along with Eupachydiscus. The fossil bramble shark (Echinorhinus wadanohanaensis) teeth from the Himenoura Group in the Hinoshima Formation are much larger than those of extant Echinorhinus cookei (almost double the tooth width ratio) (Kitamura, 2013). Similarly, large fossil bramble shark teeth have been found associated with the Upper Cretaceous (Santonian) Yezo Group (Kaneko et al., 2012). In addition, it has been suggested that fossil bramble shark (E. eyrensis) teeth were deposited in shallow coastal environments (Pledge, 1992). However, fossil evidence of the genus Echinorhinus from the Hinoshima Formation indicates a similar habitat to Chlamydoselachus in Wadanohana, suggesting that in the Late Cretaceous Echinorhinus inhabited the same deeper offshore environments as the frilled shark Chlamydoselachus.

Figure 8.

Numbers of species and total number of specimens (by order) in the Hinoshima Formation and other areas. Paleomap from Smith et al. (2004). New Mexico, USA (Santonian); Bourdon et al. (2011). Antarctica, Santa Marta Formation, late Coniacian–early Campanian, late Campanian?–early Maastrichtian; Kriwet et al. (2006). Angola (Campanian–Maastrichtian); Antunes and Cappetta (2002). Hinoshima Formation (present study), Santonian. For each locality, the upper circles show the numbers of species by order, and the lower circles are the total numbers of specimens.

Table 2.

Comparison of Late Cretaceous (mainly Santonian) shark taxa from the Hinoshima Formation and other areas worldwide.

Continued.

Figure 9.

Coexistence relationships of large lamniform sharks, hexanchiform genera (Notidanodon and Chlamydoselachus), and the echinorhiniform genus Echinorhinus in world regions, primarily in the Late Cretaceous. North America: Cumbaa et al., 2010. Europe: Siverson, 1995; Jagt et al., 2006; Cook et al., 2010; Adnet et al., 2012; Sørensen et al., 2013. Angola: Antunes and Cappetta, 2002. Australia: Chapman, 1908; Kemp, 1991; Pledge, 1992; Siverson, 1996, 1999. New Zealand: Consoli, 2008. Antarctica: Kriwet et al., 2006. Japan: Hinoshima Formation, Kumamoto Prefecture (Kitamura, 1997, 2013; Goto and The Japanese Club for Fossil Shark Tooth Research, 2004), Osaka and Hyogo (Tanimoto et al., 2001a, 2001b; Goto and The Japanese Club for Fossil Shark Tooth Research, 2004), Hokkaido (Research Group for Mesozoic Fossil Shark, 1977; Uyeno and Matsui, 1993; Kaneko et al., 2012).

Comparisons with other fauna

Although many studies have reported the Upper Cretaceous shark fauna of the late Early and early Late Cretaceous (e.g. Siverson, 1996; Case, 2001; Vullo et al., 2007; Cumbaa et al., 2010), and the “last Cretaceous” (e.g. Case, 1987; Case et al., 2001; Becker et al., 2004), there have been few studies of the Santonian period (sometimes referred to as the “Santonian gap”; Welton and Farish, 1993).

Table 2 compares the Late Cretaceous shark fauna from the Hinoshima Formation with that from Hokkaido, the Futaba Group (Iwaki, Fukushima Prefecture), North America (Texas and New Mexico), Europe (France), Africa (Angola), and Antarctica. Figure 8 also shows the occurrence and number of species (by order) found in the Hinoshima Formation, North America (Texas and New Mexico), Africa (Angola), and Antarctica. Three faunae from Western Australia (Albian and middle Cenomanian), Kansas (USA; Cenomanian), and Sweden (Campanian) are included for further comparison (Table 2).

Hokkaido (Santonian) and Iwaki City Fukushima Prefecture (Coniacian), Japan.—Active highly motile predators of the coast and offshore zones, including Cretalamna and Sphenodus, and slow-swimming bottom and shelf-dwelling genera, including Ptychodus, Chlamydoselachus, and Echinorhinus are observed, as in the Hinoshima Formation (Table 2; Nabana, 1990, 1991, 1992; Uyeno and Suzuki, 1995; Goto and the Japanese Club for Fossil Shark Tooth Research, 2004; Kaneko et al., 2012). Far more diverse Late Cretaceous shark taxa are evident in the Hinoshima Formation than at Hokkaido and Iwaki, but the Upper Cretaceous shark fauna at Hokkaido and in the Futaba Group consist of fast-swimming predators and sluggish bottom-dwelling predators similar to those of the Hinoshima Formation.

