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.     

Experimentally observed soft‐tissue preservation near a marine brine seep

A sea urchin placed on the sea floor near an active brine seep was recovered after 13 years with detailed soft‐tissue preservation. Growth of an amorphous calcium carbonate solid with small amounts of the mineral bassanite occurred on the spines and test. The solid also exhibits striations at both the macro‐ and microscopic scales that preserve the muscle texture of the sea urchin. Such soft‐tissue replacement and mineralization could lead to exquisite fossilization. Soft‐tissue mineralization has been previously replicated in controlled laboratory conditions; however, this is the first report of the lithologic replication of soft tissues in an open marine experiment. Examples of extraordinary fossil preservation, or Lagersätten, give a distinct snapshot of the past and have led to a greater understanding of the history of life. Soft‐tissue lithification occurs in special circumstances in which local chemical conditions (often mediated by decay or bacterial factors) promote early diagenetic mineralization, the first steps of which are observed in this instance. The preservation of articulated skeletons, especially within echinoderms, is normally attributed to rapid burial, but that may not be necessary given that this urchin was at or very near the sediment–water interface for 13 years.     

Unveiling biases in soft‐tissue phosphatization: extensive preservation of musculature in the Cretaceous (Cenomanian) polychaete Rollinschaeta myoplena (Annelida: Amphinomidae)

The process of soft‐tissue phosphatization (the replication of labile tissues by calcium phosphate) is responsible for many instances of high‐resolution soft tissue preservation, often revealing anatomical insights into the animals that so preserved. However, while much work has gone into exploring key issues such as biases and micro‐controls, phosphatization remains poorly understood as a taphonomic process. Here, using camera lucida, plain‐light microscopy and SEM imagery, we address this issue by describing the taphonomy and fidelity of the musculature of Rollinschaeta myoplena Parry et al., a phosphatized annelid from the Cretaceous Konservat‐Lagerstätten of Hakel and Hjoula, Lebanon, with an unprecedented quantity of three‐dimensional soft‐tissue preservation. Analysis highlights two strong, previously recognized biases affecting the process of phosphatization: (1) a taxonomic bias restricted to R. myoplena that triggers unusually extensive phosphatization; and (2) a tissue bias whereby longitudinal and parapodial musculature show markedly higher fidelity in comparison to the musculature of the intestine and body wall circular muscles. Potential explanations for these biases include internal phosphate‐enrichment by relative muscle density, the relative rate of decay and the physiology of musculature. Incongruence between experimental decay series for polychaetes and the prevalence of labile tissue preservation over recalcitrant tissues in R. myoplena exposes the limits of decay experiments for understanding exceptional preservation.     

The role of experiments in investigating the taphonomy of exceptional preservation

In the last 20 years, much taphonomic experimentation has focused on the interpretation of exceptionally preserved fossils. Decay experiments have been used to interpret the features preserved in soft‐bodied fossils and to determine the sequence of character loss and its impact on phylogenetic position. Experiments on the impact of microbial communities on decay and mineralization have started to illuminate the processes involved in the fossilization of soft tissues, including embryos. The role of decay in promoting authigenic mineralization has been used to investigate the formation of Ediacaran macrofossils and concretions. Maturation experiments have shown how the constituents of animals and plants are transformed over time to a macromolecular material that converges on a similar stable composition. Other maturation experiments have explained how structural colours in fossils are altered from the original. A major area requiring investigation is the role of specific types of microbes in decay and their impact on sediment and pore water chemistry, as well as the environmental controls that determine their presence and level of activity. Microbial activity has received less attention than other factors in attempts to explain why the occurrence and nature of exceptional preservation varies in time and space through the fossil record.     

Three-dimensional soft tissue preservation revealed in the skin of a non-avian dinosaur

The most commonly preserved soft tissues associated with ornithischian dinosaurs are skin remains. The apparent resistance of hadrosaur skin to decay, and its abundance in the fossil record relative to that of other tetrapods, has been attributed to factors such as thickness and composition. Here we report additional intrinsic factors within hadrosaur skin: 3D-preserved eumelanin-bearing bodies, dermal cells and blood vessel fragments in an organic matrix composed of protein fossilization products. The skin is much thinner than that of living mammals of similar size. It is likely that the preservation of hadrosaur skin is related to the arrangement of the layers composing it.     

