Digesting an ancient ecosystem: coprolites from the Grippia bonebed, Lower Triassic, Svalbard

Morphology

Morphotype A (Fig. 3) is elongated cylindrical with a near-constant diameter and typically displays an anisopolar configuration, with one end being rounded and the other slightly tapered. The morphotype is divided into three sub-types: A1 cigar (Fig. 3A), A2 amphipolar, where the whole length of the specimen shows an even spiral (Fig. 3D) (Hunt & Lucas, 2012); A3 cylindrical with grooves (Fig. 3G).

Variants A1 and A2 may occasionally be isopolar, possessing either two rounded or two tapering terminations. Sub-morphotypes A1 and A2 are rarely flattened and usually have a polished black surface. The overall shape of A1 is akin to a straight cigar with a smooth surface (Fig. 3A). In contrast, A2 is characterized by an amphipolar spiral that coils 1–2 times (Fig. 3D). Some A2 specimens such as PMO 250.858 (Fig. 2E), have an uneven structure on the surface interpreted to be tight spiraling. This uneven pattern indicates that this sub-morphotype might have either a tight or loose spiral configuration. Spiral structures should be visible in thin sections (Jain, 1983), but this was not found. Morphotype A3 is rare and distinguished by longitudinal grooves that may run partially or entirely along the coprolite (Fig. 3G) as typical constriction marks (Northwood, 2005), and specimens are usually flattened. Specimen PMO 250.267 (Fig. S1) is the largest specimen in this study, measuring 95 mm in length and 45 mm in width, and fits the description of morphotype A3 with distinct grooves.

Inclusions

Inclusions for sub-morphotypes A1 are described by two CT-scans and five thin sections; A2 by three CT-scans and two thin sections; A3 by four CT-scans. The inclusions in all studied coprolites are evenly distributed with the largest fragments generally located toward the edges of the coprolite. The number of inclusions varies significantly within sub-morphotypes A1 and A2, with some specimens being almost empty while others are filled with angular inclusions both in CT and thin sections. The inclusions have a low grade of degradation. Sub-morphotype A3 is for the most part homogenous except for a few small fragments (Fig. 3G).

Most inclusions in CT were unrecognizable with a few exceptions in morphotypes A2 and A3 identified as fish bones, belemnoid hooks (onychites) (Hoffmann, Weinkauf & Fuchs, 2017), conodont elements, a possible shark tooth and a neural spine (Fig. 3, Fig. S2). A3 specimen PMO 250.530 is empty in CT-scan except for a collection of trace fossils in the middle of the specimen (Fig. 3H). The traces cover a total area of 3x3 mm and are typically around 0.5 mm wide. There are no signs of an entry point.

Seen in thin sections, sub-morphotypes A1 and A2 have many inclusions of bone fragments and fish scales in a fine-grained matrix. The fish scales are well preserved and have visible bone structure, growth lines, pores and enamel (Fig. 3E) (as described in Mingtao et al., 2022). The cross sections of fish scales are often cut in a way that shows the ridges on the scales surface (Fig. S2D). Bone fragments in thin sections are typically smaller and appear better digested than the fish scales in all coprolites (Fig. 3F). Many of the bone fragments found in the coprolites likely originate from fish because of their small size, and some have a strong resemblance to fish vertebrae (as seen in Mingtao et al., 2022) as well as having a high abundance in coprolites together with fish scales. Thin section of PMO 250.009 (A1) is packed with fish vertebrae similar to fig. 8C from Mingtao et al. (2022) as well as scales (Fig. 3C). PMO 250.004 (A1) contains two pieces of highly porous bone fragments typical for tetrapod bones (Fig. 3B). Bone structures like this suggests that the bone may be ichthyopterygia (Sander, 2021).

Morphology

Morphotype B (Fig. 4) is anisopolar, generally exhibiting a teardrop-like shape with one end broader than the other. The widest end may be rounded, flat or slightly concave. While a few specimens are somewhat flattened, the majority retain their rounded cross section.

Morphotype B is divided into B1 rounded spiral (Fig. 4A) and B2 teardrop (Fig. 4D). B1 is characterized by a heteropolar spiral which means that the spiral covers a maximum 75% of the coprolite at the posterior end (Hunt & Lucas, 2012). Four specimens might exhibit a more amphipolar condition but are poorly preserved. B1 usually has an overall teardrop shape with one exception that has an oval shape (PMO 250.865). Only PMO 250.841 (Fig. 2J) displays distinct spiral lines indicative of an amphipolar spiral. Six of the B1 specimens are either broken or end abruptly with a flat edge, obscuring spiral type determination. Sub-morphotype B2 shares B1’s overall shape, but differs with a smooth, polished surface that lacks any texture.

