Nonmarine stromatolites sporadically occur in the Lower Cretaceous Kanmon Group in northern Kyushu, Japan. We examined the mode of occurrence and morphological variations of the stromatolites that were found in the Wakino area, the stratotype of the Wakino Subgroup of the Kanmon Group, and analyzed their mineralogical compositions. These stromatolites occur at 7 horizons all from mudstone-dominant facies of the Barremian Lower Wakamiya Formation. The associated tepee structure, mud cracks, and gypsum pseudomorphs suggest that the stromatolites of the Lower Wakamiya Formation were deposited in extremely shallow-water environments with intermittent subaerial exposure. The studied stromatolites comprise 3 distinct morphotypes: flat, columnar, and nodular. XRD analysis confirms that all 3 types have the same mineralogical composition, i.e., calcite, quartz, and clay minerals. They are composed of alternating clastic layers and calcareous layers, or alternating siliciclastic carbonate layers and organic carbon-rich carbonate layers on a submillimeter scale. Based on their morphological characteristics, a sequential transition is suggested from the flat type to columnar type, then to nodular type. The columnar type has the greatest morphological variety, and shows a characteristic pattern of branching in which the bifurcation always initiates from an episodically intervened thick layer of siliciclastics. This suggests that the branching of stromatolite columns is likely triggered by blocking the upward growth of bacterial mats with intermittent supply of a thick sediment cover.
Introduction
Stromatolites are microbially formed three-dimensional structures. They flourished mainly in the Proterozoic, and survived into the Phanerozoic, although restricted to some unique environments (e.g., Walter, 1976; Hoffmann, 1998; Awramik and Sprinkle, 1999). Studies of modern examples demonstrate that cyanobacteria played the main role in forming their unique morphology (e.g., Black, 1933; Logan, 1961; Stolz, 1983; Walter et al., 1992; Reid et al., 2000). Stromatolites show a great variation in morphology mostly from Precambrian rocks, and they are potentially useful in stratigraphic correlations (e.g., Gebelein, 1974; Bertrand-Sarfati and Walter, 1981); however, the formation mechanism of stromatolites is not yet fully understood. In addition to well known shallow marine hypersaline environments (e.g. Shark Bay in Western Australia), nonmarine settings provide another habitable environment for modern stromatolites (e.g., Great Salt Lake and Green Lake in USA) as reported by Carozzi (1962) and Eggleston and Dean (1976).
The nonmarine Lower Cretaceous Kanmon Group in Kyushu, Japan, yields some varieties of stromatolites (Ishijima 1977, 1979; Seo et al. 1994). The occurrence of nonmarine stromatolites is rare and thus details on their stratigraphic distribution and morphology have not yet been well documented. Nonetheless, they are important not only for the paleoenvironmental study of the Cretaceous nonmarine basins in East Asia, but also for microbiological study of nonmarine stromatolites in general.
During a two-season field study the first author recognized stromatolites at eight localities in the Wakino area in northern Kyushu, the stratotype of the Wakino Subgroup of the Kanmon Group (Figure 1). This article reports new occurrences of fresh-water stromatolites from the Lower Cretaceous sequence in northern Kyushu, in particular, their stratigraphic horizon and mode of occurrence in the field. With these new data we discuss the geological/paleoecological implications of these rare occurrences, with particular focus on their morphological significance.
Figure 1.
A. Geologic map of the Wakino area in northern Kyushu, showing distribution of the Early Cretaceous Wakino Subgroup (modified from Seo et al., 1994; Nishimura and Shibata, 1989) with the localities of the stromatolite-bearing sections. B. Stratigraphic subdivision of the Wakino Subgroup in northern Kyushu after Ota (1953) and Ota and Yabumoto (1998).

