Non-technical Summary
Fossil evidence shows that trilobites—an extinct group of marine arthropods—continued to evolve during the middle Permian period. One group, Pseudophillipsia, was especially successful, producing many different species. However, it is unclear whether their abundance reflects broad changes in rock layers (stratigraphy) or is related to specific environments where they lived. To investigate this, we studied Pseudophillipsia fossils from 260-million-year-old rocks in northeastern Japan and examined how these animals were buried and preserved. We identified two species, Pseudophillipsia spatulifera and Pseudophillipsia sp. indet., found in sandstone and mudstone layers. The sandstone was likely deposited in shallow water near the shore, whereas the mudstone formed in deeper water, sometimes disturbed by storms. The way that the fossils are preserved suggests that outstretched specimens were buried at their living site, whereas rolled-up ones might have been transported and buried by storm currents. Mudstone layers also show more evidence of disturbance by other animals burrowing in the sediment, which could explain why fossils there are more often disarticulated. These patterns suggest that one species, Pseudophillipsia spatulifera, lived in both sandy and muddy areas, whereas the other, Pseudophillipsia sp. indet., preferred sandy environments. Because the rocks containing these trilobites were only found in a small area, we think their presence reflects how they adapted to local conditions, rather than a widespread shift in their overall distribution over time.
Introduction
In contrast to the high diversity of the early to middle Paleozoic, trilobites declined dramatically after the Late Devonian extinction that eliminated all trilobite orders except the Proetida (Owens, Reference Owens1990; Bault et al., Reference Bault, Balserio, Monnet and Crônier2022). Despite this decline, changes in trilobite diversity and abundance continued throughout the late Paleozoic. During the late Carboniferous to the early Permian, cosmopolitan proetids dominated and persisted throughout the late Paleozoic Ice Age (Brezinski, Reference Brezinski2023). In turn, trilobite diversity increased during the middle Permian, particularly in the Wordian, reaching its highest number of genera (Lerosey-Aubril and Feist, Reference Lerosey-Aubril, Feist and Talent2012; Bault et al., Reference Bault, Balserio, Monnet and Crônier2022). Geographically, the middle Permian trilobite fauna can be divided into three main provincial assemblages: (1) the western margin of North-Central America, (2) the Paleo-Tethyan province, e.g., Japan, China, Russia, and the Middle East, and (3) the Tethyan province, e.g., Italy and Timor (e.g., Kobayashi and Hamada, Reference Kobayashi and Hamada1984; Brezinski, Reference Brezinski1999, Reference Brezinski2023; Owens, Reference Owens2003; Lerosey-Aubril, Reference Lerosey-Aubril2012; Fortey and Heward, Reference Fortey and Heward2015). Cosmopolitan genera such as Pseudophillipsia Gemmellaro, Reference Gemmellaro1892 and Cheiropyge Diener, Reference Diener1897 appeared across these provinces, suggesting complex biogeographic connections during the middle Permian (Brezinski, Reference Brezinski2023).
Although the decline of Permian trilobites began in the Capitanian, their habitable environments changed markedly during the Permian. Trilobite diversity during the Permian is known to be closely associated with variations in paleoenvironments and habitat preferences. The diversification of middle Permian trilobites has been attributed to the development of shelf-edge reefs, which promoted faunal provincialism (Brezinski, Reference Brezinski1999, Reference Brezinski2023; Owens, Reference Owens2003; Lerosey-Aubril, Reference Lerosey-Aubril2012). Data-based paleontological analyses indicate that trilobites in the early Permian (Cisuralian) occupied a broad range of marine environments, from inner platforms (e.g., shallow subtidal zones, reefs, and shorefaces) to outer platforms (e.g., deep subtidal zones, shelf-margin reefs, and offshore areas) (Bault et al., Reference Bault, Balserio, Monnet and Crônier2022). In contrast, during the middle Permian (Guadalupian), trilobites expanded their habitats to include shallower environments, e.g., foreshore, lagoonal, and delta-plain settings, as well as slope and basinal regions (Bault et al., Reference Bault, Balserio, Monnet and Crônier2022). However, in the late Permian (Lopingian), when trilobite diversity declined, occurrences in outer-platform and slope/basin settings significantly decreased (Bault et al., Reference Bault, Balserio, Monnet and Crônier2022). These trends suggest that benthic conditions, including depth- and substratum-related factors with relevant resource availability, played a key role in altering trilobite diversity (Hopkins, Reference Hopkins2014). However, the specific ecological characteristics of proetids that led to the adaptive radiation during the middle Permian remain poorly understood.
Recently, new evidence of a trilobite fauna became available from Japan, in which five genera of trilobites—Ampulliglabella Kobayashi and Hamada, Reference Kobayashi and Hamada1984, Cheiropyge, Ditomopyge Newell, Reference Newell1931, Neogriffithides Toumansky, Reference Toumansky1930, and Weania Campbell in Campbell and Engel, Reference Campbell and Engel1963—occurred in the muddy lithofacies of the middle Permian (Wordian) Hoso-o Formation in the Kamiyasse area of the Southern Kitakami Terrane (Flick and Shiino, Reference Flick and Shiino2021). According to taxonomic and biogeographic interpretations, the trilobite fauna in the Kamiyasse area includes both endemic (e.g., Ampulliglabella) and cosmopolitan (e.g., Cheiropyge and Ditomopyge) species, showing a variety of supposed feeding behaviors, e.g., predators/scavengers (e.g., Ampulliglabella, Ditomopyge, Neogriffithides, and Weania: Owens, Reference Owens2003; Flick and Shiino, Reference Flick and Shiino2021) and filter-chamber feeders (Cheiropyge: Owens, Reference Owens2003; Flick and Shiino, Reference Flick and Shiino2021). Of these, Ampulliglabella and Cheiropyge also occur in similar lithofacies of the Kurosawa Formation in the Omote-matsukawa area (~ 4 km south of the Kamiyasse area), which is the youngest formation of the middle Permian in this area (Kobayashi and Hamada, Reference Kobayashi and Hamada1984, upper part of the Kanokura Formation). In contrast, the Kamiyasse Formation (Capitanian), overlying the Hoso-o Formation and underlying the Kurosawa Formation, has yielded only the phillipsiide trilobite Pseudophillipsia (Pseudophillipsia) spatulifera Kobayashi and Hamada, Reference Kobayashi and Hamada1980 so far (Kobayashi and Hamada, Reference Kobayashi and Hamada1980; Shiino et al., Reference Shiino, Suzuki and Kobayashi2011). Given that the sedimentary environments of the Hoso-o and Kurosawa formations were deeper and more offshore than that of the Kamiyasse Formation, differences in trilobite assemblages are more likely attributable to local shifts in facies rather than larger scale evolutionary patterns.
A clue to understanding middle Permian trilobite diversity is the resources available in their habitat. The benthic habitat can be determined not only from sedimentary lithology but also from the burial processes of trilobite fossils (e.g., Speyer and Brett, Reference Speyer and Brett1985; Hughes and Cooper, Reference Hughes and Cooper1999; Hunda et al., Reference Hunda, Hughes and Flessa2006). However, determining whether trilobites were preserved in situ (autochthonous) or transported post-mortem (allochthonous) cannot be explained by a single hypothesis because their exoskeletons are highly prone to disarticulation soon after death, often obscuring their original depositional context (Speyer, Reference Speyer and Donovan1991).
The aim of this study is to describe the middle Permian phillipsiide trilobite Pseudophillipsia from the Kamiyasse Formation in the Southern Kitakami Terrane, Japan, with a focus on its detailed morphology and preservation. Analyses of polished rock slabs and sequential images obtained through microfocus X-ray computed tomography (CT) provided the basis for biostratinomic interpretation. Based on the results, we examined the burial processes of trilobites, which are essential for the reconstruction of their habitats, to thus gain an insight into middle Permian trilobite diversity.