Skeletal completeness of the non‐avian theropod dinosaur fossil record

Non‐avian theropods were a highly successful clade of bipedal, predominantly carnivorous, dinosaurs. Their diversity and macroevolutionary patterns have been the subject of many studies. Changes in fossil specimen completeness through time and space can bias our understanding of macroevolution. Here, we quantify the completeness of 455 non‐avian theropod species using the skeletal completeness metric (SCM), which calculates the proportion of a complete skeleton preserved for a specimen. Temporal patterns of theropod skeletal completeness show peaks in the Carnian, Oxfordian–Kimmeridgian and Barremian–Aptian, and lows in the Berriasian and Hauterivian. Lagerstätten primarily drive the peaks in completeness and observed taxonomic diversity in the Oxfordian–Kimmeridgian and the Barremian–Aptian. Theropods have a significantly lower distribution of completeness scores than contemporary sauropodomorph dinosaurs but change in completeness through time for the two groups shows a significant correlation when conservation Lagerstätten are excluded, possibly indicating that both records are primarily driven by geology and sampling availability. Our results reveal relatively weak temporal sampling biases acting on the theropod record but relatively strong spatial and environmental biases. Asia has a significantly more complete record than any other continent, the mid northern latitudes have the highest abundance of finds, and most complete theropod skeletons come from lacustrine and aeolian environments. We suggest that these patterns result from historical research focus, modern climate dynamics, and depositional transportation energy plus association with conservation Lagerstätten, respectively. Furthermore, we find possible ecological biases acting on different theropod subgroups, but body size does not influence theropod completeness on a global scale.     

Exceptionally well‐preserved vegetal remains from the Upper Cretaceous of ‘Lo Hueco’, Cuenca,Spain

Vegetal remains are considered labile structures that quickly become decayed in ecosystems. However, certain lignified tissues (woody plants) can largely resist decomposition, becoming sometimes exceptionally well preserved. At the Upper Cretaceous site of ‘Lo Hueco’ (Cuenca, Spain), those woody remains (trunks and branches) with resinous material in the inner tracheids and parenchyma cells that were buried rapidly under anoxic conditions experienced a low degree of maturation, becoming exceptionally well preserved. Those woody remains deposited under oxic conditions (sub‐aerial or sub‐aquatic exposure) were more intensely biodegraded and subsequently carbonified, partially or completely mineralized in gypsum and covered by a ferruginous crust. These two modes of preservation are scarce, with silicification or carbonification processes much more common, and both can be considered as ‘exceptional preservation’. Other vegetal remains, such as carbonified leaves, stems and roots, were collected in the site. The different modes of preservation depend directly on: depositional micro‐environment (sandy distributary channel, muddy flood plain); and type (trunk, branch, stem, leave, root) and state (presence or absence of resinous material) of the material. The great abundance and diversity of fossils in ‘Lo Hueco’ identify it as Konzentrat‐Lagerstätten, sequentially formed by alternated events of flooding and drying depositional events, but the exceptional quality and rarity of determinate vegetal macroremains preservation suggest that certain deposits of this site can be considered as conservation deposits.     

Tube foot preservation in the Devonian crinoid Codiacrinus from the Lower Devonian Hunsrück Slate,Germany

Fossilized tube feet are described on Codiacrinus schultzei Follmann from the Lower Devonian Hunsrück Slate of Germany. This is the first definitive proof of tube feet on any fossil crinoid. Three lightly pyritized, flattened tube feet are preserved in a single interray of this cladid crinoid. The tube feet were at least 7 mm long. Their preservation is very similar to the tube feet reported previously from a Hunsrück ophiuroid, except that the Codiacrinus tube feet have small papillae, similar to living crinoids.     

The Sirius Passet Lagerstätte: silica death masking opens the window on the earliest matground community of the Cambrian explosion

The Sirius Passet Lagerstätte (SP), Peary Land, North Greenland, occurs in black slates deposited at or just below storm wave base. It represents the earliest Cambrian microbial mat community with exceptional preservation, predating the Burgess Shale by 10 million years. Trilobites from the SP are preserved as complete, three‐dimensional, concave hyporelief external moulds and convex epirelief casts. External moulds are shown to consist of a thin veneer of authigenic silica. The casts are formed from silicified cyanobacterial mat material. Silicification in both cases occurred shortly after death within benthic cyanobacterial mats. Pore waters were alkali, silica‐saturated, high in ferric iron but low in oxygen and sulphate. Excess silica was likely derived from remobilized biogenic silica. The remarkable siliceous death mask preservation opens a new window on the environment and location of the Cambrian Explosion. This window closed with the appearance of abundant mat grazers later as the Cambrian Explosion intensified.     

