The rapid appearance of bilaterian clades at the beginning of the Phanerozoic is one of the most intriguing topics in macroevolution. However, the complex feedbacks between diversification and ecological interactions are still poorly understood. Here, we show that a systematic and comprehensive analysis of the trace-fossil record of the Ediacaran–Cambrian transition indicates that body-plan diversification and ecological structuring were decoupled. The appearance of a wide repertoire of behavioural strategies and body plans occurred by the Fortunian. However, a major shift in benthic ecological structure, recording the establishment of a suspension-feeder infauna, increased complexity of the trophic web, and coupling of benthos and plankton took place during Cambrian Stage 2. Both phases were accompanied by different styles of ecosystem engineering, but only the second one resulted in the establishment of the Phanerozoic-style ecology. In turn, the suspension-feeding infauna may have been the ecological drivers of a further diversification of deposit-feeding strategies by Cambrian Stage 3, favouring an ecological spillover scenario. Trace-fossil information strongly supports the Cambrian explosion, but allows for a short time of phylogenetic fuse during the terminal Ediacaran–Fortunian.
The Ediacaran–Cambrian transition represents a critical time in the history of the biosphere both in terms of animal diversity and ecosystem construction [1–4]. Historically, two conflicting views on the early evolution of animals have emerged. One view takes the fossil record at face value, envisaging a scenario of rapid origination of modern phyla (the Cambrian explosion), whereas the other emphasizes the imperfect nature of the fossil record, assuming deep Precambrian roots in the evolutionary history of animals (the slow phylogenetic fuse) [5,6]. In this second view, the Cambrian explosion is an artefact resulting from an increase in preservability of body fossils related to the acquisition of mineralized skeletons, probably linked to major changes in the chemistry of the oceans [7,8]. This debate has mostly revolved around two different datasets: the body-fossil record and molecular clocks. Although the body-fossil record supports the notion that the Cambrian event of diversification is real and unparalleled in the history of life [9,10], interpretation of molecular clock evidence has been quite controversial. Earlier studies did not support the explosion scenario, suggesting deeper divergence among animals [11,12]. Although a growing number of recent studies tend to be more consistent with the body-fossil record, divergence times are still hard to reconcile with the explosion scenario [13,14].
There is an approximately 20 Myr gap between the youngest exceptional preservation of Ediacaran body-fossil assemblages, the Nama assemblage (549–541 Ma), and that of the Cambrian Stage 3 Burgess shale-type assemblages, such as Chengjiang and Sirius Passet (521–514 Ma). However, trace fossils, namely trackways, trails, burrows and borings , offer an independent line of evidence to calibrate the Cambrian explosion. A systematic trace-fossil survey of Ediacaran–Cambrian sections worldwide, involving the construction of a comprehensive database (see the electronic supplementary material), demonstrates that the record of animal–sediment interactions across the Ediacaran–Cambrian boundary is far more continuous than the body-fossil record, particularly with respect to that of soft-bodied organisms. Accordingly, trace fossils represent a key element to evaluate the timing of diversification and ecosystem construction during the Cambrian explosion. Bilaterian diversification resulted in the appearance of ecosystem engineers that actively modified sedimentary substrates, altering and creating habitats . However, our understanding of the driving mechanisms and complex feedback loops involved in these processes during the Ediacaran–Cambrian transition is quite limited.
The aims of this paper are to (i) demonstrate that the trace-fossil record strongly supports the Cambrian explosion scenario, (ii) provide solid evidence that body-plan diversification and the establishment of a Phanerozoic benthic ecological structure were distinct and decoupled events, and (iii) provide insights into the differential role of ecosystem engineers and feedback loops during the successive phases of the radiation. Prior to this study, animal diversification and colonization of the infaunal ecospace have been considered roughly synchronous .
