Palaeoecology of Macaronichnus segregatis degiberti: Reconstructing the infaunal lives of the travisiid polychaetes

Palaeogeography, Palaeoclimatology, Palaeoecology 516 (2019) 284–294

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Palaeoecology of Macaronichnus segregatis degiberti: Reconstructing the infaunal lives of the travisiid polychaetes

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Masakazu Naraa, , Koji Seikeb a b

Department of Biological Sciences, Kochi University, 2-5-1 Akebono-cho, Kochi 780-8520, Japan Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology (AIST), Central 7, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8567, Japan

A R T I C LE I N FO

A B S T R A C T

Keywords: Macaronichnus segregatis degiberti Travisia Ethology Interindividual behaviour Exploration

Macaronichnus segregatis degiberti, a relatively large ichnosubspecies of Macaronichnus segregatis, is an almost straight to gently curved, cylindrical, fossilized burrow, oriented horizontal to oblique to the bedding plane. It is interpreted as a pascichnial trace fossil formed through selective sand feeding and excretion of a free-living polychaete, such as a relatively large travisiid (formerly classified as opheliid or scalibregmatid) polychaete Travisia. While the other ichnosubspecies, i.e., M. s. segregatis, M. s. lineiformins, M. s. meandriformis, and M. s. spiriformis, are commonly 2–5 mm in diameter and occur exclusively in foreshore deposits, M. s. degiberti attains a diameter of up to 15 mm and shows wide environmental distribution, ranging from tidal channels, tidal sand bars, tidal sandridges, tidal flats, upper to lower shorefaces, bioturbated sandy shelves, shelf storm-sheets, to shelf sand ridges. The core of M. s. degiberti, consisting mainly of light mineral-rich sand grains, is composed of alternating lamellae of light mineral-rich and heavy mineral-rich sands, arranged oblique to the bedding plane. On the other hand, the mantle, composed mainly of heavy mineral-rich sands, has a smooth outline, or evenly spaced lobes flanked on both sides. The morphology of the mantle lobes and core lamellae suggests repeated pulses of sediment probing and excreting behaviour of the tracemaker. Two or more burrows of this ichnosubspecies tend to occur adjacently, sometimes intertwining. As Travisia develops directly, lacking any planktic larval stages, aggregations of the burrows can be interpreted to reflect the burrowers' interindividual exploratory behaviour with the aim of copulation. Travisia, also known as a “stink worm”, secretes volatile chemical substances that might act as sex pheromones to attract other individuals for reproduction within the substrate. Therefore, a new category of ethological classification of trace fossils “sequorichnia” (sequor, follow; and ichnia, traces), for exploration of other individuals, is proposed here. This is the first record of interindividual exploratory behaviour of infaunae.

1. Introduction Trace fossils, also known as “fossil behaviours (Seilacher, 1967)”, have long been used to reconstruct the ethology of ancient tracemakers (cf., Seilacher, 2007). Such ethology-oriented ichnological studies have achieved high success (e.g., Ekdale and Bromley, 2001; Nara and Ikari, 2011). This is because: 1) observation of the behaviour of modern infauna is difficult because biogenic structures are concealed within the substrate, 2) their traces have higher potential for preservation than those of epifauna, and 3) diagenetic processes and differential weathering may enhance the visibility of subtle and minute structures suggesting how they were formed (cf., Akiyama and Nara, 2007; Savrda, 2007). These factors enable ichnology to be used as a powerful tool to delineate such hidden infaunal lives.

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Macaronichnus segregatis Clifton and Thompson (1978), a fossil burrow characterised by mineralogical segregation between the core and mantle, is an almost straight to strongly curved, cylindrical structure (mostly 2–9 mm in diameter) oriented parallel or oblique (very rarely perpendicular) to the bedding plane. It is characteristic of shallow marine sandy substrates (e.g., Clifton and Thompson, 1978; Nara, 1994; Bromley, 1996; Pemberton et al., 2001; Gingras et al., 2002; Nara and Seike, 2004; Uchman and Krenmayr, 2004; Bromley et al., 2009; Quiroz et al., 2010; Seike et al., 2011; Uchman et al., 2016; Buatois et al., 2017). Based on various studies, ranging from the analysis of fossil material to observations of modern trace-makers, freeliving and selective deposit-feeding polychaetes (family: Opheliidae), which feed on epigranular biofilms and organic detritus in sand (cf., Clifton and Thompson, 1978; Rouse and Pleijel, 2001), were found to

Corresponding author E-mail addresses: [email protected] (M. Nara), [email protected] (K. Seike).

https://doi.org/10.1016/j.palaeo.2018.12.011 Received 17 July 2018; Received in revised form 6 December 2018; Accepted 16 December 2018 Available online 19 December 2018 0031-0182/ © 2018 Elsevier B.V. All rights reserved.

