A palynological study was conducted for the first time on the Lower Devonian Nakazato Formation in the South Kitakami Belt, northeast Japan. The palynomorphs were primarily examined using a scanning electron microscope as they exhibited opaqueness due to very high thermal maturity and coalification. The palynological assemblage comprises cryptospores, spores, tubular remains and conducting structures. However, species-level identification was proven challenging for many obtained palynomorphs. Nevertheless, the assemblage exhibited notable similarities to the Pragian to early Emsian palynoassemblages from South China in terms of composition and representation of genera. The age estimate derived from the palynological data slightly predates those obtained from marine invertebrates (Emsian to Givetian). To reconcile this discrepancy, a comprehensive comparison between terrestrial and marine biostratigraphies in Asia is necessary.
Introduction
The Silurian–Devonian is a key period for understanding the process of terrestrialization and early diversification of embryophytes (Richardson, 1996). The Early Devonian witnessed major innovations in plants with the rise of early terrestrial ecosystems (Kenrick and Crane, 1997; Edwards and Richardson, 2004). The Lochkovian was characterized by an extinction of primitive rhyniophytes and a diversification of the zosterophylls and lycophytes, with in particular an increase in plant size and complexity of body architectures (e.g. Fanning et al., 1992; Edwards et al., 2014). These plants have produced a more diverse and larger quantity of spores than previously (e.g. Morris and Edwards, 2014). Then, Cladoxylopsida, the possible ancestral lineage of the monilophytes, appeared by the late Emsian (e.g. Stein and Hueber, 1989; Kenrick and Crane, 1997), while progymnosperms emerged by the early Givetian (Schweitzer, 1999).
The geologic settings of Japan for pre-Mesozoic ages are very complicated due to the extensive tectonic activities (Wakita et al., 2018). In Japan, Silurian to Devonian fossil-bearing sediments are mainly distributed in three terranes: the Hikoroichi and Arisu areas of South Kitakami Terrane in Northeast Japan, the Fukuji and Kuzuryu areas of the Hida Gaien Terrane in central Japan, and the Yokokurayama area of Shikoku and Gionyama area of Kyushu included in the Kurosegawa Terrane in Southwest Japan (Kato et al., 1980; Williams et al., 2014; Isozaki, 2019). These sediments yield a rich fauna dominated by corals but also include a wide range of biostratigraphically informative taxa such as trilobites, brachiopods, ostracods, etc. (e.g. Kobayashi and Hamada, 1977; Tazawa and Chen, 2001; Williams et al., 2014). On the contrary, there exist only a few reports on terrestrial plant remains from the Siluro–Devonian of Japan, except for Cyclostigma, Leptophloeum (Protolepidodendrales, Lycophyta) and Aphyllopteris (unclassified) reported from the Upper Devonian Tobigamori Formation in Iwate Prefecture, Northeast Japan (Tachibana, 1950, 1959), the Rosse Formation in Gifu Prefecture, central Japan (Tazawa et al., 2000), and the Naidaijin Formation in Kumamoto Prefecture, Southwest Japan (Kimura et al., 1986).
Figure 1.
Location of the sampling site where the Nakazato Formation outcrops. A, Location of Ofunato City, Iwate Prefecture, Northeast Japan. B, Location of the studied area along the upper stream of the Higuchizawa river, northwest of Ofunato City. C, Geological map of the Hikoroichi area modified from Editorial Committee of TOHOKU, Part 2 of Regional Geology of Japan (1989).
Here, we report a new plant microfossil assemblage obtained from the Lower Devonian Nakazato Formation of the South Kitakami Belt, Northeast Japan. The microfossil assemblage is compared to those reported from the South China block where the South Kitakami Belt was placed closely during the Early Devonian. We also attempt to infer the paleovegetation of Japan during the Early Devonian for the first time.
