First report of the ichnogenus Phymatoderma from the Hayama Group (Miocene, Japan): Paleobiological and paleoecological implications

Geobios 48 (2015) 321–329

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Original article

First report of the ichnogenus Phymatoderma from the Hayama Group (Miocene, Japan): Paleobiological and paleoecological implications§ Kentaro Izumi Center for Environmental Biology and Ecosystem Studies, National Institute for Environmental Studies, 16-2, Onogawa, Tsukuba, Ibaraki 305-8506, Japan

A R T I C L E I N F O

A B S T R A C T

Article history: Received 10 February 2015 Accepted 5 June 2015 Available online 29 June 2015

The trace fossil Phymatoderma cf. granulata is described for the first time from the deep-marine deposits of the Hayama Group (Miocene) of Japan. This ichnotaxon is a burrow system composed of horizontal, straight to slightly curved tunnels ranging from 7.7 to 20.4 mm in diameter (mean = 14.98 mm), occasionally representing branching. Each tunnel is filled with ellipsoidal pellets with aspect ratios generally ranging from 1.4 to 2.4. Based on the comparison between the Hayama specimens and other Phymatoderma specimens from tectonically and paleoenvironmentally similar settings, a deep-sea echiuran worm is suggested as the possible trace-maker. Morphometric analysis demonstrates that the pellet aspect ratios do not show any correlation with the tunnel diameter, suggesting that there was not a significant change in digestive and/or excretory systems from the smaller to the larger trace-producing animals. In addition, microscopic analysis of the pelletal infill of P. cf. granulata revealed that the tracemaker actually fed on freshly deposited organic detritus and microorganisms, such as planktic foraminifera and radiolaria. ß 2015 Elsevier Masson SAS. All rights reserved.

Keywords: Trace fossils Phymatoderma Echiuran worm Fecal pellets Microfossils Miocene Miura Peninsula

1. Introduction The ichnogenus Phymatoderma Brongniart, 1849 is a morphologically distinctive, horizontal to subhorizontal burrow system comprising clusters of radiating tunnels filled with ellipsoidal pellets (Fu, 1991; Seilacher, 2007; Miller, 2011). Owing to the pelletal infill that has been interpreted as fecal pellets, Phymatoderma has been regarded as a product of a deposit feeder (Seilacher, 2007). Although Miller and his co-authors demonstrated that the Phymatoderma-producer was engaged in both surface and subsurface deposit-feeding activities (Miller and Aalto, 1998; Miller and Vokes, 1998), surface deposit-feeding behavior was more common in many cases (e.g., Izumi, 2012). As pointed out by Miller and Vokes (1998), because of the morphological similarity with other ichnogenera such as Chondrites and Zonarites, Phymatoderma has generally been misidentified as ‘‘Zonarites’’, ‘‘large Chondrites’’, or ‘‘pellet-filled Chondrites’’ during the 1950s up to the 1990s (Simpson, 1957; Sellwood, 1970; Brenner and Seilacher, 1978; Savrda and Bottjer, 1989; Kotake, 1991). However, since Fu (1991) has successfully rectified the complicated ichnotaxonomic situation by re-describing Phymatoderma, and summarized the morphological difference between

§

Corresponding editor: Davide Olivero. E-mail address: [email protected]

http://dx.doi.org/10.1016/j.geobios.2015.06.003 0016-6995/ß 2015 Elsevier Masson SAS. All rights reserved.