SOFT‐MI: A novel microfabrication technique integrating soft‐lithography and molecular imprinting for tissue engineering applications

An innovative approach has been employed for the realization of bioactive scaffolds able to mimic the in vivo cellular microenvironment for tissue engineering applications. This method is based on the combination of molecular imprinting and soft‐lithography technology to enhance cellular adhesion and to guide cell growth and proliferation due to presence of highly specific recognition sites of selected biomolecules on a well‐defined polymeric microstructure. In this article polymethylmethacrylate (PMMA) scaffolds have been realized by using poly(dimethylsiloxane) (PDMS) microstructured molds imprinted with FITC‐albumin and TRITC‐lectin. In addition gelatin, an adhesion protein, was employed for the molecular imprinting of polymeric scaffolds for cellular tests. The most innovative aspect of this research was the molecular imprinting of whole cells for the development of substrates able to enhance the cell adhesion processes. Biotechnol. Bioeng. 2010;106: 804–817. © 2010 Wiley Periodicals, Inc.     

A new mode of ammonite preservation – implications for dating of condensed phosphorite deposits

Unusual phosphatic casts of the ammonites Mortoniceras (Subschloenbachia) sp. and Stoliczkaia sp. from the upper Albian condensed phosphorite bed at Annopol, Poland, are discussed in terms of their taphonomic history. These specimens are interpreted as ‘secondary’ external casts of ammonite replicas preserved originally as attachment scars on oyster shells. The following genetic history is suggested for this previously undocumented mode of ammonite preservation: (1) settling of shells of dead ammonites on the seafloor; (2) colonization of these shells by oysters and formation of ammonite replicas on left valves of oysters; (3) dissolution of ammonite shells; (4) reworking and fragmentation of oyster shells; (5) casting of ammonite replicas by phosphatic material; and (6) separation of ammonite casts from oyster shells, either through mechanical disintegration or dissolution of the latter. The specimens studied were formed after dissolution of the ammonite conchs, not prior to this event as in the case of typical ammonite steinkerns (internal moulds). Therefore, they are here referred to as ‘pseudo‐steinkerns’. The time interval between loss of the original ammonite shells and the formation of oyster‐mediated pseudo‐steinkerns may be very extensive. Therefore, the pseudo‐steinkerns may potentially mislead in biostratigraphic dating of condensed phosphorite deposits.     

Soft–part preservation in heteromorph ammonites from the Cenomanian–Turonian Boundary Event (OAE 2) in north–west Germany

Abstract: From thinly laminated marlstones of the Hesseltal Formation, representing the Late Cenomanian Oceanic Anoxic Event (OAE) 2, at Lengerich in the Teutoburger Wald (Westfalen, north‐west Germany), 17 sediment‐compacted baculitid ammonites with carbonised and partially phosphatised soft parts are recorded. Some preserve remains of the buccal mass, including jaws (occasionally articulated) and radulae, as well as of the cephalic cartilage, such as eye capsules. Such have not yet been recorded previously for the order Ammonoidea. In addition, originally unmineralised parts found preserved in these specimens include extensive portions of the digestive tract, the siphonal tube, false colour patterns (megastriae), as well as traces of what would appear to be the oviduct. At the same levels, patches with numerous isolated horny upper and rarer lower jaws as well as radulae occur; these may represent regurgitates or faeces of larger predators. The cephalopod remains described were deposited in an epicontinental setting, possibly at palaeodepths between 200 and 600 m. In this particular Late Cretaceous fossil Lagerstätte, upper jaws and anaptychi of ammonites rank among the commonest fossils.     

Synchrotron x‐ray fluorescence analysis reveals diagenetic alteration of fossil melanosome trace metal chemistry

A key feature of the pigment melanin is its high binding affinity for trace metal ions. In modern vertebrates trace metals associated with melanosomes, melanin‐rich organelles, can show tissue‐specific and taxon‐specific distribution patterns. Such signals preserve in fossil melanosomes, informing on the anatomy and phylogenetic affinities of fossil vertebrates. Fossil and modern melanosomes, however, often differ in trace metal chemistry; in particular, melanosomes from fossil vertebrate eyes are depleted in Zn and enriched in Cu relative to their extant counterparts. Whether these chemical differences are biological or taphonomic in origin is unknown, limiting our ability to use melanosome trace metal chemistry to test palaeobiological hypotheses. Here, we use maturation experiments on eye melanosomes from extant vertebrates and synchrotron rapid scan‐x‐ray fluorescence analysis to show that thermal maturation can dramatically alter melanosome trace element chemistry. In particular, maturation of melanosomes in Cu‐rich solutions results in significant depletion of Zn, probably due to low pH and competition effects with Cu. These results confirm fossil melanosome chemistry is susceptible to alteration due to variations in local chemical conditions during diagenesis. Maturation experiments can provide essential data on melanosome chemical taphonomy required for accurate interpretations of preserved chemical signatures in fossils.     