Geologic setting
The South Kitakami Belt consists of early Paleozoic igneous and metamorphic basement rocks covered by shallow marine sediments deposited from the late Ordovician to early Cretaceous (Ehiro et al., 2016). Silurian and Devonian sediments are mainly outcropping in the Hikoroichi and Arisu areas of Iwate Prefecture. In the Hikoroichi area, they are represented by the Kawauchi, Ohno and Nakazato formations in ascending order. The Nakazato Formation (originally named “Nakazato Group” by Yabe and Sugiyama, 1937) conformably overlies the Ohno Formation and is probably unconformably overlain by the Tobigamori Formation (Suzuki and Minato, 1958; Kato et al., 1980). It is estimated to be more than 750 m in thickness, consisting predominantly of volcaniclastic rocks (Minato et al., 1974). The Nakazato Formation has been divided into the N1 to N4 members in ascending order (Minato et al., 1979). The N3 Member, from which samples of the present study were collected, consists of alternating sandstone and mudstone beds. This member had been assigned to the Emsian to Givetian age based on trilobites (Kobayashi and Hamada, 1977). Kaneko (2007) further constrained the trilobite-bearing strata of the N3 Member to the latest Emsian (Early Devonian) to earliest Eifelian (Middle Devonian) based on biostratigraphic correlation by trilobites.
Figure 2.
Route map (left) and columnar section (right) of the sampling site. Occurrences of palynomorphs are shown along with sampling horizons and key beds. Loc. 1, trilobite-bearing layer; Loc. 2, tuffaceous sandstone (N20°E, 90°); Loc. 3, tuffaceous sandstone (N10°E, 90°); Loc. 4, trilobite-bearing layer; Loc. 5, muddy sandstone (N16°E, 90°).
Material and methods
We collected 22 mudstone samples from the Nakazato Formation in the Hikoroichi area of the South Kitakami Belt, outcropping along the upper stream of the Higuchizawa river, around 5 km northwest of Ofunato City, Iwate Prefecture, Northeast Japan (39° 06′ 59″ N, 141° 40′ 20″ E; Figures 1, 2). Brachiopods and corals were observed on the field in many horizons when collecting the samples along with trilobites including Rhinophacops suggesting age of the Emsian/Eifelian boundary (Kaneko, 2007).
Microfossils were extracted following the methods of Legrand et al. (2021). Samples were crushed into small pieces, then immersed in cold 50% hydrofluoric acid for 24 hours, followed by a treatment in hot 36% hydrochloric acid until reaching the boiling point. After sieving, the fraction with a diameter between 10 and 125 µm was oxidized with 69% nitric acid in a boiling water bath. The organic residue was concentrated by centrifugation and mounted on slides with Canada balsam. Palynomorphs were observed under a differential interference contrast microscope (DM 2500, Leica, Wetzlar, Germany). The position of palynomorphs on the slide was recorded using an England Finder graticule (Pyser Optics, Edenbridge, England). Palynomorphs are of very high thermal maturity and remained black and opaque even after the oxidation, thus identifications are largely based on the scanning electron microscope (SEM) images. Due to this suboptimal preservation state, most palynomorphs could not be identified to species level, while some were assigned or conferred to a known species. Microfossils for SEM observation were mounted on aluminum stubs, coated with platinum using a magnetron sputter coater (JUC-5000, JEOL, Tokyo, Japan), and observed under a SEM (JSMIT100, JEOL). Terminology and classification of miospores follows the scheme of Grebe (1971) and Wellman and Richardson (1993). Classification of tubular remains follows the artificial classification proposed by Burgess and Edwards (1991). Samples and residues are housed in the Palynological collections of the Department of Geosciences, Faculty of Science, Shizuoka University, Japan. The microscopic glass slides and SEM stubs are housed in the Paleobotanical collections of the National Museum of Nature and Science, Tsukuba, Japan (NSM-PP).
Figure 3.
Trilete spores (A–G), plant fragments (H, I) and scolecodont (J) from the Nakazato Formation photographed under the differential interference contrast microscope. A, B, cf. Retusotriletes spp. (A, 2021.12.10-20a, P57/3; B, 2021.12.10-21a, C42/2); C, Ambitisporites avitus (2021.12.10-22a, M53); D, Dibolisporites sp. (2021.12.10-21a, L39/2); E, Dictyotriletes sp. (2021.12.10-21a, O50/4); F, Apiculiretusispora sp. (2021.12.10-21a, O47/2); G, Aneurospora sp. (2021.12.10-21a, T59/3); H, Conducting tissue (2021.12.10-20a, F45/2); I, Laevitubulus tenuis (2021.12.10-21a, Y49); J, Scolecodont (2021.12.10-21a, W60/1). Scale bar, 10 µm.