Phymatoderma and superficially similar ichnogenera, Phymatoderma has been correctly identified and recognized by geologists from many localities of various ages and environments (Miller and Aalto, 1998; Miller and Vokes, 1998; Leszczyn´ski, 2004; Olivero et al., 2004; Ponce et al., 2007, 2008; Seilacher, 2007; Uchman and Gaz´dzicki, 2010; Izumi, 2012, 2013, in press; Lima and Netto, 2012; Izumi et al., 2014; Izumi and Uchman, 2015; Izumi and Yoshizawa, in press). The current ichnotaxonomy of Phymatoderma was recently summarized by Miller (2011). Although recent studies have especially focused on paleoecological interpretations of the trace-maker of Phymatoderma such as diet, mode of feeding, and interactions with other ichnogenera (Olivero et al., 2004; Miller, 2011; Izumi, 2012, 2013, in press; Izumi et al., 2014), the trace-maker itself could not be identified by these previous studies. However, in a very recent study by Izumi and Yoshizawa (in press), Phymatoderma and associated star-shaped horizontal trace fossil have been discovered from the Mio-Pliocene deep-marine Misaki Formation of Japan, leading these authors to conclude that the fecal pellets of Phymatoderma were excreted by an echiuran worm. Therefore, because the most likely trace-maker is now proposed (Izumi and Yoshizawa, in press), new discoveries of Phymatoderma and further paleoecological studies become increasingly important. In this context, the present paper is the first report on the occurrence of Phymatoderma from the Miocene deep-marine Hayama Group, Miura Peninsula, central Japan. In addition to an

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in-depth systematic description of the newly-described specimens, paleobiological and paleoecological interpretations are discussed based on their morphometrical and microscopic analyses. 2. Geological and tectonic settings of the Miura Peninsula The Miocene to Pleistocene sedimentary sequence in the Miura Peninsula, central Japan (Fig. 1), is characterized by a thick accumulation of alternating clastics and hemipelagic rocks with abundant synsedimentary deformation structures associated with tight folding and faulting, which are interpreted to have been formed in a convergent tectonic setting (Ogawa et al., 1985; Saito, 1992). In particular, the sedimentary sequence was controlled by the tectonics around the collision zone of the Izu-Bonin arc (i.e., subduction of the Philippine Sea Plate; Ogawa et al., 1985; Fig. 2). The distribution of this sedimentary sequence is separated by the

Hayama-Mineoka uplift zone, which is located at the middle part of the Miura Peninsula (Fig. 1(A)) into the southern and northern areas (Kanamatsu et al., 2001; Hirata, 2012). The Hayama-Mineoka uplift zone is mainly composed of the Mineoka Group (Eocene–Oligocene ophiolitic rocks; Takahashi et al., 2012) and the Hayama Group (Miocene siliciclastic rocks; Ebiko and Shibata, 2012), but the Mineoka Group crops out only in the Boso Peninsula (Takahashi et al., 2012). The paleoenvironment of the Hayama-Mineoka uplift zone has been interpreted as an ancient trench-slope break (Kanamatsu et al., 2001; Fig. 2). The sedimentary sequence in the southern and northern parts of the Miura Peninsula is generally subdivided into the Miura Group (Middle Miocene–Pliocene), and the Pleistocene Kazusa Group and Miyata Formation (Fig. 1). The Hayama Group crops out in the middle part of the Miura Peninsula (Fig. 1). In terms of lithology, the group is composed mainly of coarse-grained, poorly sorted sandstones, white- to pale

Fig. 1. Geology and stratigraphy of the Miura Peninsula, central Japan. A. Simplified geological map of the Miura Peninsula (modified from Kanamatsu and Herrero-Bervea, 2006 and Yamamoto et al., 2009). Plate boundaries are drawn based on Taira (2001). Sampled localities are indicated by open stars. GPS coordinates of each locality: Nobi: 358120 36.50 0 N, 1398410 59.100 E; Morito: 368160 18.900 N, 1398340 12.500 E. B. Simplified lithostratigraphy of the Miura Peninsula (slightly modified from Hirata, 2012, and Shibata, 2012). Ages of tuff key beds and igneous rocks are based on: Andesite: Imanaga and Yamashita (1999); Mk tuff: Yoshida et al. (1984); Ok tuff: Kasuya (1987); So tuff: Kasuya (1987); Hk tuff: Saito et al. (1997); Kd38 tuff: Fujioka et al. (2003).

