Mode of formation
The overall morphology and variability in the preservation of the Naranco Formation trace fossils analysed here are best regarded as the result of different facets of a single anatomy defining a behavioural continuum. In this context, the almost pristine body impression with transverse furrows defining the segments observed in best-preserved specimens of morphotype 1 (Fig. 3a–c) can be related to the effacement of these features in morphotype 2 (Fig. 3d–f). This suggests that these differences correspond to morphotype 1 documenting momentary pause (i.e. stasis) and elongated morphotype 2 recording significant translational movement through the sediment. However, the fact that the axial lobe and central elevated ridge are consistently expressed in both morphotypes indicates that, although morphotype 1 records for the most part a stationary structure producing an impression that mimics the dorsal anatomy of the tracemaker, there was a subtle displacement involved in its generation (contra body fossil interpretation). This is revealed by the continuous nature of the midline ridge, most likely recording discrete spines/keel in the exoskeleton of the producer (cf. Figs. 3b and 4b). The variability of the anterior part of morphotype 1, locally with a fan-like mounded morphology (S1b–d), indicates disturbance of the sediment related to animal-sediment interaction, therefore supporting a trace fossil origin. In fact, there is a real gradation between morphotypes 1 and 2, reflecting a morphological and behavioral continuum as clearly documented by some long specimens of morphotype 2 (Figs. 3d,e and S2). This evokes similarities with intergrading Rusophycus and Cruziana, which are widely regarded as biogenic structures recording resting/stationary (Rusophycus) and combined locomotion and feeding activity (Cruziana) of benthic deposit feeding euarthropods with homonymous limbs15. Morphotype 1 implies the docking of the dorsal part of the exoskeleton in the firm mud, producing an oval symmetrical structure superficially resembling Rusophycus, whereas morphotype 2 involves concatenated morphotype 1 specimens resulting in an elongated structure recording linear movement through the sediment akin to Cruziana (Fig. 4e). In particular, the concatenation of truncated morphotype 1 specimens can be compared with the gradation between R. eutendorfensis and the resultant C. tenella generated by repeated, partially overlapping R. eutendorfensis segments16.
Comparisons with some ichnospecies of Rusophycus and Cruziana refer only to the stop-start mechanism resulting in concatenated static elements (i.e. Rusophycus-like segments) to create linear structures recording locomotion (Cruziana-like). Contrary to Rusophycus and Cruziana, however, the Naranco Formation trace fossils are not the result of the interaction of walking legs or ventral anatomy against the sediment; they lack leg striations (i.e. “scratch imprints”) or any kind of appendage impressions (e.g. coxal impressions, exopodite brushings) found in legitimate euarthropod trackways and burrows. Instead, these trace fossils are best interpreted as the product of the dorsal exoskeleton of an euarthropod pressed infaunally against the cohesive muddy sediment. This resulted in the distinctive trilobate morphology with a deeper axial lobe and segmented appearance expressed in morphotype 1, and the effaced surface of elongated morphotype 2 with the axial ridge. Initial anchoring of the dorsal exoskeleton (morphotype 1) was occasionally followed by subsequent dragging and re-anchoring in an adjacent consecutive position generating partially overlapping replicas of the dorsal anatomy in a continuous structure (morphotype 2). Successive animal body re-adjustments are recorded by subtle angle changes defining nested curve segments in morphotype-2 cross-sectional profile (Fig. S2b,c). In this context, it is worth drawing attention to the moulting behavior of some extant chelicerates (e.g. arachnids), in which ecdysis is performed in a supine position inside a burrow, and in which the emerging individual escapes the exuvium through an aperture of the anterior exoskeletal margins4.
The tracemaker and its environmental preference
Attribution of a trace fossil to a particular producer is exceptional in the ichnological record. There is a genuine interest in palaeobiology, however, in deciphering tracemakers. Linking these two records could unravel previously inaccessible ecological and evolutionary information. A trilobite producer is unlikely, as the detailed preservation of the Naranco Formation trace fossils would allow the identification of diagnostic morphological features, such as the axial ring ornamentation and pleural furrows1,3,8,9. Although the identification of the producer of the Naranco Formation trace fossils poses a significant challenge, the exquisite preservation of some specimens of morphotype 1 allows for direct comparison with the enigmatic non-trilobite euarthropod Camptophyllia eltringhami from the upper Carboniferous (i.e. Pennsylvanian) British Coal Measures17,18. In fact, the enigmatic Naranco trace fossils closely resemble the dorsal trunk exoskeleton of Camptophyllia in overall shape, size range, the presence of paired longitudinal furrows forming three lobes, wide axial lobe with an elevated central keel, the presence of nine segments that taper in width posteriorly, and even a pointed back end (Fig. 4a,b), strongly supporting that the producer was in all likelihood a Camptophyllia-like, benthic euarthropod. The Naranco Formation trace fossils differ only from the exoskeleton of Camptophyllia in the absence of pleural spines and the shape of the anterior region, which display wide variability in the sedimentary biogenic structure, suggesting anatomical disturbance of this region during animal-substrate interaction resulting in emergence. Despite the close morphological similarities between the Naranco Formation trace fossils and the dorsal exoskeleton of Camptophyllia18, it is difficult to assess whether this euarthropod and the trace maker were phylogenetically closely related, or simply the result of convergent evolution, given the lack of ventral anatomical information in both cases. The higher affinities of Camptophyllia are a source of controversy all by themselves, as its exoskeleton has prompted comparisons with oniscid isopod crustaceans, arthropleurid myriapods, and even euthycarcinoids18. Given this uncertainty, we argue for a conservative interpretation of the Naranco Formation trace fossils as being produced by a Camptophyllia-like euarthropod with a dorsal exoskeleton that closely resembles that of a oniscid isopod based only on their similar dorsal morphology.