Geological setting
The Permian shelly sequence of the Southern Kitakami Terrane is well exposed in the Kamiyasse area of Kesennuma City, Miyagi Prefecture, northeastern Japan (Tazawa, Reference Tazawa1973, Reference Tazawa2016; Misaki and Ehiro, Reference Misaki and Ehiro2004; Shiino et al., Reference Shiino, Suzuki and Kobayashi2011; Fig. 1). The strata of the study area consists of four formations, in ascending order: the Nakadaira Formation, Hoso-o Formation, Kamiyasse Formation, and Kurosawa Formation (Misaki and Ehiro, Reference Misaki and Ehiro2004). Of these, the Kamiyasse Formation has yielded a variety of fossils, including the trilobites considered during this study (Kobayashi and Hamada, Reference Kobayashi and Hamada1980; Reference Kobayashi and Hamada1984). Based on biostratigraphic studies using fusulines and cephalopods, the Kamiyasse Formation has been correlated with Capitanian in the current international timescale (Misaki and Ehiro, Reference Misaki and Ehiro2004; Shiino et al., Reference Shiino, Suzuki and Kobayashi2008, Reference Shiino, Suzuki and Kobayashi2011; Kobayashi et al., Reference Kobayashi, Shiino and Suzuki2009). More information on the local geology is provided in Supplementary Data 1, and the distribution of trilobite species in various stratigraphic sections is shown in Supplementary Figure S2.
Figure 1. Locality map and columnar section along the surveyed routes: (1) location of the Kamiyasse area; (2) geological map along the Imo-sawa, Tateishi-sawa, Minami-sawa, Toya-sawa, Shigeji-sawa, and Doya-sawa Creeks in the Kamiyasse area, showing fossil localities; (3) columnar section of route Ss1–3; the generalized columnar section and its stratigraphic age were modified from Shiino et al. (Reference Shiino, Suzuki and Kobayashi2008, Reference Shiino, Suzuki and Kobayashi2011), Kobayashi et al. (Reference Kobayashi, Shiino and Suzuki2009), and Masunaga and Shiino (Reference Masunaga and Shiino2021).
The Kamiyasse Formation is subdivided into two units (Shiino et al., Reference Shiino, Suzuki and Kobayashi2011; Fig. 1.3). The lower unit, so-called unit-3, is characterized by calcareous mudstone with abundant skeletal debris and poorly sorted fine-grained sandstone. The upper unit, so-called unit-4, is characterized by alternating beds of fine-grained sandstone and thin, fossiliferous layers (Shiino and Suzuki, Reference Shiino and Suzuki2007; Shiino et al., Reference Shiino, Suzuki and Kobayashi2011).
The base of unit-3 starts with medium- to coarse-grained sandstone, showing hummocky cross stratification (Shiino et al., Reference Shiino, Suzuki and Kobayashi2011). The overlying calcareous mudstone consists of abundant skeletal remains, e.g., brachiopods (e.g., Leptodus sp. indet.), tubular sponges, bryozoans, and bivalves. The shells are commonly truncated without abrasion but some skeletal remains, e.g., fenestrate bryozoans and productid brachiopods, exhibit their original life postures. The poorly-sorted, very fine-grained sandstone beds consist of thin layers of fragmented skeletal remains that contain brachiopods, vinculariiform bryozoans, tubular sponges, and the fusuline Monodiexodina sutchanica Dutkevich, Reference Dutkevich and Likharev1939.
The base of unit-4 starts with matrix-supported conglomerates, showing a sharp, erosive base (Shiino et al., Reference Shiino, Suzuki and Kobayashi2011). The overlying very fine-grained sandstone is poorly sorted because of extensive bioturbation that generally destroyed the primary sedimentary structures. The very fine-grained sandstone includes several fossiliferous layers consisting of brachiopods (e.g., Waagenoconcha imperfecta Prendergast, Reference Prendergast1935), crinoid columns, bryozoans, and bivalves. The components of the assemblages are commonly disarticulated and exhibit a convex-up orientation. In contrast, the bryozoans and Waagenoconcha imperfecta in the sandy layers exhibit their original life postures.
During the middle Permian, the Kamiyasse Basin was located at low- to mid-latitudes at the western side of Panthalassa (Ehiro, Reference Ehiro2015; Tazawa, Reference Tazawa2016). Based on the sedimentary analysis, the sedimentary environment of unit-3 began in the lower shoreface as indicated by hummocky cross stratification, and the overlying calcareous mudstone was more likely formed in a deeper offshore setting (Shiino et al., Reference Shiino, Suzuki and Kobayashi2011). Fragmented reef-building corals in unit-3 suggest the presence of a reef nearby, where bryozoans, sponges, and brachiopods flourished. The fossiliferous layers of unit-4 were formed by distal storm flows in an offshore to outer shelf environment (Shiino et al., Reference Shiino, Suzuki and Kobayashi2011). Both units yielded outstretched, enrolled, and exuviae trilobite specimens although it is still unclear if these specimens are autochthonous or allochthonous.
Materials and methods
Fossil specimens
For the taxonomic study, we used 236 trilobite specimens collected from the calcareous mudstone and the very fine-grained sandstone of unit-3 and unit-4 of the Kamiyasse Formation, respectively (Table 1). Although the holotype specimen of Pseudophillipsia (Pseudophillipsia) spatulifera (UMUT PA16699) has been lost, its plaster cast was used for taxonomic comparisons and to examine a mode of occurrence. Almost all of the specimens exhibited cast-and-mold preservation and lacked original skeletal material. To reconstruct the original morphology of the trilobites, the silicone putties Exafast and Exafine (GC, Japan) were used to create replicas for photographs. Figure 2 shows schematic illustrations of the trilobites present along with the terminology adopted herein, which was based on Whittington (Reference Whittington and Kaesler1997b).
Table 1. Abundance of preservation modes in Pseudophillipsia (Pseudophillipsia) spatulifera Kobayashi and Hamada, Reference Kobayashi and Hamada1980 and Pseudophillipsia (Carniphillipsia) cf. P. (Carniphillipsia) raggyorcakaensis Qian, Reference Qian1981. *Complete, outstretched specimens of Pseudophillipsia (Pseudophillipsia) spatulifera includes the holotype material (UMUT PA16699)
Figure 2. Morphological terminology of the present trilobites. The schematic illustrations are based on Pseudophillipsia (Pseudophillipsia) spatulifera Kobayashi and Hamada, Reference Kobayashi and Hamada1980.
Preparation of polished sections
To analyze the sedimentary and biostratinomic characteristics, a total of 21 rock samples were collected from unit-3 (8 samples) and unit-4 (13 samples) of the Kamiyasse Formation. The rock samples were cut using a rock cutter, and the surfaces in vertical view were initially ground with 150-grit silicon carbide abrasives (Nichika Inc., Japan) to produce a rough surface. Final polishing was performed using 600-grit silicon carbide abrasives (Nichika Inc., Japan) to prepare the polished cross-sectional rock slabs. Based on the observations of outcrops and polished rock slabs, ichnogenera of trace fossils were identified according to morphological criteria described by Knaust (Reference Knaust2017) and Ishizaki and Shiino (Reference Ishizaki and Shiino2023).
Three-dimensional modeling
To investigate the internal structure of the fossil specimens, sequential cross-sectional images were obtained using microfocus X-ray CT, MCT225 (Nikon Corporation, Japan) at the Industrial Research Institute of Niigata Prefecture. Subsequently, the volume data were converted into surface morphological data in a Standard Triangulation Language (STL file type) format using the image-based modeling software InVesalius (Centro de Tecnologia da Informação Renato Archer, Brazil).
Repositories and institutional abbreviations
All specimens examined during this study are deposited in the collections of the University Museum, the University of Tokyo (UMUT), Japan.
Systematic paleontology
Class Trilobita Walch, Reference Walch1771
Order Proetida Fortey and Owens, Reference Fortey and Owens1975
Family Phillipsiidae Oehlert, Reference Oehlert1886
Subfamily Ditomopyginae Hupé, Reference Hupé and Piveteau1953
Genus Pseudophillipsia Gemmellaro, Reference Gemmellaro1892
Type species
Pseudophillipsia (Pseudophillipsia) sumatrensis (Roemer, Reference Roemer1880), from the Wordian of the western coast of Sumatra, Indonesia.