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Fig. 2. Schematic and simplified reconstruction (not to scale) of the tectonic setting and paleogeography around the Miura Peninsula during the late Miocene to early Pliocene (ca. 5 Ma) (slightly modified from Shibata, 2012). Note that sedimentation of the Hayama Group had already occurred in the hemipelagic realm prior to 5 Ma.

gray-colored siliceous mudstones, volcaniclastic conglomerates, and tuff layers (Ogawa et al., 1985; Ebiko and Shibata, 2012). Coarse-grained sandstones are generally massive, but are occasionally intercalated with fine-grained sandstones with convolute or parallel laminae (Ebiko and Shibata, 2012). White- or graycolored mudstones are interpreted to representing hemipelagic deposition (Ebiko and Shibata, 2012). Sandstones and mudstones of the Hayama Group are generally deformed by faults and folds, and slide or slump deposits are common in this group (Ogawa et al., 1985). The age of the Hayama Group has been interpreted as Miocene (Fig. 1(B)). Although the Hayama Group does not contain any key tuff layers, an early to middle Miocene age is most likely based on studies on benthic and planktic foraminifera (Kurihara, 1971), diatoms (Haga and Suzuki, 1999), radiolaria (Ling and Kurihara, 1972), and calcareous nannofossils (Eto et al., 1987). In addition, recent studies demonstrated the occurrence of radiolaria indicating an age of 17.92 to 14 Ma (Suzuki and Kanie, 2010; Suzuki, 2012), further confirming the previous data. A relatively deep-marine environment (1200–1600 m water depth, corresponding to the bathyal zone) has been reconstructed on the basis of benthic foraminiferal data (Akimoto et al., 1995). In addition, cold seep carbonate concretions and seep-related fossils (e.g., Calyptogena, Acharax, and fossil tube worms) have been occasionally discovered from the Hayama Group, suggesting a strong resemblance to the depositional environment of the modern seeps located at the continental slope setting in the Sagami Bay (Naganuma et al., 1995; Kanie, 1996). In contrast to the occurrence of diverse body fossils and microfossils mentioned above, only two ichnogenera have been recognized from the Hayama Group so far: namely, Tasselia (Kanie et al., 2012) and Zoophycos (Kotake, 2014). In this study, the occurrence of further ichnogenera (e.g., Chondrites, Phycosiphon, Phymatoderma) is documented from the mudstones of the Hayama Group. In particular, Phymatoderma, which is the focus of this study, was recognized at two different localities: Nobi and Morito Coasts (Fig. 1).

3. Analytical methods Observation of general morphology of Phymatoderma and measurement of morphometric parameters were primarily carried out during fieldwork, although dimensions and aspect ratio of the pellets were measured in the laboratory using the imageprocessing program ImageJ. Paleoecological interpretations are based on thin-section and SEM observations of the pelletal infill