Geologic Setting
Marine and nonmarine Lower Cretaceous rocks of continental affinity occur extensively in northern Kyushu and western Honshu in southwest Japan. Since Kobayashi and Suzuki (1936), these rocks in northern Kyushu have been designated as the Kanmon (Kwanmon) Group that comprises the Wakino and Shimonoseki subgroups in ascending order. These are correlated with the Gyeongsang Supergroup in the Korean peninsula (Chough et al., 2000). Stromatolites were previously reported from two localities in the Wakino Subgroup (Ishijima, 1977, 1979; Seo et al., 1994). In the stratotype area in northern Kyushu the Wakino Subgroup is subdivided into four formations; Sengoku, Nyoraida, Lower Wakamiya, and Upper Wakamiya in ascending order (Figure 1; Ota, 1953; Ota and Yabumoto, 1998). Although the Wakino Subgroup yields various gastropods and fish remains, they are not very useful for dating, thus the precise age of the subgroup is not yet well constrained (Ota, 1953; Hase, 1960; Yabumoto, 1994). Through regional correlations, however, Matsumoto et al. (1982) concluded that the Wakino Subgroup likely belongs to the Barremian (Lower Cretaceous).
In the Wakino area the Wakino Subgroup unconformably overlies latest Carboniferous high-P/T metamorphic rocks of the Sangun Range, and a mid-Cretaceous granodiorite has intruded the former (Nishimura and Shibata, 1989; Seo et al., 1994; Figure 1). The total thickness of the Wakino Subgroup is over 1,000 m. The lowermost unit, the Sengoku Formation, ca. 400 m thick, consists of conglomerate, coarse-grained sandstone, and interbedded sandstone and mudstone that sporadically contain stromatolites and an enriched freshwater gastropod fauna dominated by Brotiopsis wakinoensis. The Nyoraida Formation, 120–150 m thick, is composed of basal conglomerate and interbedded sandstone/mudstone. This unit is almost barren in fossils except for the nonmarine gastropod Viviparus onogensis (Hase, 1960).
The Lower Wakamiya Formation, 350–600 m thick, mostly comprises conglomerate and interbedded sandstone/mudstone with various mollusk fossils. The equivalent sequence in the neighboring area contains diverse fish fossils (Yabumoto, 1994). The Upper Wakamiya Formation, 350 m thick, is made of conglomerate and interbedded sandstone/mudstone that contain few fossils.
We found new stromatolites at eight localities at Sengoku, Ryutoku, and Yurino in the Wakino area (Figure 1). Due to their good preservation, we focused solely on those from the Lower Wakamiya Formation at Ryutoku and Yurino. Figure 2 illustrates columnar sections of the Lower Wakamiya Formation at three sections where we recognized stromatolites, i.e., Ryutoku West, Ryutoku East, and Yurino. The horizons of stromatolites are numbered 1–7. Note that the Lower Cretaceous rocks at Ryutoku and Yurino were previously assigned to the Nyoraida Formation (e.g., Seo et al., 1992); however, their lithological similarity indicates that these rocks are correlative with the Lower Wakamiya Formation at its stratotype.
Figure 2.
Columnar sections of the stromatolite-bearing Lower Wakamiya Formation at Ryutoku West, Ryutoku East, and Yurino. Note the occurrence of tepee structure, mud cracks, and gypsum pseudomorphs intimately associated with the stromatolites.

At Ryutoku there is an abandoned quarry with two cutting faces, Ryutoku East and Ryutoku West that are mutually separated by a local fault that trends NNW-SSE. With no reliable key beds the two faces are not easily correlatable. Stromatolites were found at four horizons at Ryutoku West (Horizons 1–4) and at two horizons at Ryutoku East (Horizons 5 and 6) (Figure 2). At Yurino stromatolites occur at a single horizon of coaly shale (Horizon 7). Likewise this horizon is not precisely correlated with those at Ryutoku owing to the absence of reliable key beds and fossil age control; all occur in a mudstone-dominant facies of the Lower Wakamiya Formation. The stromatolite-bearing mudstone-dominant facies of the Lower Wakamiya Formation is characterized by unique sedimentary features suggesting extremely shallow-water environments; e.g., tepee structure, mud cracks, and pseudomorphs of gypsum (Figures 2, 3c). The stromatolites found in the Sengoku Formation at Sengoku are ill preserved, thus they are not dealt with in this article.