Results
All samples contained spores and plant fragments, although these were carbonized and often fragmented or deformed due to a low grade metamorphism (Figure 3). Identified taxa were shared between several samples, suggesting that the dispersed spore assemblages were all very similar in their composition and belonged to the same paleoflora. Most abundant and well-preserved palynomorphs were obtained from horizons 2021.12.10–20 and –21 (Figure 2).
Figure 4.
Cryptospores (A, B) and trilete spores (C–O) from the Nakazato Formation observed under the scanning electron microscope. A, Pseudodyadospora petasus (2021.12.11-02); B, Laevolancis sp. in loosely attached dyad (2021.12.11-02); C, K, L, N, Aneurospora spp. (C, 2021.12.10-20; K, L, 2021.12.11-03; N, 2021.12.10-21); D, F, Deltoidospora (Leiotriletes) priddyi (D, 2021.12.10-20; F, 2021.12.10-20); E, Calamospora atava (2021.12.11-03); G, Apiculiretusispora sp. (2021.12.10-20); H, Granulatisporites cf. muninensis (2021.12.10-20); I, Verrucosisporites cf. polygonalis (2021.12.10-21); J, Retusotriletes cf. triangulatus (2021.12.11-03); M, Brochotriletes cf. foveolatus (2021.12.11-03); O, P, Dibolisporites cf. echinaceus (2021.12.10-18). Scale bar, 10 µm (A–O), 1 µm (P).
The microfossil assemblage is composed of two species of cryptospores and 13 species of trilete spores, associated with abundant plant fragments including masses of conducting cells, tabular remains and cuticles (Figures 3–5; Appendix 1). Cryptospores are represented by fused permanent dyads (pseudodyads) of Pseudodyadospora petasus Wellman and Richardson (1993) (Figure 4A) and monads or loosely attached dyads of Laevolancis sp. (Figure 4B). The trilete spore assemblage is dominated in number and diversity by retusoid laevigate spores of probable Retusotriletes (Figure 4J: R. cf. triangulatus (Streel, 1964) Streel, 1967, Figure 3A, B: cf. R. spp.), crassitate spores of Ambitisporites avitus Hoffmeister (1959) (Figure 3C), and trilete laevigate spores of Calamospora atava (Naumova, 1953) McGregor (1964) (Figure 4E), Deltoidospora (Leiotriletes) priddyi (Berry, 1937) McGregor (1973) (Figure 4D, F).
Figure 5.
Longitudinal view of conducting tissues observed under the scanning electron microscope. A, tracheary element with uniseriate pitting (2021.12.10-21); B, wall fragment of a water-conducting tube showing randomly distributed minute pores of various size (2021.12.11-03). Scale bar, 10 µm.
While ornamented spores are not commonly found, they nonetheless display a wide range of diversity. These include apiculate spores of Aneurospora spp. (Figures 3G, 4C, K, L, N), Apiculiretusispora sp. (Figures 3F, 4G), granulate spores of Granulatisporites cf. muninensis Allen (1965) (Figure 4H), verrucate spores of Verrucosisporites cf. polygonalis Lanninger (1968) (Figure 4I), reticulate spores of Dictyotriletes sp. (Figure 3E) and Brochotriletes cf. foveolatus Naumova (1953) (Figure 4M), and spores of Dibolisporites showing characteristic compound sculptural projections consisting of baculae, coni and spinae (Figure 4O, P: Dibolisporites cf. echinaceus (Eisenack, 1944) Richardson, 1965, Figure 3D: Dibolisporites sp.).
We counted 158 spores on one slide from horizon 2021.12.10–21, which yields the richest and best preserved palynomorphs among samples observed, although the opaque nature of the spores does not permit precise identifications. The count reveals a composition of approximately 63% laevigate spores (possibly assigned to Retusotriletes, Ambitisporites, Deltoidospora, or Calamospora), 11% verrucate spores (Verrucosisporites), 9% granulate or apiculate spores (Apiculiretusispora or Granulatisporites), 15% conate/baculate/foveolate spores (Aneurospora, Dictyotriletes, Brochotriletes, or Dibolisporites), and 2% dyads (Pseudodyadospora or Laevolancis).