of Phymatoderma. For SEM analysis, a field emission scanning electron microscope (FE-SEM; JSM-7000F, JEOL) has been used at the Department of Earth and Planetary Science, The University of Tokyo. In the preparation of material for microscopic analysis, small chips of Phymatoderma-bearing rocks were cut and attached to glass slides (28  48 mm), and were then polished with a graded series of carborundum. 4. Systematic ichnology Phymatoderma specimens including thin sections and polished sections are housed at The University Museum, The University of Tokyo, Tokyo, Japan (UMUT). Specimen list is summarized in Table 1. Ichnogenus Phymatoderma Brongniart, 1849 Phymatoderma cf. granulata (Schlotheim, 1822) Material: Fourteen specimens studied in the field in Nobi and Morito Coasts (Fig. 1(A)), and four specimens collected (UMUT-CW31810–31813). Description: P. cf. granulata is a burrow system composed of horizontal, straight to slightly curved tunnels, occasionally showing first-order branching (Fig. 3(A, B)). The tunnels range from 7.7 to 20.4 mm in diameter (Table 1), with a mean value of 14.98 mm (n = 11). Each tunnel is slightly compressed and is filled with white-colored, or very light gray-colored ellipsoidal pellets (Fig. 3(C, D)). In two specimens (Mr01, Mr03), tunnels were reburrowed with another ichnogenus (Chondrites; Fig. 4). In general, pellets range from 0.26 to 2.37 mm in width (short axis) and from 0.41 to 4.64 mm in length (long axis). Although pellet aspect ratios vary greatly (from 1.13 to 3.42), average values are generally similar (from 1.77 to 1.90) regardless of the tunnel diameter (Table 1; Fig. 5). Both the tunnels and pellets have no linings. Lithology and color of the pelletal infill differs from those of the surrounding host pale gray- to greenish gray-colored mudstones. Remarks: It could be possible to assign the studied specimens to the ichnogenus Alcyonidopsis, which is a simple, straight and cylindrical burrow filled with elongate fecal pellets. However, Alcyonidopsis is mostly a few millimetres wide (Wetzel and Uchman, 2012), which is much smaller than the studied trace fossils (Table 1). Furthermore, some of the studied specimens have branching (Fig. 3(A)), although Alcyonidopsis does not show any branched features. Therefore, the specimens from the Hayama Group are ascribed to Phymatoderma. With respect to the ichnospecies, the studied specimens might be ascribed to P. granulata or P. melvillensis Uchman and Gaz´dzicki,

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Table 1 List of the studied specimens of Phymatoderma cf. granulata from the Miocene Hayama Group. Pellet width (mm) Pellet length (mm) Pellet aspect ratio View Locality Specimen Tunnel No. diameter (average  SD) (average  SD) (average  SD) (mm)a Nobi

Morito

Nb01

17.6

N.A.

N.A.

N.A.

Nb02

–

N.A.

N.A.

N.A.

Nb03

–

–

–

–

Nb04

12.05

0.82  0.37

1.48  0.74

1.82  0.40

Nb05

13.8

0.47  0.13

0.84  0.22

1.81  0.32

Nb06

13.05

N.A.

N.A.

N.A.

Nb07

20.05

N.A.

N.A.

N.A.

Mr01

11.75

0.84  0.65

1.49  1.24

1.77  0.22

Mr02

20.4

1.24  0.42

2.24  0.77

1.83  0.40

Mr03

12.85

0.82  0.16

1.48  0.35

1.81  0.36

Mr04

17.5

0.58  0.13

1.04  0.31

1.80  0.36

Mr05

7.7

0.58  0.14

1.05  0.31

1.83  0.46

Mr06

–

–

–

–

Mr07-07’

18.05

1.08  0.39

1.95  0.63

1.90  0.61

Slightly-moderately oblique to the bedding plane –

Vertical to the bedding plane Slightly oblique to the bedding plane Maybe parallel to the bedding plane Slightly oblique to the bedding plane Slightly oblique to the bedding plane Slightly oblique to the bedding plane Slightly oblique to the bedding plane Slightly oblique to the bedding plane Parallel to the bedding plane Slightly oblique to the bedding plane Vertical to the bedding plane Parallel to the bedding plane

Note

UMUT collection No.

Sampling

UMUT-CW31810

Doubtful specimen (pellets are only weakly visible or non-visible)

Sampling

UMUT-CW31811

Reburrowed with Chondrites

Probably reburrowed with ?Chondrites

Sampling

UMUT-CW31812

Sampling, thin-section analysis, SEM analysis

UMUT-CW31813

UMUT: The University Museum, The University of Tokyo; N.A.: not analyzed. a Tunnel diameter was measured at more or less parallel surface to the bedding plane.