Subgenus Pseudophillipsia ( Pseudophillipsia ) Gemmellaro, Reference Gemmellaro1892
Remarks
The genus Pseudophillipsia was founded on Phillipsia sumatrensis Roemer, Reference Roemer1880 by Gemmellaro (Reference Gemmellaro1892). This genus is characterized by a relatively flat cephalon with the glabella declining anteriorly; a bulbous anterior border; generally possessing L2–L4, always presenting the median preoccipital lobe; a very long pygidium with 14–31 axial rings and 8–18 pleural ribs, axis trapezoidal in transverse view and extending far posteriorly to the well-separated marginal border (Owens, Reference Owens, Briggs and Lane1983; Hahn et al., Reference Hahn, Hahn and Yuan1989, Reference Hahn, Hahn and Brauckmann2001).
Genus Pseudophillipsia consists of three subgenera: Pseudophillipsia, Carniphillipsia Hahn and Braukmann, Reference Hahn and Brauckmann1975, and Nodiphillipsia Kobayashi and Hamada, Reference Kobayashi and Hamada1984. Originally, Hahn and Braukmann (Reference Hahn and Brauckmann1975) divided Pseudophillipsia into Pseudophillipsia (Pseudophillipsia) and Pseudophillipsia (Carniphillipsia). The subgenus Pseudophillipsia, mainly occurring in the upper Permian, is characterized by broad and deep lateral glabellar furrows forming a garland-like structure called festooning; and a pygidium with 20–27 axial rings and 12–17 pleural ribs (Kobayashi and Hamada, Reference Kobayashi and Hamada1984; Hahn et al., Reference Hahn, Hahn and Brauckmann2001). The subgenus Carniphillipsia is characterized by a rounded pyriform glabella; weakly incised or missing lateral glabellar furrows; a very distinct preoccipital lobe; and a long pygidium with 17–21 axial rings and 9–13 pleural ribs (Owens, Reference Owens, Briggs and Lane1983; Kobayashi and Hamada, Reference Kobayashi and Hamada1984; Hahn et al., Reference Hahn, Hahn and Yuan1989, Reference Hahn, Hahn and Brauckmann2001). The cephalon of Pseudophillipsia (Carniphillipsia) is similar to that of the genus Ditomopyge, but the former has an elongated pygidium (Owens, Reference Owens, Briggs and Lane1983). Based on this similarity, it is possible that Carniphillipsia should be treated as a subgenus Ditomopyge rather than Pseudophillipsia (see Mychko, Reference Mychko2025).
Kobayashi and Hamada (Reference Kobayashi and Hamada1984) established a new subgenus, Pseudophillipsia (Nodiphillipsia), based on the presence of lateral glabellar nodes instead of the festooning lateral glabellar lobes. This subgenus is defined by three pairs of lateral glabellar nodes or tubercles in place of the lateral lobes; effaced lateral glabellar furrows; and a pygidium with 22–28 or more axial rings and 10–18 pleural ribs (Kobayashi and Hamada, Reference Kobayashi and Hamada1984). However, Hahn et al. (Reference Hahn, Hahn and Brauckmann2001) suggested that the difference between lateral glabellar nodes and lateral lobes is not a diagnostic feature, but a preservation problem of whether the specimen exhibits an external or internal mold. Consequently, Hahn et al. (Reference Hahn, Hahn and Brauckmann2001) defined Pseudophillipsia (Nodiphillipsia) as having a highly specialized blade-like genal spine as observed in Pseudophillipsia (Pseudophillipsia) spatulifera. Recently, Lerosey-Aubril and Angiolini (Reference Lerosey-Aubril and Angiolini2009) proposed the diagnosis of this subgenus as a cephalic border composed of a flat and rather wide rim with a crest at its margin; a partially upturned cephalic doublure with a V-shaped cross section; and a blade-like genal spine.
However, there are some issues with the definition of Pseudophillipsia (Nodiphillipsia). First, the genal spines of most specimens of Pseudophillipsia (Nodiphillipsia) are broken; thus, the identification of whether the spines have a blade-like shape must rely on the base of the genal spine. The vertically-wide base of genal spine, possibly a blade-like genal spine, is known not only in Pseudophillipsia (Nodiphillipsia) but also in Pseudophillipsia (Carniphillipsia) (e.g., Pseudophillipsia kemerensis Lerosey-Aubril and Angiolini, Reference Lerosey-Aubril and Angiolini2009; Pseudophillipsia sagittalis Kobayashi and Hamada, Reference Kobayashi and Hamada1978). In addition, a flat and wide cephalic border of Pseudophillipsia (Pseudophillipsia) spatulifera as shown in Kobayashi and Hamada (Reference Kobayashi and Hamada1980, fig. 3) occasionally occurs by means of secondary deformation whereby the anterior border has suffered vertical compaction as observed in the present study (Fig. 3.7–3.15). Consequently, the valid characteristics of Pseudophillipsia (Nodiphillipsia) only apply to Pseudophillipsia obtusicauda (Kayser, Reference Kayser and von Richthofen1883) and Pseudophillipsia aff. Pseudophillipsia obtusicauda; therefore, we consider Nodiphillipsia to be a junior subjective synonym of Pseudophillipsia.
Figure 3. The complete exoskeletons and cephalon of Pseudophillipsia (Pseudophillipsia) spatulifera Kobayashi and Hamada, Reference Kobayashi and Hamada1980: (1) silicone rubber cast of the holotype specimen (UMUT PA16699); (2) lateral view of (1); (3) lateral view of an incomplete enrolled specimen (UMUT PA34243); most of the pygidium is covered by rock; (4) three-dimensional (3D) model of (3); (5) magnified thoracic segments of (4); (6) lateral view of a complete enrolled specimen (UMUT PA34241); (7) outstretched specimen (UMUT PA34238); the specimen suffered vertical compaction; (8) 3D model, dorsal view, of (7); (9) lateral view of (8); (10) ventral view of (8); (11) detail of (10); (12) a cephalon lacking right side of free cheek (UMUT PA34266); (13) 3D model, dorsal view, of (11); (14) lateral view of (12); (15) ventral view of (12). ap, apodeme; fa, fossular apodeme; fs, fossula; poa, postannulus; pra, preannulus.
Pseudophillipsia ( Pseudophillipsia ) spatulifera Kobayashi and Hamada, Reference Kobayashi and Hamada1980
Reference Araki1961 Pseudophillipsia sp. indet.; Araki, p. 226, figs. 1–5.
Reference Endo and Matsumoto1962 Pseudophillipsia obtusicauda (Kayser, Reference Kayser and von Richthofen1883); Endo and Matsumoto, p. 115, pl. 1, figs. 1–3, 5, 6.
Reference Jimbo1966 Pseudophillipsia obtusicauda; Jimbo, p. 594, figs. 2, 3.
Reference Araki and Koizumi1968 Pseudophillipsia obtusicauda; Araki and Koizumi, p. 155, 156, pl. 1, figs. 1–4, pl. 2, fig. 7.
Reference Koizumi and Sasaki1978 Pseudophillipsia aff. Pseudophillipsia obtusicauda; Koizumi and Sasaki, p. 307, pl. 2, figs. 1–3.
Reference Kobayashi and Hamada1980 Pseudophillipsia spatulifera Kobayashi and Hamada, p. 196, figs. 1–3.
Reference Kobayashi and Hamada1984 Pseudophillipsia spatulifera; Kobayashi and Hamada, pl. 5, figs. 1–3, pl. 6, figs. 1–3, pl. 8, figs. 7, 8.
Reference Kobayashi and Hamada1984 Pseudophillipsia sasaki Kobayashi and Hamada, pl. 6, figs. 4–6.
Holotype
Outstretched, complete specimen (UMUT PA16699) from the Kamiyasse Formation, of the Southern Kitakami Terrane, Japan, (Kobayashi and Hamada, Reference Kobayashi and Hamada1980, p. 196, figs. 1, 2).
Materials
In addition to a plaster cast of the holotype (UMUT PA 16699), nine complete and 199 disarticulated specimens were collected (UMUT PA34238–34420). The smallest cranidium is 4.3 mm in length and 3.2 mm in width. The largest cranidium is 19.6 mm in length and 20.5 mm in width. The smallest pygidium is 1.6 mm in length and 1.1 mm in width. The largest pygidium is 23.8 mm in length and 24.6 mm in width.