Among the numerous plant fragments observed in preparations, we could recognize smooth aseptate tubes of Laevitubulus tenuis Burgess and Edwards (1991) (Figure 3I) and a variety of conducting cells (Figures 3H, 5A, B). Wall fragments with numerous minute rounded perforations of various size (Figure 5B) are widely observed in pro-tracheophytes (Kenrick and Crane, 1991) which are similar to hydroid walls of some extant bryophytes (Ligrone et al., 2000). On the other hand, tracheids characterize vascular plants. Tracheid elements with uniseriate bordered pits (Figures 3H, 5A) are observed in some late Early Devonian trimerophytes like Psilophyton (Hartman and Banks, 1980). Additionally, the investigated samples also yield numerous opaque plant fragments and cuticles of unknown origin.
No aquatic palynomorphs were observed. They were possibly destroyed during the fossilization process because of their generally less resistant structure, especially by the low-grade metamorphism as noted above. However, we could observe several scolecodonts (Figure 3J).
Discussion
Possible age for the N3 member of the Nakazato Formation based on palynoassemblage
While we present the Middle Devonian palynoassemblage from Japan for the first time, the data obtained are fragmentary due to the thermal degradation of palynomorphs. Nevertheless, notable similarities exist with the Early Devonian palynoassemblages from the South China Block, where the hinterland of the Nakazato Formation was closely situated (Wakita et al., 2018). The abundance of Apiculiretusispora and Retusotriletes is shared between the Nakazato palynoassemblage and those from the Longhuashan (= Xujiachong) Formation in Yunnan (Gao, 1981; Wellman et al., 2012). The presence of the following genera is common between them: Dictyotriletes, Ambitisporites, Aneurospora, Verrucosisporites, Dibolisporites, Brochotriletes, Pseudodyadospora. Gao (1981) assigned the Assemblage Zone IV to the assemblages from the Xujiachong Formation and suggested a correlation of his zone with the late Pragian to early Emsian of Western Europe. Tian et al. (2011) further defined spore assemblage zones for the upper Silurian to Lower Devonian of southwest China based on the first appearance datum (FAD) of characteristic species in this region. The Nakazato assemblage closely resembles the Verrucosisporites polygonalis–Dibolisporites wetteldorfensis assemblage zone corresponding to the Pragian which is most characterized by FADs of Dib. eifeliensis and V. polygonalis (Tian et al., 2011).
On the other hand, the Nakazato assemblage is different from those of the Xujiachong Formation (Wellman et al., 2012) in the absence of zonate spores (Camptozonotriletes, Leiozonotriletes), laevigate monolete spores (Latosporites) and permanent tetrads (Tetrahedraletes, Cheilotetras). Furthermore, Dictyotriletes and Brochotriletes are scarce in the Xujiachong Formation (Wellman et al., 2012) in contrast to the moderate occurrence of these genera in the Nakazato Formation. Since spore genera absent in the Nakazato assemblage are only represented by a few grain-types in the well-preserved assemblages of the Xujiachong Formation (Wellman et al., 2012), the absence could be explained by the poor preservation state in the Nakazato Formation. Alternatively, there could be slight difference in age between the Nakazato and Xujiachong assemblages. Nevertheless, the comparison of the Nakazato assemblage to the Early Devonian assemblages of South China seems reasonable, as the Nakazato assemblage lacks Rhabdosporites, Hystricosporites, and Lophozonotriletes, which characterize the Middle Devonian Zones V and VI (Gao, 1981).
In summary, palynological data suggests a Pragian to early Emsian age for the N3 Member of the Nakazato Formation. This estimate is slightly older than those based on marine indices, i.e., the latest Emsian–earliest Eifelian by the trilobite (Kobayashi and Hamada, 1977; Kaneko, 2007) and the Eifelian by brachiopods (Tazawa and Chen, 2001). On the other hand, the ages of South China assemblages were determined through palynostratigraphical comparisons mainly with the West European standard (Richardson and McGregor, 1986; Streel et al., 1987; Steemans, 1989). The reason for this discrepancy might be understood by comprehensive comparison of terrestrial and marine biostratigraphies in Asia.