2010 based on their overall morphology. Tunnel filled with pelleted sediments that show local meniscate structure is a diagnostic feature of P. melvillensis (Uchman and Gaz´dzicki, 2010). However, P. granulata from the Lower Jurassic of Germany also shows pellets with a transversally backfilled pattern (Fu, 1991; Seilacher, 2007), although this feature can be seen only at the margins of each tunnel due to preservation problems (Fu, 1991). Actually, Phymatoderma specimens from the Cenozoic of Argentina (i.e., upper Eocene Cerro Colorado Formation, lower Oligocene Marı´a Cristina beds) and from the Pliocene Onzole Formation in Ecuador display packed pellets and local menisci (Miller and Aalto, 1998; Miller and Vokes, 1998; Ponce et al., 2007). Thus, further ichnotaxonomic studies on P. granulata and P. melvillensis are required. Local meniscate structures were not recognized in the pelletal infill of the present specimens (Fig. 3), although the number of studied specimens is quite small (Table 1). The type material of P. granulata from the Lower Jurassic of Germany shows secondorder branches, which are similar to Chondrites, and small appendages in some cases (Fu, 1991; Seilacher, 2007; Izumi, 2012, 2013; Izumi et al., 2014). However, second-order branches and small appendages were not recognized in the present specimens from the Hayama Group. With respect to the pellet morphology, mean value of the pellet aspect ratios of the studied specimens ranges from 1.77 to 1.90 (Table 1; Fig. 5(A)), which is similar to that of P. granulata from the Lower Jurassic of Germany (1.71  0.36; Izumi et al., 2014; Fig. 5(A, B)). In contrast, aspect ratios of pellets of P. melvillensis from the Miocene Cape Melville Formation of Antarctica and P. cf. melvillensis from the Krishna–Godavari Basin are much larger: 2.41  0.62 and 2.3  0.20, respectively (Mazumdar et al., 2011; Izumi and Uchman, 2015; see also Fig. 5(A, B)). However, further studies are required to verify the utility of pellet morphology as an ichnotaxobase of

Phymatoderma. Considering all these lines of evidence, the present specimens are ascribed to P. cf. granulata. 5. Results of microscopic observations As a result of thin-section analyses, abundant dark brown- to black-colored amorphous organic debris of various sizes were recognized within the pelletal infill of P. cf. granulata (Fig. 6(A, B)), along with inorganic mineral particles that are the main component. In addition, several types of microfossils, such as planktic foraminifera and radiolaria, were commonly recognized in the pellets (Fig. 6(C, D)). Fragmented tests of indeterminate microfossils were also recognized during SEM observation (Fig. 6(E)). Furthermore, SEM analysis revealed the common occurrence of occasionally aggregated framboidal pyrite grains in the pellets (Fig. 6(F, G)). 6. Discussion 6.1. Possible trace-maker Recent ichnological study of the Miocene–Pliocene Misaki Formation of central Japan suggested that the trace-maker of Phymatoderma was a deep-sea echiuran worm, considering the co-occurrence of a horizontal star-shaped trace fossil and Phymatoderma (Izumi and Yoshizawa, in press). Based on the integration of morphological comparison and deep-sea biology, the star-shaped trace fossil and Phymatoderma were interpreted to have been echiuran feeding and fecal traces, respectively. Therefore, it may be interpreted that the trace-maker of Phymatoderma was an echiuran worm, if co-occurrence of a star-shaped trace fossil and Phymatoderma is recognized from the

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Fig. 3. Phymatoderma cf. granulata from the Miocene Hayama Group. A. Overall morphology of the specimen showing first-order branching. Dashed lines represent the inferred tunnel contours. Arrow emphasizes the branching. Specimen Mr02. B. Slightly curved tunnel. Specimen Nb01. C. Magnified photograph of the tunnel. Note the presence of ellipsoidal pellets (arrow). Specimen Mr06. D. Cross-sectional view of the tunnel. Note the presence of well-preserved ellipsoidal pellets (arrow). Specimen Mr07070 . Scale bars: 2 cm (A), 5 mm (C, D).

