Soft‐Bodied Fossils Are Not Simply Rotten Carcasses – Toward a Holistic Understanding of Exceptional Fossil Preservation

Exceptionally preserved fossils are the product of complex interplays of biological and geological processes including burial, autolysis and microbial decay, authigenic mineralization, diagenesis, metamorphism, and finally weathering and exhumation. Determining which tissues are preserved and how biases affect their preservation pathways is important for interpreting fossils in phylogenetic, ecological, and evolutionary frameworks. Although laboratory decay experiments reveal important aspects of fossilization, applying the results directly to the interpretation of exceptionally preserved fossils may overlook the impact of other key processes that remove or preserve morphological information. Investigations of fossils preserving non‐biomineralized tissues suggest that certain structures that are decay resistant (e.g., the notochord) are rarely preserved (even where carbonaceous components survive), and decay‐prone structures (e.g., nervous systems) can fossilize, albeit rarely. As we review here, decay resistance is an imperfect indicator of fossilization potential, and a suite of biological and geological processes account for the features preserved in exceptional fossils.     

Experimental analysis of soft‐tissue fossilization: opening the black box

Taphonomic experiments provide important insights into fossils that preserve the remains of decay‐prone soft tissues, tissues that are usually degraded and lost prior to fossilization. These fossils are among the most scientifically valuable evidence of ancient life on Earth, giving us a view into the past that is much less biased and incomplete than the picture provided by skeletal remains alone. Although the value of taphonomic experiments is beyond doubt, a lack of clarity regarding their purpose and limitations, and ambiguity in the use of terminology, are hampering progress. Here we distinguish between processes that promote information retention and those that promote information loss, in order to clarify the distinction between fossilization and preservation. Recognizing distinct processes of decay, mineralization and maturation, the sequence in which they act, and the potential for interactions, has important consequences for analysis of fossils, and for the design of taphonomic experiments. The purpose of well‐designed taphonomic experiments is generally to understand decay, maturation and preservation individually, thus limiting the number of variables involved. Much work remains to be done, but these methodologically reductionist foundations will allow researchers to build towards more complex taphonomic experiments and a more holistic understanding and analysis of the interactions between decay, maturation and preservation in the fossilization of non‐biomineralized remains. Our focus must remain on the key issue of understanding what exceptionally preserved fossils reveal about the history of biodiversity and evolution, rather than on debating the scope and value of an experimental approach.     

Experimental taphonomy of Artemia reveals the role of endogenous microbes in mediating decay and fossilization

Exceptionally preserved fossils provide major insights into the evolutionary history of life. Microbial activity is thought to play a pivotal role in both the decay of organisms and the preservation of soft tissue in the fossil record, though this has been the subject of very little experimental investigation. To remedy this, we undertook an experimental study of the decay of the brine shrimp Artemia, examining the roles of autolysis, microbial activity, oxygen diffusion and reducing conditions. Our findings indicate that endogenous gut bacteria are the main factor controlling decay. Following gut wall rupture, but prior to cuticle failure, gut-derived microbes spread into the body cavity, consuming tissues and forming biofilms capable of mediating authigenic mineralization, that pseudomorph tissues and structures such as limbs and the haemocoel. These observations explain patterns observed in exceptionally preserved fossil arthropods. For example, guts are preserved relatively frequently, while preservation of other internal anatomy is rare. They also suggest that gut-derived microbes play a key role in the preservation of internal anatomy and that differential preservation between exceptional deposits might be because of factors that control autolysis and microbial activity. The findings also suggest that the evolution of a through gut and its bacterial microflora increased the potential for exceptional fossil preservation in bilaterians, providing one explanation for the extreme rarity of internal preservation in those animals that lack a through gut.     