Vegetational characteristics of the Nakazato palynoassemblage
The assemblage recovered from the Nakazato Formation is dominated by spores (Ambitisporites avitus, Granulatisporites cf. muninensis) along with a few cryptospores (Laevolancis sp., Pseudodyadospora petasus) with possible affinities to the rhyniophytes (Bhutta, 1987; Fanning et al., 1991; Balme, 1995; Wellman et al., 1998a, b). Although exact affinity should be clarified in future, there are many palynomorphs which could be shed from either of the rhyniophytes, zosterophyllophytes, trimerophytes (Calamospora atava, Deltoidospora (Leiotriletes) priddyi, R. cf. triangulatus, cf. Retusotriletes spp., Apiculiretusispora sp.) (McGregor, 1973; Allen, 1980; Gensel, 1980; Bhutta, 1987; Balme, 1995). Verrucosisporites cf. polygonalis and Aneurospora spp. may have been produced by lycopsids (Allen, 1980; Balme, 1995). Cladoxylopsida could be represented by Dibolisporites cf. echinaceus, Dib. sp. and Dictyotriletes sp. (Balme, 1995). The conducting structures recovered from the Nakazato Formation probably belonged to rhyniophytes and/or zosterophyllophytes, lycophytes, trimerophytes.
The Nakazato palynoassemblages reflect a vegetation consisting of only herbaceous plants. The abundance of laevigate spores represented by Retusotriletes might imply that the zosterophyllophytes constituted major vegetation in the backland of the Nakazato Formation because Zosterophyllum yunnanicum Hsü (1966) and Huia gracilis Wang and Hao (2001) bear R. sp. and R. cf. triangulatus (Hsü, 1966; Cai and Schweitzer, 1983; Hao, 1985; Wang and Hao, 2001; Wang et al., 2002; Wang, 2007), respectively.
Acknowledgments
This study was partly supported by the Grant-in-Aid from the Japan Society for the Promotion of Science (JSPS) to T. Yamada (Grant no. 21H02553) and T. Komatsu (Grant no. 19K04059). The authors thank Ofunato City for permitting the field research; the Museum of Natural and Environmental History, Shizuoka, Japan, for facilitating the SEM observation. We would like to thank three reviewers and Y. Shiino, co-editor of Paleontological Research, for their constructive and helpful suggestions and comments, which improved the quality of the manuscript. The authors wish to thank A. Kitamura for his valuable advice during the study.
© by the Palaeontological Society of Japan
References
Author contributions
A. M. and J. L. initiated the study and were primarily responsible for the field survey and palynological analysis. T. K. and T. Y. conducted the field investigation and contributed to the interpretation of the data. All authors contributed to the writing of the paper.
Appendices
Appendix 1. Taxonomical notes on the palynomorphs described in this study.
Laevolancis sp. (Figure 4B).—Hilate cryptospore, in monads or loosely attached dyads. The amb circular to subcircular, 21–24 µm in diameter. An equatorial crassitude 3–4 µm wide delimits a circular hilum collapsed. Exine laevigate, unfolded.
Pseudodyadospora petasus (Figure 4A).—Pseudodyad of two rounded laevigate spores, 25 µm in diameter, invaginated and attached with a junction entirely fused.
Ambitisporites avitus (Figure 3C).—Trilete microspore with an amb subtriangular to subcircular, 35 to 40 µm in diameter. The laesurae are straight, extending from 4/5 to full distance to the equator. Exine laevigate. Equatorial crassitude well defined, 3 µm wide.
Aneurospora spp. (Figures 3G, 4C, K, L, N).—Small trilete microspore. Amb rounded triangular, 20 to 40 µm in diameter. The laesurae are straight, narrow, extending to an equatorial crassitude around 1 µm wide. Exine smooth to finely punctate on the proximal face, and densely ornamented with grana and coni 1.5–2 µm high on the distal face.
Apiculiretusispora sp. (Figures 3F, 4G).—Microspore with an amb rounded triangular, 38–42 µm in diameter. The laesurae are not observed. Exine densively covered with grana and small coni and spinae, less than 1 µm high.
