2. Studied succession

The present study was performed in the reference section of the Pliensbachian of Peniche, West Portugal, just below the Toarcian Global Boundary Stratotype Section and Point (GSSP; e.g., Duarte, Reference Duarte and Rocha2007; Rocha et al. Reference Rocha, Matiolli, Duarte, Pittet, Elmi, Mouterde, Cabral, Comas-Rengifo, Gómez, Goy, Hesselbo, Jenkyns, Littler, Mailliot, Oliveira, Osete, Perilli, Pinto, Ruget and Suan2016; Duarte et al. Reference Duarte, Silva, Felix, Comas-Rengifo, Rocha, Mattioli, Paredes, Mendonca Filho and Cabral2017). The investigated succession, located in the distal sector of the Lusitanian Basin (Fig. 1A, B), covers the Marly limestones with organic facies (MLOF) member of the Vale das Fontes Formation and the upper part of the Lemede Formation, both marl-limestone units assigned to the Pliensbachian and well dated by ammonites, calcareous nannofossils and dinoflagellates (Figs 1C, 2, 3; Duarte & Soares, Reference Duarte and Soares2002; Duarte et al. Reference Duarte, Silva, Oliveira, Comas-Rengifo and Silva2010; Silva et al. Reference Silva, Duarte, Comas-Rengifo, Mendonça Filho and Azerêdo2011, Reference Silva, Duarte, Comas-Rengifo and Ramkumar2015; Correia et al. Reference Correia, Riding, Duarte, Fernandes and Pereira2018; Ferreira et al. Reference Ferreira, Mattioli, Sucherás-Marx, Giraud, Duarte, Pittet, Suan, Hassler and Spangenberg2019). Corresponding to two largely fossiliferous units, between nektonic (ammonites and belemnites) and benthic (brachiopods, bivalves, crinoids and gastropods) macrofauna, these units differ in the type of marl-limestone alternations.

Figure 1. Locality overview. (A) Location of the Peniche section in the context of the Lower Jurassic carbonate deposits cropping out in the Lusitanian Basin (based on Duarte et al. Reference Duarte, Silva, Felix, Comas-Rengifo, Rocha, Mattioli, Paredes, Mendonca Filho and Cabral2017). (B) Simplified geological map of the Peniche Peninsula indicating the studied localities (based on Camarate-França et al. Reference Camarate França, Zbyszewski and Moitinho de Almeida1960). (C) Stratigraphical log of the Upper Sinemurian–Aalenian (?) succession at Peniche: lithostratigraphy, sequence stratigraphy (2nd-order Transgressive (T)–Regressive (R) cycles) and main sedimentary features (adapted from Duarte et al. Reference Duarte, Silva, Felix, Comas-Rengifo, Rocha, Mattioli, Paredes, Mendonca Filho and Cabral2017). PMb – Polvoeira Member; PPLMb – Praia da Pedra Lisa Member; MLUP Mb – Marls and limestones with Uptonia and Pentacrinus member; LML Mb – Lumpy marlstones and limestones member; MLOF Mb – Marly limestones with organic facies member; CC1 to CC5 Mb – Cabo Carvoeiro members 1 to 5.

Figure 2. Studied localities. (A) Topmost part of Marly limestones with organic facies member of the Vale das Fontes and base of the Lemede Formation at the Portinho da Areia do Norte. (B) Lemede Formation at the Ponta do Trovão, the GSSP for the base Toarcian.

Figure 3. Outcrop photographs illustrating the fossil associations and their taphonomy. Marly limestones with organic facies member of the Vale das Fontes Formation, Portinho da Areia do Norte (B, C, F) and Lemede Formation, Ponta do Trovão (A, D, E, G–J). Scale bars are 10 mm long. (A) Pyrite aggregates (i.e., ‘worms’, a), partly encrusted belemnites (b), oysters (o) and a burrow shaft (s). (B) Dense accumulation of pyrite aggregates. (C) Pyrite aggregates, partly entombed in their silty burrows, and scattered in the matrix. (D) Bone (rib) (arrows). (E) Ammonite (cross-section) with pyritized periostracum. (F) Gastropod with pyritized periostracum. (G) Brachiopod in life position. (H) Probably a vertebrate regurgitalite. (I) Vertebrate coprolite containing mollusc remains. (J) Vertebrate regurgitalite, mainly containing belemnites.