Decay and mineralization of soft tissue in Early Devonian boring ctenostome bryozoans

The Early Devonian of Podolia, Ukraine, has yielded phosphatized colonies of the boring ctenostome bryozoan Podoliapora doroshivi with 3‐D preservation of soft tissues. However, the feeding zooids are not anatomically complete, their preserved soft tissues comprising decay‐resistant structures such as the protective cuticular polypide sacs with presumed parietal muscles inside the wall of the sacs, the setigerous collars, the membranous orificial walls and remains of the muscle tissues. Early diagenetic apatite mineralization occured in numerous feeding zooids of Podoliapora at different stages of decay and may be important for the interpretation of decay processes in these colonial soft‐bodied fossil organisms. A setigerous collar, which is a characteristic of extant ctenostomes, occurs in P. doroshivi in several stages of decay showing progressive collapse and eventual complete loss. This study indicates that the morphological changes of collars induced by decay often resulted in connection with the membranous orificial wall, producing false anatomical structures, unrelated to structures observed in the earlier stages of decay or to the anatomical structures of extant ctenostomes. The most decay‐resistant cuticular polypide sacs mineralized as cryptocrystalline apatite in early stage of decay became degraded in later stages of decay. These data provide evidence that the anatomical interpretation of soft‐bodied fossils preserved only in the later stages of decay may have led to imprecise morphological interpretations.     

Atlas of vertebrate decay: a visual and taphonomic guide to fossil interpretation

Like many other important evolutionary transitions, our knowledge of the origin of vertebrates is limited to windows of exceptional preservation of soft‐bodied fossils. Unfortunately, these fossils are rare and have been subjected to complex taphonomic filters including decay, collapse and distortion. To maximize our ability to utilize these crucial fossils to reconstruct the timing and sequence of evolutionary events, we are in the need of a robust taphonomic framework with in which to interpret them. Here, we report the results of a series of experiments designed to examine patterns of transformation and loss during decay of important anatomical characters of chordates and primitive vertebrates (ammocoete, adult lamprey, hagfish, juvenile chondrichthyans and a non‐vertebrate chordate, Branchiostoma). Complex and repeated patterns of transformation during decay are identified and figured for informative character complexes including eyes, feeding apparatus, skull and brain, muscles, branchial apparatus, axial structures, viscera, heart and fins. The resulting data regarding character decay and relative loss serve as a guide to recognition and interpretation of the anatomy of non‐biomineralized fossil vertebrates. The methods and techniques outlined are eminently applicable to other soft‐bodied groups and present a new way to interpret the exceptionally preserved fossil record.     

Influence of microbial biofilms on the preservation of primary soft tissue in fossil and extant archosaurs

Background

Mineralized and permineralized bone is the most common form of fossilization in the vertebrate record. Preservation of gross soft tissues is extremely rare, but recent studies have suggested that primary soft tissues and biomolecules are more commonly preserved within preserved bones than had been presumed. Some of these claims have been challenged, with presentation of evidence suggesting that some of the structures are microbial artifacts, not primary soft tissues. The identification of biomolecules in fossil vertebrate extracts from a specimen of Brachylophosaurus canadensis has shown the interpretation of preserved organic remains as microbial biofilm to be highly unlikely. These discussions also propose a variety of potential mechanisms that would permit the preservation of soft-tissues in vertebrate fossils over geologic time.

Methodology/Principal Findings

This study experimentally examines the role of microbial biofilms in soft-tissue preservation in vertebrate fossils by quantitatively establishing the growth and morphology of biofilms on extant archosaur bone. These results are microscopically and morphologically compared with soft-tissue extracts from vertebrate fossils from the Hell Creek Formation of southeastern Montana (Latest Maastrichtian) in order to investigate the potential role of microbial biofilms on the preservation of fossil bone and bound organic matter in a variety of taphonomic settings. Based on these analyses, we highlight a mechanism whereby this bound organic matter may be preserved.

Conclusions/Significance

Results of the study indicate that the crystallization of microbial biofilms on decomposing organic matter within vertebrate bone in early taphonomic stages may contribute to the preservation of primary soft tissues deeper in the bone structure.     

Unlocking the early fossil record of the arthropod central nervous system

Extant panarthropods (euarthropods, onychophorans and tardigrades) are hallmarked by stunning morphological and taxonomic diversity, but their central nervous systems (CNS) are relatively conserved. The timing of divergences of the ground pattern CNS organization of the major panarthropod clades has been poorly constrained because of a scarcity of data from their early fossil record. Although the CNS has been documented in three-dimensional detail in insects from Cenozoic ambers, it is widely assumed that these tissues are too prone to decay to withstand other styles of fossilization or geologically older preservation. However, Cambrian Burgess Shale-type compressions have emerged as sources of fossilized brains and nerve cords. CNS in these Cambrian fossils are preserved as carbon films or as iron oxides/hydroxides after pyrite in association with carbon. Experiments with carcasses compacted in fine-grained sediment depict preservation of neural tissue for a more prolonged temporal window than anticipated by decay experiments in other media. CNS and compound eye characters in exceptionally preserved Cambrian fossils predict divergences of the mandibulate and chelicerate ground patterns by Cambrian Stage 3 (ca 518 Ma), a dating that is compatible with molecular estimates for these splits.     

