The Evolutionary Significance of Cambrian Ecdysozoan Trace Fossils

Home , Cruziana, Graham Budd, Kouphichnium, Monomorphichnus, Priapulus caudatus, Rusophycus

Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1926

GIANNIS KESIDIS

ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6214 ISBN 978-91-513-0928-6 UPPSALA urn:nbn:se:uu:diva-407940 2020 Abstract Kesidis, G. 2020. The Evolutionary Significance of Cambrian Ecdysozoan Trace Fossils. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1926. 47 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-513-0928-6.

The origin of most of the animal phyla is tied to the Cambrian explosion, a rapid diversification event that took place from about 540 million years ago. This diversification is coupled with a great number of concurrent metazoan body plan innovations such as the development of the coelom, antagonistic muscles and a through-gut. While the body fossil record and molecular clocks document this apparent diversification, albeit with somewhat divergent results, there exists a third much more accurate record for the timing of life’s journey: the trace fossil record. The ecdysozoan trace fossil record first appears in the terminal Ediacaran and extends into the Cambrian. It exhibits a similar pattern of diversification to the body fossil record, pointing to a rapid ethological expansion through this interval. Here, I investigate particular ethologies of early Cambrian ecdysozoan trace fossils and frame the corresponding trace fossil morphologies in an evolutionary context. The first part of the thesis includes observations on the Cambrian representatives of the ichnogenera Cruziana and Rusophycus. I identify the links between the two morphologies and suggest that some Cambrian Cruziana are formed by the concatenation of distinct Rusophycus. This organisation might be more prevalent than previously expected in the Palaeozoic. This study is further supplemented by 3D virtual ichnology and the production of false colour depth maps produced for the first time for invertebrate trace fossils. With virtual ichnological techniques, subtle morphological characters can be readily observed and enhance the analysis of specimens. Investigating the early Cambrian ecdysozoan fossil record, I analysed Cambrian treptichnid trace fossils with cast-like impressions of their makers that can allow the assignment of their producers to at least stem-ecdysozoans. Actualistic experiments show that extant Priapulus caudatus produce similar trace fossils and therefore priapulid-like stem ecdysozoan producers are to be expected for the treptichnid burrows appearing at the Ediacaran- Cambrian GSSP. Although Rusophycus is the first trace fossil that can be firmly attributed to euarthropods, the simple ridge pattern of Monomorphichnus that appears even earlier than Rusophycus is a potential arthropod produced trace fossil. I investigate the morphologies of the earliest Monomorphichnus and address the problems with assigning these simple trace fossils to euarthropods. I also discuss the possibility that a part of its known record might be best described as tool marks rather than trace fossils.

Keywords: Cambrian, trace fossil, Cruziana, Rusophycus, Treptichnus, Ecdysozoa

Giannis Kesidis, Department of Earth Sciences, Palaeobiology, Villav. 16, Uppsala University, SE-75236 Uppsala, Sweden.

ISSN 1651-6214 ISBN 978-91-513-0928-6 urn:nbn:se:uu:diva-407940 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-407940)

To my family all over the world and most of all to my mom

List of Papers

This thesis is based on the following papers, which are referred to in the text by their Roman numerals.

I Kesidis, G., Budd, G. E. and Jensen, S., 2019. An intermittent mode of formation for the trace fossil Cruziana as a serial repetition of Rusophycus: the case of Cruziana tenella (Linnarsson 1871). Lethaia, 52(1):133–148 II Kesidis, G., Slater, B. J., Jensen, S. and Budd, G. E., 2019. Caught in the act: priapulid burrowers in early Cambrian substrates. Proceedings of the Royal Society B, 286(1894), 20182505. III Kesidis, G. and Belvedere, M., 2020 Application of 3D photogrammetry to invertebrate trace fossils: achievements and future developments. Manuscript submitted to Palaeontologia Elec- tronica. IV Kesidis, G., Budd, G. E. and Jensen, S., 2020. Monomorphichnus and the first appearance of euarthropods. Manuscript submitted to Palaeontology.

Reprints were made with permission from the respective publishers.

Statement of authorship

Paper I: G.K. and S.J. Collected material, G.K. conducted the analyses, in- terpreted the results and authored the manuscript with input from S.J. and G.B.

Paper II: G.K. and S.J. conducted neoichnological experiments. G.K. and B.J.S. authored the manuscript with input from S.J. and G.B.

Paper III: G.K. and M.B. produced the 3D models, M.B. produced figures with input from G.K. and G.K. authored the manuscript with input from M.B.

Paper IV: G.K., S.J and G.B authored the manuscript.

Contents

Introduction ...... 11 Research aims of this thesis ...... 13 The science of ichnology ...... 15 Trace fossils – key concepts ...... 18 Trace fossils of the Cambrian Radiation ...... 20 The evidence for the Cambrian Radiation ...... 20 Trace fossils as a record of ecological revolutions ...... 23 Establishment of the seafloor mixed layer – The effect of bioturbation ...... 23 Ecdysozoan evolution, insights from trace fossils ...... 25 Lower Cambrian (total-group) ecdysozoan trace fossils ...... 25 Trace fossils and the first appearance of arthropods ...... 26 Behavioural innovations of Cruziana producers ...... 27 Advances in ichnological research ...... 30 Neoichnology ...... 30 Virtual Ichnology ...... 33 Accomplishments and Future Directions ...... 35 Svensk Sammanfattning ...... 37 Acknowledgments...... 40 References ...... 41

Abbreviations

MA Million Years Ago MSM Mickwitzia Sandstone Member ECR Ediacaran – Cambrian Radiation GSSP Global Boundary Stratotype Section and Point GIS Global Imaging System FAD First Appearance Datum

Introduction

Man has always been fascinated by nature. We have time and again attempted to study, categorize and understand every aspect of the natural world of which we form a part. Animal diversity has been of particular interest throughout the ages. Our concerted efforts became for the first time a science with Carl Von Linné’s “Systema Naturae” (Linnaeus, 1758) that made binomial classification the system by which all life can be put into a comprehensive, ordered system. Classification of organisms in hierarchical structures from Species and Genera to Phyla and Kingdoms is based on the identification of characters that distinguish organisms. While the extensive study of extant organisms of- fers a wealth of information regarding current ecosystem composition and diversity, it does not provide a corresponding understanding of the early processes and mechanisms that led to the great variety of forms that we observe today. One of the most important events in the diversification of animal life occurred during the interval between 600-500Ma, specifically from c. 540Ma onwards it has been dubbed the “Cambrian explosion” (reviewed in e.g. Mar- shall, 2006; Wood et al., 2019). The “Cambrian explosion”, or Cambrian radiation, was not only the period of metazoan clade diversification but also the period in which the ecosystem structure of the Phanerozoic was established (Brasier et al., 1994; Erwin et al., 2011; Erwin and Tweedt, 2012; Mángano and Buatois, 2016). To answer the most fundamental questions about how metazoan diversity originated and how it took shape during its early evolutionary stages, palaeontologists have investigated the extensive animal fossil. While the study of body fossils provides a considerable amount of information about the organization of early animal body plans and the emergence of stem and crown groups, it rarely presents an accurate representation of their ethological evolution. Adding to this caveat, the most crucial time interval above the Precam- brian – Cambrian boundary (541-520 Ma) is distinctly lacking in body fossils of motile metazoans (Budd and Jensen, 2000; Budd, 2003). With the first appearance of unequivocal ecdysozoan body fossils (in the form of trilobites) at approximately 521 Ma (Daley et al., 2018) the question arises as to what occurred in the 40 Ma gap in the body fossil record from the terminal Ediacaran to Cambrian Series 2. It is therefore the study of the behaviours employed by these early animals, preserved as trace fossils that provides insights for this critically important period of life on earth. The aim of

11 this thesis, then, is to evaluate the evolutionary significance of early Cambrian trace fossils for the ecdysozoan clade, both in terms of their mode of formation as well as a reassessment of their morphology.

12 Research aims of this thesis

The importance of studying trace fossils, especially at time intervals of significant evolutionary upheaval such as the Ediacaran-Cambrian transition and the early Cambrian, is well founded (e.g. Jensen, 2003; Mángano and Buatois, 2016). The scope of this thesis is to investigate and reanalyze enigmatic Cam- brian trace fossils attributable to the wider ecdysozoan group. I reinterpret the mode of formation and implications for the behavioural innovations taking place within this critical time interval for the ecdysozoans and their stem group using novel methodologies. This topic has been approached through the following research projects: • Examination of lower Palaeozoic Cruziana to interpret its mode of formation and consequently infer potential evolutionary progression of the formation of Cruziana throughout the Palaeozoic. This question has been addressed in Paper I via a reinterpretation of the formation of Cruziana tenella as a serial repetition of distinct Rus- ophycus eutendorfensis using observations on the material and associated statistical analysis. Results were further corroborated in Paper III through the utilization of 3D models of trace fossils and the production of false colour depth maps that illustrate the segmental nature of lower Palaeozoic Cruziana. • Investigation of distinctly ecdysozoan-produced early Cambrian trace fossils from the Mickwitzia Sandstone Member, Västergöt- land, Sweden. The trace fossils presented in Paper II have a range of morphological characters that can robustly assign their makers to at least stem-ecdysozoans. These findings, coupled with actualistic experiments, support a priapulid-like stem ecdysozoan for similar burrows appearing shortly above the Ediacaran-Cambrian GSSP. • In order to better understand the morphology and mode of formation of Cruziana and the intergrading relationship with Ruso- phycus I employed 3D ichnology techniques for the first time in invertebrate trace fossils. In Paper III, we introduce these techniques, explore their applicability and reassess the morphology of Cruziana using this novel approach.