Diagnosis (emended)
Cephalon with narrow anterior border and long, blade-like genal spines. Hypostome with three spines at posterior margin. Parabolic pygidium with 25 axial rings and 12 pleural ribs.
Occurrence
Shigeji-sawa, Imo-sawa, Tateishi-sawa, Toya-sawa, Minami-sawa, Doya-sawa and Chyaya-sawa in the Kamiyasse area, Kesennuma City, Miyagi Prefecture, Japan (Fig. 1; Supplementary Data 1). Here, the species occurs from the middle Permian Kamiyasse Formation, which correlates with the Midian in the Tethyan stage and the Capitanian in the current international timescale (Misaki and Ehiro, Reference Misaki and Ehiro2004; Kobayashi et al., Reference Kobayashi, Shiino and Suzuki2009). One-hundred fifteen specimens were collected from the mudstone and 17 specimens were collected from the sandstone of unit-3. Fifty specimens were collected from the sandstone of unit-4 in the area (Fig. 1; Supplementary Data 1).
Description
The cephalon and pygidium are similar in size (i.e., isopygous) whereas the thorax is slightly shorter.
The outline of the cephalon is parabolic in dorsal view (Fig. 3). In this view, the glabella is slightly elongated pyriform in outline and expands anteriorly three times the width of the posterior margin (Fig. 3.8, 3.12, 3.13). In lateral view, the glabella is raised moderately posterior to the preglabellar furrow, with the highest level near S4 to S3 in sagittal transect (Fig. 3.2, 3.14). Three pairs of lateral glabellar furrows extend adaxially from axial furrows (Fig. 4.1, 4.5, 4.6); S2 are deep and combine with each other at the midline (i.e., the transglabellar furrow), separating the median preoccipital lobe from the glabella; S3 are wide and shallow; S4 is similar to S3 but slightly shallower. Three pairs of lateral glabellar lobes are distinguished by lateral glabellar furrows (Fig. 4.1, 4.5, 4.6); L2, the largest lobes, are positioned at the posterolateral corners of glabella; L3 are slightly smaller than L2; and L4 are the smallest lobes. The preoccipital lobe is narrower than the maximum width of the glabella (Figs. 3.1, 3.7, 3.8, 3.12, 3.13, 4.5, 4.6). It is subdivided by a pair of preoccipital furrows (S1) into a pair of lateral preoccipital lobes (L1) and median preoccipital lobe (Fig. 4.1, 4.5, 4.6). Deep and narrow preoccipital furrows are arranged in the exsagittal direction, connecting with S2 and the occipital furrow at the anterior and posterior ends (Fig. 4.1, 4.5, 4.6). The lateral preoccipital lobes are long and taper anteriorly in dorsal view (Fig. 4.1, 4.5, 4.6). The median preoccipital lobe is wide and suboval (Fig. 3.7, 3.8, 3.12, 3.13). In lateral view, the level of the lateral preoccipital lobes and median preoccipital lobe is higher than that of palpebral lobe but is somewhat lower than that of the glabella (Fig. 3.2, 3.14). The occipital ring is subpentagonal with a width similar to that of the preoccipital lobe in dorsal view (Figs. 3.1, 3.7, 3.8, 3.12, 3.13, 4.1, 4.5, 4.6). There is no median node on the occipital ring. In lateral view, the occipital ring is lower than the glabella and the median lobe (Fig. 3.2, 3.14).
Figure 4. The disarticulated components of cephalon and thorax of Pseudophillipsia (Pseudophillipsia) spatulifera Kobayashi and Hamada, Reference Kobayashi and Hamada1980: (1) silicon rubber cast, dorsal view, of external mold of a cephalothoraco (UMUT PA34247); (2) lateral view of (1); (3) 3D model, dorsal view, of a free cheek (UMUT PA34246); (4) lateral view of (3); (5) silicon rubber cast of external mold of the cranidium without palpebral lobes (UMUT PA34269); (6) internal mold of (5); (7) cross sectional view of 3D model of the outstretched specimen in Figure 3.7 (UMUT PA34238); (8) 3D model, ventral view, of the hypostome (UMUT PA34240); (9) lateral view of (8); (10) ventral view of the cephalon in Figure 3.3 (UMUT PA34243); (11) 3D model of a rostral plate (UMUT PA34243); (12) transverse view of a 3D model of a first thoracic segment (UMUT PA34240); (13) lateral view of (12); (14) dorsal view of (12) and the second thoracic segments; (15) silicon rubber cast of a magnified thoracopygon (UMUT PA34253); seventh, eighth, and ninth thoracic segments are articulated with pygidium. aw, anterior wing; cr, cranidium; db, doublure; es, eye socle; esf, eye socle furrow; fa, facet; fc, free cheek; hy, hypostome; lg, lateral glabellar lobe; or, occipital ring; pl, preoccipital lobe; pw, posterior wing; rp, rostral plate; sor, subocular ridge.
The periphery of the cephalon is characterized by quite narrow anterior borders, lateral borders, and genal spines. The anterior border is very narrow and almost disappears near the midline, which fuses with the anteriormost part of the glabella. The border furrow is deep and bends adaxially at a level slightly posterior to that of the occipital ring, forming a pair of V-shaped border furrows in the posterolateral regions of the cephalon (Fig. 3.1, 3.8, 3.12, 3.13). The preglabellar furrows are distinct, connecting with the border furrow in the midline, and become deep toward the fossulae (Fig. 3.13, fs). The fossula is strongly concave, deepening toward the posteroventral direction, and can be observed in ventral view as a fossular apodeme (Figure 3.15, fa). The axial furrows are generally distinct except near the palpebral lobe (Fig. 3.12, 3.13). The anterior half of the axial furrows is shallow and wide but deepens and narrows toward the cephalic posterior border (Fig. 3.12, 3.13). In ventral view, the posteriormost part of the axial furrows is reflected as apodemes (Fig. 3.15: ap). The palpebral lobes have Landolt C-shaped outlines in dorsal view (Fig. 3.1, 3.8, 3.12, 3.13) and are subhorizontal in lateral and frontal views (Fig. 3.2–3.4, 3.6, 3.14). Holochroal eyes are suboval, never exceeding high above the palpebral lobe in lateral and frontal views (Fig. 3.2–3.4, 3.14). The eye socle beneath the visual surface is wide as well as half of the visual surface, with a faintly developed eye socle furrow (Fig. 4.1, 4.2). Faint subocular ridges extend from the lateral sides of the eyes, and the posterolateral corners are slightly inflated (Fig. 4.1, 4.2). Facial sutures are well developed (Fig. 3.12): α-β is short with the position of β situated more abaxially than δ; β-γ is long; ε-ω is parabolic; ω is situated more abaxially than β. Genal spines are long, bold, and blade-like in form (Figs. 3.8, 4.3, 4.4). In the best-preserved specimen with a cephalon length of 1.1 cm, the posterior ends of the genal spines extend to the fifth thoracic segment (Fig. 3.1, 3.8). In lateral view, the posterior ends of the genal spines are cut off from the ventral corner of the tip, similar to a Japanese Samurai sword (Fig. 3.2, 3.9, 3.14).
In ventral view, the rostral suture is curved with the outline of the anterior border, which is the boundary of the rostral plate (Figs. 3.15, 4.10). The rostral plate has a wide, subpentagonal outline with its anterolateral corners somewhat getting into the sutures between the anterior border and the cephalic doublure (Fig. 4.10, 4.11). The posture of the rostral plate and the adjacent part of cephalic doublure bend dorsally at ~ 45° (Fig. 4.7). The hypostome attaches to the rostral plate and the adaxial side of the cephalic doublures via a hypostomal suture situated at the middle of the glabella (Fig. 3.10, 3.11). The outline of hypostome is triangular and tapers posteriorly, and the posterior margin reaches to almost the same level of the median preoccipital lobe (Figs. 3.10, 3.11, 4.7–4.9). The anterior wings of the hypostome develop abaxially and dorsally to the fossular apodemes. The posterior wings are not very distinct. The hypostome has a narrow lateral border and a broad posterior border with three small spines (Fig. 4.8). The cephalic doublure is broad. There is no detailed information on the terrace ridge, macula, and pore because of the quality of fossil preservation.