Accurate forest projections require long‐term wood decay experiments because plant trait effects change through time

Whether global change will drive changing forests from net carbon (C) sinks to sources relates to how quickly deadwood decomposes. Because complete wood mineralization takes years, most experiments focus on how traits, environments and decomposer communities interact as wood decay begins. Few experiments last long enough to test whether drivers change with decay rates through time, with unknown consequences for scaling short‐term results up to long‐term forest ecosystem projections. Using a 7 year experiment that captured complete mineralization among 21 temperate tree species, we demonstrate that trait effects fade with advancing decay. However, wood density and vessel diameter, which may influence permeability, control how decay rates change through time. Denser wood loses mass more slowly at first but more quickly with advancing decay, which resolves ambiguity about the after‐life consequences of this key plant functional trait by demonstrating that its effect on decay depends on experiment duration and sampling frequency. Only long‐term data and a time‐varying model yielded accurate predictions of both mass loss in a concurrent experiment and naturally recruited deadwood structure in a 32‐year‐old forest plot. Given the importance of forests in the carbon cycle, and the pivotal role for wood decay, accurate ecosystem projections are critical and they require experiments that go beyond enumerating potential mechanisms by identifying the temporal scale for their effects.     

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.     

Distinguishing geology from biology in the Ediacaran Doushantuo biota relaxes constraints on the timing of the origin of bilaterians

The Ediacaran Doushantuo biota has yielded fossils that include the oldest widely accepted record of the animal evolutionary lineage, as well as specimens with alleged bilaterian affinity. However, these systematic interpretations are contingent on the presence of key biological structures that have been reinterpreted by some workers as artefacts of diagenetic mineralization. On the basis of chemistry and crystallographic fabric, we characterize and discriminate phases of mineralization that reflect: (i) replication of original biological structure, and (ii) void-filling diagenetic mineralization. The results indicate that all fossils from the Doushantuo assemblage preserve a complex mélange of mineral phases, even where subcellular anatomy appears to be preserved. The findings allow these phases to be distinguished in more controversial fossils, facilitating a critical re-evaluation of the Doushantuo fossil assemblage and its implications as an archive of Ediacaran animal diversity. We find that putative subcellular structures exhibit fabrics consistent with preservation of original morphology. Cells in later developmental stages are not in original configuration and are therefore uninformative concerning gastrulation. Key structures used to identify Doushantuo bilaterians can be dismissed as late diagenetic artefacts. Therefore, when diagenetic mineralization is considered, there is no convincing evidence for bilaterians in the Doushantuo assemblage.     

Evidence for seafloor microbial mats and associated metazoan lifestyles in Lower Cambrian phosphorites of Southwest China

The increase in the depth and intensity of bioturbation through the Proterozoic-­Phanerozoic transition changed the substrates on which marine benthos lived from being relatively firm with a sharp sediment-water interface to having a high water content and blurry sediment-water interface. Additionally, microbial mats, once dominant on normal marine Proterozoic seafloors, were relegated to stressed settings lacking intense metazoan activity. This change in substrates has been termed the 'agronomic revolution', and its impact on benthic metazoans has been termed the 'Cambrian substrate revolution'. The shallow marine phosphorites of the Lower Cambrian Meishucun Formation of southwest China contain evidence suggestive of the presence of seafloor microbial mats. This evidence includes abundant and distinctive red-colored bedding planes enriched in heavy iron minerals and mica, interpreted as resulting from mat-decay mineralization and mica trapping by microbial mats. The radular grazing trace fossil Radulichnus is also found in this formation, indicating a firm, microbial mat-bound substrate. These radular scratches are always preserved with circular impressions around 10 cm in diameter, possibly the fossils of soft-bodied organisms. The first relatively intense bioturbation in this region is found in this formation and is dominated by horizontal Thalassinoides burrows, which could represent undermat mining behavior. The evidence for the presence of microbial mats in the Lower Cambrian Meishucun Formation, and for metazoan lifestyles associated with such mat-bound seafloors, reveals that normal marine environments dominated by typical Proterozoic-style soft substrates still existed during the Cambrian substrate revolution.     