13 • Reexamination of the formation and nature of the ichnogenus Mon- omorphichnus in Paper IV. Monomorphichnus is generally attributed to arthropods and with an appearance already at the base of the Cambrian potentially provides the earliest record of euar- thropds. In this paper we explore the many problems involved in the interpretation of such a morphologically simple trace fossil.

14 The science of ichnology

Ichnology is the study of the behaviour of organisms through the traces, burrows and trails they leave behind as a record of their activities (Buatois and Mángano, 2011). Ichnology can be subdivided into two subdisciplines; palaeoichnology, which is the study of fossilized aspects of the behaviour of extinct animals (i.e. trace fossils), and neoichnology, which is the study of con- temporary traces. Palaeontologists have studied the fossilized remains of extinct life forms for hundreds of years, but a similar attention to trace fossils, i.e. the fossilized aspects of the behaviour of extinct animals, was achieved at a much later point in time. While throughout the history of our own species we became accustomed to the tracks and traces of animals, we were quite late to approach the subject of ichnology scientifically, with the first mention of ichnology appearing in the works of William Buckland and the first comprehensive work including the term “Ichnology” (Hitchcock, 1858) emerging during the latter half of the 19th century. Unsurprisingly, owing to the enigmatic nature of trace fossils and the apparent morphological similarity to repetitive patterns, early trace fossil workers often misidentified the material as the fossilized remains of plants (for example, the fucoids in Murchison, 1847); indeed many early “trace fossil” workers were botanists such as Adolphe Brogniart (1801-1876). A significant number of ichnotaxa, still valid today, bear names resembling plant species (e.g. Zoophycos and Rusophycus; for further examples see Osgood, 1970) but the time of the fucoids ended with Nathorst’s (1881) seminal work and the complete disassociation of trace fossils from plant remains. The study of trace fossils experienced a revival following the introduction of the concept of ichnofacies (Seilacher, 1953, 1955; 1967; Bromley, 1996; Baucon et al., 2012). Seilacher (1967) introduced the assemblage-level study of trace fossils throughout the Phanerozoic to allow for the interpretation of the palaeonvironmental conditions at the time of their formation. The ichnofacies concept rapidly took hold of the ichnological world and for the first time the focus of trace fossil research became the ethology represented and the taphonomic processes permitting trace fossil preservation. Ichnology as a science finds itself at the intersection of the fields of palaeontology, sedimentology and biology. It provides, therefore, a unique means of approaching questions regarding animal ecology, ethology and evolution by synthesizing and advancing distinct sources of information (McIlroy, 2008). The study of trace fossils often provides considerable insights to a degree unattainable via body

15 fossils with regards to these fields. Ichnology has wider applications in geology as well as further applicability in the commercial sector for petroleum exploration. Bioturbators, organisms that churn the sediment, have a profound effect as environmental engineers (Mángano and Buatois, 2014). Assemblage level ichnological studies assist in determining the palaeoenvironment and sedimentary properties at the time of their formation (Knaust, 2012) thus en- abling the identification of likely reservoir candidates (Gingras et al., 2007; Knaust, 2017). Trace fossils are in essence, fossilized snapshots of behaviour. They record the interaction between an organism and the environment in which it acted (Minter, 2007). It is this interaction between an organism and the substrate that influences the morphology of trace fossils (Bertling et al., 2006). The resulting trace fossil morphology and the preservation potential it has are closely dependent on both the morphology of the organism and the depositional environment (in terms of sediment grain size, consolidation and energy levels). The wide morphological variability of (mainly) invertebrate trace fossils and the distinctly rare occurrence of trace fossil producers in situ alongside their associated trace fossils present a challenge to working with trace fossils. In a way, the lack of body fossils from trace fossil rich outcrops is to be expected, because of the general prevalence of trace fossils in porous sandstones that preclude the preservation of body fossils (Baldwin, 1977; Seilacher, 2007). Only rarely do we have examples of concurrent preservation of trace fossil with their putative producer, as is the case for the trilobite Flexicalymeni meeki and the trace fossil Cruziana semiplicata (Fortey and Seilacher 1997; Mángano et al., 2020) or the preservation of the “death march” of Mesolimulus walchi (Fig. 1) in the Solnhofen Konservat-Lagerstätte (Lomax and Racay, 2012). Nevertheless, such associations are rare, and while informative for the specific ichnotaxon – taxon genetic linkage, an ethological classification of trace fossils is preferred over attempts at identifying trace fossils with particular producers. While this is a basic tenet of ichnological research (Seilacher, 2007; Buatois and Mángano, 2011), I argue that for select cases, the morphology (Paper II) and a more precise reinterpretation of the represented behaviour (Paper I) of key trace fossil specimens can be informative, both for the purpose of inferring the morphology of their putative maker and also for ena- bling wider evolutionary inferences for, in the case of this thesis, the associated ecdysozoan clade.

Figure 1. The trace fossil Kouphichnium isp with the associated producer Mesolimu- lus walchi at its end. This type of preservation is rare. The example is provided from, the Solnhofen Konservat – Lagerstätte. Wikimedia commons.

17 Trace fossils – key concepts

Trace fossils include a wide array of biologically produced sedimentary structures preserved in the substrate. They are the result of an organism’s life activity (Bertling et al., 2006). As organisms tend to respond similarly to environmental conditions, they tend to produce corresponding trace fossil morphologies which can be systematically grouped into distinct ichnogenera (Bromley, 1996; McIlroy, 2004). Minor differences in morphology within an ichnogenus can adequately subdivide them in distinct ichnospecies. Trace fossils are ubiquitous throughout the sedimentological record, owing to the fact that a single trace maker can produce a great number of trace fossils in its lifetime and multiple producers can create similar trace fossil morphologies in similar environmental conditions. This also gives trace fossils expansive temporal ranges. Trace fossils are, therefore, in general poor time markers (Seilacher, 1970). An advantage trace fossils have over body fossils, however, is that they are almost always found in situ in the sediment that they were formed in (Seilacher, 1967). This eradicates any effect of sediment reworking giving a significant advantage for biostratigraphy and palaeoenvironmental analysis. Trace fossils can be used in conjuction with the traditional stratigraphic methodologies through microfossils and body fossils to at least supplement bio- stratigraphic inferences. Dating of poorly fossiliferous strata can sometimes be supported by the introduction of trace fossil stratigraphical schemes. An example of this application can be seen in the erection of a stratigraphical scheme of the Cambrian-Ordovician successions of Gondwana via identification of the distinct ornament of Cruziana (Crimes, 1969; Crimes and Marcos, 1976; Seilacher, 1970). As a body fossil example, one might consider the trilobites (Babcock et al., 2017), which have proved a valuable tool for the correlation of Palaeozoic sequences mainly owing to their variability of form and distinct separation into readily identifiable morphological taxa. The corresponding application of ichnology to biostratigraphy would by analogy thus be largely dependent on the correct assignment of trace fossils specimens to distinct ichnotaxa, some- thing that has challenged ichnologists over the past decades. While the focus of the present thesis is not on ichnospecific characterization per se, I introduce new techniques (Paper III) to the of study invertebrate trace fossils, the suc- cessful application of which have implications for the way we approach and interpret the morphology of trace fossils.

18 Stratigraphically useful trace fossils should therefore bear a significant amount of morphological detail. As mentioned above, the trace fossils Cruzi- ana have been used to erect a stratigraphic scheme for Gondwana (Fig. 2) precisely because they exhibit a wide array of distinct morphologies throughout the Palaeozoic in the form of a variety of arrangements and alignments of ridges on the parallel lobes, pleural spine imprints and occasional cephalic impressions. Such trace fossils exemplify the wide applicability of trace fossils for the correlation of unfossiliferous rock units but also enable us to study the record of major evolutionary changes such as the evolution of predation and the effect of bioturbation from the Cambrian onwards and the manner in which this has been paramount in ecosystem engineering.

Figure 2. Gondwanan Cruziana stratigraphy. Figure recreated from Seilacher, 2007

19 Trace fossils of the Cambrian Radiation

The evidence for the Cambrian Radiation The Cambrian Radiation is the rapid radiation of metazoan clades into most extant phyla (Conway Morris, 1989, 1998; Knoll and Carroll 1999; Budd and Jensen 2000). The evidence for the early evolution of animals first appears at the onset of metazoan diversification before the beginning of the Cambrian with the still somewhat enigmatic Ediacara Biota (Narbonne, 2005; Budd and Jensen, 2017). The early diversification of metazoans is followed by the appearance of the first biomineralizing organisms (Murdock and Donoghue, 2011; Wood, 2018) with increased preservation potential and their resulting body fossil record that forms a major part of the Phanerozoic fossil record (Valentine, 2002). A number of hypotheses attempting to define the causes of the Cambrian Radiation exist and fall in three main categories: ecological, genetic and environmental. It is now widely accepted that no singular trigger would suffice to explain the Cambrian explosion and a multifaceted approach is preferred (Smith and Harper, 2013). A window into early Cambrian animal diversity is opened by the relatively rare Konservat-Lagerstätten (e.g. Conway Morris, 1977; Briggs et al., 1994; Vannier and Martin, 2017). Soft-bodied organisms with otherwise low fossilization potential can be preserved in particularly high detail (e.g. Fig. 3) under the specific conditions that allow this type of preservation (Butterfield, 2003; Butterfield et al., 2007; Gaines et al., 2008, 2012). Unfortunately, Konservat- Lagerstätten are not only rare but appear to be missing during a critical time interval of the early radiation and evolution of metazoans (approximately 541- 520Ma) (Budd, 2003; Slater et al., 2018). More recently a wealth of new material in the form of Small Carbonaceous Fossils (SCF) has added a new line of evidence via the identification of cryptic soft bodied early Cambrian biotas (Smith et al., 2015; Slater et al., 2017, 2018) by way of scalids and teeth corresponding to those found in the exceptionally preserved faunas of the later appearing Konservat-Lagerstätten.