The thorax consists of nine very similar thoracic segments (Figs. 3.1, 3.7, 4.1, 4.12–4.15). Each segment is subdivided into an axial ring and a pleura by deep axial furrows. The axial furrow results in well-developed apodeme in ventral and transverse views (Fig. 4.12). The axial ring is subdivided into the articulating half-ring, preannulus, and postannulus in the posterior order, with the boundaries of the horizontal furrows being the so-called articulating furrow and intra-annular furrow, respectively (Fig. 4.14). The articulating half ring is slightly narrower abaxially, and its lateral margin does not contact the pleura (Fig. 4.13, 4.14). In the case of enrolled specimens, most of the articulating half rings are almost hidden below the segment (or the occipital ring of the cephalon) in front (Fig. 3.5). The preannulus is wide and tapers abaxially, which is mostly exposed in enrollment (Fig. 3.5). The postannulus is narrower than the preannulus, but wider in the nearby axial furrow (Fig. 4.1, 4.2, 4.13, 4.14). The pleura is subdivided into an inner portion and outer portion by the geniculation of the fulcrum (Fig. 4.12). The inner portion of the pleura extends horizontally (Fig. 4.12). There are no pleural furrow or other sculptures in the inner portion (Fig. 4.1, 4.13–4.15). The outer portion of the pleura bends ventrally at ~ 75° to the inner portion (Fig. 4.12). The facet is situated in the anterior part of the outer portion and covers more than half of its area (Fig. 4.14, fa).
The outline of the pygidium is parabolic in dorsal view (Fig. 5.1, 5.4, 5.10–5.13). The pygidial border is broad and becomes narrow posteriorly. The maximum width of the axis is one-third of the pygidium width, slightly tapering posteriorly in dorsal view (Fig. 5.1, 5.4, 5.10–5.13) and is trapezoidal-shaped in transverse view (Fig. 5.3, 5.6, 5.8). In lateral view, the axis moderately decreases in height posteriorly and strongly bends posteroventrally near its posterior end (Fig. 5.2, 5.5). The axis consists of 25 axial rings with deep ring furrows (Fig. 5). The more posterior the axial ring, the shorter the length. In the internal surface of the axis, a short ridge (a furrow in an internal mold) extends from the pygidial border (Fig. 5.7, 5.8, white arrowheads). There is a pair of nodes in the lateral corner on the top of each axial ring (Fig. 5). The pleural region has 12 pleural ribs with deep pleural furrows (Fig. 5). The pleural ribs have rounded outlines in sagittal cross-sectional view, and the length and width of each pleural rib decreases posteriorly, similar to the axial rings (Fig. 5). The pleural furrows run obliquely from the axial furrow, running anteriorly in the adaxial part and posteriorly in the abaxial direction (Fig. 5). In the external surface of the pygidial doublure, a thin groove (a ridge in the internal mold) is present at the posterior end of the midline (Fig. 5.7, 5.8, black arrowheads), and terrace ridges are developed along the pygidial margin (Fig. 5.7, 5.8, 5.10).
Figure 5. The pygidium of Pseudophillipsia (Pseudophillipsia) spatulifera Kobayashi and Hamada, Reference Kobayashi and Hamada1980: (1) dorsal view of a moderately large pygidium (UMUT PA34391); (2) lateral view of (1); (3) posterior view of (1); (4) dorsal view of a moderately small pygidium (UMUT PA34328); (5) lateral view of (4); (6) posterior view of (4); (7) ventral view of silicon rubber cast of internal surface of pygidium (UMUT PA34251); (8) internal mold of (7); (9) dorsal view of pygidium (UMUT PA34374); original exoskeleton is partially preserved; (10) internal mold of a pygidium (UMUT PA34239); (11) internal mold of a pygidium (UMUT PA34288); (12) silicon rubber cast of an external mold of a pygidium (UMUT PA34397); (13) internal mold of the smallest pygidium (UMUT PA34405). White arrowheads mark a short ridge (furrow in internal mold) extending from pygidial border.
Remarks
The morphology of Pseudophillipsia (Pseudophillipsia) spatulifera is similar to those of Pseudophillipsia obtusicauda, Pseudophillipsia hanaokensis Kobayashi and Hamada, Reference Kobayashi and Hamada1984, Pseudophillipsia ozawai Kobayashi and Hamada, Reference Kobayashi and Hamada1984, and Pseudophillipsia sasaki Kobayashi and Hamada, Reference Kobayashi and Hamada1984. The present species is very similar to Pseudophillipsia obtusicauda in the lateral glabellar lobes, occipital ring, and pygidium (Kobayashi and Hamada, Reference Kobayashi and Hamada1984), but differs in having a larger median lobe. Pseudophillipsia hanaokensis and Pseudophillipsia ozawai each have a cranidium and pygidium similar to the present species (Kobayashi and Hamada, Reference Kobayashi and Hamada1984), in which the pygidium shows a different number of pleural ribs—Pseudophillipsia (Pseudophillipsia) spatulifera, 12 pleural ribs; Pseudophillipsia hanaokensis, 10 or 11 pleural ribs; Pseudophillipsia ozawai, 17 pleural ribs. In addition, Pseudophillipsia hanaokensis has a tubercle on the center of the occipital ring, but this is absent in Pseudophillipsia (Pseudophillipsia) spatulifera.
According to a previous study (Kobayashi and Hamada, Reference Kobayashi and Hamada1984), Pseudophillipsia sasaki has a thick, rounded anterior border, which seems to be unique to this species. However, our specimens show both types of anterior borders in Pseudophillipsia sasaki and Pseudophillipsia (Pseudophillipsia) spatulifera as variations due to secondary deformation. Based on this observation, we have synonymized Pseudophillipsia sasaki with Pseudophillipsia (Pseudophillipsia) spatulifera.
There is no direct evidence of the relationship between the cephalon and hypostome in Pseudophillipsia, but our results clearly show that the genus has an impendent type of hypostome caused by the glabella extending anteriorly (Fortey, Reference Fortey1990). In ventral view, the cephalon of Pseudophillipsia resembles that of the Carboniferous Phillipsiidae Griffithides acanthiceps Woodward, Reference Woodward1883. Although the hypostome of Pseudophillipsia (Pseudophillipsia) spatulifera has a narrower doublure laterally and posteriorly than that of G. acanthiceps, both species have the rostral plate extending dorsally, indicating that the hypostome is raised slightly above the substratum. According to Whittington (Reference Whittington1988), proetid hypostomes, e.g., Proetus Steininger, Reference Steininger1831 and Paladin Weller, Reference Weller1936, are situated more ventral to the cephalic margin in lateral view. Such a difference in the hypostomal position could suggest a difference in the feeding strategy of proetid trilobites. The ventral disposition of the hypostome in Pseudophillipsia (Pseudophillipsia) spatulifera might lead to a narrower space in the stomach cavity, although expanding the glabella forward could compensate for any reduction in size of the stomach due to the position of the hypostome, as observed in the morphological trend of proetid trilobites (Fortey and Owens, Reference Fortey and Owens1999).
Subgenus Pseudophillipsia ( Carniphillipsia ) Hahn and Braukmann, Reference Hahn and Brauckmann1975
Pseudophillipsia ( Carniphillipsia ) cf. Pseudophillipsia ( Carniphillipsia )
raggyorcakaensis Qian, Reference Qian1981
Figure 6. The disarticulated exoskeletons of Pseudophillipsia (Carniphillipsia) cf. Pseudophillipsia (Carniphillipsia) raggyorcakaensis Qian, Reference Qian1981: (1) internal mold of a cranidium lacking palpebral lobe (UMUT PA34423); (2) internal mold of a cranidium (UMUT PA34423); (3) internal mold, dorsal view, of the free cheek (UMUT PA34432); (4) external mold, lateral view, of (3); (5) internal mold of a thoracopygon (UMUT PA34421); (6) silicon rubber cast of external mold of a pygidium (UMUT PA34439); (7) silicon rubber cast of external mold of a pygidium (UMUT PA34438); (8) silicon rubber cast of external mold of a pygidium (UMUT PA34441); (9) internal mold of (7).