The MLOF member of the Vale das Fontes Formation, assigned to the top of the Ibex – Margaritatus ammonite Zone interval, is marl-dominated, very rich in organic matter (including black shales) and well observed in other points of proximal sectors of the Lusitanian Basin (Duarte et al. Reference Duarte, Silva, Oliveira, Comas-Rengifo and Silva2010; Silva et al. Reference Silva, Duarte, Comas-Rengifo, Mendonça Filho and Azerêdo2011, Reference Silva, Duarte, Comas-Rengifo and Ramkumar2015; Silva & Duarte, Reference Silva and Duarte2015). This unit, locally deposited under anoxic conditions, is associated with a second-order maximum flooding event (Duarte et al. Reference Duarte, Silva, Oliveira, Comas-Rengifo and Silva2010; Silva et al. Reference Silva, Duarte, Comas-Rengifo and Ramkumar2015; Fig. 1C).

The Lemede Formation, assigned to the Margaritatus – extreme base of the Polymorphum ammonite Zone, is carbonate-dominated, bioturbated and composed of centimetre- to decimetre-thick limestone-marlstone alternations, at Peniche around 23 m in thickness. This unit marks a second-order regressive phase, ending with the marly deposits that characterize the lower Toarcian (Cabo Carvoeiro Formation; Duarte et al. Reference Duarte, Silva, Oliveira, Comas-Rengifo and Silva2010, Reference Duarte, Silva, Felix, Comas-Rengifo, Rocha, Mattioli, Paredes, Mendonca Filho and Cabral2017; Fig. 1C). The top of the Lemede Formation defines the Toarcian GSSP.

4. Description

A wide range of morphologies of elongate pyritic aggregates exists in the studied section, which abundantly occur in the exposed limestone and marlstone beds. Semi-quantitative estimations indicate that up to several hundred specimens may be preserved within the upper 5 cm of a bedding plane per square metre. Despite the morphological variability, so far, five main groups of aggregates with recurrent occurrence can be distinguished, based on their type of preservation (e.g., mineralization, internal structure, external ornamentation), overall morphology, size range, body proportions and associated burrow types. They were observed in the MLOF member of the Vale das Fontes Formation of the Portinho da Areia do Norte (groups 1, 4, 5) and the Lemede Formation at the Ponta do Trovão (groups 1–3, 5) (Figs 1B, 2, 3).

Group 1 contains elongate, round or slightly dorsoventrally flattened bodies preserved in brown limonite (Fig. 4). They are several centimetres long, 1–3 mm wide and straight to slightly winded along the bedding plane. Specimens preserved to a longer extent are slightly undulating in a vertical sense (i.e., into the bedding plane; Fig. 4C, J). Broken segments either show a massive fill with amorphous limonite or are structured into a thick outer (partly multiple) layer and a sediment-filled or sparry calcite core (Fig. 4B, C, G, L–N). Some specimens preserve a proboscis-like extension (Fig. 4J, K). The slender aggregates have a smooth surface and are often aligned within their shallow burrows.

Figure 4. Group 1 aggregates in vertical section (A) and on bedding planes (B–N), comparable with Nemertea. Lemede Formation, Ponta do Trovão (A–C, F–N) and third member (MLOF) of the Vale das Fontes Formation, Portinho da Areia do Norte (D, E). Scale bars are 5 mm long. (A) Specimen with partly worn outer layer. (B) Flattened specimen (upper part) with a thin outer layer (epithelium) surrounding a thick core (rhynchocoel). The other specimens in the lower part are consistent with polychaetes of Group 2. (C) Elongate specimen with a round head region (left) and varying diameter, partly buried in sediment. (D) Middle portion with an ornament of faint longitudinal ridges. (E) Long specimen with the head region preserved (left). (F) Body segment with a multiple outer layer (epithelium and muscles) surrounding a core (rhynchocoel), preserved in its horizontal burrow. (G) Incomplete specimen with a thin limonitic coat and a massive calcite core (partly visible right). (H) Limonitic body fragment. (I) Incomplete specimen with a thin limonitic coat and a massive calcite core (visible left), as well as an attached smaller aggregate, probably a nematode (arrow). (J) Limonitic aggregate with a proboscis-like extension (left). (K) Close-up view of J. (L) Broken body portion showing a thick limonitic outer layer (epithelium and muscles) and a calcite-filled core (rhynchocoel). (M) Body fragment with a thick outer layer, which is partly shredded. (N) Elongate specimen broken into three pieces with cross-sections showing the internal structure into a thick limonitic layer (epithelium and muscles) and a calcite core (rhynchocoel). The enlarged portion (right) is due to enhanced pyritization.