Figure 3. A specimen of Ottoia prolifica (NMNH 57622) from the Burgess Shale Cambrian Series 3, Stage 5, Fossil Ridge, British Columbia. The exceptional preservation of soft bodied organisms is characteristic of Konservat-Lagerstätten. Speci- men illustrated in Smith et al. 2015.

A further line of evidence, and a relatively understudied one, can be found in the extensive trace fossil record of early metazoans (Jensen, 2003; Mángano and Buatois, 2016). The bilaterian trace fossil record commences after 560 Ma and increases in complexity throughout the Cambrian (Martin et al., 2000; Droser et al., 2002). The first metazoans were likely non-or poorly mineralized organisms and therefore their trace fossil record is of particular significance when discussing the emergence of animal clades at the Ediacaran-Cambrian

21 transition (Jensen et al., 2005; for a claim that it is possible to identify an early producer, see Evans et al. 2020). As discussed earlier, the trace fossil record is much less affected by taphonomic biases compared to biomineralized animal remains. The nature and timing of the Cambrian explosion has been a subject of debate with two opposing views, the first taking into consideration the fossil record of the Bilateria as evidence for a “real” Cambrian explosion (Budd and Jensen 2000; Budd, 2008; c.f. Budd and Mann, 2020) and the second, based on molecular clocks (Wray et al., 1996; Dos Reis et al., 2015; Cunningham et al., 2017) arguing for much deeper origins and considering lack of body fossils as a taphonomical artefact of preservation (Fortey et al., 1996; Sperling and Stockey 2018). Molecular clock data appear relatively inconsistent with their predictions for the divergence point of the Bilateria but more recent studies support the existence of a rapid diversification in the Cambrian (Peterson et al., 2004; 2008). Even so, the most recent efforts suggest an important gap remains between the apparent fossil record and the most conservative molecular clock estimates (e.g. Dos Reis et al., 2015); even though it is possible that this gap could be closed if certain statistical features of molecular clock techniques are taken into account (Budd and Mann, 2019) The trace fossil record of the Bilateria from the terminal Ediacaran to the middle early Cambrian (Stage 2, when a more diverse record of body fossils appear) lends support to the argument that the fossil record represents the actual course of evolutionary events (Budd and Jensen, 2000). The trace fossil record supplements the apparent gap in fossilization at this interval providing an ‘independent line of evidence’ (Mángano and Buatois, 2014) for the calibration of the Cambrian explosion. The trace fossil record of the bilaterians extends into the Ediacaran (ca 560 Ma) with representatives being simple sediment – water interface trace fossils (Jensen, 2003, Jensen et al., 2005) that nevertheless record the ‘widening behavioural repertoire’ (Conway Morris, 1987) of their producers towards the Cambrian. Metazoan clades exhibit a host of body plan innovations such as the development of the coelom that serves as a preadaptation to the then novel burrowing behaviour of early bioturbators (Budd and Jensen 2000, 2017). While the significance of key innovations such as the development of the coelom and burrowing are generally not disputed, recent modeling approaches to investigating the Cambrian radiation suggest that the existence of large clades in fact necessitates an early burst of diversification. Thus high initial diversification rates of extant clades need not necessarily indicate any biological privilege of the group, but rather exist as necessary statistical artifacts (Budd and Mann, 2018; 2020). Nevertheless, the rapid expansion of morphological, behavioural and ecological diversity and complexity in this period remains a point of fas- cination and genuine, albeit challenging, scientific inquiry.

22 The fate of the Ediacara Biota is not as clearly defined. Lately support has been presented for the biotic replacement hypothesis, and the increase in bioturbation at the Ediacaran-Cambrian boundary suggests a direct link between ecosystem engineering and the decline of the Ediacara biota (Cribb et al., 2019) but it is also known that bioturbators are likely to have coexisted with Ediacaran organisms (Jensen, 2003, Seilacher et al., 2005, Jensen et al., 2006, Mángano and Buatois, 2014) since approximately 560Ma. That indicates that the interrelationship between Ediacaran organisms and early metazoan might have been more complex or even beneficial for early metazoans (Budd and Jensen, 2017). In addition, recent modelling of stem and crown groups suggests that the rapid disappearance of stem groups after their respective crown group has emerged is to be expected as a null-hypothesis of random diversification (Budd and Mann 2020).

Trace fossils as a record of ecological revolutions

Establishment of the seafloor mixed layer – The effect of bioturbation The relatively serene benthic ecological landscape of the Ediacaran allowed for the formation of a number of somewhat simple trace fossils. Ediacaran trace fossils are typically horizontal, unbranched trails that were emplaced at or near the sediment-water interface (Jensen, 2003). In the Cambrian, concur- rently with the documented expansion of metazoan phyla, an increase in deeper tier exploitation of the sediment and in the complexity of burrow morphologies can be observed (Mángano and Buatois, 2017). Here we see for the first time branching trace fossils and a drastic increase in the diversity and size of burrows and trails, and the depth to which they enter the seafloor. The significance of trace fossils in documenting this paradigm shift in behavioural complexity and related evolution of derived morphologies has been shown, by the increase in complexity of trace fossils across the Ediacaran-Cambrian boundary (Seilacher, 1956; Jensen, 2003). A concerted worldwide investigation of boundary sections leads to the observation that groups of trace fossils appear relatively consistently in sequential order. This has led to the erection of trace fossil zones (Crimes, 1987, 1992; Crimes and Fedonkin, 1994; Nar- bonne et al., 1987) with a (relatively) consistent worldwide first order of appearance. The appearance of metazoan clades close to the Ediacaran-Cambrian boundary transformed earth systems, global geochemical cycles and ecology (Bottjer et al., 2000; Butterfield, 2007; Budd and Jensen, 2017). Foremost among these transformations, is the effect of sediment churning bilaterians on the relatively stagnant benthic sediments of the terminal Proterozoic

23 (Mángano and Buatois, 2017). Modern oceanic seafloors exhibit a character- istically fluidized homogeneous upper layer of sediment that extends up to 10cm downwards from the sediment-water interface (Rhoads and Young, 1970; Thayer, 1979, 1983). The biogenic reworking (bioturbation) of sediment is the process that culminates in the upper mixed layer as seen in modern benthic environments as well as the majority of Phanerozoic sequences (Bromley and Ekdale, 1986; Teal et al., 2008, 2010). The process of sediment mixing appears to be a protracted process throughout the Palaeozoic towards the Silurian which indicates that the associated increase in bioturbation is likely attributable to behavioural innovation rather than ecological drivers (Tarhan et al., 2014). Nevertheless, recent studies on the Burin Peninsula, Chapel Island Formation indicate that the establishment of the mixed layer might have occurred in the early Cambrian (529Ma) (Gougeon et al., 2019) The introduction, therefore, of bioturbators regardless of the exact timing of the process, had a drastic effect on the establishment of modern seafloor geochemical properties and the evolution of associated behaviours is a significant aspect of the Palaeozoic metazoan radiation.

24 Ecdysozoan evolution, insights from trace fossils

Lower Cambrian (total-group) ecdysozoan trace fossils The widespread preservation of trace fossils in poorly fossiliferous strata has significance for studies pertaining to the early evolutionary diversification of metazoans in the Cambrian. A number of trace fossils attributable to at least total-group ecdysozoans appear well before the first appearance of their sclerotized or, for soft bodied organisms, exceptionally preserved putative producers (Budd and Jensen, 1998; Daley et al., 2018). Arguably, some poorly sclerotized stem ecdysozoans would have been able to produce trace fossils comparable to those of the crown group and even illuminate potential symple- siomorphies shared within the ecdysozoan clade (i.e. between the (stem) Ar- thropoda-Cycloneuralia). Given that key innovations of the bilaterian body plan are likely to have accrued in relatively large benthic organisms (Budd and Jensen 2000), the corresponding trace fossil record of the early Cambrian demands attention. The first appearance of coelomate animals in the fossil record can only be gauged by their trace fossil record with trace fossils indic- ative of sediment exploitation first being reported from the terminal Ediacaran (Jensen, 2006; but see Evans et al. 2020). The base of the Cambrian is marked by the appearance of large, branching probing burrows of the trace fossil Treptichnus pedum (Droser et al., 1999). The first appearance of Treptichnus pedum in the Chapel Island Formation, Burin Peninsula, Newfoundland is used to mark the Global Boundary Strato- type Section and Point (GSSP) for the Cambrian (Narbonne et al, 1987). While a tentative association of treptichnids with priapulid-like scalidophorans has been previously suggested (Dzik, 2005; Vannier et al., 2010) robust evidence for the association where lacking until now. In Paper II I present unequivocal anatomical evidence preserved on trace fossils (Fig. 4) of the Mickwitzia Sandstone Member, Sweden that set apart such morphologies as product of at least stem-scalidophoran origin. Given the morphological similarity of treptichnids and their deep first appearance it is likely that scalidophoran or stem ecdysozoans have their origin in the terminal Ediacaran.

Figure 4. Trace fossil of a priapulan origin, the anterior of the trace fossil captures in cast-like accuracy the anterior morphology of a scalidophoran vermiform organism. Scale bar 2mm.