Stromatolites
We measured the three-dimensional morphology of the stromatolites in the field, studied their detailed microstructure in thin section by optical microscope, analyzed their mineralogical composition by XRD, and undertook element mapping for Ca and Si by XRF.
Composition
Microscopic observations confirm that all the stromatolites are composed of alternating calcareous and clastic layers; the former is composed of micritic calcite and the later of clay minerals. XRD analysis demonstrate that all types of stromatolites have the same mineralogical composition; i.e., calcite, quartz, and clay minerals (illite) (Figure 4).
Mode of Occurrence
All the stromatolites occur in a black mudstone of the Lower Wakamiya Formation. The brown to greenish gray stromatolites contrast with the surrounding black mudstone. There are three distinct types of stromatolites, flat, columnar, and nodular (Figures 3, 6, 9). These types are mutually distinct, and they never occur together in the same horizon. The flat type occurs at Ryutoku East, the columnar type at Horizons 1, 3 at Ryutoku West and Horizon 5 of Ryutoku East, and the nodular type solely at Yurino (Horizon 7). Details of each type are described below.
Flat type (Figure 3).—This occurs as ca. 6–8 cm-thick beds separated by 2–3 mm-thick mudstone or fine-grained sandstone (Figure 3b). At the top of each bed small-scale tepee structures and/or desiccation cracks most likely suggest an intermittently drying depositional condition (Figure 3c). Calcite veins with a comblike alignment of microcrystals may represent gypsum pseudomorphs. The flat-type stromatolite is composed of alternating white siliciclastic layers (S) and black micrite layers (C) (Figure 3d, e). Both S and C layers are mostly 0.1 mm thick or less; however, ca. 15% of S layers are over 0.3 mm thick (Figure 5). This type sometimes includes microscopic columnar parts (Figure 3d) with flat-bottom and convex-top surfaces.
Figure 3.
The flat-type stromatolite of Horizon 6 at the Ryutoku East. a. mode of occurrence of the stromatolite bed in mudstone. b. a polished surface of the stromatolite. Arrows indicate the bed boundaries, c. close-up view of the framed area in b (inverted image) showing the presence of mud cracks and tepee structure. d. thin section view of interbedded S-C layers (open nicols) with an arrow pointing to a nascent columnar stromatolite. e. XRF element mapping images of Ca and Si.

Columnar type (Figure 6).—This occurs as a ca. 10–40 cm thick bed with flat-bottom and convex-top surfaces within black mudstone (Figure 6a, b). Each bed contains multiple individuals of columnar structures (Figure 6f), the size of which changes from the lower half to the upper half of the bed; i.e., smaller at the base (<2 mm wide, <5 mm tall) and becoming larger towards the top (up to 1 cm wide, 5 cm tall). The millimeter-scale intercolumnar spaces are filled with siltstone. The smaller columns often show branching (Figure 9), whereas the larger ones in the upper part rarely branch.
The interior of each column is well laminated (Figure 6c, d, e); however, the smaller columns in the basal part and the larger ones in the upper part are different in composition. The columns of the basal part are composed of alternating S and C layers, similar to that of the flat type. In contrast, the columns forming the upper part are composed of alternating siliciclastic-rich carbonate layers (SC) and organic carbon-rich carbonate layers (OC). The SC-OC alternation shows a striped fabric that is similar to the structures of bacterial origin (Monty, 1976). Figure 7 shows the thickness distribution of the columnar-type stromatolite at Yurino. The lower middle part of the bed corresponds to a transitional interval between the two. XRF element-mapping confirmed the abundance of silica in the basal part and of carbonates in the upper part (Figure 6f).
Figure 4.
X-ray powder diffraction (XRD) pattern of a flat-type stromatolite (Horizon 6). Note the dominance of quartz and calcite.

A remarkable feature among all stromatolites is the development of branches strictly in the basal part where smaller columns are concentrated (Figure 8). In contrast, there are no branching types in the upper part of the bed. Figure 8b–d shows sketches of the branching portions of the columnar-type stromatolite at Yurino.