Figure 7. Schematic illustration of Pseudophillipsia (Carniphillipsia) cf. Pseudophillipsia (Carniphillipsia) raggyorcakaensis Qian, Reference Qian1981.
Type specimens
Two cranidia and one pygidium (NIGP 48373–48375), reported from Changhsingian, Raggyorcaka Formation, Shunanghu district, Xizang (Tibet), China (Qian, Reference Qian1981, p. 335, pl. 1, figs. 2–4), none of which was designated as the holotype. Therefore, all of the specimens are considered as syntypes under the International Code of Zoological Nomenclature (ICZN, 1999).
Materials
Fifty-five disarticulated specimens were used for identification (UMUT PA34420–34474). The smallest cranidium is 5.58 mm in length and 4.9 mm in width. The largest cranidium is 6.0 mm in length and 6.1 mm in width. The smallest pygidium is 5.9 mm in length and 3.8 mm in width. The largest pygidium is 8.2 mm in length and 7.4 mm in width.
Occurrence
Shigeji-sawa, Toya-sawa, Chyaya-sawa, and Minami-sawa in the Kamiyasse area, Kesennuma City, Miyagi Prefecture, Japan (Fig. 1; Supplementary Data 1). Here, the species occurs from the middle Permian Kamiyasse Formation, which correlates with the Midian in the Tethyan stage and the Capitanian in the current international timescale (Misaki and Ehiro, Reference Misaki and Ehiro2004; Kobayashi et al., Reference Kobayashi, Shiino and Suzuki2009). Fifty-five specimens occurred from the fine- to medium-grained sandstone of unit-4. One single pygidium occurred from the sandy mudstone of unit-3.
Description
The anterior border of the cranidium is broad and flat (Fig. 6.1, 6.2). The adjacent border furrow is broad and shallow and fuses with the preglabellar furrow at its extreme anterior (Fig. 6.1, 6.2). The preglabellar furrow is shallow in the anterior area and becomes deeper toward the fossulae (Fig. 6.1, 6.2). The axial furrows extend along the exsagittal line, both of which are shallower in the anterior half than in the posterior half (Fig. 6.1, 6.2). In dorsal view, the width of glabella is generally large in the anterior part, becoming much wider anterior to the fossula (Fig. 6.1, 6.2). No lateral glabella furrows or lateral lobes were observed. The preoccipital lobe is trisected by shallow preoccipital furrows into a pair of small lateral preoccipital lobes and one median preoccipital lobe (Fig. 6.2). The width of the occipital ring is similar to that of the preoccipital lobe. The lateral border of the free cheek is flat (Fig. 6.4). In dorsal view, the lateral and posterior border furrows are continuous and meet at an angle of ~ 90°, forming a V-shaped geniculation in the posterolateral region of the free cheek (Fig. 6.3). The posterior border is straight and directed laterally, forming a right angle where it joins the base of the genal spine (Fig. 6.3). The genal spine is relatively long and flat (Fig. 6.3, 6.4). The eye socle is one-quarter in width relative to the height of the visual surface (Fig. 6.4). Subocular ridges and subocular areas are faint (Fig. 6.3, 6.4).
The pygidium has a triangular outline in dorsal view (Fig. 6.5–6.9). The pygidial border broadens posteriorly (Fig. 6.5–6.9). The axis of the pygidium is long, narrows posteriorly in dorsal view, and is subdivided into ~ 24 axial rings by narrow ring furrows (Fig. 6.5–6.9). In transverse view, the axis is trapezoidal to semicircular in shape. The pleural region is subdivided into 13 or 14 pleural ribs by deep, narrow pleural furrows (Fig. 6.5–6.9).
Remarks
Based on the morphology of the cranidium and pygidium (Fig. 7), the present species is identified as belonging to the subfamily Ditomopyginae. Three candidate species are considered: juvenile Ditomopyge benkei Flick and Shiino, Reference Flick and Shiino2021, Pseudophillipsia (Pseudophillipsia) spatulifera, and Pseudophillipsia (Carniphillipsia) raggyorcakaensis. The present species is similar to that of juvenile D. benkei in having a cranidium with a broad anterior border and trisected preoccipital lobe, but differs in having flat lateral borders, much shorter genal spines, and a much larger number of ribs on the pygidium. Pseudophillipsia (Pseudophillipsia) spatulifera is also similar to the present species, but differs in having a cranidium with a narrow anterior border, distinct lateral glabella lobes, and a thick lateral border of the free cheeks. The cranidium and pygidium of the present species are very similar to those of Pseudophillipsia (Carniphillipsia) raggyorcakaensis, which is known only from cranidia and pygidia (Qian, Reference Qian1981). According to Qian (Reference Qian1981), the preoccipital lobe of Pseudophillipsia (Carniphillipsia) raggyorcakaensis is large and distinct, and that seems to differ from the present species. Such a difference is solely a morphological gap between the previous external and the present internal shapes. Based on the photograph of Pseudophillipsia (Carniphillipsia) raggyorcakaensis shown by Qian (Reference Qian1981), the pygidium seems to have more than 22 axial rings and more than 12 pleural ribs. It is still premature to assign it to a particular species, hence we describe it here as Pseudophillipsia (Carniphillipsia) cf. Pseudophillipsia (Carniphillipsia) raggyorcakaensis.
Results: occurrence and preservation of trilobites
All of the specimens of Pseudophillipsia (Pseudophillipsia) spatulifera and Pseudophillipsia (Carniphillipsia) cf. Pseudophillipsia (Carniphillipsia) raggyorcakaensis occur in the fossiliferous sandstone and mudstone of the Kamiyasse Formation. Of these, Pseudophillipsia (Pseudophillipsia) spatulifera is the dominant species, occurring frequently in both the sandstone and mudstone beds of the Kamiyasse Formation (Fig. 8; Table 1). In contrast, Pseudophillipsia (Carniphillipsia) cf. Pseudophillipsia (Carniphillipsia) raggyorcakaensis occurs less frequently than Pseudophillipsia (Pseudophillipsia) spatulifera, and is from the sandstone beds of unit-4 except for one specimen collected from the fossiliferous mudstone of unit-3. There are nine modes of preservation in the Kamiyasse Formation. Four of these involve articulated material represented by (1) outstretched individuals, (2) enrolled individuals, (3) cephalothoraxes, and (4), thoracopyga. The others are various disarticulated sclerites, represented by (5) cephala, (6) cranidia, (7) free cheeks, (8) thoracic segments, and (9) pygidia. Isolated pygidia represent the most abundant preservational mode (Table 1). In the case of Pseudophillipsia (Pseudophillipsia) spatulifera, pygidia account for 53 out of 84 specimens in the sandstone beds and 86 out of 126 specimens in the mudstone beds (Fig. 8; Table 1). In contrast, only nine complete specimens of Pseudophillipsia (Pseudophillipsia) spatulifera were collected from the sandstone beds, including only two outstretched specimens (Fig. 8; Table 1). In the mudstone beds, partially articulated specimens, e.g., cephalothoraxes and thoracopyga, were collected, but no single complete specimen was collected during this study.
Figure 8. Preservation modes of Pseudophillipsia (Pseudophillipsia) spatulifera Kobayashi and Hamada, Reference Kobayashi and Hamada1980 in sandstone and mudstone.
Occurrence in sandstone beds (complete specimens)
Based on the sedimentary structures present, the sandy lithofacies are divided into well-laminated, fine- to medium-grained sandstone, and bioturbated fine-grained sandstone (Fig. 9). The fine- to medium-grained sandstone occurs in < 20 cm thickness of each bed, with well-developed sedimentary structures, e.g., horizontal, swaley-, and planar-cross laminations. The layers just above the erosional base of cross laminations sometimes exhibit well-sorted fossiliferous layers of the fusuline Monodiexodina Sosnina, Reference Sosnina1965, the longitudinal axes of which are in a similar direction (Fig. 9.1, 9.6). The fine-grained sandstone beds show intense bioturbation, with 1–5 cm thickness of well-sorted fossiliferous layers including crinoid columns, bivalves, and productid brachiopods. The sedimentary structures parallel to the swaley-cross laminations are partially preserved, but almost all layers are homogenized by the bioturbation, resulting in poorly sorted sandstone with lens-like occurrences of skeletal debris (Fig. 9.2, 9.3, 9.7, 9.8).