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produce identical structures while foraging and excreting (Clifton and Thompson, 1978; Nara, 1994; Nara and Seike, 2004; Dafoe et al., 2008a, 2008b; Gingras et al., 2008; Seike et al., 2011). Although the behaviour of the opheliids is usually hidden in the sandy substrates, up to a few decimetres below the surface (Nara and Seike, 2004), it has mostly been revealed by neoichnological studies on the modern counterpart of M. segregatis. For example, Seike (2007, 2008, 2009) studied incipient M. segregatis, i.e., modern burrows produced by the polychaets Thoracophelia (former Euzonus: Blake, 2011) in a wave-dominated sandy beach of Japan, and found that this worm left several morphologically distinctive traces in response to beach morphodynamic processes, as follows. Under relatively stable fair-weather conditions, the polychaete Thoracophelia almost freely burrowed around in the sand with a slight preference of orientation, perpendicular to the coastline. On the other hand, it moved preferentially normal to the shoreline under highly erosive storm conditions, in order to avoid exhumation from the substrate due to storm-induced coastal erosion (Seike, 2007, 2008, 2009). Thoracophelia thus varies its behaviour in response to the beach morphodynamics, i.e., erosion versus deposition, of their habitats. This knowledge can be used to reconstruct “fossilized-polychaete behaviour” in the rock record, as discussed by Seike et al. (2015). To reconstruct tracemaker behaviour, scrutiny of trace fossil morphology is essential (cf., Nara, 1995, 2006; Olivero and Lopez Cabrera, 2010). However, the size and constituent material of most M. segregatis, that is, a few-millimetre-thick burrows consisting of fine- to mediumgrained sand grains, make it difficult to record minute structures to elucidate their formative processes. Moreover, the structures are too small to be easily observed, preventing M. segregatis from being fully understood palaeoecologically (Seike et al., 2011). Macaronichnus segregatis degiberti Rodríguez-Tovar and Aguirre, 2014 is a relatively large ichnosubspecies of M. segregatis, with a diameter commonly of 5–9 mm, and rarely 15 mm (Curran, 1985). This ichnosubspecies is found in sandy deposits of various shallow-marine environments, ranging from upper slope to tidal flat. Although size itself is not a valid ichnotaxobase in general, some ichnotaxa are classified based largely on their sizes (Bertling et al., 2006). Moreover, such size segregation between M. s. degiberti and other ichnosubspecies can be seen in many sedimentary bodies of various ages and places (Seike et al., 2011). These facts validate separation of the large morphotype from the other morphotypes. Furthermore, the size of M. s. degiberti may enable observation of its detailed structures for ethological reconstruction (Seike et al., 2011). Thus, the authors made detailed observations of M. s. degiberti based on specimens from Palaeozoic to Cenozoic deposits of North America, Europe, and Asia, in addition to “topotype” specimens of M. s. degiberti occurring in Miocene deposits of southern Spain, and modern incipient burrows (cf., Seike et al., 2011) (Fig. 1), and obtained new insights on autecology of the tracemakers as described here.

Fig. 1. Map showing the localities of the specimens detailed in the following figures. A: The Middle Ordovician Naranco Formation, Spain. B: Upper Miocene deposits along the El Roqueo Beach, where “topotype” specimens of M. s. degiberti occur. Spain. C: The Miocene Tatsukushi Formation, Japan. D: The Miocene Taliao Formation, Taiwan. E: Modern deposits in the Nijigahama Coast, Japan. F: The Lower Cretaceous Inubozaki Formation, and Pleistocene Ichijiku, Kongochi, Yabu, and Kioroshi formations, Japan. G: The Middle Miocene Shirahama Formation, Japan. H: The Upper Cretaceous Horseshoe Canyon Formation, Canada.

(Curran, 1985). In most cases, the core is seemingly composed of structureless sediments. However, it is actually made up of a series of imbricate lamellae, with alternating lamellae of slightly light mineral- and heavy mineral-rich sands (Figs. 5–8). Such characteristics are particularly obvious when using X-ray radiographs (Fig. 6). Each lamella has a shallow trough-like shape (Figs. 6, 7), and can be seen as a meniscate structure in horizontal section (Figs. 6E, F, 8). On the other hand, the mantle consists of almost regularly spaced lobes flanked on both sides (Figs. 3, 6, 9). Each lobe partly crosscuts the adjoining lobe, and is, in turn, partly crosscut by another lobe on the opposite side (Fig. 6E, F). The burrow may partially lack a mantle (Fig. 3). Smooth, non-lobed mantles may also be present (Fig. 3). Branching of the burrows may be common (Fig. 9), and can be classified as secondary successive branching (sensu Bromley, 1996), or false branching (Pearson et al., 2013; Rodríguez-Tovar and Aguirre, 2014; Caruso and Monaco, 2015). If the burrow lacks its mantle at the branching point, two cores seemingly merge together (Fig. 3). Such a branching pattern may be almost identical to a primary branching (sensu Bromley, 1996). 2.2. Mode of occurrence M. s. degiberti is distributed with varying density in sandstone (Fig. 2). Even in neighbouring sedimentary units, the densities present considerable local differences (Fig. 2B, C). For example, Fig. 2B shows the concentration of M. s. degiberti in Piscichnus waitemata, a fill of a rayfeeding pit (Gregory, 1991; Kotake and Nara, 2002). On the other hand, Fig. 2C shows the marked contrast of the burrow densities between a sparsely burrowed storm sand sheet and erosively overlying storm sands with abundant M. s. degiberti. False branching or burrow overlap is quite common, especially in densely occurring specimens. Moreover, a burrow tends to occur alongside a single or multiple burrow(s), even in sparsely occurring cases (Figs. 2E, 3, 4, 9). Such specimens appear to be paired or entangled. Cases that are paired or entangled can be traced together for more than a few decimetres, before they segregate. If such a deviated burrow meets another, the former may then start following the latter (Fig. 9B).