same lithological unit, especially in the case of deep-marine strata. Although horizontal star-shaped trace fossils were not discovered from the Hayama Group, it may be reasonable to assume that the trace-maker of Phymatoderma from the Hayama Group was also a deep-sea echiuran worm because of the following reasons. The first reason is tectonic and paleoenvironmental similarities between the Hayama Group and Misaki Formation According to previous tectonic studies, the sedimentary sequence in the Miura Peninsula is an accretionary complex that was formed by the subduction of the Philippine Sea Plate (Ogawa et al., 1985; Fig. 2). Thus, the lithological units of the southern (Misaki Formation) and middle parts (Hayama Group) of the Miura Peninsula are tectonically and paleogeographically closely related (Fig. 2). In addition, paleobathymetrical settings of the Misaki Formation and Hayama Group were generally similar (e.g., bathyal to abyssal zone; Akimoto et al., 1991, 1995; Kitazato, 1997), although the Misaki Formation represents a slightly deeper environment (2000-3000 m water depth; Akimoto et al., 1991; Kitazato, 1997). Considering these lines of evidence, it is likely that the ancient echiuran worms belonging to probably the same or closely related

species, which were the possible trace-makers of Phymatoderma (Izumi and Yoshizawa, in press), lived within the sea-floor sediments of both the Hayama Group and Misaki Formation (Fig. 2). The second reason is the morphometric similarity of Phymatoderma specimens from the Hayama Group and Misaki Formation Table 2 summarizes the morphometric parameters (tunnel diameter and pellet aspect ratio) of Phymatoderma from both units. As Fig. 7 clearly shows, Phymatoderma specimens from the Hayama Group and from the Misaki Formation do not significantly differ (P > 0.05) based on both tunnel diameter and pellet aspect ratio. Although a characteristic star-shaped trace fossil was not found from the Hayama Group, such morphometric similarity probably suggests that the same echiuran worm or a closely related species was the trace-maker of Phymatoderma in both units. In addition, reburrowed nature of Phymatoderma (Fig. 4) may be consistent with the interpretation that the trace-maker was a deep-sea echiuran worm. Because deep-sea echiurans excrete nitrogenous-rich fecal pellets that could be utilized by fecal symbionts (Jumars et al., 1990), such ‘‘microbe-rich’’ echiuran fecal

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Therefore, further investigation is needed for more precise discussion about the trace-maker identification. 6.2. Ontogeny of the trace-maker

Fig. 4. Field photograph of Phymatoderma cf. granulata that was reburrowed with Chondrites (arrow). Specimen Mr01. Scale bar: 5 mm.

material might have been reburrowed by other smaller benthic organisms (e.g., Chondrites-producer) as a feeding locus. Nevertheless, as mentioned earlier in this section, horizontal star-shaped trace fossil, which might be interpreted as feeding trace of a deepsea echiuran worm, could not be recognized in the Hayama Group.

It is demonstrated that there is a positive correlation between the size of fecal pellets and tunnel diameter (Fig. 5(C); Table 2), although the data vary widely. Because it is reasonable to assume that the pellet size is a good proxy for the size of gut/anus of the trace-maker, Fig. 5(C) suggests that a larger echiuran worm, which is a possible trace-maker (see Section 6.1), has larger gut and/or anus. However, aspect ratios of fecal pellets do not show any significant correlation with the tunnel diameter (P > 0.05; Fig. 5(A)). This fact possibly indicates that there was no significant change in digestive and/or excretory systems from the smaller to the larger echiuran worms. Furthermore, early development of Echiura includes a planktic trochophore larva (Ruppert et al., 2003) and it is reasonable to consider that burrowing into the sea-floor sediments started only after settlement and full development of a young specimen of an echiuran worm. Considering all these lines of evidence, it can be suggested that small P. cf. granulata was produced by smaller, younger (but not larval) echiuran individuals of the same species as the larger ones. Thus, the positive correlation