Trace fossils and the first appearance of arthropods Unequivocal evidence for the appearance of total group euarthropods in the fossil record comes from the earliest trilobites at ca. 521 Ma (Maloof et al., 2010 and references therein). Apart from the trilobites, the majority of Cam- brian representatives of stem and crown group euarthropods are derived from the productive but rare Konservat-Lagerstätten sites such as Chengjiang (Zhang et al., 2008), Sirius Passet (Harper et al., 2019) and the Burgess Shale (Whittington, 1979). While the terminal Ediacaran witnessed the first appearance of stem-ecdysozoans, the first appearance of euarthropods cannot be confidently placed below the first appearance of the unequivocally arthropod produced Ruso- phycus (between 530-535Ma (Jensen et al., 2013)). The appearance of Ruso- phycus well below the first appearance of trilobites in several early Cambrian outcrops around the world including Newfoundland, Spain and Siberia, signi- fies that the appearance of the euarthropods precedes trilobites by a considerable time interval, assuming the absence of a cryptic trilobite record (Paterson et al., 2019). The earliest Rusophycus provide a conservative indicator for the

26 appearance of euarthropods as they exhibit bilateral symmetry and ridges/imprints that were the product of paired appendages (Crimes and Anderson, 1985) and have been use as a calibration for the appearance of the euarthropods (Daley et al., 2018). It is notable that these early representatives are un- usually large indicating that they were produced by a large benthic organism. Given that a putative producer has not been identified in the fossil record (e.g. a large “trilobite” existing approximately 10Ma before the reported first appearance of the clad), it is likely the producer was in fact not a mineralised arthropod but rather a member of the relatively poorly-scleritised stem group. However, researchers even suggested even earlier dates (i.e. below the FAD of Rusophycus) for the FAD of euarthropods based on the sparse and equivo- cal evidence of simple trace fossil morphologies reminiscent of arthropod limb activity that appear just above the Ediacaran-Cambrian boundary. One such example is the trace fossil Monomorphichnus, a set of simple ridges with apparent alignment. Monomorphichnus has been found just above the Ediacaran – Cambrian GSSP in Newfoundland (Narbonne et al. 1987; Laing et al. 2019), and has been associated with arthropod activity thus providing an even deeper but disputed origin for the euarthropods. In Paper IV I examine the earliest reported Monomorphichnus and associated purported morphologies with the intent to clarify which of these structures could indicate a euarthropod producer. It appears that while a number of early Cambrian Monomorphichnus morphologies can be attributed to arthropods it is debatable if they are life activities. Furthermore, several of the earliest Monomorphichnus are morphologically very simple ridges for which interpretations other than that of an eauarthropod must be considered. To assign these structures to (stem) arthropods would require at least a set of characters in the form of dactylic imprints to indicate an arthropod limb. .

Behavioural innovations of Cruziana producers This project also focused on arthropod produced trace fossils and specifically the iconic Cruziana and, Rusophycus. The two ichnogenera are closely related with a variety of almost indistinguishable intermediate forms and relatively confidently identifiable end members (Seilacher, 1953, 1970; Crimes, 1970). In common with most trace fossils, the two ichnogenera have a wide temporal range throughout the Palaeozoic (Seilacher, 2007) but can also exhibit characteristic “fingerprinting” and a range of distinct characters (Seilacher, 1970). The current consensus for the formation of Cruziana describes it as a continuously forming infaunal trace fossil (Seilacher, 1970). This mode of formation is examined in Paper I as well as recent publications (Sadlok, 2014). While the debate on the formation of Cruziana has mostly focused on the position of the organism in relation to the sediment (Crimes, 1970; Goldring, 1985; Seilacher,

27 1985) it is important to study the formation of the trace fossils as an indicator of the behavioural and anatomical capabilities of their producers. Given the relatively undifferentiated morphology of at least trilobite limbs and their biomechanics, a fully infaunal lifestyle for most trilobites is somewhat unlikely. Furthermore, some lower Palaeozoic Cruziana (Jensen, 1997) appear not to be formed continuously which might be an indication of different behavioural pattern of their makers as compared to younger ichnospecies. For example, Cruziana tenella is a small Cambrian trace fossil with two parallel lobes bearing transverse ridges at a wide angle. Its width varies but is generally below 5mm and length below 8cm as the trace fossil extends in a straight to sinusoidal path. Similarly to other Cruziana it can be found in close association with Rusophycus (here R. eutendorfensis). In Paper I I analyse the relationship between Rusophycus eutendorfensis and Cruziana tenella (Fig. 5), showing that the latter is formed as a serial concatenation of rusophycid elements owing to the oblique angles between individual segments revealing individual segments.

Figure 5. Cruziana tenella from the MSM, observe the undulations along the extent of the trace fossil corresponding to distinct rusophycid elements. Scale bar 5mm. Lugnås. RM X11033.

The behaviours inferred are a direct result of the organism’s capabilities in terms of muscle organization and locomotion. Through my findings in Paper I and with the support of the 3D models produced for Paper III (e.g. Fig. 6) it becomes apparent that at least some other lower Cambrian Cruziana apart from C. tenella appear segmental in comparison to their Ordovician counter- parts with frequent interruptions along their axis of propagation corresponding to rusophycid elements. This is an indication of behavioural evolution as sedimentary properties might have remained relatively consistent throughout the Palaeozoic (Tarhan, 2014).

Figure 6. A. Trace fossil Cruziana rusoformis of the MSM. B. Decoulorised 3D model of the specimen. C. 3D depth map of the specimen indicating differential depth of excavation at intervals of activity, illuminating the possible segmental nature of early Cambrian Cruziana

29 Advances in ichnological research

Neoichnology While palaeoichnology is focused on analysing behaviours recorded in the fossil record of extinct organisms through the study of the morphology of trace fossils, its counterpart neoichnology, focuses on the study of tracks, traces and burrows of extant organisms. A plethora of organisms can be used for this kind of study with a corresponding setup that monitors aspects of their behaviour such as speed, gait, alterations in direction and responses to environmental stimuli (e.g. Milàn, 2006). In common with palaeoichnology, two broad interest groups exist: one focused on invertebrate tracks and the other on invertebrate traces, burrows and borings. Arguably a great amount of interest has been given to vertebrate tracks and the mechanisms and sediment properties facilitating their preservation (Milàn, 2006; Genise et al., 2009; Kubo, 2010). This is likely an effect of the interest dinosaur research has received over the past decades from the general public and consequently from the funding bodies. Neoichnology provides considerable insight into the variability of trace fossils and therefore assists in ichnospecific characterization and the identification of intermediate morphologies (Minter et al. 2007). Considering this, it is becoming increasingly important to study experimentally produced behaviours under controlled laboratory conditions in order to better understand aspects of the mode of formation of trace fossils. Neoichnology serves to create analogous behavioural models for the interpretation of extinct animal behaviour and has resulted in numerous publications attempting to decode aspects of the behaviour of extinct animals through the study of close analogues (e.g. Genise et al., 2009; Curth et al., 2014). In- vertebrate neoichnology is experiencing renewed interest (Davis et al., 2007). There exist a number of studies focused on the locomotion of terrestrial arthropods (e.g. Manton, 1977; Davis et al., 2007) and an increasing interest in the study of marine invertebrate neoichnology (Dashtgard and Gingras, 2012). The study of invertebrate traces presents us with a drastically different con- ceptual model to vertebrate locomotion that alongside a diverse range of morphologies limits the depth of our understanding of invertebrate locomotion and general behaviour. Invertebrate biology encompasses a diverse range of modes of locomotion including basal organism locomotion facilitated by cili- ated epithelia or muscle contractions along the trunk of the organism and later

30 reaching a level of organization reminiscent to that of vertebrates but funda- mentally different for the arthropod clade. The lack of a strongly developed invertebrate-specific framework, I suggest, inhibits our investigations from reaching a similar degree of comprehensiveness of behavioural aspects of invertebrates comparable to that of vertebrates. As previously discussed, ichnology brings together aspects of sedimentology and ethology and interprets the causal influences for the morphology of invertebrate trace fossils. In a sense, a similar principle to Lyell’s uniformitar- ianism for geological processes can be observed in metazoan trace fossils. Throughout the Phanerozoic record organisms of widely divergent clades respond similarly to environmental factors (McIlroy, 2004), (sediment consistency, current energy, salinity fluctuations, intensity of sedimentation etc.) producing roughly corresponding burrow and trace morphologies. Neoichnology can be utilized to extrapolate the morphology of trace fossils of obscure trace makers by studying burrows or traces produced by extant animals alongside the morphology of the trace makers themselves. For this endeavor it is of great significance to establish extant analogues for explaining the behaviour and general anatomy of the trace producer and its ethological/neurological capabilities. A generalized experimental procedure for a study of marine invertebrates could be summarized as an artificial recreation of a seafloor of predetermined properties that simulate a desired environment of deposition. The study organism is released under the set laboratory conditions and allowed to interact with the substrate, going through the range of behaviours that are allowed to be recorded by the setup. After completion of the observations, the morphology of the traces or burrows can be recorded and studied (e.g. Vannier et al., 2010). As I show in the case of Cambrian basal ecdysozoan burrows investigated on Paper II, we analyzed the morphology and behaviour of extant priapulids (Priapulus caudatus) (Fig. 7) in order to associate the body plan of a putative early Cambrian vermiform stem group scalidophoran with the resulting trace fossil from the Cambrian locality of the Mickwitzia Sandstone Member. We were thus able to narrow down the maker of the Cambrian trace fossil through the study of the behaviour and morphology of living Priapulus caudatus in a laboratory setting.

Figure 7. Experimental production of burrows of Priapulus caudatus. The experimental setup requires an aquarium with a plastic divider partitioning a side of the aquarium to be filled with sediment. The organism is then allowed to burrow and recorded in real time to study its behavioural pattern.

