Introduction

Ophiomusium and Ophiosphalma are closely related genera that have previously been assigned to the family Ophiolepididae (O'Hara et al., 2014). The former is a species-rich extant genus with an extensive fossil record ranging from the Triassic to the Neogene (Stöhr et al, 2014), although the genus-level assignment of the lower Mesozoic records requires re-assessment (e.g. Jagt, 2000). In fact, most fossils of Ophiomusium have been identified solely on the basis of dissociated lateral arm plates and other ossicles (e.g. Hess, 1966; Kutscher and Hary, 1991; Jagt, 2000; Štorc and Žítt, 2008; Thuy and Kroh, 2011), hampering a meaningful comparison with modem relatives. Previous records of fossil Ophiomusium from Japan were Ophiomusium sp. from the middle Miocene Itsukaichimachi Group in Tokyo Prefecture (Paleontological subgroup of Itsukaichi Basin Research Group, 1985), from the middle Miocene Amatsu Formation in Chiba Prefecture (Ishida, 2004b) and from the lower Miocene Morozaki Group in Aichi Prefecture (Ishida, 1988, 1993), and Ophiomusium cf. lymani from the lower Miocene Morozaki Group in Aichi Prefecture (Ishida, 1988, 1993). Another extant genus, Ophiosphalma, is morphologically very similar to Ophiomusium but is distinguished on the basis of a difference in the number of tentacle pores of basal arms (Clark, 1941). This had no previous fossil record.

Recently, well preserved articulated body fossils of Ophiomusium were discovered in the lower Miocene Ichishi Group in Mie Prefecture (Ishida, 2004b, 2013). In addition, an articulated specimen assignable to Ophiosphalma was found in the lower Miocene Oigawa Group in Shizuoka Prefecture. The present study aims at a detailed morphological description of the new material of Ophiomusium and Ophiosphalma, a systematic interpretation of their distinction, paleoenvironment and taphonomic context.

Materials and methods

More than 75 articulated discs with arms and over 170 semi-articulated arm fragments of specimens of Ophiomusium were examined (Figure 1). They were found at three localities near Misato, Tsu City, Mie Prefecture, central Japan, about 13 km west of Tsu Railway Station on JR Kisei Line (1–3 in Figure 1A; co-ordinates 34°43′43″N, 136°22′51″E, 34°43′27″N, 136°23′52″E, and 34°42′49″N, 136°23′29″E, respectively). Ophiomusium-bearing strata, assigned to the Mitsugano Tuffaceous Siltstone and Sandstone Member, Oi Formation (Ichishi Group), consist of a series of thick sandstones alternating with thinner sandstone and mudstone layers (Yoshida et al., 1994). The specimens of Ophiomusium originate from thin sandstone layers (Figure 2). The age of the Oi Formation is early Miocene as suggested by associated planktonic foraminifera (Yoshida, 1991). The Oi brittle stars are preserved both as external molds lacking any remains of the original skeletal calcite and as calcitic body fossils. Recent Ophiomusium lymani from collections deposited at the National Museum of Nature and Science, Japan (NSMT E-2688, 2745, 2833, 2105) were used for morphometrical and morphological comparisons with the fossil specimens.

Figure 1.

Maps showing the position of the localities (marked by ×) that have yielded the two ophiuroid species described here. A, Ophiomusium lymani from the Mitsugano Member of the Oi Formation, Tsu City, Mie Prefecture; B, Ophiosphalma cancellata from the Shida Formation, Fujieda City, Shizuoka Prefecture. A and B showing part of “Tsu-seibu” and “Ieyama and Shizuoka” 1:50,000 topographic maps by the Geographical Survey Institute, respectively.

In order to assess the taphonomy of Ophiomusium lymani from the Oi Formation, the anatomy of vertebrae and associated muscles was examined using both specimens (NSMT E-7844) of Ophiura sarsii (Ophiuridae, Ophiurinae) and individuals of Ophiomusium lymani (NSMT E-2105). The arm skeleton was partly macerated using household bleach (approximately 5% sodium hypochlorite solution).

One articulated disc with arms of Ophiosphalma was examined from a locality situated at Uchiseto, Fujieda City, Shizuoka Prefecture, central Japan, about 3.2 km west of Fujieda Railway Station on JR Tokaido Line (coordinates 34°50′45″N, 138°13′13″E; see Figure 1B). Ophiuroid-bearing strata, assigned to the Shida Formation (Oigawa Group), consist of mudstone (Sugiyama, 1980; Sugiyama et al., 1982). The Shida Formation is of early Miocene age on the basis of benthic foraminifera (Kato et al., 1992) and molluscan faunas (Shibata and Kato, 1975; Kato et al., 1992). The specimen is preserved as an external mold without any remains of the original skeletal calcite.