2. Material, methods and concepts
The global database (see the electronic supplementary material) is based on systematic and critical examination of the literature, collection material and field data. Six time slices (two informal Ediacaran subdivisions—Vendian and Nama —and the four official Lower Cambrian stages) are considered. An older subdivision (Avalon) has not been included, because uncontroversial bilaterian trace fossils are not known from this time slice. Although our study addresses the macroevolutionary changes that took place at the beginning of the Cambrian, the Ediacaran is included in order to calibrate the ichnological record of the evolutionary explosion against the much more limited Ediacaran record. In particular, the Nama bin is critical because it records the appearance of some behavioural types that represent a prelude to the Cambrian explosion and because of the controversies surrounding some of the Vendian bin trace fossils. Information was compiled from 369 stratigraphic units. About 20% of these units have been examined by the authors in the field. Another 20% of the units were analysed based on collection specimens. The remaining units were evaluated based on detailed and critical literature review. The trace-fossil database includes taxonomical composition, preservation styles, ethology, feeding strategies, degree of bioturbation, tiering structure, architectural designs, potential tracemakers, age and depositional environment. Critical reassessment of published identifications was of paramount importance (see also [17,18]). Synonyms have been checked, and we have adopted a consistent taxonomical approach to trace fossils. Each original taxonomic determination has been revised based on re-examination of the original material, photographs and descriptions.
Assessment of degree of bioturbation followed standard ichnological practice using a bioturbation index (BI) . The BI indicates the extent to which the primary sedimentary fabric is still visible. In this scheme, BI = 0 is characterized by no bioturbation (0%), and the primary fabric remains intact. BI = 1 (1–4%) is for sparse bioturbation with few discrete traces locally overprinting the well-preserved sedimentary fabric. BI = 2 (5–30%) is represented by low bioturbation in sediment that still has well-preserved sedimentary structures. BI = 3 (31–60%) describes an ichnofabric with discrete trace fossils, moderate bioturbation and still distinguishable bedding boundaries. BI = 4 (61–90%) is represented by intense bioturbation, high trace-fossil density, trace fossils and primary sedimentary structures mostly erased. BI = 5 (91–99%) is characterized by sediment with completely disturbed bedding and intense bioturbation. BI = 6 (100%) is for completely bioturbated and reworked sediment, related to repeated overprinting of trace fossils. In the cases of units analysed by the authors in the field, BI was assessed for individual beds and summarized by facies types. In the case of units not studied by the authors in the field, BI was assessed by evaluating representative samples or by checking the literature based on original determinations and photos.
Tier classification follows previously established schemes (see  for review). The shallow tier comprises structures produced in the upper 6 cm of the substrate, the mid-tier those produced between 6 and 12 cm of the substrate, and the deep tier those emplaced below 12 cm. The 6 cm boundary reflects approximately a depth above which organisms are challenged by disturbance rather than by maintaining contact with the sediment–water interface and below which these difficulties are reversed in severity. The 12 cm boundary marks a boundary within the sediment below which stresses linked to limited food supply and oxygen content, as well as by increased substrate compaction, become extreme limiting factors. A very deep tier (more than 100 cm) may also be considered, but it has been essentially empty prior to the Mesozoic marine revolution.
Temporal trends in trace-fossil distribution were assessed by a combined analysis of (global and alpha) ichnodiversity and ichnodisparity [15,20] (table 1; electronic supplementary material, table S1). Global ichnodiversity (i.e. number of ichnogenera per time slice) provides a proxy to behavioural changes and evolutionary innovations during the Earth's history. To account for the different duration of the time slices, ichnodiversity has been standardized per Myr following usual practices in analytical palaeobiology. Alpha ichnodiversity (i.e. number of ichnogenera recorded for individual trace-fossil suites) provides a glimpse into ecological complexity at the scale of individual communities. Although ichnodiversity simply refers to trace-fossil richness, ichnodisparity (i.e. number of trace-fossil architectural designs) provides a measure of the variability of basic morphological plans in biogenic structures, and consequently best records innovations in body plan, locomotory system and behavioural programme . It is the tacit premise in our reasoning that, in most cases, major changes in trace-fossil architecture and in fabricational design are biologically wired. The fact that ichnodiversity and ichnodisparity are not necessarily concordant is illustrated in this study. Assessment of morphological and behavioural complexity follows previous studies [15,20,22].