32 Virtual Ichnology

3D Photogrammetry Novel imaging techniques – applications on invertebrate traces

This project also aimed to further develop methodologies to better and faster investigate the morphology of my study material as well as illuminate obscure aspects of morphology that could aid our understanding of the mode of formation for these trace fossils. This endeavor would enable a better ethological characterization for trace fossils that frequently intergrade to composites and also to further be able to identify intermediate forms. As mentioned above, the trace fossils at the core of the present thesis, Cruziana and Rusophycus exhibit a great amount of variability and their interrelationships are unclear. While end members of the two ichnogenera can relatively confidently be ascribed to distinct ichnogenera, the great variability of intermediate morphologies com- plicates identification. A further problem is that we do not have a robust understanding of the way these trace fossils were originally formed and the possible linkage between the two ichnogenera. 3D photogrammetry as applied for the first time in this type of material (Paper III) highlights small morphological variations that aid in the identification of characters significant for the ethological characterization of these ichnospecies. The minute features and low relief of Cruziana tenella poses a significant obstacle to the imaging, ethological interpretation and dissemination of observations. Cruziana tenella has already been recognized as a good candidate for alternative imaging techniques that greatly enhance resolution of individual specimens and the morphology associated with these minute traces (Hammer et al., 2002). I aimed to eliminate artefacts of imaging in our analysis and I therefore utilized 3D photogrammetry protocols that have found applicability in the more standardized vertebrate ichnology. The advancements in digital imaging and the development of 3D object manipulation software have produced a new sub-discipline for ichnology focusing on the production and handling of virtual material known as digital ichnology. The discipline encompasses a wide range of techniques including laser scanning, close range photogrammetry and GIS to approach the study material from different perspectives. The aim is in general to create virtual models in 3D so as to be able to virtual manipulate the material and study aspects of the morphology in a non-destructive fashion in ways that would otherwise require at least partial destruction of the specimen. Digital ichnology has been, for a long time now, a commonly used tool in vertebrate ichnology. This was the incentive to apply for the first time these techniques to invertebrate trace fossils. In Paper III I apply digital ichnology techniques (3D photogrammetric models, false-colour depth maps, contour-

33 lines and cross-sections) to specimens of Cambrian and Ordovician Cruziana and Rusophycus (Fig. 8). Digital models offer many advantages to palaeonto- logical research that are already known from vertebrate ichnology. These include digital manipulation of samples, virtual cross-sections and depth analysis of the material through depth maps. Importantly it allows the virtual preservation of material at risk of erosion or difficult to collect outcrops. The study undertaken here provides insights for the potential of digital ichnology for the interpretation of the behaviour represented in invertebrate trace fossils. The digital models allow a detailed investigation of the ornament as well as slight variations in depth along the axis of propagation of Cruziana. The ability to manipulate virtual trace fossils by creating depth maps of their relief, cut along planes that would require the destruction of the original and illustrate details that traditional imaging techniques fail to fully grasp makes this novel approach integral to the present study.

Figure 8. A. Trace fossil Cruziana tenella of the MSM. B. Decoulorised 3D model of the specimen. C. 3D depth map of the specimen with a colour gradient highlight- ing subtle morphological details such as the segmental character of the trace fossil and the distinct Rusophucus eutendorfensis elements along the axis of propagation of the trace fossils.

34 Accomplishments and Future Directions

These projects have provided novel insights pertaining to the formation of lower Palaeozoic ecdysozoan produced trace fossils. I have addressed the significance of behavioural innovation for metazoans and the need to push towards a better understanding of how the morphology of some of the most well- known trace fossils came about. I suggest that behavioural mechanisms gov- erning trace fossil formation should come under further scrutiny. Trace fossil research should regain focus on the ethological interpretation of trace fossil morphologies and not only be satisfied with ichnofacies and ichnofabric analysis but also attempt to analyse the evolutionary implications of the expansive record of trace fossil. For some arthropod produced trace fossils I have shown, through the study of key material from the trace fossil “Lagerstätte” of the Mickwitzia Sand- stone Member, Sweden (Paper I), that the association of Cruziana and Ruso- phycus, at least in the Cambrian, is much more intimately linked and does not only represent an ethological alternation of burrowing depth. These observations also suggest that these Cruziana are not solely a motion trail (i.e. repich- nion), but rather reflect significantly energy-intense digging activity for which the motivation was presumably resource acquisition for deposit feeders. With these findings as a foundation I believe that future investigation into the morphology of Cruziana will be beneficial in uncovering the nature of later appearing forms. Expanding a detailed study focused on the formation of Cruziana to Ordovician (and younger) representatives either will result in illuminating similar patterns to those observed for the early Cambrian material or set these younger ichnogenera apart. A number of hypotheses could be for- mulated as to why either might be the case, but in the case of a distinct mode of formation, ethological evolution in the arthropod clade would be the likely answer. Coupled with observations on the evolution of sediment properties throughout the Phanerozoic such findings will enable a better understanding of the evolutionary progression of behaviour of the earliest arthropod representatives in the fossil record. The uncertainties pertaining to the producers of the trace fossil record of the Ediacaran-Cambrian transition have been investigated in Paper II. With a combination of actualistic experiments and morphological observations of exceptionally preserved trace fossil of the MSM I present evidence tying ecdysozoan producers to treptichnids of this period. These observations corrob- orate a likely latest Ediacaran origin for the ecdysozoans.

35 I also introduced state-of-the-art imaging techniques that improve on the time required and resolution of surface detail for the study of invertebrate trace fossils (Paper III). 3D virtual palaeontology is rapidly picking up pace and is fast becoming a staple of both traditional palaeontology focused on body fossils and vertebrate trace fossils. While a standardized framework has been established for the above mentioned material, little was known until now regarding the applicability of these techniques on invertebrate trace fossils. The production of virtual 3D models of invertebrate trace fossils allows the non-destructive manipulation of the material and the creation of virtual cross sections that can have wide applicability for invertebrate trace fossil research. Similarly, depth maps of the surface area of trace fossils (as illustrated for Cruziana) can aid in the ethological interpretation of trace fossils and the assessment of subtle alterations in behavioural patterns recorded. Since the surface of the 3D model is recreated virtually it is possible to eradicate artefacts of imaging, which is particularly useful for heavily oxidized material, for which traditional imaging is insuffi- cient. With the applicability of these techniques now being proven for this material, I expect widespread utilization of 3D imaging for the study of invertebrate trace fossils as well as the virtual preservation and dissemination of material/samples. A caveat is the requirement for more standardized shape descriptors or landmarks to be able to further compare morphologies in an analogous way to that already developed for vertebrate trace fossils. This endeavor will require more time and effort to materialize. Lastly, in Paper IV I address the importance of the earliest putative trace fossil record for the euarthopods close to the Cambrian boundary and clarify- ing the significance of differentiating between the various morphologies of Monomorphichnus. Caution is advised for utilizing these simple morphologies to calibrate the appearance of the euarthropods. This study has implications for molecular clock calibration or other studies that require fossil data as the indicators for the first appearance of clades.

36 Svensk Sammanfattning

Ichnologi är vetenskapen som utforskar organismers beteende genom de spår såsom grävda tunnlar som bevaras som fossil i sedimentet. Denna avhandling berör så kallade spårfossil, just sådana avtryck av organismers aktiviteter i det fossila registret. Spårfossil är enkelt uttryckt fossiliserade spår av organismers beteende och rörelser. De fångar interaktionen mellan organismen och miljön inom vilken den befann sig. Ett spårfossils morfologi och form varierar mycket beroende på depositionsmiljön samt organismens beteende och dess morfologi. Ryggradslösa djurs spårfossil uppvisar precis detta slags variabilitet. En organism kan lämna efter sig flera olika slags spårfossil och en viss typ av- spårfossil kan produceras av fler än ett slags organism. För denna avhandling undersökte jag spårfossil från organismer i djurgruppen Ecdysozoa, dvs. spår- fossil skapade av leddjur samt deras närmaste masklika släktingar. Jag foku- serade på tidigkambriska spårfossil från Sverige bevarade i Mickwitzia- sandstenen i Västergötland. Mitt arbete komplementerades med material ut- anför Sverige för att bättre illustrera mina resultat. Materialet kommer nästan helt från lämningar från kambrium. Kambrium är en särskilt viktig geologisk period när det gäller evolutionens gång. Det var under denna tid (541-495 miljoner år sedan) som den största majoriteten av de distinkta djurgrupper som vi ser idag uppstod. Den kambriska perioden är förstås välkänd för detta och hundratals studier har publicerats på fossila läm- ningar av djur från denna tid. Mindre välkänt och än mindre förstått är att leddjurens tidigaste fossila lämningar är kända från ungefär 520 miljoner år gamla avlagringar vilket lämnar ett 10-20 miljoner års gap mellan början av kambrium och den första kända, relativt välutvecklade, morfologin hos ledd- djuren. Frågan som uppstår är vad som faktiskt skedde under denna tid? Svaret kan skönjas i spårfossilsregistret som är relativt kontinuerlig genom hela pa- leozoikum. Spårfossil bevarar alltså ett slags beteendesevolution, vilket möjliggör slut- ledning av den associerade morfologin hos dess skapare. Det följer rimligtvis att enkla hål skapades av masklika organismer medan mer komplexa spår skapades av organismer med bilateral symmetri, ben och ett bredare utbud av beteenden. Första delen av avhandlingen fokuserar på en omtolkning av beteendet hos de djur som skapade spårfossilen Cruziana och Rusophycus (Artikel I). Dessa spårfossil är välkända och högst variabla exempel på spårfossil skapade av