Figure 9. Sedimentary facies and trilobite occurrence in sandstone: (1) vertical section of fine- to medium-grained sandstone with fusulines; lower part of fusulinid layer shows cross lamination; (2) vertical section of fine-grained sandstone with parallel to weakly crossed lamination; (3) vertical section of fine-grained sandstone; fossiliferous layers are discontinuous due to abundant bioturbation (white arrowheads); (4) lateral view of colorized 3D model showing an outstretched Pseudophillipsia (Pseudophillipsia) spatulifera; (5) trilobite assemblage with enrolled specimen; (6) plan view of fossiliferous layer with fusuline Monodiexodina Sosnina, Reference Sosnina1965; dashed circle shows a pygidium of Pseudophillipsia (Carniphillipsia) cf. Pseudophillipsia (Carniphillipsia) raggyorcakaensis; (7) plan view of fossiliferous layer with disarticulated crinoid columns; dashed circle shows a fragmented, abraded pygidium of Pseudophillipsia sp. indet.; (8) plan view of fossiliferous layer, including smaller skeletal remains of crinoids, bivalves, and Pseudophillipsia (Carniphillipsia) cf. Pseudophillipsia (Carniphillipsia) raggyorcakaensis (Prg) just above a layer with large cranidia of Pseudophillipsia (Pseudophillipsia) spatulifera (Psp) and bivalves. eb, erosional base; fl, fossiliferous layer; Ne, ichnofossil Nereites isp. indet.; Ph, ichnofossil Phycosiphon isp. indet.; Prg, Pseudophillipsia (Carniphillipsia) cf. Pseudophillipsia (Carniphillipsia) raggyorcakaensis; Psp, Pseudophillipsia (Pseudophillipsia) spatulifera; Rz, ichnofossil Rhizocorallium isp. indet.
Complete specimens of outstretched and enrolled Pseudophillipsia (Pseudophillipsia) spatulifera are rarely found in fine-grained sandstone. The outstretched specimen shows dorsal-side-up orientation, lying slightly above a fossiliferous layer with a vertically-grown vinculariiform bryozoan (Fig. 9.4). The lithofacies for the holotype of Pseudophillipsia (Pseudophillipsia) spatulifera is the fine-grained sandstone of the Kamiyasse Formation, although it is not clear whether the dorsal or ventral side is upward (Fig. 3.1, 3.2). Enrolled specimens sporadically occur in several bioturbated layers of unit-3 and unit-4 (Fig. 9.5), but not in the laminated layers. For fossil assemblages including the enrolled specimens, the skeletal debris shows a similar size including cephalothoraco, thoracopygon, cephalon, and pygidium, with random orientations in the bed (Fig. 9.5).
Cranidia and pygidia are frequently discovered in fossiliferous layers, sometimes showing fragmentation and abrasion (Fig. 9.7). There could be multiple occurrences of the same parts of similar size (Fig. 9.8). Among the specimens that enable determining the upward direction, most specimens of cranidium and pygidium occur in the convex-up orientation (Fig. 9.6, 9.8).
Occurrence of mudstone beds (disarticulated specimens)
The mudstone of unit-3 is characterized by abundant skeletal remains, including a variety of fossil taxa, e.g., trilobites, brachiopods, bryozoans, fusulines, sponges, and corals. In general, the skeletal remains are poorly sorted with a dispersed arrangement, partially forming packstone layers 1–2 cm thick (Fig. 10.1, 10.2). We divided it into sandy mudstone and fossiliferous mudstone based on the number of sandy grains (Figs. 1, 10). The sandy mudstone contains abundant trace fossils of Rhizocorallium isp. indet. that intersect and homogenize the layers of skeletal remains (Fig. 10.1, white arrowheads). The fossiliferous mudstone is similar to the sandy mudstone, but differs in trace fossils of Nereites isp. indet. and Phycosiphon isp. indet. instead of Rhizocorallium isp. indet. in the sandy mudstone (Fig. 10.2).
Figure 10. Sedimentary facies and trilobite occurrence in mudstone: (1) vertical section of sandy mudstone with abundant trace fossils of Rhizocorallium isp. indet.; white arrowhead points to the cross section shown in (4) and (5); (2) vertical section of fossiliferous mudstone; dashed circle shows a pygidium of Pseudophillipsia; (3) 3D model of Pseudophillipsia (Pseudophillipsia) spatulifera reconstructed using microfocus X-ray CT; (4, 5) selected tomographic images of 3D model in (3) showing several rows of trace fossils Rhizocorallium isp. indet. (dashed lines of spreite); (6) plan view of fossiliferous mudstone with brachiopod Leptodus sp. indet. and Pseudophillipsia (Pseudophillipsia) spatulifera (dashed circle); (7) cephalothoraco of Pseudophillipsia (Pseudophillipsia) spatulifera; (8) thoracopygon of Pseudophillipsia (Pseudophillipsia) spatulifera. cr, cephalon; fc, free cheek; fl, fossiliferous layer; Ne, ichnofossil Nereites isp. indet.; py, pygidium; Rz, ichnofossil Rhizocorallium isp. indet.; th, thoracic segment.
Although we could not find complete specimens, articulated specimens of cephalothoraco and thoracopygon occurred in the sandy mudstone and fossiliferous mudstone (Fig. 10.2–10.8). One specimen appears as a set of cephalothoraco and thoracopygon slightly far from each other, with several rows of trace fossil Rhizocorallium isp. indet. separating them (Fig. 10.3–10.5). Cephalons, cranidia, and pygidia of various sizes and orientations frequently occur in mudstone (Fig. 10.2, 10.6). Unlike the occurrence in sandstone, the trilobite fossils exhibited no fragmentation or abrasion.
Discussion
Biostratinomic interpretations of trilobite occurrences
When considering biostratinomic history, it is evident that trilobite skeletal remains can be preserved as fossils through multiple pathways (e.g., Speyer and Brett, Reference Speyer and Brett1986; Brett, Reference Brett1995). During their lifetimes, trilobites can become rapidly buried by sudden sedimentary events, resulting in the preservation of complete specimens (Brett and Baird, Reference Brett and Baird1998; Karim and Westrop, Reference Karim and Westrop2002; Fig. 11). However, after death, their skeletal remains experience various degrees of postmortem alteration, sometimes leading to disarticulation and reorientation (Brett et al., Reference Brett, Allison, Tsujita, Soldani and Moffat2006; Fig. 11). In addition to burial processes, disarticulated parts can result from dead individuals and exuvial remains. In trilobites except Phacopida, exuvial remains can be identified when cephalic parts, e.g., free cheek, rostral plate, and hypostome, are found separately (Whittington, Reference Whittington and Kaesler1997a; Drage, Reference Drage2019; Fig. 11). To understand trilobite habitats and ecology, it is essential to examine their burial processes.
Figure 11. Taphonomic pathways of trilobites. Trilobite specimens include dead individuals and exuvial skeletal remains, and the two can only be identified by the condition of cephalon in proetids.
According to a previous sedimentological study (Shiino et al., Reference Shiino, Suzuki and Kobayashi2011), the fine-grained sandstone in which the outstretched specimens occur forms alternating beds with fossiliferous layers during storm events. Within a bed of fine-grained sandstone, the intense bioturbation overlying the layer parallel to the swaley laminations suggests post-storm and fair-weather colonization by burrowing animals (Pemberton and MacEachern, Reference Pemberton, MacEachern, Brett and Baird1997). The outstretched specimens occur in a bioturbated horizon just above a thin fossiliferous layer at the base of a storm deposit, which could have been buried under the post-storm conditions.