Evidence for targeted elasmobranch predation on thalassinidean shrimp in the Miocene Taliao Formation,NE Taiwan

Terrestrial and marine invertebrate organisms both leave records of their activities in the sediment in the form of trace fossils, at least during certain stages of their ontogeny. In contrast, trace fossils produced by vertebrate organisms are scarce, although terrestrial trace fossils provide exclusive insights into the social behaviour of their producers. In the marine realm, vertebrate trace fossils are relatively rare, difficult to identify and problematic to interpret. However, in certain settings, observations on serendipitously preserved and exposed trace fossils can shed light on the predatory behaviour of marine vertebrates. In Miocene outer shelf to nearshore sandstones of the Taliao Formation in NE Taiwan, large numbers of bowl‐shaped trace fossils can be observed. Morphology and size range (diameter typically 10–30 cm, average depth around 10 cm) of these trace fossils agree well with feeding traces of modern stingrays, and the trace fossil Piscichnus waitemata, which has been attributed to bottom feeding rays. Stingrays direct a jet of water from their mouths to excavate a bowl‐shaped pit to expose their prey. In the material filling the excavated bowl, broken pieces of two other common trace fossils, Ophiomorpha and Schaubcylindrichnus, are often found, and in a number of cases, vertical shafts of Ophiomorpha surrounded by dispersed pieces of wall material have been observed. In contrast, surrounding sediment rarely contains this kind of broken pieces of wall material. These observations clearly indicate that stingrays specifically targeted the producers of the trace fossils: thalassinoid crustaceans and worms, respectively. The targeted predation of these relatively deep burrowers furthermore suggests that the rays used their electroreceptive organs to locate the prey; as such, direct targeting of buried prey only based on olfactory senses has been shown to be ineffective in experiments with extant myliobatiform rays.     

Two-stepping through time: mammals and viruses

Recent studies have identified ancient virus genomes preserved as fossils within diverse animal genomes. These fossils have led to the revelation that a broad range of mammalian virus families are older and more ubiquitous than previously appreciated. Long-term interactions between viruses and their hosts often develop into genetic arms races where both parties continually jockey for evolutionary dominance. It is difficult to imagine how mammalian hosts have kept pace in the evolutionary race against rapidly evolving viruses over large expanses of time, given their much slower evolutionary rates. However, recent data has begun to reveal the evolutionary strategy of slowly-evolving hosts. We review these data and suggest a modified arms race model where the evolutionary possibilities of viruses are relatively constrained. Such a model could allow more accurate forecasting of virus evolution.     

Microbial Activity in Caves−A Geological Perspective

Caves are commonly the home of diverse microbial biotas, the sites of active mineral precipitation, and/or receptacles for the deposition of sediment. Mineral precipitation is commonly considered to be abiogenic despite the fact that microbes are present in caves, especially in the twilight zone. Detailed analysis of cave substrates from a geological perspective shows that microbes can mediate constructive (microbe calcification, trapping and binding, mediation of crystal growth) and destructive (substrate etching and breakdown) processes. Potentially these processes can significantly influence the formation and preservation of any cave deposit. Preservation of microbes is possible if mineralization takes place while the microbe is alive or shortly after its demise. If not, all record of the microbe will be lost to decay. Even if the microbes are preserved, it may be difficult to determine if they played an active or passive role in the formation of the deposits in which they are entombed. For old cave deposits, such an assessment must rely on spatial relationships and comparison of textures with those known to form as a result of microbial activity. Nevertheless, available evidence indicates that microbes can play a major role in the formation and modification of cave deposits. Equally, however, it is apparent that the full scope and impact of microbial activity on cave deposits has yet to be realized. Recognition of microbial activity in old CaCO 3 cave deposits relies on (1) documentation and recognition of mineralized microbes, (2) recognition of stromatolitic structures that formed through microbial activity, and/or (3) the identification of fabrics/textures that are known to be indicative of microbial activity. All of these criteria fundamentally rely on the interpretation of fabrics preserved in the cave deposits. Virtually all of these interpretations are open to debate.     