2. The trace fossil Macaronichnus segregatis degiberti 2.1. Morphology It is a gently curved, cylindrical burrow, oriented almost parallel to oblique to the bedding plane, and is composed of a core and a mantle, both of which are characterised by mineralogical segregations. The core and mantle usually consist of light mineral-rich, and heavy mineral- or lithic fragment-rich sand grains, respectively (Figs. 2, 3). However, the opposite combination, with a heavy mineral-rich core and light mineral-rich mantle, also exists in very rare cases (Nara, 2014) (Fig. 4). The core is normally circular in cross-section but is sometimes elliptical due to compaction. Although the maximum range of the core diameter is 2–15 mm, it commonly ranges from 5 to 9 mm (in width for the probable compacted ones). The largest specimen (15 mm) is a very rare example and was reported from the Cretaceous deposits of Delaware

2.3. Environments The ichnosubspecies present wide environmental distribution, ranging from intertidal to continental shelves. They have been found to occur in sandy deposits of tidal channels (Nara et al., 2007), tidal bars 285

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Fig. 2. Photographs showing Macaronichnus segregatis degiberti. A: Upper shoreface specimens of the Pleistocene Yabu Formation, Kisaradu City, central Japan. Vertical section. B: Offshore transition specimens occurring in a fill of Piscichnus waitemata. Lower Miocene Taliao Formation, Yehliu, northern Taiwan. Horizontal section. C: Offshore transition specimens of the middle Miocene Shirahama Formation in Shirahama Town, central Japan. The mechanical pencil is for scale. Vertical section. D: “Topotype” specimens of M. s. degiberti occurring in Miocene sandy shelf deposits near Cádiz, SW Spain. Vertical section. E: Sparsely occurring lower shoreface specimens of the Lower Cretaceous Inubozaki Formation, Choshi, Japan. The finger shows the scale. Note that they sometimes exist in pair. Horizontal section. F: Upper shoreface specimen of the Upper Cretaceous Horseshoe Canyon Formation, Drumheller, Canada. Vertical section. Note that the specimens are flattened owing to compaction.

reported in previous studies (e.g., Masuda and Yokokawa, 1988; Nara, 1998; Tamura and Masuda, 2005).

and sandridges (Olariu et al., 2012; Pearson et al., 2013), tidal-flat sand sheets (Nara et al., 2007, 2017), shorefaces (Masuda and Yokokawa, 1988; Nara, 1998; Tamura and Masuda, 2005; Kotake, 2007; Seike et al., 2011), bioturbated sandy shelf (personal observation by MN), shelf storm-sheets (Nara, 1998; Aguirre et al., 2010), shelf sandridges (Nara, 2014; Rodríguez-Tovar and Aguirre, 2014) (Fig. 10), and upper slopes (Pérez-Asensio et al., 2017). Despite such wide environmental distribution, it has not been found in wave-dominated foreshore sands (Seike et al., 2011), where other smaller ichnosubspecies such as M. s. segregatis Clifton and Thompson, 1978, M. s. lineiformins Bromley and Uchman in Bromley et al., 2009, M. s. meandriformis Bromley and Uchman in Bromley et al., 2009, M. s. spiriformis Bromley and Uchman in Bromley et al., 2009, typically occur (cf., Seike et al., 2011) (Figs. 10, 11). Such environmental segregation between M. s. degiberti and the other ichnosubspecies is clear. For example, comparative studies of burrow sizes in a prograding shoreface-to-beach section showed that shoreface sediments commonly yield larger groups of Macaronichnus than those in foreshore settings (Figs. 10, 12, 13). This trend has been

2.4. Stratigraphic and geographic range Records of the ichnospecies of M. segregatis date back to the Early Cambrian age (Knaust, 2017). On the other hand, definite M. s. degiberti, or previously reported specimens identifiable with the ichnosubspecies based on descriptions and figures have been reported from Palaeozoic to Cenozoic sediments of various places. These include sediments from the Ordovician of Norway (Knaust, 2004), the Ordovician of Spain (personal observation by MN: Fig. 9C), the Carboniferous of Brazil (Gandini et al., 2010), the Permian of Australia (Ban and Fielding, 2004), the Cretaceous of England (Middlemiss, 1962) and the United States (MacEachern and Pemberton, 1992; Walker and Bergman, 1993), the Eocene of Spain (Olariu et al., 2012), the Miocene of Japan (Hatai and Kotaka, 1961; Kotake, 2007; Nara and Aikou, 2016), Patagonia (Carmona et al., 2008, 2009), Denmark (Radwanski et al., 1975), Spain (Rodríguez-Tovar and Aguirre, 2014; Pérez-Asensio Fig. 3. Light-coloured cores and dark-coloured mantles. A: Polished surface of the specimens from the middle Miocene Shirahama Formation, Japan. Section parallel to the bedding plane. B: Schematic drawing of A. Outlines of the mantle are either protruded (solid triangles) or smooth (open triangle). The mantle may lack certain parts (solid circle). The cores are seemingly merged where the burrows lack their mantle (open circle).

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Fig. 4. Although most specimens of the Macaronichnus segregatis degiberti consist of light-coloured core fills and dark-coloured mantles, those with darker cores and lighter mantles are rare. A: Specimens occurring in shelf sandridge sediments of the middle Pleistocene Ichijiku Formation, central Japan (cf., Nara, 2014). Vertical section. Note that two or three burrows occur side-by-side. B: Ichijiku specimens. Paired occurrences are also seen. Horizontal section. C: A specimen in upper shoreface sediments of the upper Pleistocene Kioroshi Formation, central Japan. Note, a dark-coloured fill specimen occurs with “normal” specimens that have lighter-coloured fills. Horizontal section. D: A drawing of figure C.