Figure 2.

Columnar section at the fossil locality (marked ‘2’ in Figure 1A) in the Mitsugano Member of the Oi Formation.

Figure 3.

Ophiomusium lymani from the Mitsugano Member of the Oi Formation. A–E, synthetic resin casts; A, entire specimen in ventral view (MFM 38065-02); B, detailed view of A (MFM 38065-02); C, disc and proximal arms in dorsal view of another specimen (MFM 38065-01); D, arm segments indicated by arrow in A in lateral view (MFM 38065-02); E, proximal arm segments in lower part of lateral view (MFM 38065-04; the original was detached from the boulder of Figure 7B). Abbreviations: Aop, adoral plate; Asp, arm spine; Dap, dorsal arm plate; Dsc, disc scale; Vap1, first ventral arm plate; Gsc, genital scale; Gsl, genital slit; Lap, lateral arm plate; Opa, oral papilla; Op, oral plate; Osh, oral shield; Sp, spur on outer proximal edge; Rsh, radial shield; To, tooth; Tpo, tentacle pore; Tsc, tentacle scale; Vap, ventral arm plate. Scale bars: A–C = 5 mm; D–E = 1 mm.

Detailed morphologies of both fossil ophiuroid taxa were analyzed by preparing synthetic resin casts, made by manually pressing the resin on the specimens. Selected specimens were drawn using a camera lucida device, and disc diameters were measured using a caliper square. The mode of occurrence of Ophiomusium specimens was documented using transparent paper placed on the specimens found in the boulders.

Results

The specimens of Ophiomusium and Ophiosphalma were found to belong to extant species, as discussed below.

Figure 4.

Camera-lucida drawings of specimens of Ophiomusium lymani from the Mitsugano Member of the Oi Formation. A (ventral view), B (dorsal view), C (lateral view) and D (lateral view) correspond to B, C, D and E of Figure 3, respectively. Abbreviations see Figure 3. Scale bars: A–B = 5 mm; C–D = 1 mm.

Figure 5.

Ophiosphalma cancellata (NMNS PA 18294) from the Shida Formation. A—C, synthetic resin casts. A, entire specimen in ventral view; B, detailed view of A; C, arm segments shown by arrow in A in lateral-ventral view. Abbreviations see Figure 3. Scale bars: A–B = 5 mm; C = 1 mm.

Figure 6.

Camera-lucida drawings of specimen of Ophiosphalma cancellata from the Shida Formation. A (ventral view) and B (lateral-ventral view) correspond to A, B and C of Figure 5, respectively. Abbreviations see Figure 3. Scale bars: A = 5 mm; B = 1 mm.

Figure 7.

Mode of occurrence of specimens of Ophiomusium lymani from the Oi Formation. A, MFM 38069, body fossils. B, MFM 38065 (1, MFM 38065-01; 2, MFM 38065-02; 3, MFM 38065-03), mold of specimens. Abbreviations: Ar, dissociated arm; Do, dorsal view; Ve, ventral view. Scale bars = 5 cm.

Figure 8.

Sketch showing the mode of occurrence of specimens of Ophiomusium lymani from the Oi Formation. The orientation of discs and arms is indicated by the patterns. A and B conespond to A and B in Figure 7, respectively. Abbreviations see Figure 7. Scale bars = 5 cm.

Discussion

Ophiomusium lymani from the Oi Formation and Ophiosphalma cancellata from the Shida Formation are both interpreted as early Miocene (c. 17 Ma) in age on the basis of associated planktonic (Yoshida, 1991) and benthic foraminifera (Kato et al., 1992), respectively. Both species occurrences represent the oldest fossil record of an extant ophiuroid species to date, predating the previous oldest records of Ophiura sarsii sarsii from the uppermost middle Miocene to the lowermost upper Miocene in Japan (Ishida and Fujita, 2001b; Ishida et al., 2004).

Our results imply that the genera Ophiomusium and Ophiosphalma had diverged by the early Miocene at the latest. The distinguishing character, i.e., the number of between-plate tentacle pores, however, can only be observed on well preserved articulated skeletons in which the ventral side is exposed. As a result, many of the fossil specimens reported in the literature as Ophiomusium, especially those based solely on lateral arm plates, might in fact be assignable to Ophiosphalma.