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.     

Epidermal and dermal integumentary structures of ankylosaurian dinosaurs

Ankylosaurian dinosaurs are most notable for their abundant and morphologically diverse osteoderms, which would have given them a spiky appearance in life. Isolated osteoderms are relatively common and provide important information about the structure of the ankylosaur dermis, but fossilized impressions of the soft‐tissue epidermis of ankylosaurs are rare. Nevertheless, well‐preserved integument exists on several ankylosaur fossils that shows osteoderms were covered by a single epidermal scale, but one or many millimeter‐sized ossicles may be present under polygonal, basement epidermal scales. Evidence for the taxonomic utility of ankylosaurid epidermal scale architecture is presented for the first time. This study builds on previous osteological work that argues for a greater diversity of ankylosaurids in the Dinosaur Park Formation of Alberta than has been traditionally recognized and adds to the hypothesis that epidermal skin impressions are taxonomically relevant across diverse dinosaur clades. J. Morphol. 275:39–50, 2014. © 2013 Wiley Periodicals, Inc.     

The first non‐marine ostracod fauna from the Lower Barremian dysodiles of Lebanon

Dysodiles are finely laminated sedimentary rocks rich in organic matter and in exceptionally well‐preserved fossils, hence their petroleum and palaeontological interest. However, few studies focused on the dysodiles of Lebanon, leaving their palaeontological content and their depositional environment largely unknown. Our previous investigations show a variety of well‐preserved lacustrine fossils including ichthyofauna, chelonians, insects, plant debris, gastropods, palynomorphs and ostracods. The present study focuses on the ostracods of five sampling localities from the Lower Barremian of Lebanon. Being the most abundant fossils, ostracods raise some taphonomic and palaeoecological questions that may help us understand the depositional environment and enrich the story of these Early Barremian lakes. Faunal differences between the sampled sections provide clues to the specific characteristics of each lake. The abundance of ‘butterfly’ preservation of carapaces, together with the association of adults and juveniles, indicates calm depositional environments without post‐mortem transport. The assemblages comprise ostracods with known swimming ability (Cyprois and Zonocypris) or that are thought to have been swimmers (Cypridea), while non‐swimmers are absent, suggesting that nektobenthonic ostracods must have lived only in the shallow margins of the lakes or among floating vegetation because hypolimnion conditions were hostile to benthos. This study provides different scenarios on how this fauna ended up preserved in the laminated lake sediments.     

Preservational modes of some ichthyosaur soft tissues (Reptilia,Ichthyopterygia) from the Jurassic Posidonia Shale of Germany

Konservat-Lagerstätten, such as the Toarcian (Early Jurassic) Posidonia Shale of southwestern Germany, are renowned for their spectacular fossils. Ichthyosaur skeletons recovered from this formation are frequently associated with soft tissues; however, the preserved material ranges from three-dimensional, predominantly phosphatized structures to dark films of mainly organic matter. We examined soft-tissue residues obtained from two ichthyosaur specimens using an integrated ultrastructural and geochemical approach. Our analyses revealed that the superficially-looking ‘films’ in fact comprise sections of densely aggregated melanosome (pigment) organelles sandwiched between phosphatized layers containing fibrous microstructures. We interpret this distinct layering as representing condensed and incompletely degraded integument from both sides of the animal. When compared against previously documented ichthyosaur fossils, it becomes readily apparent that a range of preservational modes exists between presumed ‘phosphatic’ and ‘carbonized’ soft-tissue remains. Some specimens show high structural fidelity (e.g. distinct integumentary layering), while others, including the fossils examined in this study, retain few original anatomical details. This diversity of soft-tissue preservational modes among Posidonia Shale ichthyosaurs offers a unique opportunity to examine different biostratinomic, taphonomic and diagenetic variables that potentially could affect the process of fossilization. It is likely that soft-tissue preservation in the Posidonia Shale was regulated by a multitude of factors, including decay efficiency and speed of phosphatic mineral nucleation; these in turn were governed by a seafloor with sustained microbial mat activity fuelled by high organic matter input and seasonally fluctuating oxygen levels.