This approach provides an insight into the complex history of interactions between animals and sediment, and among organisms also at the community level. Although a univocal link between the animal producer and the trace fossil is not commonly possible, the appearance of some architectural designs may be directly linked to a group of producers, such as trackways (arthropods) and pentameral-shaped impressions (asteroids and ophiuroids), revealing evolutionary innovations in the fossil record. In addition, the appearance of other architectural designs (e.g. vertical simple burrows, burrows with horizontal or vertical spreiten), although more equivocal in terms of the affinities of the producer, certainly reflects novel ways of interacting with the sediment, allowing us to picture in finer detail the early steps of the Cambrian diversification event.
A global maximum of 10 ichnogenera has been documented for the Ediacaran. Of these, nine ichnogenera were already known from the Vendian and seven were recorded in the Nama (table 1 and figure 1). Standardization to reflect ichnodiversity per geological time shows very low values (0.9 and 0.8 ichnogenera per Ma, respectively), further reinforcing the view of limited behavioural diversity during the Ediacaran (table 1). Alpha ichnodiversity is up to 6; 52% of occurrences are monospecific, in sharp contrast to Phanerozoic ichnofaunas. Ichnodisparity and behavioural complexity are also remarkably limited, with only six architectural designs recorded globally. Simple horizontal grazing trails, mostly associated with microbial mat textures, are by far the dominant elements, representing matground grazing (59% of all recorded cases). Shallow-tier, actively filled (massive) horizontal burrows (e.g. Torrowangea) record incipient substrate penetration.
Fan-like arrangements of paired scratch marks produced on microbial mats are in some cases directly associated with Kimberella . Ichnological evidence (e.g. the animal located at the apex of the fan) suggests that Kimberella was the producer of the scratch traces, recording epibenthic grazing on microbial mats. However, the phylogenetic affinity of Kimberella remains controversial. Possible resting and locomotion trace fossils (Epibaion) produced by dickinsonids occur in direct association with Dickinsonia and Yorgia [31–33]. However, passive transport has been suggested as an alternative . Because the affinities of Dickinsonia are uncertain  and its morphology is hard to reconcile with a bilaterian origin, Epibaion is not included in table 1.
With the exception of the problematic Nenoxites (a controversial ichnogenus that needs further revision) and Epibaion, which are restricted to the Ediacaran, all the other ichnogenera present in the Ediacaran continue into the Phanerozoic, and their production by bilaterians is well supported by neoichnological data, making ad hoc to assume that in the Ediacaran identical structures were produced by non-bilaterians. Feeding modes include epifaunal to very shallow infaunal grazers, and non-attached, absorptive or chemosymbiotic feeders. Restriction of biogenic structures to bedding planes indicates a negligible use of the infaunal ecospace and the virtual absence of infaunal tiering. Information from the Nama bin reveals some changes in ichnofaunal composition. Very shallow, three-dimensional burrow systems occur, for the first time, in the Nama , revealing an increase in complexity. In any case, these three-dimensional burrow systems are far simpler than their Cambrian counterparts, including T. pedum, whose first appearance datum is indicative of the Ediacaran–Cambrian boundary . The degree of bioturbation (as seen in cross-section) is invariably 0 in the Vendian, reaching 1 occasionally in the Nama (table 1 and figure 1).
Of equal importance is the absence of trace fossils produced by some key players of Phanerozoic communities. Structures previously interpreted as guided meandering grazing trails are no longer considered trace fossils, because careful re-analysis fails to reveal the presence of actual meanders, suggesting that these were body fossils instead [17,18,33,37]. Therefore, animals displaying sophisticated feeding strategies involving strophotaxis (i.e. proclivity to make U-turns so that the animal turns around 180° at intervals), phobotaxis (i.e. tendency to avoid crossing its own and other trails) or thigmotaxis (i.e. propensity to keep close contact with a former segment of the trail) are not present in Ediacaran rocks. Arthropod trace fossils are strikingly absent. Unquestionable examples of vertical burrows in high- to moderate-energy facies recording activities of suspension feeders have not been documented from the Ediacaran.