The genus Ophiomusium has often been reported in the fossil record, from the Triassic to the Neogene (Stöhr et al., 2014). Most of the assumed extinct Ophiomusium specimens were identified on the basis of dissociated lateral arm plates; e.g. O. dizluense Kristan-Tollmann, Tollmann and Hamedani, 1979 from the Upper Triassic of Iran (Kristan-Tollmann et al., 1979), O. solodurense Hess, 1962 from the Lower Jurassic of Switzerland (Hess, 1962), O.? sinemurensis Kutscher and Hary, 1991 from the Lower Jurassic of Luxemburg (Kutscher and Hary, 1991), O. praecisum Hess, 1966 from the Upper Jurassic of France (Hess, 1966), O. mammillatum Hess, 1966 from the Upper Jurassic of Switzerland (Hess, 1966), Ophiomusium sp. from the Lower Cretaceous of France (Thuy and Kroh, 2011), O. sinuatum Kutscher and Jagt in Jagt, 2000 from the Upper Cretaceous of Belgium and Germany (Jagt, 2000), Ophiomusium sp. from the Upper Cretaceous of the Czech Republic (Štore and Žítt, 2008), and O. biconcavum Kutscher and Jagt in Jagt, 2000 from the Upper Cretaceous of Belgium and Germany (Jagt, 2000). Some were identified on the basis of articulated arm segments, e.g. O. vermiculatum Valette, 1914 and O. rugosum Valette, 1914 from the Upper Cretaceous of France (Valette, 1914), and O. cf. lymani from the lower Miocene of Japan (Ishida, 1988, 1993, 2003). The development of the tentacle pores is obviously difficult, if not impossible, to examine on such fragmentary material.

On the other hand, several specimens are preserved as fully articulated skeletons and most of these have more than just two to three between-plate tentacle pores. Those questionable fossil records include Ophiomusium geisingense Kutscher, 1992 from the Lower Jurassic of Germany (Kutscher, 1992), O. ferrugineum Boehm, 1889 from the Middle Jurassic of Switzerland (Hess and Holenweg, 1985), O. weymouthiense (Damon, 1880) from the Middle Jurassic of England (Hess, 1964), and O. cf. gagnebini (Thurmann, 1851) from the Upper Jurassic of Switzerland (Hess, 1966). In other cases, the morphology of the tentacle pores is unknown as a result of insufficient preservation, e.g. O. fitchii (Spencer, 1907) from the Upper Cretaceous of England (Spencer, 1907), O. sp. from the middle Miocene of Japan (Paleontological sub-group of Itsukaichi Basin Research Group, 1985), O. sp. from the lower Miocene of Japan (Ishida, 1988, 1993, 2003). The following two fossil records are the only ones to have the typical two between-plate tentacle pores in the proximalmost arm segments: O. lux from the Upper Cretaceous of the Netherlands, and O. granulosum from the Upper Cretaceous of the Netherlands, Belgium, Germany and Poland. Fossil specimens which have three between-plate tentacle pores at basal arms have not been reported yet. Ophiomusium and Ophiosphalma are similar in shape, and are distinguished on the basis of the number of between-plate tentacle pores (Clark, 1941). At the present state of knowledge, the specimen from the Shida Formation described here is the first fossil record of the genus Ophiosphalma.

Specimens of Ophiomusium lymani from the Oi Formation occur in dense aggregations in two of the boulders, with both dorsal and ventral sides exposed on the bedding plane (Figures 7, 8). The arms are long and mostly straight (Figures 7A, 8A), slightly bent in some specimens (Figures 7B, 8B). Most disarticulated arms are simply broken into long pieces, not further disarticulated into ossicles. The individuals are in contact with each other (Figures 7B, 8B) or even overlap (Figures 7A, 8A). The aggregation densities measured on the surface area of the boulders amount to 355 inds./m² (calculated from 13 inds./366 cm², Figures 7A, 8A) and 428 inds./m² (calculated from 55 inds./1258 cm², Figures 7B, 8B). Ophiuroids usually disarticulate rapidly one day to two weeks after death (Brett et al., 1997; Kerr and Twitchett, 2004). Accordingly, the present specimens of Ophiomusium lymani were probably transported alive from the vicinity and rapidly buried. Extant Ophiomusium lymani occurs in relatively high densities on the deep-sea floor, reported as 3–11 inds./m² (1,243–2,000 m deep) in the Atlantic Ocean off North America (see Fujita, 1992, table 1). Similarly dense populations are also assumed to occur in Japanese waters because of the sheer numbers of specimens sampled by dredging (Irimura et al., 1995; Fujita, unpubl. data). Fossil Ophiomusium lymani might have formed a similarly dense aggregation.