3. Palaeoecology 3.1. Identity of the tracemaker The trace fossil Macaronichnus segregatis is considered a pascichnial trace of an actively burrowing polychaete that feeds on epigranular biofilms and organic detritus in sand (Clifton and Thompson, 1978; Nara, 1994; Dafoe et al., 2008a, 2008b; Seike et al., 2011). Based on field and experimental studies, Clifton and Thompson (1978) confirmed that the modern opheliid polychaete, Ophelia limacina, living in the modern intertidal sands, segregates sand particles while feeding. Other opheliids, such as Thoracophelia, have also been confirmed to be tracemakers (Gingras et al., 2002; Nara and Seike, 2004; Seike, 2007, 2008, 2009; Dafoe et al., 2008a, 2008b). Later, Seike et al. (2011) found modern burrows identical to M. s. degiberti from shoreface sand bar deposits in Japan. They also collected large (up to 8 mm in diameter and 80 mm in length: Seike et al., 2011) polychaete Travisia japonica from the same locality. The worms lived in the same sediment that contained the burrows, had body sizes comparable to the burrows, and, based on the analysis of gut contents, selectively ingested light mineral-rich sands (Seike et al., 2011). These findings led to the conclusion that the worms were the tracemakers of the incipient M. s. degiberti (Seike et al., 2011). Travisia is a short but stout, actively burrowing, and deposit-feeding polychaete, with a relatively large body size (Fauchald and Jumars, 1979; Seike et al., 2011, and references therein). Although the genus was formerly classified into the family Opheliidae (e.g., Rouse and Pleijel, 2001) or Scalibregmatidae (Bleidorn et al., 2003; Paul et al., 2010), it is now assigned to the family Travisiidae (Read and Fauchald, 2018) based on molecular phylogenetic studies. The polychaets Travisia are widely distributed around the world, and their habitats range from tidal flats to the deep sea (Seike et al., 2011). However, they have never been found in foreshore deposits in wave-dominated sandy beaches, where the smaller opheliid characteristically inhabited (Seike et al., 2011). This environmental distribution pattern of modern Travisia matches well with that of M. s. degiberti (Seike et al., 2011). Seike et al. (2011) ascribed such habitat segregation to the worms' preference (or tolerance) to the substrate. In the foreshore setting, the sandy substrates are harder than those of subtidal substrates due to slight compaction caused by suction dynamics (negative pore-water pressure relative to atmospheric air pressure) associated with tide- and

Fig. 5. Magnification of the sediment peel reported by Seike et al. (2011). A: Specimens of the incipient Macaronichnus segregatis degiberti. B: Line drawing of A. Note imbricate lamellae seen in the longitudinal section of the core (centre). Each lamella presents a trough-like shape and bends downward in the cross section (lower and upper). Vertical section. Specimens from the Nijigahama Beach, Hikari City, SW Japan.

et al., 2017), and Azores (Mayoral et al., 2013), the Pliocene of Spain (Aguirre et al., 2010), Pleistocene of Japan (Masuda and Yokokawa, 1988; Nara, 1998; Seike et al., 2011; Nara, 2014), Italy (Caruso and Monaco, 2015), Holocene of Japan (Tamura and Masuda, 2005), and modern seafloor sediment of Japan (Seike et al., 2011).

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Fig. 6. X-ray radiographs and respective line drawings of Macaronichnus segregatis degiberti. A, B: Two cross-sections are seen. Note, lamellate structures in the cores. A specimen from the middle Pleistocene Kongochi Formation. Vertical to the bedding plane. C, D: Longitudinal section. The lamellae of the core are obliquely arranged. From the middle Pleistocene Kongochi Formation. Perpendicular to the bedding plane. E, F: Longitudinally sectioned specimens running parallel to the bedding plane. Note, the lamellate structures can be seen as meniscate core fills, because each lamella is shaped like a shallow trough. The mantles consist of alternately arranged lobes. Middle Pleistocene Ichijiku Formation.

Fig. 7. Construction of Macaronichnus segregatis degiberti. The core, usually 5–9 mm but may attain 15 mm in diameter, and is composed of a series of shingled lamellae (=angle-of-repose laminae) consisting of light mineral-rich and slightly heavy mineral-rich sands. The entire core and mantle consist of light mineral-rich sand grains and heavy mineral-rich sand grains, respectively. However, the opposite combination with a heavy mineral-rich core and a light mineral-rich mantle also exists in very rare cases (Fig. 5).

Fig. 8. Weathered specimen of Macaronichnus segregatis degiberti on the bedding plane of an offshore-transition storm sand sheet, Miocene Tatsukushi Formation, SW Japan (cf. Nara and Aikou, 2016). As weathering made evenly spaced lamellae conspicuous, the burrow at the centre appears to show Arthrophycus-, Beaconites-, or Imponoglyphus-like expression.

wave-induced groundwater-level changes (e.g., Sassa and Watabe, 2007). The stiffer sediments were considered to have prevented relatively large Travisia from burrowing (Seike et al., 2011), because the optimal sediment hardness for burrowing worms was largely dependent on their body size (Sassa et al., 2009). In fact, during the course of a study, one of the present authors (KS) observed the effect of disturbances caused by large tsunami waves induced by the 2011 M9.0 Tohoku-Oki earth quake (e.g., Seike et al., 2013, 2018). An increase in the populations of Travisia sp. in subtidal sediments along the Sanriku Coast, NE Japan, was observed after the catastrophic event (personal observation by KS). Reworking and softening of the surface sediments by huge tsunami waves likely enhanced colonisation by the worms. The preference of burrowing in loosened sediment by the M. s. degiberti-producers can explain the contrasting burrow densities shown in Fig. 2B and C. The densely burrowed Piscichnus-fill, once reworked by a

ray's feeding (Gregory, 1991; Kotake and Nara, 2002), probably served looser sandy bottoms, which attracted the burrowers, as discussed by Kotake (2007). Reworking of the seafloor by storms also made sandy substrates looser than the underlying substrates, which were deposited at earlier times and underwent slight compaction (Fig. 2C). 3.2. Mode of production As noted above, M. segregatis is generally considered a pascichnial trace of a selective deposit-feeding polychaete. In other words, the light-mineral-rich sediment filling the core is probably composed of faeces from the tracemaker, which selectively ingested light-mineral 288