Group 2 consists of more compact, cylindrical aggregates with preserved lengths of several centimetres and diametres of 3–6 mm (Fig. 5). They are slightly winded within their sub-horizontal burrows and mainly consist of limonite. Some bodies gently disappear into the subsurface under a low angle (Fig. 5A, C, D, F). Their rough surface is textured with a sub-millimetric limonitic network enclosing crystalline calcite meshes (Fig. 5A–H, L, M). Better-preserved specimens show a dense segmentation and superficial ornamentation (e.g., knobs and ridges; Fig. 5I–K), as well as lateral appendages (e.g., parapodia; Fig. 5H). If preserved, terminations are blunt with a reduced diameter (e.g., head region; Fig. 5J), while some body cross-sections appear to be pentagonal (Fig. 5E).

Figure 5. Group 2 aggregates on bedding planes (A–J, M) and in vertical section (K, L), chiefly comparable with Polychaeta. Lemede Formation, Ponta do Trovão. Scale bars are 5 mm long. (A) Slightly undulating specimen. (B) Winding specimen. (C) Fragments of several bodies embedded within their shallow burrows. (D) Sinusoidal body partly emerging from its burrow, attached by supposed nematode remains (arrows). (E) Body fragment partly strongly recrystallized, and a body with pentagonal cross-section (upper right). (F) Undulating specimen partly burrowed within the sediment. (G) Specimen partly burrowed, with a rough surface. (H) Incomplete winding specimen with a rough surface and numerous short, lateral appendages (parapodia). (I) Slightly compacted body fragment with weakly preserved segmentation and superficial ornamentation. (J) Two specimens with a pharynx-shaped head region (arrows). (K) Body fragment with weakly preserved segmentation. (L) Two partly preserved bodies with a rough surface. (M) Enlarged body fragment showing a rough surface with alternating pyrite and calcite crystals.

Group 3 comprises robust and fleshy aggregates consisting of pyrite, which are preferably found in vertical position within their burrow shafts, although obliquely and horizontally oriented specimens occur too (Fig. 6). The cylindrical to dorsoventrally flattened bodies are preserved with a length of 3–5 cm and have a diameter/width of 5–8 mm. The size of the aggregates can be increased due to strong recrystallization, where aligned pyrite crystals mimic surficial ornamentation (Fig. 6A, B, D, E). The bodies are typically preserved within the mound-like aperture of their burrow shaft on the bedding surface, which is 3–8 cm in diameter. The inner margin of the shaft can have faint striae (Fig. 6F). Many pyrite aggregates are contorted and worn, and no internal structure is preserved.

Figure 6. Group 3 aggregates (anterior regions) within the aperture of their burrow shafts with a ring-like rim on bedding planes (A–D, F) and in vertical section (E), comparable with Polychaeta. Lemede Formation, Ponta do Trovão. Scale bars are 5 mm long. (A) Bent specimen. (B) Contorted and strongly recrystallized aggregate. (C) Curved specimen with ornamented surface. (D) Contorted specimen with several smaller aggregates belonging to Group 2 (Polychaeta). (E) Curved, fleshy aggregate. (F) Elongate body with ornamented (striated) inner burrow margin.

Group 4 is made up of slender, dorsoventrally flattened aggregates of limonite and pyrite, with a preserved length of several centimetres and a width of 1–4 mm (Fig. 7). No connection with burrows has been observed. The bodies are slightly undulating (Fig. 7A, B, F) and are covered laterally by an array of dense appendages (e.g., parapodia, chaetae), which are arranged perpendicularly to or obliquely to the main body axis and have a length of ca. 0.5 mm (Fig. 7A–E). Broken body parts reveal a thick outer layer consisting of limonite, surrounding a massive pyritic core that can show evidence of an inner core (e.g., intestinal lumen; Fig. 7D, E). Diagenetic precipitation of gypsum is affecting the bedding planes containing these bodies (Fig. 7A).

Figure 7. Group 4 aggregates on bedding planes, comparable with Polychaeta. Third member (MLOF) of the Vale das Fontes Formation, Portinho da Areia do Norte. Scale bars are 5 mm long. (A) Elongate, dorsoventrally flattened specimen with a dense array of lateral appendages (parapodia, chaetae), overprinted by gypsum precipitation. (B) Winding body part. (C) Close-up view of B with preserved chaetae. (D) Longitudinal cut through an apparently complete specimen, showing the limonitic head region, cuticle with parapodia and chaetae, the muscular layer, as well as the pyritic body cavity with the intestinal lumen. (E) Annotated line drawing of D. (F) Winding body with partly removed limonitic layer (cuticle and muscular layer), revealing the pyritic body cavity.