Fig. 5. Pellet aspect ratios and dimension of Phymatoderma. Plot and bar represent the sample mean and standard deviation values, respectively. A. Phymatoderma cf. granulata from the Miocene Hayama Group. Note that pellet aspect ratios do not show any significant correlation (P > 0.05) with the tunnel diameter. B. Other Phymatoderma specimens. Data based on: Lower Jurassic P. granulata: Izumi et al. (2014): Miocene P. melvillensis: Izumi and Uchman (2015); Holocene P. cf. melvillensis: Mazumdar et al. (2011). C. Relationship between the size of fecal pellets and tunnel diameter. Note the presence of a positive correlation between these parameters.

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Fig. 6. Photomicrographs of the pelletal infill of Phymatoderma cf. granulata from the Hayama Group. Specimen Mr07-070 . Thin-section photomicrographs focusing on the presence of dark brown- to black-colored organic debris (A, B), planktic foraminifer (C), and radiolarian (D). E. SEM photomicrograph (secondary ion image) showing the presence of fragments of an indeterminate microfossil (possibly radiolarian). F, G. SEM photomicrographs (backscattered electron images) focusing on framboidal pyrite grains. In some cases, scattered distribution of framboidal pyrite grains is observed (F), but occasionally they occur as aggregate (G). Scale bars: 200 mm (A, B), 100 mm (C, D), 10 mm (E), 20 mm (F, G).

between the size of pellets and tunnel diameter probably reflects the ontogenic change of the trace-making echiuran worms. To verify this interpretation, it is important to compare the pellet aspect ratios of modern deep-sea echiuran worms of various sizes with those in the studied Phymatoderma. However, most deep-sea echiurans produce L-shaped burrows and excrete fecal pellets into the subsurface burrows (Ohta, 1984; de Vaugelas, 1989). Therefore, fecal pellets of modern deep-sea echiurans cannot be observed by sea-floor photography. Further investigation using a novel burrow casting method (see Seike et al., 2012) will probably enable the direct observation of the fecal pellet morphology of modern deep-sea echiuran worms. 6.3. Diet of the trace-maker Potential food sources for all deposit feeders are fresh organic fractions in ingested sediment particles, such as microbes,

plankton, meiofauna, microalgae and non-living organic matter (Lopez and Levinton, 1987; Levinton, 1989; Mayer, 1989). Therefore, in the case of fossil fecal pellets excreted by deposit feeders, it is highly reasonable to assume that organic matter and/ or microfossils preserved within the pellets were the actual diets of the producers. In particular, amorphous organic debris (e.g., phytodetritus) and various types of microfossils (e.g., coccoliths, diatoms, dinoflagellates, planktic foraminifera, and radiolaria) have been actually observed within the pelletal infill of Phymatoderma (Miller and Vokes, 1998; Olivero et al., 2004; Miller, 2011; Izumi, 2013; Izumi et al., 2014; Izumi and Yoshizawa, in press). This study provides new evidence that amorphous organic debris, which may be interpreted as having a phytodetritial origin, and several types of microfossils (planktic foraminifera and radiolaria) are preserved in the fecal pellets of P. cf. granulata from the Miocene Hayama Group (Fig. 6(A–D)). This suggests that such materials were the main dietary sources for the trace-maker.

Table 2 Morphometric comparison of Phymatoderma between the Hayama Group and Misaki Formation. For the latter, pellet aspect ratios were newly measured using ImageJ based on Izumi and Yoshizawa (in press: fig. 2-3 to 2-6).