Extinct Ophiomusium lymani shows striking similarities in the mode of occurrence to fossil Ophiura sarsii, but some different postures are observed between the two species. Some of the fossil Ophiura sarsii display an escape posture, with arms bending symmetrically and tilted discs (Ishida, 1999, 2004a; Ishida and Fujita, 2001a). The fossil specimens of Ophiomusium lymani, in contrast, fail to show such postures (Figures 7, 8). Interestingly, their arms are very rigid and can be hardly bent and almost all fixed specimens of Recent Ophiomusium lymani collected by dredging (more than two hundred specimens, NSMT E-2668, 2745, 2833, 2015) have straight arms. The spurs on the lateral arm plates in O. lymani (Figures 3D, 4C, 9A; see Thuy and Stöhr, 2011, figure 24) assumedly act as mechanical stabilizing structures in the articulation between neighboring arm segments. The distal muscle attachment areas of the vertebrae of Recent Ophiura sarsii are more deeply concave than those of Recent Ophiomusium lymani (Figure 9), thus allowing for a greater bending capacity of the arms in Ophiura sarsii. As a result, it can be speculated that the specimens of Ophiomusium lymani from the Oi Formation were simply unable to bend their arms in such a way to escape from the sediment cover.

The paleodepth of the Oi and Shida formations is estimated to have been upper bathyal based on the associated molluscan Macoma-Lucinoma and Neilonella-Periploma assemblages (Shibata and Itoigawa, 1980) and the benthic foraminifera Ammodiscus spp., Bathysiphon spp., Cyclammina spp., Cribrostomoides spp., Martinottiella communis (Kato et al., 1992), respectively. This is in line with the depth at which Ophiomusium lymani and Ophiosphalma cancellata commonly occur in present-day Japanese waters (Matsumoto, 1917; Irimura et al., 1995).

Figure 9.

Vertebrae with muscles of Recent ophiuroids. A, Ophiomusium lymani, NSMT E-2105 (disc diameter 24.2 mm), dorsal view of basal arm segments. Dorsal arm plates, lateral arm plates and arm spines are removed. B, Ophiura sarsii, NSMT E-7844 (disc diameter 11.6 mm), dorsal view of basal arm segments. Dorsal arm plates are removed. Abbreviations: Ms, muscle; Ver, vertebra; for others see Figure 3. Scale bars = 1 mm.

Conclusions

More than 75 specimens from the lower Miocene Oi Formation (Ichishi Group), Mie Prefecture and one specimen from the lower Miocene Shida Formation (Oigawa Group), Shizuoka Prefecture, central Japan, were identified as the extant species Ophiomusium lymani and Ophiosphalma cancellata, respectively. These occurrences constitute the oldest fossil record of these present-day brittle star species, and, in the latter case, the first fossil record for the genus Ophiosphalma. The new material documents that the closely related genera Ophiomusium and Ophiosphalma had already diverged by the early Miocene.

Most previously known fossil ophiuroids assigned to Ophiomusium were known exclusively on the basis of isolated lateral arm plates, thus precluding observations on the number of between-plate tentacle pores. Only two Ophiomusium species from the Upper Cretaceous, known from articulated specimens, unambiguously had two between-plate tentacle pores at the basal arm segments. No fossil specimen with three tentacle pores has been reported yet. The distinguishing character, the number of tentacle pores, is very difficult to observe in imperfectly preserved fossils, and the records of dissociated lateral arm plates assigned to Ophiomusium might, in fact, include yet unrecognized Ophiosphalma occurrences.

The present specimens of Ophiomusium lymani might have formed a similarly dense aggregation as Recent counterparts. Judging from their mode of occurrence, they were probably transported alive from the vicinity and rapidly buried.

The arms of Ophiumisium lymani from the Oi Formation are long and mostly straight. On the basis of the anatomical observations of arm bending capacities and lateral arm plate structure, it is assumed that the Ophiomusium individuals were simply unable to bend their arms to escape from the sediment cover.

The ancient Ophiomusium lymani and Ophiosphalma cancellata inhabited the same upper bathyal environment as their Recent counterparts.