Inclusions

Inclusions in sub-morphotype B1 are described by three CT-scans, and B2 by four CT-scans and one thin section. Morphotype B includes fish scales and bone fragments. The inclusions are either angular or rounded. The bone fragments are likely from fish because of their co-occurrence with fish scales in the same specimens. Fish scales are usually more complete compared to bone inclusions which are highly degraded and fragmented.

Sub-morphotype B1 is almost empty with the exception of a couple of small, rounded fragments and fish scales (Figs. 4B, 4C) in CT scans. In contrast, morphotype B2 is packed with both rounded and angular inclusions in CT and thin sections. Two specimens in sub-morphotype B2 contain onychites in both the normal and inverted CT-reconstruction (Fig. 4F). PMO 250.265 is unique among all coprolites described in this study as it contains sponge spicules in CT (Fig. 4E). The spicules measure 0.5–1 mm and are straight or hexagonal.

Morphology

The overall shape of morphotype C (Fig. 5) is sub-rounded, including specimens that are almost perfectly spherical (Fig. 5A) as well as slightly flattened specimens that appear oval. The sub-rounded coprolites have a perfectly smooth to irregular surface texture with the spherical specimens being the smoothest.

Inclusions

Inclusions in morphotype C are described by three CT-scans and four thin sections. Morphotype C is mostly homogenous in both CT-scans and thin sections with only a few rounded bone inclusions. The CT-scan of PMO 250.277 includes a few small fragments as well as one larger unidentified bone fragment measuring 10.7 mm in length (Fig. 5B). This large bone fragment has deep longitudinal grooves that gradually twist along its length. It seems abruptly broken off at one end and slightly fragmented on the other side (Fig. 5C). PMO 250.271 has a large number of cone-shaped borings inwards from the surface (Fig. 5D) in addition to a few small unidentified fragments. The widest part of the borings is located at the outer edges of the coprolite measuring 0.03 mm–0.16 mm in width and 0.8 mm–1.3 mm in depth. The only fragments seen in thin sections are small and degraded. Only PMO 250.002 has a coarse-grained matrix consisting of highly degraded bone fragments (Fig. 5E), while the remaining thin section specimens have a fine-grained matrix with no recognizable elements (Fig. 5F).

Morphology

Morphotype D (Fig. 6) has an overall reniform, or beanlike shape (Fig. 6A). They are isopolar with two rounded ends and typically have a smooth surface. Half of the specimens are flattened.

Inclusions

Inclusions in morphosype D are described by one CT-scan and two thin sections. Morphotype D coprolites are packed with angular inclusions observed in both CT and thin sections. The inclusions vary significantly in shapes and sizes within one specimen, and are interpreted to stem from a variety of prey. The CT-scan of specimen PMO 250.528 stands out from the rest by having inclusions in only half of the specimen, while the remaining part is empty (Fig. 6B). It includes several long, thin inclusions interpreted as possible gill rakers as they have a needle-like shape with a sharp point and slight bend (Fig. 6C). The possible gill rakers measure 3.6 mm and 5.4 mm in length which correlates in both size and shape to Fig. 7, E-I from De Lange et al. (2023).

Thin sections show a fine-grained matrix with bones (Fig. 6D), fish scales and secondary mineralized infill after dissolved inclusions in a variety of shapes that are unique for this morphotype (Fig. 6E). SEM/EDS results show that the infill consists of calcite. At least three of the mineralized infills are interpreted to be pseudomorphs after onychites when compared with CT orthoslices from other morphotypes (comparable to PMO 250.282 Fig. 8B). The onychites have a long oval shape with lower density in the middle when seen in orthoslice.

Morphology

Morphotype E (Fig. 7) has a wide, cylindrical shape. The ends are isopolar with flat or concave terminations. The surface is a combination of being smooth and having a wrinkle-like texture.

Many morphotype E coprolites were found as two or more separate pieces that were glued back together.

Inclusions

Inclusions of morphotype E are described by one inclusion visible in the hand-held specimen, two CT-scans and two thin sections. This wide cylindrical morphotype has a homogenous matrix in thin section with large angular fragments of bones and cephalopod remains in CT, and small bone fragments in thin sections.

