Organic preservation of fossil musculature with ultracellular detail

The very labile (decay-prone), non-biomineralized, tissues of organisms are rarely fossilized. Occurrences thereof are invaluable supplements to a body fossil record dominated by biomineralized tissues, which alone are extremely unrepresentative of diversity in modern and ancient ecosystems. Fossil examples of extremely labile tissues (e.g. muscle) that exhibit a high degree of morphological fidelity are almost invariably replicated by inorganic compounds such as calcium phosphate. There is no consensus as to whether such tissues can be preserved with similar morphological fidelity as organic remains, except when enclosed inside amber. Here, we report fossilized musculature from an approximately 18 Myr old salamander from lacustrine sediments of Ribesalbes, Spain. The muscle is preserved organically, in three dimensions, and with the highest fidelity of morphological preservation yet documented from the fossil record. Preserved ultrastructural details include myofilaments, endomysium, layering within the sarcolemma, and endomysial circulatory vessels infilled with blood. Slight differences between the fossil tissues and their counterparts in extant amphibians reflect limited degradation during fossilization. Our results provide unequivocal evidence that high-fidelity organic preservation of extremely labile tissues is not only feasible, but likely to be common. This is supported by the discovery of similarly preserved tissues in the Eocene Grube Messel biota.     

Experimental taphonomy of giant sulphur bacteria: implications for the interpretation of the embryo-like Ediacaran Doushantuo fossils

The Ediacaran Doushantuo biota has yielded fossils interpreted as eukaryotic organisms, either animal embryos or eukaryotes basal or distantly related to Metazoa. However, the fossils have been interpreted alternatively as giant sulphur bacteria similar to the extant Thiomargarita. To test this hypothesis, living and decayed Thiomargarita were compared with Doushantuo fossils and experimental taphonomic pathways were compared with modern embryos. In the fossils, as in eukaryotic cells, subcellular structures are distributed throughout cell volume; in Thiomargarita, a central vacuole encompasses approximately 98 per cent cell volume. Key features of the fossils, including putative lipid vesicles and nuclei, complex envelope ornament, and ornate outer vesicles are incompatible with living and decay morphologies observed in Thiomargarita. Microbial taphonomy of Thiomargarita also differed from that of embryos. Embryo tissues can be consumed and replaced by bacteria, forming a replica composed of a three-dimensional biofilm, a stable fabric for potential fossilization. Vacuolated Thiomargarita cells collapse easily and do not provide an internal substrate for bacteria. The findings do not support the hypothesis that giant sulphur bacteria are an appropriate interpretative model for the embryo-like Doushantuo fossils. However, sulphur bacteria may have mediated fossil mineralization and may provide a potential bacterial analogue for other macroscopic Precambrian remains.     

A soft-bodied lophophorate from the Silurian of England

Soft-bodied taxa comprise an important component of the extant lophophorate fauna, but convincing fossils of soft-bodied lophophorates are extremely rare. A small fossil lophophorate, attached to a brachiopod dorsal valve, is described from the Silurian (Wenlock Series) Herefordshire Lagerstätte of England. This unmineralized organism was bilaterally symmetrical and comprised a subconical body attached basally to the host and partially enclosed by a broad ‘hood’; the body bore a small, coiled lophophore. Where the hood attached laterally, there is a series of transverse ridges and furrows. The affinities of this organism probably lie with Brachiopoda; the hood is interpreted as the homologue of a dorsal valve/mantle lobe, and the attachment as the homologue of the ventral valve and/or pedicle. The ridges are arranged in a manner that suggests constructional serial repetition, indicating that they are unlikely to represent mantle canals. Extant brachiopods are not serially structured, but morphological and molecular evidence suggests that their ancestors were. The new organism may belong to the brachiopod stem group, and might also represent a significant element of the Palaeozoic lophophorate fauna.     

The role of iron in the formation of Ediacaran ‘death masks’

The Ediacara biota are an enigmatic group of Neoproterozoic soft-bodied fossils that mark the first major radiation of complex eukaryotic and macroscopic life. These fossils are thought to have been preserved via pyritic “death masks” mediated by seafloor microbial mats, though little about the chemical constraints of this preservational pathway is known, in particular surrounding the role of bioavailable iron in death mask formation and preservational fidelity. In this study, we perform decay experiments on both diploblastic and triploblastic animals under a range of simulated sedimentary iron concentrations, in order to characterize the role of iron in the preservation of Ediacaran organisms. After 28 days of decay, we demonstrate the first convincing “death masks” produced under experimental laboratory conditions composed of iron sulfide and probable oxide veneers. Moreover, our results demonstrate that the abundance of iron in experiments is not the sole control on death mask formation, but also tissue histology and the availability of nucleation sites. This illustrates that Ediacaran preservation via microbial death masks need not be a “perfect storm” of paleoenvironmental porewater and sediment chemistry, but instead can occur under a range of conditions.     