Nodular type (Figure 9).—This type does not show any bed form but occurs as isolated blocks floating within coaly mudstone and/or rippled sandstone (Figure 9a). Each stromatolite is composed of several ball-like structures with internal lamination (Figure 9b) made up of alternating SC and OC layers. The average thickness of each couple of these layers is 0.9 mm. In view of the lamination pattern and composition the nodular type is most similar to the upper part of the columnar type mentioned above. These ball-like structures are not regarded here as oncolites because the growth directions of individual balls are oriented randomly and because their internal laminations are not concentric (Figure 9c). The surrounding coaly mudstone contains pseudomorphs of gypsum crystals (Figure 9d).
Patterns of lamination and branching
All three types of stromatolite from the Lower Wakamiya Formation occur in more or less the same shallow lacustrine setting; nonetheless, they each show distinct differences in lamination pattern. In terms of lamination pattern the stromatolites are classified into two groups; 1) with a clastic-dominant S-C alternation, and 2) with a clastic-poor SC-OC alternation. The former is observed strictly in the flat type and in the basal part of the columna type, whereas the latter is in the upper part of the columnar-type and in the nodular type. These contrasting lamination patterns suggest that each represents a distinct process of lamina formation.
Figure 5.
Thickness of layers of a flat-type stromatolite (Horizon 5 at Ryutoku East). a. distribution of thickness, b. gradual upward change of layer thickness. Clastic (S) layers over 0.2 mm thick are abundant. Note that most layers are less than 0.3 mm thick and that layers over 0.3 mm thick are more common in clastic (S) layers than in calcareous (C) ones.

Among the three distinct types of the stromatolites from the Lower Wakamiya Formation, the most visually outstanding is the columnar type that looks similar to many Precambrian and modern domal stromatolites. As to the columnar-type stromatolites, branching of columns occurs frequently in the basal part of the beds, but rarely in the upper part (Figures 6, 8). A unique feature of the layering occurs at every branching portion of the columnar-type stromatolites. At the separating point of two distinct but connected columns, branching always starts within a relatively thick S layer, as typically observed in Figure 8b, c. In contrast, in the upper part of the beds, no branching occurs even in some thick siliciclastic (SC) layers.
Figure 6.
The columnar-type stromatolites observed at Ryutoku East and Yurino. a. lenslike mode of occurrence in mudstone of Horizon 6. b. bedded mode of occurrence of Horizon 5. c. striped fabric (crossed nicols / Yurino). d, e. thin-section view of a column with bedded S-C (d) and SC-OC (e) layers (Yurino). f. polished surface and XRF element map of a columnar-type stromatolite (Yurino). Note the clear change in layering pattern in the columnar-type stromatolite.

Discussion
Depositional environment
Based on lithofacies and absence of marine fauna the Wakino Subgroup has been explained as a nonmarine lacustrine deposit of the extensive Wakino paleo-lake that possibly developed over northern Kyushu and southern Korea (e.g., Kobayashi, 1941; Seo et al., 1994). In this conventional view on the depositional framework, the mudstone-dominant facies was considered to represent a deep-water environment around the depocenter of the “Wakino paleo-lake” (e.g., Seo et al., 1994). Accordingly, the stromatolites in the mudstone-dominant facies were considered to have formed in relatively deep-water settings.
Figure 7.
Thickness of layers of the columnar-type stromatolite (Yurino). a. distribution of thickness, b. gradual upward change of layer thickness. Note the abundance of calcareous (C) layers over 0.3 mm thick. Most calcareous (C) layers are thicker than clastic (S) layers.

The present study, however, has clarified several contradictory lines of evidence against the previous interpretation of the sedimentary setting of the Wakino stromatolites. These include 1) tepee structure, 2) mud cracks, and 3) pseudomorphs of gypsum, which are closely associated with the stromatolites and the surrounding beds (Figure 2). All of these suggest that the Wakino stromatolite formed in an extremely shallow-water environment, possibly with intermittent exposure to the air, similar to supratidal conditions. The occurrence of estherids (Crustacea) (Hayashi, 1998, 2001) supports our interpretation.