Group 5 consists of cylindrical bodies, several centimetres in length and only 0.5–2 mm in diameter (Figs 4I, 5D, 8). The composition of a limonitic coat and pyritic core is common. The aggregates are arranged horizontally in a straight or slightly sinusoidal manner, partly embedded in their shallow burrow (Fig. 8A, B). In one case, a dense accumulation of aggregates is arranged within a larger body segment of Group 1 (Fig. 8C). A characteristic feature is the attachment of these small aggregates to larger aggregates belonging to groups 1 and 2 (Figs 4I, 5D).

Figure 8. Group 5 aggregates on bedding planes, comparable with Nematoda. Third member (MLOF) of the Vale das Fontes Formation, Portinho da Areia do Norte (A) and Lemede Formation, Ponta do Trovão (B, C). Scale bars are 5 mm long. (A) Elongate, slightly sinusoidal specimen. (B) Elongate specimen (upper part) continuing into its burrow (right), and fragment of another specimen (lower part). (C) Fragment of a body of Group 1 or 2 (Nemertea or Polychaeta, respectively) with numerous small aggregates (Nematoda) concentrated in it.

5. Taxonomic assignment

Although the described pyritic and limonitic aggregates suffer from an exceptional preservation of tissues and morphological details, several features such as body shape, size, composition, segmentation, body appendages and internal structures allow comparison with or a tentative assignment to distinct phyla.

Group 1 comprises long, dorsoventrally flattened bodies without segmentation, which are closest to the body plan of Nemertea (ribbon worms). The partly multiple outer layers would correspond to the epithelium and the circular and longitudinal muscles, whereas the core is reminiscent of the rhynchocoel (e.g., Rupert et al. 2019).

Group 2 is likely a polygenetic group, but the habitus of most specimens, as well as segmentation, ornamentation and lateral appendages (e.g., parapodia) and a pharynx-shaped head region, would be consistent with Annelida (segmented worms), probably Polychaeta (bristle worms, e.g., Rouse & Pleijel, Reference Rouse and Pleijel2001). The textured surface is comparable with a complex cuticula, including collagen fibrils, providing a stable framework for tissues, but is overprinted by diagenetic mineral precipitation. A pentagonal body cross-section is defined by five longitudinal ridges, as it is the case in the polychaete Palaeoscoloplos triassicus Knaust, Reference Knaust2021 from the Triassic of Germany. Nonetheless, some specimens of Group 2 are rather poor on preserved characteristics and could also be the remains of nemerteans or maybe holothurians.

Group 3 is poor on preserved characteristics due to increased pyritization. Occurrence in life position within their burrow shafts and locally preserved striae along the inner wall of the shaft make an assignment to Polychaeta likely, which includes epibenthic carnivores (e.g., sit-and-wait predators), commensalism with other invertebrates in their tubes and burrows and burrowing forms (Jumars et al. Reference Jumars, Dorgan and Lindsay2015). Some specimens are reminiscent of holothurians, but no significant reports of holothurian ossicles exist from these layers, which makes this interpretation unlikely.

Group 4 contains the best-preserved specimens, which have a flattened habitus with numerous appendages (e.g., parapodia, chaetae) that are most consistent with an interpretation as Polychaeta. This is supported by the internal structure, consisting of a thick outer layer (i.e., circular and longitudinal muscles) and a body cavity partly preserving the supposed intestinal lumen.

Group 5 differs from all other groups by their relatively small size and a slender, sinusoidal, cylindrical body. These features suggest an assignment to Nematoda (roundworms, e.g., Ruppert et al. Reference Ruppert, Fox and Barnes2004), which cuticle encloses a pseudocoelom with the intestine. Occurrence within and attachment to other worms would be consistent with a parasitic lifestyle of nematodes.

6. Taphonomy

The remarkable preservation of the worm-like organisms (aggregates) depends on a wide range of primary (sedimentary) and secondary (diagenetic) conditions during their taphonomic pathway. The described fauna was partly preserved by pyrite replacement of soft bodies, probably driven by microbial sulphate reduction under dysoxic to anoxic conditions. In the outcrop, these pyrite aggregates were partly altered to limonite due to weathering.

The MLOF member of the Vale das Fontes Formation at Peniche and in other parts of the Lusitanian Basin contains dark-grey, organic-rich laminated mudstones (black shales) with elevated total organic carbon (TOC) values (several levels showing values above 10 wt.%), indicating dysoxic to temporary anoxic conditions (Oliveira et al. Reference Oliveira, Rodrigues, Duarte and Lemos2006; Duarte et al. Reference Duarte, Silva, Oliveira, Comas-Rengifo and Silva2010; Silva et al. Reference Silva, Duarte, Comas-Rengifo, Mendonça Filho and Azerêdo2011; Silva & Duarte, Reference Silva and Duarte2015). Redox conditions can be expected to fluctuate within a succession with numerous minor gaps of deposition (hiatuses), which allowed for benthic colonization.