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Fig. 8). They interpreted such lamellae to be angle-of-repose laminae produced by a tracemaker that actively filled the burrow lumen, a view endorsed by the present authors. As the core of Macaronichnus was of faecal origin (Clifton and Thompson, 1978; Nara, 1994), each lamella probably reflects a single pulse of tracemaker excretion, reflecting a single pulse of hindgut peristalsis. The egested sands were probably crumbly and less bound by mucus, as they were laid in an angle of repose. The excreted sand was probably sorted slightly by their specific gravity to form the alternating laminae. Dafoe et al. (2008b) reported that Thoracopelia excreted their faeces with a pendular motion of its pygidium, resulting in the efficient packing of the tunnel. To date, no information is available on the excretion behaviour of Travisia. Nevertheless, such a motion may affect the shallow trough-like morphology of the lamellae, if it also egested faeces in a similar manner. Part of the burrow without a mantle is thought to indicate that the egested faeces were preserved, as the tracemaker had not fed on that part (Fig. 14). On the other hand, the mantle might occur solely without the associated core. However, such a structure has not been found yet. The lack of a core, which is more conspicuous with its colour, might prevent the structure from being noticed. The “meniscate” burrow fill and flanking successive lobes are reminiscent of the ichnogenus Nereites (Chamberlain, 1971; Rindsberg, 1994; Uchman, 1998), although its constituent material and morphology are different. The two architectural elements are likely essential components of the pascichnial traces of selective deposit-feeding worms. Although the ichnogenus Macaronichnuns is normally characterised by a dark-coloured mantle and a pale-coloured core, there are very rare examples of the opposite combination, as mentioned above (Fig. 4). Further comparative studies would provide insights into the mineral segregation. 3.3. Interindividual behaviour As noted above, M. s. degiberti frequently overlap or occur alongside the other individuals of this ichnospecies (Figs. 2E, 3, 4, 9). These modes of occurrence clearly reflect certain interindividual relationships. When considering the ecological implications of such occurrence modes, one might be reminded of branched specimens of Protovirgularia, a locomotion trace of a protobranch bivalve, reported by Nara and Ikari (2011). They interpreted the branched burrows to have been formed by trail-following activity of the bivalve; the animals were thought to have followed the pre-existing burrow, which consisted of softer sediment than the surrounding sediment to save energy for locomotion (Nara and Ikari, 2011). However, in the case of M. s. degiberti, the burrow courses do not overlap in most cases (Fig. 9). Therefore, an alternative explanation is necessary. Most marine invertebrate phyla have species with pelagic larvae and external fertilisation (Barnes et al., 1993). In fact, more than 70% of marine invertebrates in temperate zones have planktic larval stages (Barnes et al., 1993). In the case of the Opheliidae and Travisiidae, no asexual reproduction has been documented and the sexes are separate (Hermans, 1978; Rouse and Pleijel, 2001). In addition, most appear to freely spawn gametes into the water (Hermans, 1978; Wilson, 1991; Rouse and Pleijel, 2001). However, only 79 of 306 species studied were found to exhibit this form of sexual reproduction (Glasby et al., 2001), although polychaete reproduction was traditionally thought of in terms of external fertilisation and planktic larvae. For example, in the case of Travisia forbesii, females lay large eggs in gelatinous masses on the sediment or near their burrow opening, in which their larvae develop into juveniles; there is no pelagic phase (Rouse and Pleijel, 2001). The young hatch and become freely burrowing juveniles (Hermans, 1978). That is, Travisia develops directly. Although the detailed processes of Travisia reproduction are uncertain, direct intersexual interaction, i.e., copulation, is probably necessary to fertilise their gametes within sands.

Fig. 9. Specimens of Macaronichnus segregatis degiberti tend to occur alongside the other individual(s). Because of this, the burrows frequently overlap or present false branching. See text for a full discussion. A: Specimens in a tidal flat sand-sheet of the middle Miocene, Shirahama Formation, Japan. B: The same bed as A. The triangle shows a specimen that closes two different burrows. C: The oldest specimens observed by the present author (MN). Middle Ordovician Naranco Formation, Spain.

sand grains (Clifton and Thompson, 1978; Nara, 1994; Seike et al., 2011), while the heavy mineral-rich mantle was probably its “leftovers” (Nara, 1994; Seike et al., 2011). Although Travisia were considered nonselective deposit feeders in some biological literatures (e.g., Barnes, 1987; Rouse and Pleijel, 2001), ichnological studies have revealed that they are actually selective (Seike et al., 2011). However, the detailed processes of feeding and excretion have not been documented. The present study reveals that the mantle is actually composed of a series of lobes flanking both sides of the core, which are consecutively crosscut by the adjoining lobe (Fig. 6). Because the mantle was probably formed through active grain segregation by the tracemaker while feeding (Clifton and Thompson, 1978; Nara, 1994; Seike et al., 2011), it is likely that the successive lobes were formed while feeding by the pendular motion of the tracemaker's prostomium. Each lobe was likely formed by a single probing activity (Fig. 14). On the other hand, the core may provide key information to reconstruct tracemakers' excretory processes. The imbricate lamellae developed in the core (Figs. 5, 6) are highly similar to those found in a burrow fill of Phoebichnus trochoides by Evans and McIlroy (2016, 289