Although all of the complete specimens occur in sandstone, the presence of outstretched and enrolled trilobites could reflect differences in the burial process. Enrolled trilobites are generally interpreted as biological reactions against predator attacks or environmental disturbances (e.g., Pompeckj, Reference Pompeckj1892; Berry, Reference Berry1929; Clarkson and Henry, Reference Clarkson and Henry1973; Babcock and Speyer, Reference Babcock and Speyer1987; Bruton and Haas, Reference Bruton and Haas1997). In the present study, the enrolled specimens were buried rapidly without releasing their defensive posture, suggesting that they responded to environmental changes rather than predator attacks. Oxygen-poor benthic conditions can induce trilobite enrollment as seen in extant arthropods (Babcock and Speyer, Reference Babcock and Speyer1987), but this is not the case with the present specimens because the intense bioturbation with sandy lithofacies indicates oxygenated benthic conditions (Orr, Reference Orr, Briggs and Crowther2001; Ishizaki and Shiino, Reference Ishizaki and Shiino2023). Instead, the present enrolled trilobites were likely to have been caught in storm flows and subsequently showed a defensive response as observed in Middle Devonian trilobites (Speyer, Reference Speyer1988). The cephalon and pygidium together with the enrolled specimens are similar in size, suggesting the sorting occurred during a storm event.
Based on the taphonomic pathway in trilobites (Fig. 11), the occurrence of the cephalon and cephalothoraco in fossiliferous mudstone of unit-3 represents individuals that were already dead and disarticulated. Unlike sandstone, the fossiliferous mudstone of unit-3 lacks a sedimentary structure indicative of high-energy events, e.g., storms or turbidity flows. Fenestrate bryozoans occasionally occur in life position in mudstone suggesting low-energy benthic conditions (Shiino et al., Reference Shiino, Suzuki and Kobayashi2011). However, the lenticular distribution of thin fossiliferous layers likely resulted from weak current activity that was able to sort small skeletal remains, e.g., crinoid columns and fragmented brachiopods and bryozoans. The dominance of isolated pygidia raises the possibility that sclerites were sorted by weak current activity (Adrain and Westrop, Reference Adrain and Westrop2016). In addition, the mudstone shows intense bioturbation that was enough to homogenize the original fossiliferous layers (Fig. 10.1). CT imaging revealed that the disarticulated parts are arranged in the same sequence as they were formed during enrollment, suggesting that the disarticulated remains originally represented complete enrolled trilobites (Fig. 10.3). It is likely that the set of disarticulated parts was originally enrolled individuals caught in a possible storm flow with sandy supply, eventually altered by the producers of Rhizocorallium isp. indet. Consequently, trilobites in the mudstone of unit-3 have suffered intense biological disturbances and weak fluid effects to become disarticulated specimens, as is also seen in obrution assemblages (e.g., Brett, Reference Brett1995; Brett et al., Reference Brett, Baird, Speyer, Brett and Baird1997).
A likely habitat of the present trilobites
Our results clearly demonstrate that both sandstone and mudstone in unit-3 and- 4 consist of a mix of allochthonous and autochthonous layers. Pseudophillipsia (Pseudophillipsia) spatulifera appears to have adapted to both sandy and muddy substrata, whereas Pseudophillipsia (Carniphillipsia) cf. Pseudophillipsia (Carniphillipsia) raggyorcakaensis predominantly inhabited the sandy substratum.
According to a previous sedimentological study, units-3 and -4 of the Kamiyasse Formation were believed to have been deposited offshore to the outer-shelf setting based on the characteristics of the storm deposits (Shiino et al., Reference Shiino, Suzuki and Kobayashi2011). However, this interpretation is inconsistent with the general depth zone, which places the outer shelf below the maximum storm wave base (e.g., Ando, Reference Ando1990; Mountain et al., Reference Mountain, Proust, Mclnroy and Cotterill2010). The sandstone of unit-4, previously interpreted as distal storm deposits on the outer shelf (Shiino et al., Reference Shiino, Suzuki and Kobayashi2011), contains a background sandy layer with intense bioturbated layers, indicating a shallow, low-energy benthic environment like a lower shoreface-offshore transition (Plint, Reference Plint, James and Dalrymple2010). Apart from the supposed sedimentary environment based on the depth zone, the unit-3 and -4 of the Kamiyasse Formation exhibit pronounced facies changes (Shiino et al., Reference Shiino, Suzuki and Kobayashi2011). This suggests that the sedimentary setting was not entirely open marine but somewhat sheltered even though the supposed depth zones are similar, as expected in an inner bay (MacEachern et al., Reference MacEachern, Pemberton, Gingras, Bann, James and Dalrymple2010). Such a supposedly protected environment could explain the presence of fragile skeletal animals of the brachiopod Leptodus sp. indet. and vinculariiform and fenestrate bryozoans (Shiino et al., Reference Shiino, Suzuki and Kobayashi2011).
Based on the present reinterpretation of sedimentary settings, it can be inferred that the two species of Pseudophillipsia adapted to different benthic conditions: Pseudophillipsia (Pseudophillipsia) spatulifera inhabited both sandy and muddy substrata, and Pseudophillipsia (Carniphillipsia) cf. Pseudophillipsia (Carniphillipsia) raggyorcakaensis mainly inhabited the sandy substratum (Fig. 12). Although the sandstone and mudstone of units-3 and -4 contain smaller amounts of organic materials compared to units-1 and -2, there was evidently sufficient food and oxygen to enable extensive bioturbation. A similar quiet habitat for Pseudophillipsia is known in Antalya Province, Turkey, where the sedimentary setting was a shallow, protected embayment (Lerosey-Aubril and Angiolini, Reference Lerosey-Aubril and Angiolini2009).
Figure 12. Taphonomic process of the trilobites in the Kamiyasse Formation. Complete, outstretched exoskeletons of trilobites and bryozoans are autochthonous (in situ), whereas enrolled, disarticulated exoskeletons of trilobites are para-autochthonous.
Future perspectives in shifts of the middle Permian trilobite diversity
Multiple trilobite genera are known from unit-1 of the Hoso-o Formation (Wordian), which underlies the Kamiyasse Formation, although quantitative data on generic abundances are lacking (Flick and Shiino, Reference Flick and Shiino2021). The decrease in the number of trilobite species from unit-1 to unit-4 could be closely related to the global decline in trilobite diversity observed after the Wordian-Capitanian boundary (e.g., Lerosey-Aubril and Feist, Reference Lerosey-Aubril, Feist and Talent2012). However, the trilobite faunas of the Kamiyasse area are clearly associated with sedimentary lithofacies, which reflect differences in benthic environments. Unit-1 records a relatively deep, organic-rich, outer shelf setting, which differs from the shallower environments of units-3 and -4. In the study area, only Pseudophillipsia occurs in shallow, restricted benthic habits, which supports local environmental controls of the diversity decline.
The genus Pseudophillipsia has been regarded as a cosmopolitan, thermally tolerant, and eurytopic taxon, and thus an ecological generalist (Brezinski, Reference Brezinski2023). Meanwhile, a paleobiogeographic analysis of brachiopods during the late Paleozoic Ice Age demonstrated that tropical faunas occupied narrower latitudinal ranges and exhibited more endemic characteristics (Powell, Reference Powell2005). The genus Pseudophillipsia is also known to have adapted to relatively shallow and warm marine conditions, which is consistent with the supposed endemic ecology of Pseudophillipsia (Pseudophillipsia) spatulifera described in this study.
The genus Pseudophillipsia is loosely identified with the possession of many segments in the pygidium, although a less conservative definition might suggest a parallel evolutionary shift regarding adaptation to specific environmental settings. Further investigation into the relationship between taxonomy and their environmental conditions could provide deeper insights into Permian trilobite diversity and their adaptive, evolutionary, and extinction histories.
Acknowledgments
We gratefully acknowledge F. Ulrich (Tohoku Gakuin University), Y. Ishizaki (University of Tokyo), A. Matsuoka (Niigata University), T. Kurihara (Niigata University), and H. Ueta (Niigata University) for thorough discussion. We are also grateful to Y. Takaizumi (Michinoku Amateur Paleontologists’ Club), Y. Suzuki (Shizuoka University), the Board of Education, Kesennuma city, H. Araki and K. Sasaki for provision of fossil specimens and helpful support of our investigations. T. Nagai (Industrial Research Institute of Niigata Prefecture) technically supported us in operating the microfocus X-ray CT. Thanks are also due to reviewers. This study was financially supported in part by the JSPS KAKENHI Grant Number 22K03795 and 20K04147.
Competing interests
The authors declare no competing interests in this manuscript.
Data availability statement
Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.02v6wwqj4
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