The Lemede Formation is rich in pelagic and benthic fossils and shows very low values of TOC (see Oliveira et al. Reference Oliveira, Rodrigues, Duarte and Lemos2006; Duarte et al. Reference Duarte, Silva, Oliveira, Comas-Rengifo and Silva2010). Generally, higher oxidation levels observed in the uppermost part of the sediment, compared with the Vale das Fontes Formation, allowed for colonization by burrowing organisms (Duarte et al., Reference Duarte, Silva, Felix, Comas-Rengifo, Rocha, Mattioli, Paredes, Mendonca Filho and Cabral2017). Periodic events of dysoxia might have been responsible for the pyritic preservation of the burrow-associated worms.

7. Criteria for recognition of inadequately preserved soft-body animals

Superficially, pyrite aggregates as described may fail to be recognized as fossilized soft bodies (as it has been the case for the described faunal association) but instead may be considered as burrows, concretions or simply random mineral precipitations. A closer investigation reveals several criteria that allow their distinction as fossilized ‘worms’ replaced by minerals. Their occurrence in finely laminated sedimentary rocks (such as mudstone, siltstone or micrite) makes it likely that organic remains became preserved. They are often associated with microbially induced sedimentary structures (e.g., wrinkle marks or microbialites) and are indicators of reduced bottom-water conditions (i.e., dysoxic) with an elevated amount of organic content.

The aggregates appear in the shape and size of higher vermiform taxa, such as nemerteans, annelids, nematodes and platyhelminthes, and may be preserved with a tortuosity (e.g., winding, sinusoidal, helicoidal) reflecting their original behaviour while crawling on or burrowing within the sediment. The main parts of the ‘worm’s’ composition (such as cuticula, body cavity, segmentation and appendages) may respond differently to taphonomic processes and might be replaced by different mineral phases during early diagenetic processes, which in turn might get preserved differently. Moreover, more rigid annulations and external sculpturing may be preserved, as well as appendages such as palps, bristles and antennae. Original surficial colour patterns may also get transformed. Finally, the preservation of the aggregates within burrows can be considered a reliable criterion for proving their fossil nature.

8. Remarkably preserved organisms versus Konservat-Lagerstätten

According to the recently revised definition of Konservat-Lagerstätten (Kimmig & Schiffbauer, Reference Kimmig and Schiffbauer2024), the described biota fails to fulfil the requirements of being exceptionally preserved, such as completeness, preservation of fine morphological details or associated soft tissues. Nonetheless, following Knaust (Reference Knaust2010), they can be considered as remarkably preserved benthic organisms, which fill the gap between exceptionally preserved and non-preserved soft-bodied fossils. Although they do not allow a close analysis of morphological details and evolutionary considerations (in contrast to exceptionally preserved organisms), they record the presence of a phylum or even a class and contribute to our understanding of evolutionary processes at a higher taxonomic level.

The described worms from Peniche slightly predate the Konservat-Lagerstätten known from the Toarcian Oceanic Anoxic Event (TOAE), such as the famous Posidonia Shale of Holzmaden, Germany (e.g., Muscente et al., Reference Muscente, Vinnes, Sinha, Schiffbauer, Maxwell, Schweigert and Martindale2023), and the Strawberry Bank of Somerset, England. The presented material is only a stratigraphically very selective glimpse into the manifold of preservation variants and taxonomic groups. A systematic exploration will probably result in the detection of better-preserved specimens belonging to a wider range of groups of organisms.

An important point is the general high abundance and wide stratigraphic and geographical distribution of these biota, which has been mostly overlooked so far. Following the criteria for recognition, and once recognized, remarkably preserved organisms have the potential to complete our picture of the fossil record of numerous taxonomic ranks. Such accumulations can be met in deposits with favourable conditions, including fine grain size, dysoxia and microbial mediation. Aside from the introductory cited examples, massive deposits of limestone, such as the Upper Ordovician (Katian) in the Oslo Graben, Norway; the Upper Jurassic (Oxfordian) in southern Germany; the Upper Cretaceous (Cenomanian-Turonian) chalk of England, UK; and the Miocene of Crete, Greece, have proven to be prone to remarkably preserved organisms (DK, personal observations).