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Fig. 10. Selected columnar sections showing the environmental distribution of two types of Macaronichnus. Smaller ichnosubspecies of Macaronichnus segregatis, such as M. s. segregatis, M. s. lineiformins, M. s. meandriformis, and M. s. spiriformis, typically occur in the foreshore environment, whereas M. s. degiberti occur in various subtidal environments, such as shorefaces, tidal flats, tidal channels, offshore (shelf) storm sand sheets, and shelf sandridges. Middle Pleistocene deposits of the Kongochi, Yabu and Ichijiku formations, Boso Peninsula, Japan. Middle Miocene deposits of the Shirahama Formation, Kii Peninsula, Japan. Jz, Td, m, s, and g refer to the Jizodo Formation, terrace deposits, mud, sand, and gravels, respectively.

Fig. 11. Macaronichnus segregatis segregatis, a type ichnosubspecies of the ichnogenus Macaronichnus, occurs exclusively in foreshore sediments. (A) Upper Pleistocene Kioroshi Formation, Choshi, central Japan. Perpendicular to the bedding plane. (B) Middle Pleistocene Yabu Formation, Kisaradu, central Japan. Perpendicular to the bedding plane. (C) Lower Miocene Taliao Formation, Yehliu, Northeast Taiwan. (D) Upper Cretaceous Horseshoe Canyon Formation, Drumheller, Canada.

In fact, internal fertilisation is especially characteristic of a sort of marine infaunal invertebrates (Barnes et al., 1993). In contrast to the opheliid Armandia, which swarm up in the water column to spawn using their lateral eyes (Hermans, 1978), the entirely infaunal Travisia may not be able to rely on a visual organ (if present). The worms should therefore utilise an alternative sensor to explore their spouses for mating. In fact, Travisia is notorious for its strong volatile smell, and is also known as a stink worm (Rouse and Pleijel, 2001). Volatile organic substances secreted by some polychaetes are interpreted to be sex pheromones that attract other individuals (Hardege et al., 1996). In recent years, the important role of pheromones in reproduction has been confirmed in an increasing number of marine invertebrates (Watson et al., 2003). Considering these findings, the paired, or multiple-sets of M. s. degiberti most likely reflect the burrowproducing Travisia's exploratory behaviour, seeking other conspecifics for copulation, which was likely facilitated by residual sex pheromones in the burrows (Fig. 15). The paired or multiple-set of M. s. degiberti described here represent the first record of interindividual exploratory

Fig. 12. Size comparison (core width) of the smaller ichnosubspecies and Macaronichnus segregatis degiberti, both of which occur in foreshore and shoreface deposits, respectively. Data were collected from bedding planes of the Upper Cretaceous Edmonton Group (Horseshoe Canyon Formation), Canada; middle Miocene Tanabe Group, Japan; and the middle Pleistocene Shimosa Group, Japan. Two data sets collected from the different beds of the Edmonton Group are shown separately. Bars represent the standard deviations.

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Fig. 15. Inferred formation of multiple sets of parallel-running M. s. degiberti. The tracemakers, which have direct development in their larval stage, likely move along the older trace to catch up with other individuals for copulation. As Travisia secrete volatile compounds, they likely follow the residual compounds that act as pheromones attracting other individuals.

Fig. 13. Size comparison of the smaller ichnosubspecies and M. s. degiberti, both of which occur in foreshore and shoreface deposits, respectively. Data collected from the Upper Cretaceous Edmonton Group (Horseshoe Canyon Formation), Drumheller, Canada. Heights of the light-coloured core were measured in a vertical section. Each data set is collected from a single bed. Note, the cores were strongly flattened due to compaction. For example, those of the smaller ichnosubspecies having approximately 1.5 mm in height are approximately 3 mm wide in a horizontal section as shown in Fig. 10. Bars represent the standard deviation.

3.5. Palaeoenvironmental significance Considering their biology, the habitat segregation of the modern tracemakers of M. s. degiberti and other smaller ichnosubspecies, i.e. Travisiidae vs. Opheliidae, can be well explained. Seike et al. (2011) presented the geographical and environmental distribution of the genus Travisia; this occurs worldwide in sandy or muddy substrates ranging from the shoreface to deep-sea environments. The genus, however, has never been reported in the foreshores of wave-dominated sandy beaches (Seike et al., 2011). The lack of Travisia in the sandy foreshore can be explained by its poor ability to burrow into harder sand owing to its larger body size (Seike et al., 2011). Both ichnological and biological evidence described here confirm that M. s. degiberti characteristically occur in shallow- to deep-marine environments, except for high-energy sandy foreshore, which is indicated by the smaller ichnosubspecies (Tokuhashi and Endo, 1984; Masuda and Yokokawa, 1988; Tokuhashi and Kondo, 1989; Nara, 1994; Nara and Seike, 2004; Seike, 2007, 2008, 2009; Seike et al., 2011).

behaviour by infaunae.