Texas, USA (Santonian).—The Texas fauna contains no shallow-water (< 150 m depth) or slow-swimming bottom- or shelf-dwelling shark species (Table 2; Welton and Farish, 1993). As shown in Table 2, only Lamniformes are evident in Texas (the Santonian gap) (Welton and Farish, 1993).

New Mexico, USA (Santonian).—The New Mexico fauna includes shallow-water hybodontiforms and odontaspidids, and includes the active highly motile predator genus Cretoxyrhina and slow-swimming bottom-dwelling squatiniforms and orectolobiforms of coastal to offshore waters. The orectolobiforms, hybodontiforms, squatiniforms, and the dominant species Scapanorhynchus puercoensis are evident in New Mexico, but not in the Hinoshima Formation (Table 2; Bourdon et al., 2011).

France (Santonian).—Only the genus Squalicorax is common to France and the Hinoshima Formation (Table 2; Cahuzac et al., 2007).

Angola (Africa) (Campanian–Maastrichtian).—The active predator genera Cretodus and Dwardius, slow-swimming bottom- or shelf-inhabiting members of the family Ptychodontidae, and the shallow-water shark fauna have not been found amongst the Angolan fauna. As shown in Figure 8, the numbers of species by order and specimen abundance are similar to those of the Hinoshima Formation. The hexanchiforms (genera Chlamydoselachus and Notidanodon), echinorhiniforms (genus Echinorhinus), squaliforms (genus Centrophoroides), and synechodontiforms (genus Sphenodus) in the Angolan shark fauna are similar to those in the Hinoshima Formation (Table 2; Antunes and Cappetta, 2002).

Antarctica (Santa Marta Formation) (late Coniacian–early Campanian).—Although the lamniform taxa, slow-swimming hexanchiform sharks, and echinorhiniform, squaliform, squatiniform, orectolobiform, and synechodontiform sharks are absent from the Antarctic fauna, other hexanchiform sharks in the Antarctic shark fauna are similar to those in the Hinoshima Formation (Figure 8; Table 2; Kriwet et al., 2006).

Antarctica (Santa Marta Formation) (late Campanian–? early Maastrichtian).—The Antarctica fauna has many elements in common with the Hinoshima Formation including the slow-swimming genera Chlamydoselachus and Notidanodon, and active predators including indeterminate Lamniformes and the genera Scapanorhynchus and Sphenodus. The genus Squatina is present in this fauna, but ptychodontids, the genus Hexanchus, echinorhinids, squaliforms, synechodontiforms, and a number of active predator lamniform sharks are absent (Table 2; Kriwet et al., 2006). The composition of hexanchiforms (genera Chlamydoselachus and Notidanodon) and synechodontiforms (genus Sphenodus) in the Antarctic shark fauna is similar to that in the Hinoshima Formation.

Western Australia (Albian, middle Cenomanian), Kansas, USA (Cenomanian).—Many lamniform genera found in the Hinoshima Formation fauna, including the genus Cretalamna, are evident in the Western Australian (Albian, middle Cenomanian) and Kansas, USA (Cenomanian) faunae, but the shallow-water genera Carcharias and Hybodus are not amongst the Hinoshima Formation taxa, and the slow-swimming genera are rare in the Western Australia and Kansas fauna (Table 2; Siverson, 1996, 1997; Cook et al., 2010; Cumbaa et al., 2010). In contrast with the shark fauna of the Hinoshima Formation, the dominant lamniform sharks and many slow-swimming taxa co-occur in Western Australia and Kansas.

Sweden (late early Campanian).—Comparison of the shark fauna from Kristianstad Basin (Sweden) (Table 2; Sørensen et al., 2013) and the Hinoshima Formation shows that the fauna of the Kristianstad Basin was dominated by lamniform sharks similar to those in the Hinoshima Formation. Lamniform genera including Cretalamna, Squalicorax, Cretodus, Paranomotodon, and the synechodontiform genus Synechodus have also been found in the Hinoshima Formation. However, there are a number of differences between the two faunae. Sluggish bottom-dwelling sharks including squatiniform, heterodontiform, orectolobiform, and carcharhiniform (Scyliorhinidae, Triakidae) sharks only occur among the shark fauna from the Kristianstad Basin (Compagno, 1984). Cretoxyrhina mantelli and Squalicorax kaupi, which are thought to have been top predators (Shimada and Cicimurri, 2005), are present in the Kristianstad Basin fauna. The hexanchiform genus Chlamydoselachus and the echinorhiniform genus Echinorhinus have not been reported in the shark fauna of Kristianstad Basin.