37 leddjur. Av stor vikt är att de uppvisar ett flertal karaktärer som tydligt visar på deras association med leddjur i form av bilateral symmetri, bland dem ris- por i sedimentet från ben samt avtryck av organismens ryggsköld. Omtolk- ningen av dessa spårfossil informerar både om morfologin hos deras skapare samt även mer generellt om leddjurens tidiga evolution. Det verkar som om de tidigaste Cruziana uppstår genom ett antal associerade sammanhängande Rusophycus medan de yngre formera är kontinuerliga. Detta indikerar en evolution i grävbeteendet hos de tidigare skaparna av dessa fossil och möjligtvis även skillnader i hur kompakt ytsediment var mellan tidig kambrium och se- nare kambrium samt ordovicium. Vissa spårfossil kan visa vilken slags organism som skapade dem. Detta gäller materialet i Artikel II vari spårfossil visar detaljerad avtryck av främre delen av en snabelsäckmask. Denna association gjorde det möjligt för mig att med stor säkerhet länka treptichnider, ett slags spårfossil, med denna djur- grupp. Detta är av stor betydelse eftersom treptichnida spårfossil återfinns precis vid början av kambrium vilket gör att vi kan konstatera att relativt stora djur med snabelsäcksmasksliknande morfologi fanns redan vid denna tid. Denna studie komplementerades med neoichnologiska experiment. Neoich- nologi syftar till att hitta analoga beteendemönster hos nulevande djur för att lära oss om beteendet hos utdöda djur. . I detta fallet lät vi snabelsäcksmasken Priapulus caudatus gräva gångar under laboratorieförhållanden för att kunna jämföra med ovannämnda spårfossil. De första ledjuren återfinns i det fossila registret vid ca 521 miljoner års ålder som de tidigaste trilobiterna. Majoriteten av fossilerna från kambriums stam- och krongrupper hittas i de rika men sällsynta konservat-lagerstätte. Rusophycus återfinns i långt äldre lager än de första trilobiterna i flertalet tidiga kambriska lokaliteter. De tidigaste Rusophycus förser oss med en relativt säker uppskattning äldreleddjuren då de uppvisar bilateral symmetri samt mönster som indikerar att de skapades av sammanparade ben. Ett annat slags spårfossil som antas höra ihop med leddjuren är Monomorphichnus. Det är ett relativt enkelt mönster av till synes sammanhängande skrapspår som återfinns intill gränsen mellan ediacara och kambrium och som potentiellt kan förse oss med information om ännu tidigare leddjur. I Artikel IV undersöker jag de tidigaste kända Monomorphichnus och associerade morfologier och strävar efter att klargöra vilka strukturer som eventuellt har sitt ursprung i leddjursbe- teende. Trots att ett flertal tidiga kambriska Monomorphichnusmorfologier kan länkas till leddjur är det oklart huruvida de faktiskt visar på beteenden. Dess- utom är många tidiga Monomorphichnus morfologiskt sett mycket enkla var- för andra organismer än leddjur eventuellt kan tänkas vara skapare. Avhandlingen inriktar sig också på att ytterligare utveckla metoder för att bättre kunna kvantifiera morfologin av mitt studiematerial, i synnerhet de aspekter av morfologin som skulle kunna förbättra vår förståelse för hur dessa spårfossil skapades. En sådan förståelse skulle förse oss med en bättre bild på

38 hur enskilda och sammanhängande spårfossil hör ihop samt identifiera mel- lanliggande former. För att åstadkomma detta använde jag mig av tredimens- ionell fotogrammetri - den första studien av sitt slag på spårfossils från rygg- radslöa djur (Artikel III). Metodologin upptäcker små morfologiska variat- ioner som kan användas för att informera oss om beteenden som ger upphov till dessa spårfossil. Virtuell ichnologi har vissa fördelar jämfört med mer trad- itionella metoder. Bland annat kan materialet undersökas icke-destruktivt genom att skapa digitala tredimensionella modeller. Virtuella tvärsnitt och yt- kartläggningar har med stor sannolikhet stort potential vad rör undersökningen av leddjurens spårfossillämningar. I mitt arbete med dessa metoder var fokus på ytkartläggningar av spårfossilen (illustrerades med Cruziana) och dessa gav användbar information vad rör slutledningen av vilka beteenden som gav upphov till dessa lämningar. Sammanlagt har dessa projekt resulterat i nya insikter vad rör evolutionen av beteenden hos de tidiga leddjuren samt deras efterlämnade spårfossilmor- fologier. Jag har kartlagt betydelsen av beteendesevolution för djur generellt och understrukit vikten av forskning om de mest välkända spårfossilen. Jag vidhåller att fortsatt undersökning bör riktas mot mekanismerna som ger upphov till spårfossil. Därigenom kan evolutionära mönster och implikationer skönjas.

39 Acknowledgments

This work was funded by the Marie Curie ITN ‘NEPTUNE’ grant (no. 317172), under FP7 of the European Commission. This was an opportunity to work with a fantastic network of extremely motivated researchers around the world. Throughout my time working on this thesis, a great number of people played a significant role for achieving its completion. First and foremost I want to thank my supervisors, Graham Budd and Sören Jensen for their assis- tance and support throughout all stages of manuscript writing and publication and for putting up with a few more than expected “delays”. Graham has not only been a constant support but also a good friend alongside whom I learned so much. Sören Jensen has always responded with kindness and thoughtful- ness to any and all of my questions. Ralf Jansen was exceptional at motivating me and others with his continuously highly energetic demeanor. The Palaeobiology group of Uppsala University, Geocentrum has been one of the best groups of colleagues to work, share a fika and talk with scientifically or otherwise. I wish to thank Jorintje Hendricks for her pep talks, Mi- chael Streng for sharing his knowledge of Swedish stratigraphic peculiarities and Malgorzata Moczydlowska-Vidal for taking care of all PhD students and tracking our progress. Ben Slater has always been around throughout the writing process and came up with exciting new ideas to work on together. To- gether with Illiam Jackson and Tom Claybourn, they are what made my time in Uppsala particularly enjoyable. Sharing an office with Illiam and Tom has given rise to many debates topical or not and has never been boring. Boris Karatsolis made coming to work feel like going back to Greece and gave a new, fresh feeling to the workplace. This list could go on for pages, but in short I want to thank all my colleagues, Sebastian Willman, John Peel, Aodhan Buttler, Emma Arvestål and all the younger additions to the group in the past couple of years for providing one of the most productive and joyful environments to work in. Fatima Ryttare-Okorie has always been there to lend her support on all matters administrative and took on all problems we brought to her with a smile, and for that I am grateful. My family has been incredibly important for the completion of this thesis, my mother Sossana and brother Alexandros have been by my side for the past two years and without them I probably would have had to have made some radical changes in my plans. Thank you.

40 References

Babcock, L.E., Peng, S. & Ahlberg, P., 2017. Cambrian trilobite biostratigraphy and its role in developing an integrated history of the E arth system. Lethaia, 50, pp.381–399. Baldwin, C. T. 1977. Rusophycus morgati: An asaphid produced trace fossil from the Cambro-Ordovician of Brittany and northwest Spain, Journal of Paleontology, 411–413. Baucon, A., Bordy, E., Brustur, T., Buatois, L.A., Cunningham, T., De, C., Duffin, C., Felletti, F., Gaillard, C., Hu, B. and Hu, L., 2012. A history of ideas in ichnology. In Developments in Sedimentology. 64, 3–43. Elsevier. Bertling, M., Braddy, S.J., Bromley, R.G., Demathieu, G.R., Genise, J., Mikuláš, R., Nielsen, J.K., Nielsen, K.S., Rindsberg, A.K., Schlirf, M. & Uchman, A., 2006. Names for trace fossils: A uniform approach, Lethaia, 39, p. 265–286. doi: 10.1080/00241160600787890. Bottjer, D. J., Hagadorn, J. W. & Dornbos, S. Q. 2000. The Cambrian substrate revolution, GSA today, 10, 1–7. Brasier, M., Cowie, J. & Taylor, M. 1994. Decision on the Precambrian-Cambrian boundary stratotype, Episodes Journal of International Geoscience, 17, 3–8. Briggs, D. E. G., Collier, F. J. & Erwin, D. H. 1994. The fossils of the Burgess Shale. Bromley, R.G., 1996. Trace Fossils—Biology, Taphonomy and Applications, 2nd ed. Chapman & Hall, London. Bromley, R. G. & Ekdale, A. A. 1986. Composite ichnofabrics and tiering of burrows, Geological magazine. Cambridge University Press, 123, 59–65. Buatois, L.A. & Mángano, M.G., 2011. Ichnology: Organism-substrate interactions in space and time. Cambridge University Press. Budd, G. E. 2003. The Cambrian fossil record and the origin of the phyla, Integrative and Comparative Biology, 43, 157–165. Budd, G. E. 2008. The earliest fossil record of the animals and its significance, Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 1425–1434. Budd, G. E. & Jensen, S. 1998. Trace fossils and the Cambrian explosion, Trends in Ecology & Evolution, 13, 507. Budd, G. E. & Jensen, S. 2000. A critical reappraisal of the fossil record of the bilaterian phyla, Biological Reviews, 75, 253–295. Budd, G. E. & Jensen, S. 2017. The origin of the animals and a “Savannah” hypothesis for early bilaterian evolution, Biological Reviews, 92, 446–473. Budd, G. E. & Mann, R. P. 2018. History is written by the victors: the effect of the push of the past on the fossil record, Evolution, 72, 2276–2291. Budd, G. E., & Mann, R. P. 2019. Survival and selection biases in early animal evolution and a source of systematic overestimation in molecular clocks. PaleorXiv [preprint]. doi: 10.31233/osf.io/j45yf Budd, G. E. & Mann, R. P. 2020. The dynamics of stem and crown groups, Science Advances, 6, eaaz1626.