The bivalved arthropods Isoxys and Tuzoia with soft‐part preservation from the Lower Cambrian Emu Bay Shale Lagerstätte (Kangaroo Island,Australia)

Abstract: Abundant material from a new quarry excavated in the lower Cambrian Emu Bay Shale (Kangaroo Island, South Australia) and, particularly, the preservation of soft‐bodied features previously unknown from this Burgess Shale‐type locality, permit the revision of two bivalved arthropod taxa described in the late 1970s, Isoxys communis and Tuzoia australis. The collections have also produced fossils belonging to two new species: Isoxys glaessneri and Tuzoia sp. Among the soft parts preserved in these taxa are stalked eyes, digestive structures and cephalic and trunk appendages, rivalling in quality and quantity those described from better‐known Lagerstätten, notably the lower Cambrian Chengjiang fauna of China and the middle Cambrian Burgess Shale of Canada.     

Kowala Lagerstätte: Late Devonian arthropods and non‐biomineralized algae from Poland

A rich and diverse assemblage of arthropods and non‐biomineralized macroalgae occurs in the Upper Devonian marine deposits of the Holy Cross Mountains, central Poland. The phrase Kowala Lagerstätte is herein proposed for the fossil‐bearing deposits confined to the lower Famennian marly shale and limestone succession of the famous Kowala Quarry. The arthropod fauna is represented by phosphatic exoskeletal remains that still preserve the fine micro‐ornamentation of the cuticle. The fauna includes crustaceans and crustacean‐like taxa such as thylacocephalans, phyllocarids and angustidontids (in order of abundance). The non‐biomineralized algae, represented by at least three morphotypes, occur as carbonaceous compressions of their thalli while still preserving fine details including bundles of thin tubular projections. Although their general appearance is reminiscent of some Early Palaeozoic non‐calcified Dasycladales algae, their true taxonomic position is still uncertain. Lithology, as well as faunal and phytoplankton content point to a pelagic sedimentary environment. Impoverished benthic fauna, sediment lamination and geochemical signatures indicate at least periodic bottom‐water dysoxic to anoxic conditions. Thus, the preservation of arthropod cuticle and non‐calcified algae was primarily governed by oxygen‐deficient bottom waters that prevented bioturbation and scavenging during their burial.     

Expression of TLR2/4 in the sperm‐storing oviduct of the Chinese soft‐shelled turtle Pelodiscus sinensis during hibernation season

The initiation of innate immunology system could play an important role in the aspect of protection for sperms long‐term storage when the sperms got into oviduct of turtles and come into contact with epithelium. The exploration of TLR2/4 distribution and expression in oviduct during hibernation could help make the storage mechanism understandable. The objective of this study was to examine the gene and protein expression profiles in Chinese soft‐shelled turtle during hibernation from November to April in the next year. The protein distribution of TLR2/4 was investigated in the magnum, isthmus, uterus, and vagina of the turtle oviduct using immunohistochemistry, and the gene expression of TLR2/4 was analyzed using quantitative real‐time PCR (qRT‐PCR). The results showed positive TLR2 protein expression primarily in the epithelium of the oviduct. TLR4 immunoreactivity was widely observed in almost every part of the oviduct, particularly in the epithelium and secretory gland membrane. Analysis of protein, mRNA expression revealed the decreased expression of TLR2/4 in the magnum compared with the isthmus, uterus, and vagina during hibernation. The protein and mRNA expression of TLR2 in the magnum, isthmus, uterus, and vagina was decreased in April compared with that in November. TLR4 protein and mRNA expression in the magnum, isthmus, uterus and vagina was decreased in November compared with that in April. These results indicated that TLR2/4 expression might protect the sperm from microbial infections. In contrast to the function of TLR2, which protects sperm during the early stages of hibernation, TLR4 might play a role in later stages of storage. The present study is the first to report the functions of TLR2/4 in reptiles.     