3.4. Proposition of a new ethological category Recently, a trace fossil record of such an exploratory behaviour was reported from the Lower Carboniferous non-marine deposits in Scotland (Whyte, 2018). Several Diplicnites cuithensis, trackways of probable giant millipedes such as Arthropleura, running almost parallel and mostly touching each other, were found. As the trackways were partly overlapped, with one leaving one side of the tracks, the author assumed that the millipedes crept along adjacently leaving the parallel trackways. Then, one individual mounted the other from the side, likely for mating (Whyte, 2018). This may also be reminiscent of a mating trace in the case of M. s. degiberti. However, no evidence of mating has been found to date; further analysis is necessary. Nevertheless, probable traces of interindividual exploratory behaviour have been found in terrestrial (Whyte, 2018) and marine settings (this study). The present authors thus propose a new category of ethological classification of trace fossils “sequorichnia” (sequor, follow; and ichnia, traces) for exploratory behaviour. The traces of predators chasing their prey will also be included in this category.

4. Ichnotaxonomic notes Katto (1965) reported trace fossils comparable to M. s. degiberti from the Miocene Misaki Group, SW Japan (see, Nara and Aikou, 2016) and named them as “Nankaites kochiensis”. However, this was nomen nudum, because no diagnosis and type specimens were designated. Thereafter, the ichnospecies Macaronichnus segregatis was proposed by Clifton and Thompson (1978) based on the smaller specimens, 3–5 mm in diameter, from Jurassic deposits in Greenland to modern intertidal deposits. Although this original description did not provide a Fig. 14. Formative process of Macaronichnus segregatis degiberti, a feeding and excreting structure of a travisiid polychaete. The mantle is considered to be a feeding structure formed due to selective ingestion of (mostly) light-mineral grains, and may lack partially. On the other hand, the core represents faeces of the tracemaker. Due to the intermittent excrement by the animal, angle-of-repose laminae, which can be seen as a series of menisci in the horizontal section, are formed in the core. The solitary occurrence of the mantle suggests preservation of the feeding structure only, however, this has not yet been found.

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its larger size. This ichnosubspecies presents wide environmental distribution, ranging from tidal channels, tidal sand bars, tidal sandridges, tidal flats, upper to lower shorefaces, bioturbated sandy shelves, shelf storm-sheets, to shelf sand ridges, but is never found in wave-dominated foreshore sands, where smaller ichnosubspecies typically occur. The detailed morphology of mantle and core lamellae record repeated pulses of sediment probing and excreting behaviour of the tracemaker. Two or several burrows tend to occur side-by-side. As Travisia presents direct development that lacks any planktic larval stage, such aggregated occurrences can be interpreted to reflect the burrowers' interindividual exploratory behaviour aiming for copulation. The polychaetes Travisia, which secrete volatile compounds, may follow the residual compounds that acted as pheromones. Therefore, a new category of ethological classification of trace fossils “sequorichnia” (sequor, follow; and ichnia, traces) for exploration of other individuals is proposed. This is the first record of interindividual exploratory behaviour of infaunae.

diagnosis, Bromley and Uchman in Bromley et al. (2009) designated a diagnosis, validating the name M. segregatis. They also subdivided the ichnospecies into the four smaller ichnosubspecies, as noted above. Nara (1998) and Seike et al. (2011) highlighted the significance of their size separation of the larger morphotype. However, they still treated it as an open nomenclature and called it Macaronichnus isp. Later, Rodríguez-Tovar and Aguirre (2014) treated the large morphotype as ichnosubspecies of M. segregatis, and named Macaronichnus segregatis degiberti based on the observations on late Miocene specimens in southern Spain, this view is endorsed here. Rodríguez-Tovar and Aguirre (2014) emphasised primary branching as a characteristic that distinguishes M. s. degiberti from the other M. segregatis. However, crosscutting of the burrow fills, or evidence of secondary successive branching, can be seen (albeit very faintly) in their figure purportedly showing “true branching” (Fig. 5 of RodríguezTovar and Aguirre, 2014). A crosscutting relationship of the burrow fills is sometimes difficult to observe, especially when the burrows lack their mantle at the crossing point. Moreover, considering the formative process of the burrows, the burrow lumen was likely stuffed just behind the burrower with its faeces. Thus, primary branching would be limited in their burrows. Nevertheless, the criteria used to characterise M. s. degiberti designated by the original authors should be reconsidered. Compared to other ichnosubspecies of Macaronichnus segregatis, the most prominent feature that characterises M. s. degiberti is its larger size, as noted above (Figs. 2, 11, 12, 13). However, the absolute boundary value of the size cannot be determined, because it varies between places. Moreover, smaller M. s. degiberti exist, which are most likely produced by juvenile producers. Aside from the burrow diameters, both maximum curvature and the maximum burrow density of M. s. degiberti are apparently lower than those of the smaller ichnosubspecies. It is, however, difficult to determine the boundary values, because variations of the curvature and density are wide in both M. s. degiberti and the smaller ichnosubspecies (cf., Bromley et al., 2009). One may be deluded in identifying this trace fossil because of weathering, which sometimes made the faintly lamellate core structure conspicuous (Fig. 8). Such a weathered burrow looks similar to a segmented burrow, such as Arthrophycus, Beaconites, or Imponoglyphus. The effect of weathering leading such superficial similarity should be considered. The ichnogenus has been defined by mineralogical segregation between the core and mantle (Clifton and Thompson, 1978; Pemberton and Frey, 1982; Keighley and Pickerill, 1995; Bromley et al., 2009). However, this criterion is highly dependent on the heterogeneity of the substrate. For example, if the burrow occurs in highly mature sand consisting only of quartz grains, it lacks any mantles of dark-coloured sand grains. Therefore, logically, Macaronichnus burrows cannot exist in such a substrate. An almost horizontally oriented, gently curved burrow, for which overall morphology and mode of occurrence are closely similar (or almost identical) to that of M. s. degiberti, is called Planolites beverleyensis Billings (Pemberton and Frey, 1982). P. beverleyensis occurring in mature sand or sand with less-coloured minerals would be a phenotype of M. s. degiberti.