41 Butterfield, N. J. 2003. Exceptional fossil preservation and the Cambrian explosion, Integrative and Comparative Biology, 43, 166–177. Butterfield, N. J. 2007. Macroevolution and macroecology through deep time, Palaeontology, 50, 41–55. Butterfield, N. J., Balthasar, U. W. E. & Wilson, L. A. 2007. Fossil diagenesis in the Burgess Shale, Palaeontology, 50, 537–543. Conway Morris, S. 1977. A new metazoan from the Cambrian Burgess Shale of British Columbia. Palaeontology, 20, 623–440. Conway Morris, S. 1987. The search for the Precambrian-Cambrian boundary, American Scientist, 75, 156–167. Conway Morris, S. 1989. Burgess Shale faunas and the Cambrian explosion, Science, 246, 339–346. Conway Morris, S. 1998. The evolution of diversity in ancient ecosystems: a review, Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 353, 327–345. Cribb, A.T., Kenchington, C.G., Koester, B., Gibson, B.M., Boag, T.H., Racicot, R.A., Mocke, H., Laflamme, M. & Darroch, S.A. 2019. Increase in metazoan ecosystem engineering prior to the Ediacaran–Cambrian boundary in the Nama Group, Namibia, Royal Society Open Science, 6, 190548. Crimes, T. P. 1969. Trace fossils from the Cambro‐Ordovician rocks of North Wales and their stratigraphic significance, Geological Journal, 6, 333–338. Crimes, T.P., 1970. Trilobite tracks and other trace fossils from the Upper Cambrian of North Wales. Geological Journal, 7, 47–68. Crimes, T. P. 1987. Trace fossils and correlation of late Precambrian and early Cambrian strata, Geological Magazine, 124, 97–119. Crimes, T. P. 1992. Changes in the trace fossil biota across the Proterozoic- Phanerozoic boundary, Journal of the Geological Society, 149, 637–646. Crimes, T. P. & Anderson, M. M. 1985. Trace fossils from Late Precambrian-Early Cambrian strata of southeastern Newfoundland (Canada): temporal and environmental implications, Journal of Paleontology, 310–343. Crimes, T. P. & Fedonkin, M. A. 1994. Evolution and dispersal of deepsea traces, Palaios, 74–83. Crimes, T. P. & Marcos, A. 1976. Trilobite traces and the age of the lowest part of the Ordovician reference section for NW Spain, Geological Magazine, 113, 349–356. Cunningham, J.A., Liu, A.G., Bengtson, S. & Donoghue, P.C. 2017. The origin of animals: can molecular clocks and the fossil record be reconciled?. BioEssays, 39, 1–12. Curth, S., Fischer, M. S. & Nyakatura, J. A. 2014. Ichnology of an extant belly- dragging lizard—analogies to early reptile locomotion?, Ichnos, 21, 32–43. Daley, A.C., Antcliffe, J.B., Drage, H.B. & Pates, S., 2018. Early fossil record of Euarthropoda and the Cambrian Explosion. Proceedings of the National Academy of Sciences, 115, 5323–5331. Dashtgard, S. E. & Gingras, M. K. 2012. Marine invertebrate neoichnology. In: Knaust, D., Bromley, R.G. (Eds.), Trace Fossils as Indicators of Sedimentary Environments. Developments in Sedimentology, 64, pp. 273–295. Elsevier, Amsterdam, Davis, R. B., Minter, N. J. & Braddy, S. J. 2007. The neoichnology of terrestrial arthropods, Palaeogeography, Palaeoclimatology, Palaeoecology, 255, 284–307. Dos Reis, M., Thawornwattana, Y., Angelis, K., Telford, M.J., Donoghue, P.C. & Yang, Z. 2015. Uncertainty in the timing of origin of animals and the limits of precision in molecular timescales. Current Biology, 25, 2939–2950.

42 Droser, M. L., Gehling, J. G. & Jensen, S. 1999. When the worm turned: Concordance of Early Cambrian ichnofabric and trace-fossil record in siliciclastic rocks of South Australia, Geology, 27, 625–628. Droser, M. L., Jensen, S. & Gehling, J. G. 2002. Trace fossils and substrates of the terminal Proterozoic–Cambrian transition: implications for the record of early bilaterians and sediment mixing, Proceedings of the National Academy of Sciences, 99, 12572–12576. Dzik, J. 2005. Behavioral and anatomical unity of the earliest burrowing animals and the cause of the “Cambrian explosion”, Paleobiology, 31, 503–521. Erwin, D.H., Laflamme, M., Tweedt, S.M., Sperling, E.A., Pisani, D. & Peterson, K.J. 2011. The Cambrian conundrum: early divergence and later ecological success in the early history of animals, Science, 334, 1091–1097. Erwin, D. H. & Tweedt, S. 2012. Ecological drivers of the Ediacaran-Cambrian diversification of Metazoa, Evolutionary Ecology, 26, 417–433. Evans, S. D., Hughes, I. V., Gehling, J. G., & Droser, M. L. (2020). Discovery of the oldest bilaterian from the Ediacaran of South Australia. Proceedings of the National Academy of Sciences. Fortey, R. A., Briggs, D. E. G. & Wills, M. A. 1996. The Cambrian evolutionary “explosion”: decoupling cladogenesis from morphological disparity, Biological Journal of the Linnean Society, 57, 13–33. Fortey, R. A. & Seilacher, A. 1997. The trace fossil Cruziana semiplicata and the trilobite that made it, Lethaia, 30, 105–112. doi: 10.1111/j.1502- 3931.1997.tb00450.x. Gaines, R.R., Hammarlund, E.U., Hou, X., Qi, C., Gabbott, S.E., Zhao, Y., Peng, J. & Canfield, D.E. 2012. Mechanism for Burgess Shale-type preservation, Proceedings of the National Academy of Sciences, 109, 5180–5184. Gaines, R. R., Briggs, D. E. G. & Yuanlong, Z. 2008. Cambrian Burgess Shale–type deposits share a common mode of fossilization, Geology, 36, 755–758. Genise, J.F., Melchor, R.N., Archangelsky, M., Bala, L.O., Straneck, R. & de Valais, S. 2009. Application of neoichnological studies to behavioural and taphonomic interpretation of fossil bird-like tracks from lacustrine settings: the Late Triassic– Early Jurassic? Santo Domingo Formation, Argentina, Palaeogeography, Palaeoclimatology, Palaeoecology, 272, 143–161. Gingras, M.K., Pemberton, S.G., Henk, F.B., MacEachern, J.A., Mendoza, C., Rostron, B., O'Hare, R., Spila, M. & Konhauser, K. 2007. Applications of ichnology to fluid and gas production in hydrocarbon reservoirs. In MacEachern, Pemberton, S.G. Gingras, M.K. & Bann, K.L. (Eds.), Applied Ichnology. SEPM Short Course Notes 52, 131–145. Goldring, R., 1985. The formation of the trace fossil Cruziana. Geological Magazine, 122, 65–72. Gougeon, R.C., Mángano, M.G., Buatois, L.A., Narbonne, G.M. & Laing, B.A. 2018. Early Cambrian origin of the shelf sediment mixed layer, Nature communications, 9, 1–7. Hammer, Ø., Bengtson, S., Malzbender, T. & Gelb, D. 2002. Imaging fossils using reflectance transformation and interactive manipulation of virtual light sources, Palaeontologia Electronica, 5, 1–9.

43 Harper, D.A., Hammarlund, E.U., Topper, T.P., Nielsen, A.T., Rasmussen, J.A., Park, T.Y.S. & Smith, M.P., 2019. The Sirius Passet Lagerstätte of North Greenland: a remote window on the Cambrian Explosion. Journal of the Geological Society, 176, 1023–1037. Hitchcock, E., 1858. Ichnology of New England: A Report on the Sandstone of the Connecticut Valley Especially Its Fossil Footmarks, Made to the Government of the Commonwealth of Massachusetts. William White, Boston Jensen, S. 1997. Trace fossils from the Lower Cambrian Mickwitzia sandstone, south- central Sweden. Fossils and Strata 42,1–110. Jensen, S. 2003. The Proterozoic and earliest Cambrian trace fossil record; patterns, problems and perspectives, Integrative and Comparative Biology, 43, 219–228. Jensen, S., Droser, M. L. & Gehling, J. G. 2005. Trace fossil preservation and the early evolution of animals, Palaeogeography, Palaeoclimatology, Palaeoecology, 220, 19–29. Jensen, S., Droser, M. L. & Gehling, J. G. 2006. A critical look at the Ediacaran trace fossil record, in Neoproterozoic geobiology and paleobiology. In: Xiao S., Kaufman A.J. (eds) Neoproterozoic Geobiology and Paleobiology. Topics in Geobiology, vol 27. Springer, Dordrecht, 115–157. Knaust, D. 2017. Atlas of Trace Fossils in Well Core: Appearance, Taxonomy and Interpretation. Springer, Dordrecht Knaust, D., Bromley, R.G. (Eds.), 2012. Trace Fossils as Indicators of Sedimentary Environments. Developments in Sedimentology. 64. Elsevier, Amsterdam Knoll, A.H. & Carroll, S.B., 1999. Early animal evolution: emerging views from comparative biology and geology. Science, 284, 2129–2137. Kubo, T. 2010. Extant lizard tracks: Variation and implications for paleoichnology, Ichnos, 17, 187–196. Laing, B.A., Mángano, M.G., Buatois, L.A., Narbonne, G.M. & Gougeon, R.C. 2019. A protracted Ediacaran–Cambrian transition: an ichnologic ecospace analysis of the Fortunian in Newfoundland, Canada, Geological Magazine, 156, 1623–1630. Linnaeus, C. 1758. Systema naturae. Stockholm Laurentii Salvii. Lomax, D. R. & Racay, C. A. 2012. A long mortichnial trackway of Mesolimulus walchi from the Upper Jurassic Solnhofen Lithographic Limestone near Wintershof, Germany, Ichnos, 19, 175–183. Maloof, A.C., Porter, S.M., Moore, J.L., Dudás, F.Ö., Bowring, S.A., Higgins, J.A., Fike, D.A. & Eddy, M.P. 2010. The earliest Cambrian record of animals and ocean geochemical change, Geological Society of America Bulletin, 122, 1731– 1774. Mángano, M.G., Ortega-Hernández, J., Piñuela, L., Buatois, L.A., Rodríguez-Tovar, F.J. & García-Ramos, J.C., 2020. Trace fossil evidence for infaunal moulting in a Middle Devonian non-trilobite euarthropod. Scientific Reports, 10, 1-8. Mángano, M. G. & Buatois, L. A. 2014. Decoupling of body-plan diversification and ecological structuring during the Ediacaran–Cambrian transition: evolutionary and geobiological feedbacks, Proceedings of the Royal Society B: Biological Sciences, 281, 20140038. Mángano, M.G. & Buatois, L.A. eds., 2016. The Cambrian explosion. In The Trace- Fossil Record of Major Evolutionary Events, 73–126. Springer, Dodrecht. Mángano, M. G. & Buatois, L. A. 2017. The Cambrian revolutions: Trace-fossil record, timing, links and geobiological impact, Earth-Science Reviews, 173, 96– 108. Manton, S. M. 1977. The Arthropoda: habits, functional morphology, and evolution. Clarendon Press.