Camptophyllia and walking traces tentatively attributed to it are present in late Carboniferous delta-plain lacustrine settings characterised by freshwater conditions17,18. In contrast, the Devonian trace fossils documented in this study are present in deposits that, although inferred to have been formed in connection with a river-mouth, record more distal settings where normal marine salinities were repeatedly affected by freshwater discharge, resulting in periods of brackish-water conditions. This palaeoenvironmental discrepancy could in principle be explained in two different ways. First, the producers may have originally lived in proximal delta-plain settings (as observed in Camptophyllia), but been entrained in the hyperpycnal flows and transported seaward (as observed in the Naranco Formation). Second, the producers of the Naranco trace fossils may have actually lived in these shallow marginal-marine settings. If this is the case, these Camptophyllia-like euarthropods with a similar functional morphology (and likely ecology) to that of oniscid isopods could have originated in fully marine environments during the Devonian and subsequently migrated landwards during the Carboniferous. These environmental shifts through time are not unusual, and have been detected in various arthropod groups19, including those taxa more directly comparable with Camptophyllia (i.e. oniscid isopod, arthropleurids, euthycarcinoids)18. Further exploration of Devonian and Carboniferous strata may reveal similar biogenic structures to those herein described, providing crucial evidence to evaluate these competing hypotheses.
Behavioural significance
The conclusion that the Naranco Formation trace fossils were most likely produced by Camptophyllia-like euarthropods living in shallow- to marginal-marine environments begs the question: what particular behaviour do these unusual fossils reflect? The convex hyporelief preservation (Fig. 4c), similarity with the dorsal exoskeleton of Camptophyllia (Fig. 4b), and lack of a recognizable head region indicate that the trace fossils reflect an impression of the dorsum pushed against the sediment whilst the animal was in upside down position. This configuration is consistent with the body inversion moult procedure envisaged for Devonian phacopid trilobites (Fig. 4e)1,3, which involved the active burial of the animal in an upside down position, followed by forceful thrusts of the exoskeleton against the surrounding sediment in order to facilitate the moulting process. However, the Naranco material records unusually pristine structures that seem not to involve any significant struggle in the process of ecdysis. It is worth noting that ecdysis need not to be a highly energetic strategy1,4. In the case of the Naranco Formation structures, the clue resides in the nature of the hosting sediment, in particular its high consistency. In addition to the richly ornamented trace fossils present in these deposits (e.g. Conostichus), sedimentological evidence indicates frequent erosional (e.g. groove casts) and exhumation processes providing optimal conditions for firm substrates. The preferred orientations of specimens preserved on the large surface is consistent with relatively high-energy conditions under the action of currents. In this context, morphotype 1 records an upside-down resting stance anchored in a firm mudstone, whereas morphotype 2 resulted from a more prolonged process involving successive attempts of anchoring and release of the exoskeleton. This latter process resulted in repeated, consecutive, partially overlapped structures defining a linear structure (morphotype 2) spanning several centimeters. In our interpretation, the anterior region reflects a moulting strategy involving the disarticulation of the cephalic shield (Fig. 4e). This region characterised either by an irregular, fan-like mounded protuberance or a pair of subcircular highly convex structures was strongly disturbed during emergence dislodging the remainders of the ruptured cephalic cuticle. The high density of moulting structures recorded in the surface analysed is consistent with mass moulting events, as recorded for different groups of arthropods elsewhere6,7.
The Naranco Formation trace fossils represent the first record of infaunal mass moulting in a soft-bodied euarthropod within a marginal-marine depositional setting, and significantly expand the known phylogenetic and environmental occurrence of this complex behaviour during the Palaeozoic. Previous trace fossil evidence for Palaeozoic moulting is based on the ichnogenus Rusophycus and essentially restricted to trilobites20,21. Cryptic behaviour in trilobites – including infaunal8,9 and sheltered moulting21 – has been regarded as an escalatory defensive strategy to deter predation during the vulnerable period between shedding the exuvia and the hardening of the newly formed exoskeleton. In addition, based on sedimentological context (i.e. river- and storm-flood deposits), substrate penetration may have helped to mitigate the relatively high-energy conditions at the sediment-water interface.
In this scenario, the Naranco Formation trace fossils reveal that marginal-marine soft-bodied euarthropods may have been as susceptible to predation as mid-Palaeozoic trilobites living in fully marine environments8,9,22, and indicate that infaunal moulting evolved multiple times in different euarthropod lineages as a result of these fundamental selective pressures. This study illustrates the significance of trace fossils for illuminating the evolution of adaptive complex behavioural strategies through deep time and for expanding our knowledge of ecdysis commonly recorded in the form of body fossils1,23.
Source: Ecology - nature.com