Sediment‐encased maturation: a novel method for simulating diagenesis in organic fossil preservation

Exceptional fossils can preserve diagenetically‐altered biomolecules. Understanding the pathways that lead to such preservation is vital to utilizing fossil information in evolutionary and palaeoecological studies. Experimental taphonomy explores the stability of tissues during microbial/autolytic decay or their molecular stability through maturation under high pressure and temperature. Maturation experiments often take place inside sealed containers, preventing the loss of labile, mobile or volatile molecules. However, wrapping tissues inside aluminium foil, for example, can create too open a system, leading to loss of both labile and recalcitrant materials. We present a novel experimental procedure for maturing tissues under elevated pressure/temperature inside compacted sediment. In this procedure, porous sediment allows maturation breakdown products to escape into the sediment and maturation chamber, while recalcitrant, immobile components are contained, more closely mimicking the natural conditions of fossilization. To test the efficacy of this procedure in simulating fossil diagenesis, we investigate the differential survival of melanosomes relative to proteinaceous tissues through maturation of fresh lizard body parts and feathers. Macro‐ and ultrastructures are then compared to fossils. Similar to many carbonaceous exceptional fossils, the resulting organic components are thin, dark films composed mainly of exposed melanosomes resting on the sediment in association with darkened bones. Keratinous, muscle, collagenous and adipose tissues appear to be lost. Such results are consistent with predictions derived from non‐sediment‐encased maturation experiments and our understanding of biomolecular stability. These experiments also suggest that organic preservation is largely driven by the original molecular composition of the tissue and the diagenetic stability of those molecules, rather than the tissue's decay resistance alone; this should be experimentally explored in the future.     

Decaying trees improve nesting opportunities for cavity‐nesting birds in temperate and boreal forests: A meta‐analysis and implications for retention forestry

Many studies have dealt with the habitat requirements of cavity‐nesting birds, but there is no meta‐analysis on the subject and individual study results remain vague or contradictory. We conducted a meta‐analysis to increase the available evidence for nest‐site selection of cavity‐nesting birds. Literature was searched in Web of Science and Google Scholar and included studies that provide data on the habitat requirements of cavity‐nesting birds in temperate and boreal forests of varying naturalness. To compare nest and non‐nest‐tree characteristics, the following data were collected from the literature: diameter at breast height (DBH) and its standard deviation (SD), sample size of trees with and without active nest, amount of nest and available trees described as dead or with a broken crown, and amount of nest and available trees that were lacking these characteristics. Further collected data included bird species nesting in the cavities and nest‐building type (nonexcavator/excavator), forest type (coniferous/deciduous/mixed), biome (temperate/boreal), and naturalness (managed/natural). From these data, three effect sizes were calculated that describe potential nest trees in terms of DBH, vital status (dead/alive), and crown status (broken/intact). These tree characteristics can be easily recognized by foresters. The results show that on average large‐diameter trees, dead trees, and trees with broken crowns were selected for nesting. The magnitude of this effect varied depending primarily on bird species and the explanatory variables forest type and naturalness. Biome had lowest influence (indicated by ΔAIC). We conclude that diameter at breast height, vitality, and crown status can be used as tree characteristics for the selection of trees that should be retained in selectively harvested forests.     

High‐resolution δ13Corg chemostratigraphy links the Decorah impact structure and Winneshiek Konservat‐Lagerstätte to the Darriwilian (Middle Ordovician) global peak influx of meteorites

The precise age of the Winneshiek Shale, a recently discovered Konservat‐Lagerstätte located in a very unusual depositional setting inside the Decorah impact structure, has remained uncertain in the absence of biostratigraphically highly diagnostic fossils. This chemostratigraphical study, based on δ¹³C_org data from 36 drill core samples through the shale, shows that the age ranges from the upper part of a small unnamed δ¹³C excursion in the Dw1 Stage Slice of the Darriwilian Global Stage to the lower part of the MDICE excursion in Stage Slice Dw2 of the same stage. This Dw1–Dw2 interval has an isotopic age of ~464–467 Ma. The gradational contact between the Winneshiek Shale and the underlying, rapidly deposited, impact breccia indicates minimal time difference between the impact event and the Winneshiek Shale. New age data show that the Decorah impact event was coeval with the early Darriwilian abnormally high influx of micrometeorites and meteorites recorded in sections in Baltoscandia, Russia and China and that the Decorah crater can be included among the unusually large number of meteorite craters formed during Middle and early Late Ordovician time. As is commonly the case in black shale deposits, the partly uniquely preserved Winneshiek Shale crater fauna is impoverished taxonomically and adds numerically relatively little to the conspicuous and much discussed Darriwilian global biodiversification increase.