The trace-fossil evidence from the earliest Cambrian shows a substantially different scenario with the appearance of diverse and complex ichnofaunas, revealing a wide variety of behavioural patterns (figure 2a–l) and a new cast of characters, including most notably arthropods (e.g. Rusophycus, Diplichnites, Allocotichnus). A global maximum of 42 ichnogenera has been documented for the Fortunian (table 1 and figure 1). The increase in ichnodiversity is even more remarkable when standardized to account for differences in duration between the Fortunian and the terminal Ediacaran (table 1). Alpha ichnodiversity reached 14; only 27% of occurrences are monospecific. Ichnodisparity and behavioural complexity also show a remarkable increase, with 22 architectural designs recorded globally. Some distinctive structures of selective deposit feeders consist of systematic guided meanders (e.g. Psammichnites), revealing the onset of sophisticated grazing strategies that require more advanced navigational devices. In addition, radial branching structures (e.g. Volkichnium) are recorded for the first time. Branching burrow systems (e.g. Treptichnus, Streptichnus, Multina) became more abundant and diverse, at least some of them indicating systematic probing of the sediment in search of food. Surface-coverage branching burrows (e.g. Oldhamia) are remarkably complex and characterized by closely spaced probings forming lobate and hook-like patterns that record sophisticated undermat-mining feeding strategies . Overall, these searching programmes reflect strophotactic, phobotactic and thigmotactic behaviour, and the development of a higher-grade nervous system.
The degree of bioturbation in Fortunian deposits remains notably low (average BI: 0.5, maximum BI: 3), revealing only a very slight increase with respect to Ediacaran levels (table 1 and figure 1). Although there is a significant expansion in terms of the represented architectural designs, the infaunal ecospace remains underexploited in comparison with younger Cambrian deposits. Trace fossils only penetrate the uppermost centimetres of the sediment, and are typically oriented parallel to the bedding plane, causing little disturbance in the primary sedimentary fabric. Isolated vertically oriented trace fossils are rare, being present in silty and muddy firmgrounds rather than in moderate- to high-energy shifting sands . Skolithos piperock (i.e. near-shore sandstone containing high density of vertical burrows produced by suspension feeders or passive predators) is absent.
(c) Cambrian Stage 2
A maximum number of 43 ichnogenera has been recorded worldwide for Cambrian Stage 2 (table 1 and figure 1). Alpha ichnodiversity is up to 18. Ichnodisparity and behavioural complexity show a slight increase, with 23 architectural designs recorded globally. By contrast, the degree of bioturbation shows a sharp increase with respect to previous levels (average: 2.3; maximum: 6) and a dramatic increase in maximum burrowing depth is recorded (up to 1 m).
The most important innovation is the appearance of sandstone deposits displaying profusion of vertical burrows (figure 3a–i) forming Skolithos piperock. Most of these vertical burrows are lined, representing permanent domiciles of suspension feeders and passive predators. The fact that moderate- to high-energy near-shore, non-bioturbated sandstone is a common facies in the Fortunian argues against preservational or sampling biases and in favour of the true appearance of this guild during Cambrian Stage 2. These low-diversity to monospecific assemblages indicate that worm-like coelomate organisms were able to colonize the deep infaunal ecospace in mobile sandy substrates of high- to moderate-energy coastal settings for the first time . In low-energy offshore deposits, intense bioturbation was evidenced by a diverse set of simple and branching probing structures, commonly bearing distinctive spreite and representing feeding structures of deposit feeders.
(d) Cambrian Stage 3
Cambrian Stage 3 global ichnodiversity is 55, revealing a significant further increase with respect to Cambrian Stage 2, which is even more pronounced when standardized to account for differences in duration between both stages (table 1 and figure 1). This increase took place mostly in connection with the appearance of novel deposit-feeding ichnotaxa. Maximum alpha ichnodiversity is 28. Ichnodisparity and behavioural complexity are slightly higher than those of Cambrian Stage 2, with 28 architectural designs recorded globally. No further increase in degree of bioturbation has been detected (average 2.4, maximum 6). The fact that the remarkable increase in global ichnodiversity is not paralleled by an equally significant increase in ichnodisparity suggests increasing diversity within clades and minor behavioural variations of previously established architectural plans rather than the introduction of clades and major behavioural innovations. This increase in ichnodiversity is roughly coincident with the bilaterian radiation based on skeletonized animals [2,4].