Moreover, the Wakino Subgroup, as well as its stromatolites, was most likely deposited in a shallow-water environment along the southern margin of the Wakino paleo-lake. Stromatolites usually occur in shallow marine settings and their occurrence in nonmarine environments is relatively rare (e.g., Logan, 1961; Haslett, 1976). Nonetheless, Phanerozoic examples are often reported from nonmarine rocks (e.g., Beralidi-Campesi et al., 2004). More data are needed to refine and constrain the detailed sedimentary setting of the Wakino stromatolites.
Mutual linkage among the three types
The three types of stromatolites recognized in the Lower Wakamiya Formation never occur together, suggesting that each type has a preferred depositional setting. Nevertheless, there are some similarities in lamination pattern that may suggest certain mutual genetic links, in particular between the flat type and basal columnar type and between the upper columnar type and the nodular type.
First, we discuss a possible transition from the flat type to the columnar type. The microdomal structures with a flat-bottom and convex-top morphology sporadically occur in the flat type (Figure 3d), and the overlying lamina covers conformably the convex shape of the top. Because no opposite types with convex bottoms and flat tops are observed, this upward-convex asymmetric morphology suggests that the accidental/episodic appearance of such irregular topography on flat lamina surfaces can be occasionally preserved in the overlying laminae, and that this may correspond to a nascent stage of the columnar growth of stromatolite, i.e. the shift from the flat to the columnar type.
The columnar type changes its lamination pattern from the S-C alternation in its basal part to the SC-OC alternation in the upper part (Figure 6f). The change in lamination pattern is sharp and unidirectional, and no change in the opposite direction from the SC-OC alternation to the S-C alternation was observed. The change in sediment supply may have controlled this shift, although the ultimate controlling factors have not been specified.
Second, we refer to a possible transition from the columnar type to the nodular type. The similarity in the lamination pattern suggests that these two types are closely and mutually related, although a direct change from the columnar type to the nodular type is not observed. Most stromatolites of the nodular type do not occur in a bedded manner, but they float within a matrix (Figure 8a), and the growth orientations of laminae are arranged randomly even in the same bed (Figure 8c). These relations suggest that the nodular type may have been derived from the upper part of the columnar type, probably through mechanical fragmentation of the latter and redeposition. The absence of the S-C alternation in the nodular type supports this interpretation.
Summarizing the discussion above, the three distinct types of stromatolites from the Lower Wakamiya Formation can be explained by the following growth sequence. It seems likely that the Wakino stromatolites first formed as a flat type probably in flat bacterial biomats, then the columnar type may have started from occasional topological irregularities by the incorporation of some clastic grains. The nodular type may have been derived from the columnar type possibly by mechanical fragmentation in the later stage of growth of the latter.
Branching mechanism
The columnar-type stromatolite shows a remarkable branching pattern in its lower half (Figures 6, 8). Previous studies suggested that the branching of stromatolites starts from an episodic deposition of coarse clastic particles on a bacterial mat that may block the free upward growth of the mat (Horodyski, 1977). As to the stromatolites from the Lower Wakamiya Formation, however, we cannot observe any such coarse grains at the branching points (Figure 8). Instead, we observe that the branching of columns always starts from a relatively thick layer of siliciclastics. This observation suggests that the deposition of a thick S layer may have prohibited continuous/uniform upward growth of the underlying C layer, and that this blocking may have triggered the branching of the column. Recent stromatolites also have an alternation of clastic and micritic layers that is similar to the S-C alternation of the Wakino stromatolites (Gebelein, 1969). In particular, the layers consisting of organic material in recent stromatolites are micritic and likely formed in a bacterial mat. Given that the C layers of Wakino stromatolites formed in the same way as recent examples, we consider that the S layers prohibited the upward growth of the underlying bacterial mat. Once it was branched, the lateral continuity of a mat (C layer) may have never recovered afterwards, regardless of the thickness of overlying layers (Figure 8d). On the other hand, it is apparent that the growth of some columns was prevented by the thick covering of siliciclastics (Figure 8a, c). This indicates that a threshold existed in the thickness of the cover clastics with respect to the growth rate of the underlying bacterial mat.