44 Marshall, C. R. 2006. Explaining the Cambrian “explosion” of animals, Annual Reviews of Earth and Planetary Science, 34, 355–384. Martin, M. W., Grazhdankin, D. V., Bowring, S. A., Evans, D. A. D., Fedonkin, M. A., & Kirschvink, J. L. 2000. Age of Neoproterozoic bilatarian body and trace fossils, White Sea, Russia: Implications for metazoan evolution. Science, 288, 841-845 McIlroy, D. 2004. Some ichnological concepts, methodologies, applications and frontiers, Geological Society, London, Special Publications, 228, 3–27. McIlroy, D. 2008. Ichnological analysis: the common ground between ichnofacies workers and ichnofabric analysts, Palaeogeography, Palaeoclimatology, Palaeoecology, 270, 332–338. Milàn, J. 2006. Variations in the morphology of emu (Dromaius novaehollandiae) tracks reflecting differences in walking pattern and substrate consistency: ichnotaxonomic implications, Palaeontology, 49, 405–420. Minter, N. J., Braddy, S. J. & Davis, R. B. 2007. Between a rock and a hard place: arthropod trackways and ichnotaxonomy, Lethaia, 40, 365–375. doi: 10.1111/j.1502-3931.2007.00035.x. Murchison, R.I., 1847. On the Silurian and associated rocks in Dalecarlia, and on the succession from Lower to Upper Silurian in Smoland, Öland, and Gothland, and in Scania. Quarterly Journal of the Geological Society, 3, 1–48. Murdock, D. J. E. & Donoghue, P. C. J. 2011. Evolutionary origins of animal skeletal biomineralization, Cells Tissues Organs, 194, 98–102. Narbonne, G.M., Myrow, P.M., Landing, E. & Anderson, M.M., 1987. A candidate stratotype for the Precambrian–Cambrian boundary, Fortune head, Burin Peninsula, southeastern Newfoundland. Canadian Journal of Earth Sciences, 24, 1277–1293. Narbonne, G. M. 2005. The Ediacara biota: Neoproterozoic origin of animals and their ecosystems, Annu. Rev. Earth Planet. Sci. Annual Reviews, 33, 421–442. Nathorst, A. G. 1881. Om spar af några evertebrerade djur mm och deras paleontologiska betydelse. Norstedt & Söner. Osgood Jr, R.G., 1970. Trace fossils of the Cincinnati area. Paleontographica. Americana., 41, 281–444. Paterson, J.R., Edgecombe, G.D. & Lee, M.S., 2019. Trilobite evolutionary rates constrain the duration of the Cambrian explosion. Proceedings of the National Academy of Sciences, 116, 4394–4399. Peterson, K.J., Lyons, J.B., Nowak, K.S., Takacs, C.M., Wargo, M.J. & McPeek, M.A. 2004. Estimating metazoan divergence times with a molecular clock, Proceedings of the National Academy of Sciences, 101, 6536–6541. Peterson, K.J., Cotton, J.A., Gehling, J.G. & Pisani, D. 2008. The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records, Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 1435–1443. Rhoads, D. C. & Young, D. K. 1970. The influences of deposit feeding benthos on bottom stability and community trophic structure, Journal of Marine Research, 28, 150–178 . Sadlok, G., 2014. New data on the trace fossil, Cruziana semiplicata (Furongian, Wiśniówka Sandstone Formation, Poland): origin, ethology and producer. In Annales Societatis Geologorum Poloniae, 84. Seilacher, A. 1953 Studien zur palichnologie. I. Uber die methoden der palichnologie, Neues Jahrbuch fur Geologie und Palaontologie, Abhandlungen, 96, 421–452. Seilacher, A. 1955 Spuren und fazies im Unterkambrium, in Beiträge zur Kenntnis des Kambriums in der Salt Range (Pakistan). Akademie der Wissenschaften und der Literatur zur Mainz, mathematisch-naturwissenschaftliche klasse, Abhand- lungen, 10, 373–399.

45 Seilacher, A. 1956. Der Beginn des Kambriums als biologische Wende, Neues Jahr- buch für Geologie und Paläontologie, Abhandlungen, 103, 155–180. Seilacher, A. 1967. Bathymetry of trace fossils, Marine Geology, 5, 413–428. Seilacher, A. 1970. Cruziana stratigraphy of “non-fossiliferous” Palaeozoic sandstones, Trace fossils. Seel House Press Liverpool, 2, 447–476. Seilacher, A. 1985. Trilobite palaeobiology and substrate relationships, Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 76, 231– 237. Seilacher, A. 2007. Trace fossil analysis, Springer, Berlin. Seilacher, A., Buatois, L. A. & Mángano, M. G. 2005 Trace fossils in the Ediacaran– Cambrian transition: behavioral diversification, ecological turnover and environmental shift, Palaeogeography, Palaeoclimatology, Palaeoecology, 227, 323–356. Slater, B.J., Harvey, T.H., Guilbaud, R. & Butterfield, N.J. 2017. A cryptic record of Burgess Shale‐type diversity from the early Cambrian of Baltica, Palaeontology, 60, 117–140. Slater, B.J., Willman, S., Budd, G.E. & Peel, J.S. 2018. Widespread preservation of small carbonaceous fossils (SCFs) in the early Cambrian of North Greenland, Geology, 46, 107–110. Smith, M. P. & Harper, D. A. T. 2013. Causes of the Cambrian explosion, Science, 341, 1355–1356. Smith, M. R., Harvey, T. H. P. & Butterfield, N. J. 2015. The macro‐and microfossil record of the Cambrian priapulid Ottoia, Palaeontology, 58, 705–721. Sperling, E. A., & Stockey, R. G. 2018. The temporal and environmental context of early animal evolution: considering all the ingredients of an “Explosion”. Integrative and comparative biology, 58, 605–622. Tarhan, L. G. & Droser, M. L. 2014. Widespread delayed mixing in early to middle Cambrian marine shelfal settings, Palaeogeography, Palaeoclimatology, Palaeoecology, 399, 310–322. Teal, L.R., Bulling, M.T., Parker, E.R. & Solan, M. 2008. Global patterns of bioturbation intensity and mixed depth of marine soft sediments, Aquatic Biology, 2, 207–218. Teal, L. R., Parker, E. R. & Solan, M. 2010. Sediment mixed layer as a proxy for benthic ecosystem process and function, Marine Ecology Progress Series, 414, 27–40. Thayer, C. W. 1979. Biological bulldozers and the evolution of marine benthic communities, Science, 203, 458–461. Thayer, C. W. 1983 Sediment‐mediated biological disturbance and the evolution of marine benthos, in Biotic Interactions in Recent and Fossil Benthic Communities, edited by M. J. S. Tevesz, and P. L. McCall, pp. 479–625, Plenum, New York. Valentine, J. W. 2002. Prelude to the Cambrian explosion, Annual Review of Earth and Planetary Sciences, 30, 285–306. Vannier, J., Calandra, I., Gaillard, C. & Żylińska, A. 2010. Priapulid worms: pioneer horizontal burrowers at the Precambrian-Cambrian boundary, Geology, 38, 711– 714. Vannier, J. & Martin, E. L. O. 2017. Worm-lobopodian assemblages from the early Cambrian Chengjiang biota: insight into the “pre-arthropodan ecology”?, Palaeogeography, Palaeoclimatology, Palaeoecology, 468, 373–387. Whittington, H. B. 1979. Early arthropods, their appendages and relationships. In M. R. House (ed.), The origin of major invertebrate groups, pp. 253–268. Academic Press, London.

46 Wood, R. A. 2018. Exploring the drivers of early biomineralization. Emerging Topics in Life Sciences 2, 201–212. Wood, R.; Liu, A. G.; Bowyer, F.; Wilby, P. R.; Dunn, F. S.; Kenchington, C. G.; Hoyal Cuthill, J. F.; Mitchell, E. G., and Penny, A. 2019. Integrated records of environmental change and evolution challenge the Cambrian Explosion. Nature Ecology & Evolution, 3, 528–538. Wray, G. A., Levinton, J. S. & Shapiro, L. H. 1996. Molecular evidence for deep Precambrian divergences among metazoan phyla, Science, 274, 568–573. Zhang, X., Liu, W. & Zhao, Y. 2008. Cambrian Burgess Shale-type Lagerstätten in south China: distribution and significance, Gondwana Research., 14, 255–262.

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