Explaining the occurrence of large hexanchiform sharks in the Upper Cretaceous shark fauna of Japan, including the Hinoshima Formation

The Late Cretaceous genus Notidanodon is distributed in Antarctica (Grande and Chatterjee, 1987; Kriwet et al., 2006), New Zealand (Woodward, 1886a, b), Angola (Antunes and Cappetta, 2002), South India (Underwood et al., 2011), Southern Patagonia (Bogan et al., 2016), and Japan (e.g. Goto et al., 1996; the present study), but has not been recorded from low latitudes (Cione, 1996). Siverson (1995) noted that the absence of Notidanodon from the Late Cretaceous neritic zones may have been because of competitive pressures from large cosmopolitan lamniform sharks. The only areas where Notidanodon has been reported from Campanian/Maastrichtian neritic deposits are New Zealand and Antarctica (see Figure 9). Large Late Cretaceous lamniform sharks including Cretoxyrhina mantelli, Squalicorax pristodontus, and the genus Cardabiodon have been reported (Shimada, 1997, 2008; Siverson, 1999; Siverson and Lindgren, 2005; Shimada et al., 2006; Cook et al., 2010), particularly from the Western Interior Seaway, Europe, and Australia (Figure 9). However, Figure 9 shows that there are instances of the coexistence of these large lamniform sharks and the genus Notidanodon in the Late Cretaceous, including the coexistence of the genus Notidanodon and Squalicorax pristodontus in Angola and Japan. Underwood et al. (2011) also reported the coexistence of the genus Notidanodon(?) and the lamniform sharks Cretalamna appendiculata and Dwardius sudindicus in India. The Late Cretaceous lamnoids Squalicorax and Cretoxyrhina mantelli are thought to have been active pelagic sharks (e.g. Shimada, 1997, 2008) that lived in middle to low paleolatitudes, mainly inhabiting warm waters (e.g. Underwood et al., 2011). On the other hand, the Late Cretaceous Notidanodon are thought to have been bentho-pelagic sharks (Underwood et al., 2011) inhabiting cold waters in high-paleolatitude areas (e.g. Cione, 1996; Underwood et al., 2011). Furthermore, the depositional environments have been interpreted as offshore habitats with respect to reports of Notidanodon shark teeth from South India (early Cenomanian; Underwood et al., 2011), Angola (Campanian–Maastrichtian; Antunes and Cappetta, 2002), and Japan (e.g. Santonian, the present study). The records of Late Cretaceous Notidanodon from mid-paleolatitude areas including Angola, South India, and Japan thus expand its range to low paleolatitudes. Explanations for the coexistence of these taxa may be ecological; for example, Squalicorax and Cretoxyrhina mantelli were active pelagic predators while Notidanodon was a bentho-pelagic predator. Kriwet et al. (2006) investigated the selachian fauna from the Late Cretaceous in Antarctica, and noted that the shark fauna of the Late Cretaceous Weddelian Province (Antarctica-Patagonia-New Zealand; Zinsmeister, 1979) was characterized by high-latitude selachian taxa (e.g. Notidanodon, Chlamydoselachus, Sphenodus), as also noted by Bogan et al. (2016) and Cione (1996). Thus, the diversity of the Late Cretaceous shark fauna (e.g. Notidanodon, Chlamydoselachus, Sphenodus) in East Asia including Japan (e.g. Goto et al., 1996; the present study) is similar to that of the Weddelian Province and surrounding regions during the Late Cretaceous. The characteristics of the Upper Cretaceous shark fauna in Japan (including the Hinoshima Formation) are similar to those of the contemporaneous Southern Hemisphere fauna (e.g. Angola, Australia, and Antarctica). This shows that the characteristic shark fauna in the Southern Hemisphere had spread to the middle latitudes of the Northern Hemisphere by the Late Cretaceous.