PMO 250.281 is cracked into four pieces and contains an orthoceratoid cephalopod shell fragment, visible in the hand-held specimen (Figs. 7A–7C). The fragment is possibly Trematoceras (Hansen et al., 2024). The shell measures 15.8 mm in length. CT-reconstruction of PMO 250.281 shows the cephalopod shell in detail, with visible chambers (Figs. 7D, 7E). The specimen is otherwise homogenous with only a few small bone fragments, as well as a high abundance of onychites in the inverted CT-reconstruction and in orthoslices. In contrast, specimen PMO 250.904 has no cephalopod remains, but does instead contain large angular bone fragments in CT (Fig. 7G). The largest fragment measures 3.73 mm in length.

In thin sections, morphotype E has a fine-grained matrix with small, degraded bone fragments and a few angular fragments.

Morphology

The overall shape of PMO 250.282 is irregular (Fig. 8). It is closest to being sub-rounded (morphotype C) measuring 26–35 mm in diameter but has an irregular surface with indications of being broken and reworked. Inclusions also differ from morphotype C.

Inclusions

A small bone is visible on the surface of the coprolite (Fig. 8A). One CT-scan was made and confirmed that the bone visible at the surface is not inside the coprolite, but is stuck to the exterior surface, and therefore not noted as an inclusion. Orthoslices show that this coprolite is packed with onychites in large collections. The onychites measure approximately 1.5 mm in length and are preserved both with low X-ray density, and high density as interpreted mineralized infill (Fig. 8B), where low density is most common. The CT-reconstructed 3D model as well as orthoslices show a very high abundance of onychites both in high and low density (Figs. 8C, 8D). PMO 250.282 is the coprolite with the highest number of onychites in this study (>80). Similar structures to the onychites in orthoslices can also be seen in the thin section of PMO 250.005 (Figs. 6E, 6F).

Morphotypes

Defining morphotypes is important for identifying possible producers but is hampered by the reworked and fragmented nature of the material. There is likely a sampling bias toward middle-sized coprolites as the smaller specimens are easier to overlook, whereas the larger specimens are too fragmented to be identified. Triassic marine and aquatic coprolites are commonly between 2–75 mm in length with the marine ones being the smallest (Jain, 1983; Brachaniec et al., 2015; Cueille et al., 2020; Mingtao et al., 2022), whereas the Grippia bonebed coprolites are 7–40 mm in general. Two specimens are larger with a maximum length of 95 mm. The two larger specimens imply that larger coprolites do exist but are rarely preserved in their complete form. The bias towards medium sizes is, therefore, thought to be a result of preservation and fragmentation.

Taphonomic processes may alter the morphology of the coprolites. It is possible that sub-morphotype A1 is a reworked and polished variant of A2 as they exhibit a smooth and polished surface. Another explanation may be that when spiral shaped coprolites get deposited in water, the spiral will loosen and uncoil over time until they get buried (Jain, 1983).

Loss of spiral structure possibly happened with sub-morphotype A2 as the resemblance to uncoiling coprolites in Fig. 7 from Jain (1983) is noteworthy. Some A1 specimens may also resemble A3 coprolites that have been reworked and polished, but differences in inclusions suggest that they are distinct.

As within morphotype A, it is possible that sub-morphotype B2 is a reworked and polished version of sub-morphotype B1. However, the difference in inclusions strongly suggests that they are distinct (Table 2) and therefore suggest that they are produced by different animals. The differences may still be caused by the same animal group, with species or yearly variations in diets and slightly different shapes.

Spiral coprolites are commonly grouped together in the same morphotype but are separated in this study. All shapes from the straight sub-morphotype A1 to the spiraling A2 coprolites have been found and are often hard to separate from each other indicating gradual reworking of the same morphotype. Sub-morphotype B2 differs from A2 by being more rounded like B1 and exhibiting heteropolar spiraling, as opposed to amphipolar spiraling observed in A2. While the current morphotype classification system may be changed to combine both spiral coprolites in the future, this system is considered the most practical approach for this study.

Both morphotype B and E exhibit flat to concave terminations indicating that they have been pinched off during extrusion or broke into smaller pieces while fresh (Milàn, 2012; Dentzien-Dias et al., 2020). It is therefore impossible to know the true size and spiral type of these specimens. Some of the B2 and E coprolites might even be segments of the same morphotype, where B2 would be the end pieces and E the middle segments (Milàn, 2012, fig. 3; Milàn et al., 2021). PMO 250.281 from morphotype E resembles a longer segment and suggests that the morphotype has a slight sinuous or bumpy surface structure.