(e) Cambrian Stage 4
Ichnofaunas from Cambrian Stage 4 show no significant change in global ichnodiversity, alpha ichnodiversity and ichnodisparity in comparison with those from Cambrian Stage 3 (table 1 and figure 1). An increase in ichnodiversity is apparent when data are standardized to show ichnodiversity per Myr. However, this is simply an artefact resulting from the shorter duration of Cambrian Stage 4 and the lack of biostratigraphic resolution to differentiate Stages 3 and 4 in some stratigraphic crucial units. Degree of bioturbation also remains constant. Based on available data, the most likely interpretation of this pattern is that near the end of the ‘early’ Cambrian, the evolutionary radiation was essentially over. The body-fossil record also shows no further significant increase in diversity and disparity by this time [2,4]. The consistency between the trace- and body-fossil records provides a strong support to the accepted timing of the close of the explosion.
Trace-fossil data strongly support a rapid increase of animal diversity in the Early Cambrian (i.e. the Cambrian explosion scenario). However, our systematic analysis also points to the existence of a relatively short period of phylogenetic fuse during the terminal Ediacaran and the Fortunian. By the end of the Fortunian, the diversification event evidenced by the appearance of complex architectural designs reflecting body-plan diversification and behavioural innovations was well under way. Therefore, the trace-fossil record indicates that the evolutionary radiation occurred earlier than suggested according to the classic Cambrian explosion scenario based on the appearance of the main phyla in the body-fossil record [2,4].
Under detailed scrutiny, the trace-fossil record clearly points to two major evolutionary breakthroughs—the Fortunian diversification event, and the Cambrian Stage 2 agronomic revolution that marks the establishment of a Phanerozoic-style ecology —followed by a positive spillover effect driven by the activities of benthic suspension feeders by Stage 3. In contrast to the prevailing view that diversification of animals and infaunal colonization were roughly coincident during the Cambrian explosion , our study indicates that the presence of a wide array of metazoan behaviours preceded the establishment of a modern infaunal ecological structure (i.e. mixground ecology), indicating a decoupling of cladogenesis and the major shift in benthic ecology that typifies the Phanerozoic.
The Cambrian explosion was characterized by the onset of ecosystem engineers that were capable of significantly affecting the physical and chemical environment. Physical changes may have included structural or architectural activities, sediment mixing and sediment stabilization, whereas chemical engineering encompassed nutrient transfer and oxygenation of the water column and sediment . Although some of these changes are evident from the skeletal fossils (e.g. structural modification by the formation of reefs) , other effects are more difficult to detect from the body-fossil record. Cambrian soft-bodied faunas produce additional information to evaluate ecosystem engineering, but they are absent from 541–521 Ma, a critical time for evaluating the onset of the explosion. The fact that trace fossils occur all through this interval, recording the interaction of soft-bodied organisms with the sediment, makes them ideally suited to evaluate the impact of ecosystem engineers at this critical time, allowing to establish a detailed chronology of ecological changes.
The Fortunian diversification event and the Cambrian Stage 2 agronomic revolution undoubtedly have had different impacts from the perspective of ecosystem engineering (figure 4). The first event involves the appearance of a wide repertoire of behavioural strategies reflecting the interactions of newly developed, distinctive body plans with the substrate. Most of these interactions were characterized by the reworking of fine-grained sediments by sediment bulldozers in diffusion-dominated benthic systems , as typified by bioturbation in offshore deposits. This style of biogenic reworking was probably conducive to large-scale changes in both the sediment and the water column, including promotion of water fluxes at the sediment–water interface, average deepening of the redox discontinuity surface, release of nitrogen from the sediment, increase in the sediment–water flux of iron and manganese, and several-fold increase in seawater sulfate concentration [41,42]. By being the primary determinant of oxygen concentration in the sediment, bioturbation may have also influenced the biomass of organisms, the expansion of aerobic bacteria, the rate of organic matter decomposition and the regeneration of nutrients vital for primary productivity, among other aspects [43–45]. However, the exploitation of matgrounds, a typical Ediacaran strategy, largely persisted during the Fortunian, probably as a result of the low levels of bioturbation. The restriction of most biogenic structures to lithological interfaces is in itself an indication that a significant number of the benthos exploited buried microbial mats .