A neotaphonomic experiment in pollen oxidation and its implications for archaeopalynology

Oxidation is considered to be a major taphonomic process involved in differential pollen preservation. An experimental protocol has been developed in the laboratory to test the impact of oxidation on pollen concentrations. Seven modern pollen taxa were selected among common trees, shrubs and herbaceous plants from the European flora, with regard to their typical pollen morphology (Pinus, Alnus, deciduous Quercus, Cichorioideae, Caryophyllaceae, Ericaceae and Poaceae). An aqueous solution of potassium permanganate (KMnO₄) was used to oxidise the pollen grains. The impact of oxidation was measured as a function of increasing oxidation intensity and increasing exposure time. For each taxon, the pollen concentration (grains µl⁻¹) was measured following each oxidation stage. The results show that all pollen taxa are affected by oxidation. Both low oxidant concentrations and short oxidation exposure times led to a fast decrease in pollen concentrations. The thickness of the exine and a specific morphology appear to be the deciding factors controlling the ability to withstand oxidation. A simulation of the impact of oxidation was performed on two model pollen spectra simulating a forested and an open environment. Significant differences were recorded between the initial and final pollen rates. The AP/NAP ratio is modified to a greater extent in the spectrum associated with the open environment. However, over-representation of a specific taxon in a pollen spectrum cannot be attributed to the impact of oxidation alone. For instance, when Cichorioideae are recorded with high frequencies in pollen analyses carried out in an archaeological context, oxidation should not be regarded as the only taphonomic process responsible for this over-representation. The differential conservation of pollen is a complex process in which oxidation represents but one of a variety of interacting taphonomic factors (such as pollen transport, bacterial activity, temperature, pH, hygrometry).     

The original colours of fossil beetles

Structural colours, the most intense, reflective and pure colours in nature, are generated when light is scattered by complex nanostructures. Metallic structural colours are widespread among modern insects and can be preserved in their fossil counterparts, but it is unclear whether the colours have been altered during fossilization, and whether the absence of colours is always real. To resolve these issues, we investigated fossil beetles from five Cenozoic biotas. Metallic colours in these specimens are generated by an epicuticular multi-layer reflector; the fidelity of its preservation correlates with that of other key cuticular ultrastructures. Where these other ultrastructures are well preserved in non-metallic fossil specimens, we can infer that the original cuticle lacked a multi-layer reflector; its absence in the fossil is not a preservational artefact. Reconstructions of the original colours of the fossils based on the structure of the multi-layer reflector show that the preserved colours are offset systematically to longer wavelengths; this probably reflects alteration of the refractive index of the epicuticle during fossilization. These findings will allow the former presence, and original hue, of metallic structural colours to be identified in diverse fossil insects, thus providing critical evidence of the evolution of structural colour in this group.     

Exceptional preservation requires fast biodegradation: thylacocephalan specimens from La Voulte-sur-Rhône (Callovian,Jurassic, France)

Konservat-Lagerstätten are seen as snapshots of past biodiversity for a given location and time. However, processes leading to the exceptional morphological preservation of fossils in these deposits remain incompletely understood. This results in a deficient assessment of taphonomic biases and limits the robustness/relevance of palaeobiological reconstructions. Here, we report the mineralogical characterization of crustacean fossils preserved within carbonate-rich concretions from the Jurassic Konservat-Lagerstätte of La Voulte-sur-Rhône (Ardèche, France). The combination of SEM-EDS, TEM, synchrotron-based XRF, XRD and XANES allows the mineralogical phases composing these fossils (i.e. fluorapatite, Fe-sulfides (pyrite, pyrrhotite) and Mg-calcite) and the surrounding matrix (i.e. Mg-calcite, clays and detrital silicates) to be identified. Fluorapatite and pyrite (and pyrrhotite) precipitated during decay under anoxic conditions, replacing delicate organic structures and preserving anatomical details. These mineral structures were subsequently consolidated by a Mg-calcite cement. Of note, histologically similar tissues were replaced by the same mineral phases, confirming that fossilization (in La Voulte) occurred rapidly enough to be influenced by tissue composition. Altogether, the present study shows that exceptional preservation requires fast biodegradation, thereby confirming recent experimental evidence.