Acknowledgments This study originated from the joint research of MN and Prof. N. Kotake (Chiba Univ.), when MN was a student. The late Dr. J.M. de Gibert (Univ. of Barcelona), Dr. Z. Belaústegui (Univ. of Barcelona), and Prof. J. Aguirre (Univ. of Granada) helped MN to observe the “topotype” specimens of M. s. degiberti. Mr. T. Iwayama (Kochi Univ.) helped to prepare some of the trace fossil samples. Some observations were made during fieldtrips of international meetings convened by many friends. MN received financial support from JSPS KAKENHI (Grant Numbers 24540498 and 16K05591). The manuscript was improved by the comments from the editors Profs. T.J. Algeo and I. Montanez, reviewers Profs. J. Aguirre and L. Buatois. We are grateful for their help. References Aguirre, J., de Gibert, J.M., Puga-Bernabéu, A., 2010. Proximal-distal ichnofabric changes in a siliciclastic shelf, Early Pliocene, Guadalquivir Basin, Southwest Spain. Palaeogeogr. Palaeoclimatol. Palaeoecol. 291, 328–337. Akiyama, H., Nara, M., 2007. Digging-up method: an observation technique for a crosssection of unconsolidated sediments on modern tidal flats. J. Sedimentol. Soc. Jpn. 65, 33–37. Ban, K., Fielding, C.R., 2004. An integrated ichnological and sedimentological comparison of non-deltaic shoreface and subaqueous delta deposits in Permian reservoir units of Australia. Geol. Soc. Spec. Publ. 228, 273–311. Barnes, R.D., 1987. Invertebrate Zoology. Saunders College Publishing, Philadelphia (893p.). Barnes, R.S.K., Calow, P., Olive, P.J.W., 1993. The Invertebrates, a New Synthesis. Blackwell, London (488p.). Bertling, M., Braddy, S.J., Bromley, R.G., Demathieu, G.R., Genise, J., Mikuáš, R., Nielsen, J.K., Nielsen, S.S., Rindsberg, A.K., Schlirf, M., Uchman, A., 2006. Names for trace fossils: a uniform approach. Lethaia 39, 265–286. Blake, J.A., 2011. Revalidation of the genus Thoracophelia Ehlers, 1897, replacing Euzonus Grube, 1866 (Polychaeta: Opheliidae), junior homonym of Euzonus Menge, 1854 (Arthropoda: Diplopoda), together with a literature summary and updated listing of Thoracophelia species. Zootaxa 2807, 65–68. Bleidorn, C., Vogt, L., Bartolomaeus, T., 2003. New insights into polychaete phylogeny (Annelida) inferred from 18S rDNA sequences. Mol. Phylogenet. Evol. 29, 279–288. Bromley, R.G., 1996. Trace Fossils—Biology, Taphonomy and Applications. Chapman & Hall, London (361p.). Bromley, R.G., Uchman, A., Milàn, J., Hansen, K., 2009. Rheotactic Macaronichnus, and human and cattle trackways in Holocene beachrock, Greece: reconstruction of paleoshoreline orientation. Ichnos 16, 103–117. Buatois, L.A., Wisshak, M., Wilson, M.A., Mángano, M.G., 2017. Categories of architectural designs in trace fossils: a measure of ichnodisparity. Earth Sci. Rev. 164, 102–181. Carmona, N.B., Buatois, L.A., Mángano, G.A., Bromley, R.G., 2008. Ichnology of the Lower Miocene Chenque Formation, Patagonia, Argentina: animal-substrate interactions and the modern evolutionary fauna. Ameghiniana 45, 93–122. Carmona, N.B., Buatois, L.A., Ponce, J.J., Mángano, G.A., 2009. Ichnology and sedimentology of a tide-influenced delta, Lower Miocene Chenque Formation, Patagonia, Argentina: Trace-fossil distribution and response to environmental stress. Palaeogeogr. Palaeoclimatol. Palaeoecol. 273, 75–86. Caruso, C., Monaco, P., 2015. Bichordites monastiriensis ichnofabric from the Pleistocene shallow-marine sandstones at La Castella (Crotone), Ionian Calabria, Southern Italy. Riv. Ital. Paleontol. Stratigr. 121, 381–397. Chamberlain, C.K., 1971. Morphology and ethology of trace fossils from the Ouachita

5. Conclusions To reconstruct the palaeoecology of the tracemakers of M. s. degiberti, detailed observations on the specimens from Palaeozoic to Cenozoic deposits of North America, Europe, and Asia, in addition to “topotype” specimens of southern Spain (Rodríguez-Tovar and Aguirre, 2014), and modern incipient burrows (Seike et al., 2011) are made. It is interpreted as a pascichnial trace fossil formed through selective sand feeding and excretion of a free-living worm, such as a travisiid polychaete. Compared to other ichnosubspecies of Macaronichnus segregatis, i.e., M. s. segregatis, M. s. lineiformins, M. s. meandriformis, and M. s. spiriformis, the most prominent feature that characterises M. s. degiberti is 292

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