Inclusions

Inclusions can provide a better understanding of diet, but the degree of digestion and preservation still needs to be considered. Fish scales containing ganoine have a better preservation potential than other bone material (Richter & Smith, 1995). Bone material varies from lightly to severely digested due to bones being more fragile and differences in the efficiency of the digestive system of the host animal (Bajdek et al., 2017). Invertebrates are the least preserved inclusion type and are only preserved in the Grippia bonebed coprolites if they exhibit mineralized hard parts as for example shell or silika spicules.

Sponge spicules have been found inside one entire coprolite specimen (PMO 250.265), suggesting that they were ingested rather than attached to the surface by contact with the sediment. Alternatively, the spicules could have been swallowed by accident by a scavenger or durophagous animal feeding on something off a spicule filled sediment. However, two pieces of sediment from the bonebed were CT-scanned to look for spicules, and none were found. It is therefore not likely that the Grippia bonebed sediment included spicules, although spicules have been found lower in the Vikinghøgda Formation (Foster et al., 2023). PMO 250.265 may have been produced by an animal that had ingested sponges at another locality, and then excreted feces which eventually were deposited in Grippia bonebed. Alternatively, the lack of spicules in the sediment may be the result of reworking and diagenesis.

Due to their low X-ray density, onychites are for the most part only visible in orthoslices and in inverted CT-scan 3D reconstructions. In a normal 3D-reconstruction it is possible to see zero to three onychites within each specimen, whereas the inverted model and orthoslice reveal up to 80 onychites in the same coprolites. Specimens PMO 250.005 and PMO 250.282 contain a few mineralized onychites and show that they can be preserved in two different ways; in high or low-density materials (Figs. 6E, 8B–8D).

The coprolites are very brittle and cracked. The cracks may have exposed parts of the coprolite to different types of surrounding fluids and bacteria that could have affected the type of preservation. Exactly how different types of preservation happened needs more research looking into biological, chemical, and physical factors.

Overall, the Grippia bonebed coprolites show a close relationship between the morphotypes, and amount and type of inclusions within each morphotype (Table 2) indicating that they are produced by different animal groups. There are many factors to take into consideration when analyzing coprolites and it is important to be aware of the uncertainties in deformation of morphotypes and potentially missing inclusions. The inclusions that we do see are, however, a good source of information and show which animals were preyed on. Conversely. the lack of inclusions can still be used as an indicator for a slow metabolism, a diet of soft-bodied animals or that the animal regurgitated some of its prey (Pollard, 1968; Gordon et al., 2020).

Invertebrates

The discovery of invertebrate remains in the coprolites is the first evidence of invertebrates in the Grippia bonebed. Further, sponge spicules are the first evidence of benthic organisms, and the first evidence of an animal feeding on benthic organisms in this area. Hansen et al. (2024) found almost no benthic invertebrates in the lower Vendomdalen Member, becoming more abundant in the upper part.

Cephalopod arm hooks (onychites) are found in morphotypes A2, B2, D, E and F. The number of onychites suggests that cephalopods were a common prey for the active predators in the Early Triassic Boreal Sea. Scattered belemnoid onychites as well as orthoceratoids and ammonoids have been reported from several levels in the Vendomdalen Member (Hansen et al., 2024). Most coprolites contain a variety of prey, while the producer of morphotype E may have had cephalopods as their main prey. In cases where only a few onychites were found, it may be that the producer swallowed them accidentally when ingesting a prey that had eaten a cephalopod.

Evidence of coprophagy is found in two coprolite specimens as possible burrows and borings (PMO 250.530 and PMO 250.271). Burrows inside PMO 250.530 are made parallel to the surface and have turns indicating that this pattern was made by a living organism and not just by escape of gas bubbles formed during decomposition (Wahl, Martin & Hasiotis, 1998). PMO 250.530 has burrows with no entry or exit points, likely made when the coprolite was still soft and buried rapidly. These could also be caused by organisms from digestive tract itself, such as nematodes. Nematodes have been found in marine coprolites from the Lower Triassic of Poland and may occur inside the digestive tract of marine animals (Brachaniec et al., 2015). PMO 250.271 has traces that differ from the internal burrows in PMO 250.530. The specimen has borings made from the outside going inward perpendicular to the surface, indicating the presence of unknown organisms in the Grippa bonebed. Borings are well known in the coprolite record, and are likely made after phosphatization as the entry points are still open (Tapanila et al., 2008; Milàn, Rasmussen & Bonde, 2012; Dentzien-Dias et al., 2018; Dentzien-Dias et al., 2020).