Hayama Group Misaki Formation

Tunnel diameter (mm)

Pellet aspect ratio

Note

14.98  3.99 (n = 11) 13.97  4.13 (n = 76)

1.82  0.04 (n = 8) 1.79  0.15 (n = 4)

This study Izumi and Yoshizawa (in press)

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any correlation with the tunnel diameter, suggesting that there was no significant change in digestive and/or excretory systems from the smaller to the larger echiuran worms. Furthermore, thinsection and SEM analyses revealed that organic debris, planktic foraminifera, radiolarian, and framboidal pyrite grains are commonly observed in the pelletal infill of P. cf. granulata. Therefore, fresh organic fractions and microorganisms might have been actually fed upon by the trace-maker. Acknowledgments

Fig. 7. Comparison of morphometric parameters of Phymatoderma between the Hayama Group and Misaki Formation (Table 2). Data are represented as the sample mean value  standard deviation; n.s.: not significant (P > 0.05). Data on Phymatoderma from the Misaki Formation are based on Izumi and Yoshizawa (in press). Note that the Misaki Formation is tectonically and paleoenvironmentally closely related to the Hayama Group (Fig. 2).

In addition, the occurrence of framboidal pyrite grains suggests the presence of fresh organic fractions in the fecal pellets of the trace-maker (Fig. 6(F, G)). Pyrite is a common mineral product of early diagenesis in organic-rich fine-grained sediments, and is generally formed by reactions between iron and sulphide produced by anaerobic sulphate-reducing bacteria (Berner, 1970, 1984; Berner and Westrich, 1985; Skyring, 1987). A key control on pyrite formation is the amount and reactivity of organic matter within the sediment, which controls the rate of sulfide production by these bacteria (Berner, 1970; Westrich and Berner, 1984). It is well known that the organic matter content in fecal pellets excreted by modern deposit feeders is generally higher than that in surrounding sediments, and that the inner microenvironment of fecal pellets is anoxic (Reise, 1985). Thus, it may be considered that the microenvironment of fecal pellets by deposit feeders is suitable for pyrite formation. Actually, previous studies demonstrated the occurrence of sulfate-reducing reactions within the fecal pellets excreted by modern deposit-feeding gastropods and bivalves (Jørgensen, 1977). Therefore, a common presence of framboidal pyrite grains in the pelletal infill of P. cf. granulata also suggests that fecal pellets excreted by the trace-maker originally contained, at the time of excretion, a significant amount of fresh organic fractions, a part of which might have been a dietary source. Furthermore, considering that calcareous nannofossils, diatoms, and siliceous dinoflagellates are recognized from the Hayama Group (Ling and Kurihara, 1972; Eto et al., 1987; Haga and Suzuki, 1999), these phytoplanktons might have also been fed upon by the trace-maker of P. cf. granulata. 7. Conclusions In this study, the trace fossil P. cf. granulata has been discovered and systematically described from the Miocene deep-marine deposits of the Hayama Group, Miura Peninsula, central Japan. Based on the comparison between these P. cf. granulata specimens and other Phymatoderma specimens from tectonically and paleoenvironmentally similar settings (e.g., Misaki Formation, Miura Peninsula), a deep-sea echiuran worm was interpreted as the possible trace-making animal. In addition, morphometric analysis demonstrated that the pellet aspect ratios do not show

The author thank Kazuyoshi Endo (University of Tokyo) for his supervision throughout the present study. The author is also indebted to Aya Okubo (University of Tokyo) for her assistance with SEM analysis, Megumi Saito-Kato and Kaoru Ogane (National Museum of Nature and Science, Tokyo) for their helpful information about microfossils, and Yasuhiro Ito (The University Museum, University of Tokyo) for his assistance with housing the Phymatoderma specimens at the museum. This work was financially supported by a grant from the Japan Society for the Promotion of Science awarded to K.I. (24-8818). The manuscript was greatly improved by the comments provided by the Editor in Chief (Dr. Gilles Escarguel), Associate Editor (Dr. Davide Olivero), and two reviewers (Drs. Eduardo B. Olivero and William Miller, III).

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