The second event marks a qualitative change in ecological structure, recording an increased complexity of the food route and trophic web, and a re-organization of the infaunal ecospace. The appearance of deep-tier suspension feeders is central to this second phase, revealing bioturbation in advection-dominated benthic systems . The establishment of suspension-feeding communities had a major impact in marine ecosystems, signalling the coupling between plankton productivity and the benthos . The key innovation introduced by filter-feeding mesozooplankton may have not only acted as the trigger of the evolution of large-size metazoans [43,48], but also played a role in the final turnover from matgrounds to mixgrounds. By repacking unicellular phytoplankton as nutrient-rich larger particles, zooplankton provides a more concentrated and exploitable resource for the benthos [43,48]. Because suspension feeders move and process large amounts of material, they play a major role in nutrient cycling, including regeneration of nitrogen and phosphorus to the water column [47,49]. The dramatic increase in bioturbation intensity and depth that occurred during the Cambrian Stage 2 resulted in higher irrigation levels, and was conducive to a further deepening of the redox discontinuity surface. In addition, suspension feeders can filter large volumes of water, particularly in more protected systems having longer hydrodynamic resident times, and therefore preventing eutrophication and reducing water turbidity, which makes light available for microphytobenthos [47,49,50]. In fact, the appearance of a suspension-feeder infauna may have been the driving force for a dramatic increase in ocean ventilation .
The association between ecosystem engineering and the explosion of bilaterian clades has been noted in previous studies, but it is not totally clear whether the former represented a driver of the diversification event . Our systematic evaluation of the trace-fossil record reveals a particular temporal pattern of animal–sediment interactions, suggesting complex feedback loops between diversification and ecosystem engineering, rather than a simple cause–effect link. The initial diversification (Fortunian) is coincident with the appearance of the first sediment bulldozers, but preceded the establishment of infaunal suspension-feeder faunas that were ecosystem engineers of paramount role (Cambrian Stage 2). In turn, the rapid increase in depth and extent of bioturbation associated with these suspension-feeding communities may have triggered another diversification event of biogenic structures that took place during Cambrian Stage 3, and involved the appearance of new behaviours by deposit feeders. Capture of organic particles by suspension feeders allowed enrichment of organics by biodeposition, promoting diversification of infaunal deposit feeders . Therefore, infaunal suspension feeders may have been ecological drivers of the Cambrian Stage 3 diversification phase of biogenic activity (figure 4), representing a dramatic case of ecological spillover .
To summarize, our compilation of the trace-fossil record across the Ediacaran–Cambrian transition strongly supports the Cambrian explosion scenario. However, the wide variety of trace-fossil architectural designs in the Fortunian indicates that body-plan diversification occurred earlier than suggested according to the Cambrian explosion scenario based on the appearance of the main phyla as indicated by the body-fossil record. Analysis of our database shows a decoupling between the appearance of most animal groups in the Fortunian and the subsequent establishment of Phanerozoic-style marine ecosystems during Cambrian Stage 2. By the same token, the absence of a wide repertoire of architectural designs during the Ediacaran is an outstanding fact. We underscore the role of ecosystem engineers during the Cambrian explosion by showing that both breakthroughs were accompanied by different styles of ecosystem engineering and that positive feedback loops were involved. In fact, the establishment of well-developed suspension-feeding infaunal communities, recorded worldwide by Skolithos piperock, may have acted as an ecological driver of a further diversification of deposit-feeding strategies by Cambrian Stage 3.
Financial support for this study was provided by Natural Sciences and Engineering Research Council (NSERC) Discovery grants nos 311727-05/08 and 311726-05/08/13, awarded to Mángano and Buatois, respectively.
We thank reviewers of Proc. R. Soc. B Nic Butterfield and Jonathan Antcliffe, and editors Gary Carvalho and Norman Macleod for their useful comments. Doug Erwin and Nic Minter critically read an early version of this manuscript and provided valuable feedback. A large number of colleagues showed us outcrops and collections, namely John Almond, Richard Callow, Peter Crimes, Jim Gehling, Gerard Germs, Liam Herringshaw, Richard Jenkins, Sören Jensen, Alex Liu, Duncan McIlroy, Guy Narbonne, Brian Pratt and Dolf Seilacher, further helping to shape our view on Ediacaran–Cambrian ichnology.
- Received January 7, 2014.
- Accepted January 21, 2014.
- © 2014 The Author(s) Published by the Royal Society. All rights reserved.