Brochotriletes cf. foveolatus (Figure 4M).—Trilete microspore with an amb broadly subtriangular to subcircular, around 20µm in diameter. The laesurae could not be observed in polar view. Exine foveolate to reticulate, with a mesh rounded to polygonal, 1–5 µm wide, and coarse muri about 1.5 µm wide and 1.5 µm high.
Calamospora atava (Figure 4E).—Trilete microspore with an amb subtriangular, around 40 µm in diameter. The laesurae are straight and extend 1/2 to the equator. Exine laevigate, often folded.
Deltoidospora (Leiotriletes) priddyi (Figure 4D, F).—Trilete microspore. Amb triangular, 25 to 35 µm in diameter, with straight to slightly convex sides and rounded corners. The laesurae are straight, extending from 4/5 to full distance to the equator. Exine laevigate. A number of species assigned to Leiotriletes are similar to D. priddyi (McGregor, 1964, 1973), but they are often distinguished according to their stratigraphic range, i.e., Paleozoic (Leiotriletes) or Mesozoic (Deltoidospora). We combine them here as suggested by McGregor (1973).
Dibolisporites cf. echinaceus (Figure 4O, P).—Trilete microspore with an amb subtriangular to subcircular, 35–40 µm in diameter. The laesurae are thin, slightly elevated, extending from 3/4 to full distance to the equator, where they diverge into curvuturae perfectae. Both surfaces are densely ornamented by spinae, some with spatelae tips, around 1 µm high. The specimens observed correspond in their morphological characteristics to Dibolisporites echinaceus, but are smaller than usually noted for this species; spores with a similar size were reported by Wellman et al. (2012) from the Pragian–lower Emsian Xujiachong Formation in South China.
Dibolisporites sp. (Figure 3D).—Microspore with an amb rounded subtriangular to subcircular, 30 µm in diameter. The laesurae are not observed. Surface densely ornamented with compound projections 1 to 2 µm high, consisting in baculae, coni and spinae surmounted by small spinae or pilae. Grains found in this study show typical ornamentation of this genus, and is distinct from D. cf. echinaceus by its smaller size and higher sculptural elements.
Dictyotriletes sp. (Figure 3E).—Microspore with an amb rounded, 45 µm in diameter. Exine doubly reticulate, with large polygonal lumina 8–12 µm, each again finely reticulate with lumina 1 µm. Muri slightly projecting at the amb, appearing as coni around 1.5 µm high.
Granulatisporites cf. muninensis (Figure 4H).—Tri-lete microspore with an amb subtriangular to subcircular, around 35 µm in diameter. The laesurae are straight and extend 3/4 to the equator. Exine densely granulate.
Retusotriletes cf. triangulatus (Figure 4J).—Trilete microspore with an amb circular to subcircular, 45–55 µm in diameter. The laesurae are straight, extending from 1/2 to 2/3 to the equator. Exine laevigate, about 1.5 µm thick. Morphological characteristics of specimens are consistent with those of Retusotriletes triangulatus, however their opacity prevents any observation of the typical triangular thickening needed to confirm species.
cf. Retusotriletes spp. (Figure 3A, B).—Trilete microspore with an amb subcircular, showing a wide size range, 22–39 µm in diameter. The laesurae are straight, extending from 4/5 to full distance to the equator. However, the curvature cannot be confirmed because of the opacity of the grains. Exine laevigate, about 1 µm thick. Most common taxa in the assemblage. cf. Retusotriletes spp. show a trilete mark reaching to the equator, longer than that observed in R. cf. triangulatus.
Verrucosisporites cf. polygonalis (Figure 4I).—Trilete microspore with an amb broadly subtriangular to subcircular, 35–40 µm in diameter. The laesurae are straight and extend from 3/4 to 4/5 to the equator. Exine laevigate to granate or slightly verrucate on the contact area, followed by regularly and closely spaced, isodiametric low verrucae, 1–1.5 µm wide, on the equator region and distal face.
Laevitubulus tenuis (Figure 3I).—Smooth aseptate tubes, 15–25 µm wide, straight, unflattened, unbranched and without end structures.