Figure 9.
The nodular-type stromatolites at Yurino (Horizon 7). a. mode of occurrence of the nodular-type stromatolite in mudstonel. b. close-up image of a stromatolite (a) showing circular laminae. c. vertical thin section of small balls (open nicols). Growth directions of each ball (arrows) are variable. d. photomicrograph of lignite (upper opaque part) and pseudmorphs of gypsum (lower part) in a lignite bed just under a nodular-type stromatolite-bearing mudstone.

Thus the columnar-type stromatolites of the Lower Wakamiya Formation most likely grew upwards under the strong influence of cover siliciclastics. In particular, we emphasize that their branching pattern and upward growth were intimately controlled by the amount of sediment supply. In contrast to previous studies of Proterozoic stromatolites (e.g., Horodyski, 1977) that focused on the link between the episodic/accidental deposition of coarse-grained clastics and the branching of columns, the present study demonstrates that the thickness of cover sediment may have been more influential for the branching rather than the accidental deposition of large grains. Nevertheless, the possible blocking mechanism of flat mat growth by the deposition of nonbiogenic (e.g., siliciclastic) material appears by and large the same. Although further case studies are necessary to confirm this interpretation, the branching mechanism proposed in this study may explain the growth pattern of both past and modern branched stromatolites.
Comparison
The Lower Cretaceous Gyeongsang Supergroup in South Korea is bio- and lithostratigraphically correlated with the Wakino Subgroup (Kobayashi and Suzuki, 1936), and is considered to correspond to the northern part of the Wakino paleo-lake. Woo et al. (2004) and Nehza and Woo (2006) reported the occurrence of stromatolites from the Sindong Group of the Gyeongsang Supergroup. According to their description, the Gyeongsang stromatolites are mostly poor in siliciclastics, and composed of interbedded SC and OC layers. These are probably comparable with the columnar-type stromatolites of the Wakino Subgroup reported here, in particular their upper part. Nehza and Woo (2006) suggested that the columnar stromatolites of the Gyeongsang Supergroup may have grown upwards freely in a water column, and later they were buried by younger clastics. This mechanism is considerably different from the one proposed in this paper. However, the close similarities in morphology and in pattern of lamination between the Gyeongsang and Wakino stromatolites suggest that they formed through almost identical processes. Comparative research is definitely required to constrain whether or not these stromatolites formed through common processes in similar depositional settings.
Conclusions
From our analysis of the mode of occurrence and morphological variation of nonmarine stromatolites from the Barremian Lower Wakamiya Formation of the Wakino Subgroup in northern Kyushu, the following conclusions were reached:
The stromatolites were recognized at seven horizons all from mudstone-dominant facies.
The association with tepee structure, mud cracks, and gypsum pseudomorphs suggests that the stromatolites of the Wakino Subgroup were deposited in extremely shallow-water environments with intermittent subaerial exposure, similar to supratidal conditions.
The stromatolites from the Wakino Subgroup are classified into three distinct morphotypes; i.e., flat, columnar, and nodular types.
The morphology and lamination patterns of the stromatolites suggest that the columnar type may have formed occasionally on the flat type, and that the nodular type may have derived from the upper part of the columnar type.
The columnar-type has a characteristic branching pattern that always starts from a thick siliciclastic layer. This suggests that the branching of columns was likely triggered by blocking of the upward growth of bacterial mats by an intermittent supply of thick sediment cover.
Acknowledgments
We thank H. Sano (Kyushu University, Japan) and V. C. Tewari (Wadia Institute of Himalayan Geology, India) for their constructive review comments on the original manuscript. We also thank T. Oji, T. Sasaki, and other members of the Paleobiological Seminar at Hongo and those of the Komaba Earth Science Seminar of the University of Tokyo for valuable discussions, and A. Fujii, S. Imada, and R. G. Jenkins (Yokohama National University, Japan) for their help in fieldwork. Brian F. Windley (University of Leicester, UK) corrected the English.