Australia: The Land Where Time Began

A biography of the Australian continent 

Cambrian Explosion Triggers – Hypotheses and Problems

Abrupt appearance of major bilaterian clades in the fossil record during the first three stages of the Cambrian Period has puzzled the scientific world since the 1830s. Many proposed causes including environmental, developmental, and ecological hypotheses, are reviewed in this paper. Nutrient availability, oxygenation, and change of seawater composition are commonly supposed to be environmental triggers. The nutrient input, e.g. the enrichment of phosphorus in an environment, would cause excess primary production, but it is neither directly linked with diversity nor disparity. Fluctuating abiotic conditions during the Snowball Earth and the associated oxygenation event may have stimulated the diversification of complex multicellular organisms including diversification of macroscopic and morphologically differentiated algae in the early Ediacaran, but did not lead to the ecological success of metazoan or bilaterian lineages. Further increase of oxygen level and change of seawater composition just before and during the Early Cambrian are suggested by the high weathering rate of the trans-Gondwana Mountains, Great Unconformity, and decline of oceanic salinity. These are potential candidates for environmental triggers for the Cambrian Explosion but require future, more detailed geochemical studies to confirm. The molecular phylogeny calibrated with the molecular clock data suggested that the developmental system of bilaterians was established before their divergence. This, in turn, suggests that the Cambrian Explosion requires environmental triggers. However, there still exists the contention between deep or shallow divergence of bilaterian clades, which remains to be solved in the future. The deep divergence model is supported by a majority of molecular clock studies, but is challenged by the paucity of bilaterian fossils before and during the Ediacaran Period. The shallow model is generally consistent with the fossil record, but has to explain the rapidity of increase in diversity, disparity, morphological complexity, acquisition of biomineralised shells, etc. Regardless of deep or shallow model, the conservation of lineage-specific kernels within the gene regulatory networks (GRNs) provides an explanation for the long-term stability of body plans after the Cambrian Explosion, and continuous addition of microRNAs into the GRNs seems to correspond well to the increase in morphological complexity. As for ecological causes, some hypotheses (e.g. adaptive radiation after mass extinction, cropping, and geosphere–biosphere feedbacks) cannot explain the uniqueness of the event, some others (such as Cambrian substrate revolution, predator–prey pressure, evolution of zooplankton, and roughening of fitness landscapes) fall into the trap of the chicken-and-egg problem because of considering the consequence as a cause. Expansion of ecosystem engineering in the early Cambrian might also be caused by the Cambrian Explosion. However, ecosystem engineering associated with Ediacaran ecosystems is likely a pivotal ecological prerequisite for the later ecological success of bilaterian clades, particularly the engineering effect by Ediacaran sponges that ventilated seawater by sponge pumping and removing organic material from the water column. However, the ecological abundance of Ediacaran sponges needs to be further investigated. Finally, a working plan is proposed for future research. For palaeontologists, searching for ancestors of Early Cambrian faunas is crucial to testify the earlier divergence of bilaterian lineages. Environmentally, precise values on the oxygen level and seawater composition are required during the Ediacaran–Cambrian transition.

A long standing issue in macroevolution in the Cambrian Explosion has been puzzling palaeontologists and evolutionary biologists since 1830, “William Buckland knew about it, Charles Darwin characteristically agonised over it, and still we do not understand it” (Conway Morris, 2000, p. 4426). Essentially all of the body plans, about half of the extant animal phyla, is generally accepted to have made their first appearance in the fossil record within a few 10s of millions of years during the Early Cambrian (Valentine, 2002; Erwin et al., 2011). The Cambrian Explosion has, therefore, been widely realised as the most significant evolutionary event in the history of life on Earth (Conway Morris, 2006; Marshall, 2006; Shu, 2008; Maruyama et al., 2013; Santosh et al., 2013).

The first appearances of animal fossils are obviously diachronous, though relatively abrupt in a short period of time during the Late Ediacaran to Early Cambrian (Shu et al., 2014 in this issue). The fossil record of basal animals, such as sponges and cnidarians, is extended to a period of time that is significantly earlier than the opening of the Cambrian. Therefore, it seems the Cambrian Explosion itself appears to represent the arrival of bilaterians (Budd, 2008). It was revealed by early analysis that the divergence of bilaterian clades was episodic:

Lophotrochozoans were diversified during the Terrenenuvian Epic, mainly in the Fortunian Age;

Ecdysozoans diversified at the beginning of Cambrian stage 3, in spite of the fact that their fossils can be traced back to Terreneneuvian Epoch, e.g. traces of arthropods and grasping spines of chaetognaths;

Deuterostome divergence began from the middle of the Cambrian stage 3 (Shu, 2008; Shu et al., 2009; Maloof et al., 2010; Kouchinsky et al., 2012), though the appearance of the remains and traces of bilaterian animals has remained abrupt (Erwin et al., 2011; Shu et al., 2014-in this issue).

It appears that the faunas from the Cambrian indicate that diverse animal phyla were already established in the Early Cambrian and provided a large amount of information concerning the diversity, disparity and morphological complexity of animal life at that time (Nielsen, 2001). Unfortunately, not much is preserved in the fossil record about the origin of animal phyla because the early ancestors might have been small and/or soft-bodied, for which there was little or no preservation and/or recognisable potential. According to Zhang et al. it is likely, therefore, that a period of animal evolution occurred prior to the Cambrian Explosion that is observed in the Early Cambrian. Studies of molecular diversification and comparative developmental data also indicate this (Wray et al., 1996; Bromham et al., 1998; Aris-Brosou & Yang, 2003; Peterson et al., 2004, 2008; Blair, 2009, evolution of transport proteins for oxygen (Decker & van 2011), and phylogenetic analyses of Cambrian and biogeography (Fortey et al., 1996; Lieberman, 2002), which suggests the major animal clades diverged many 10s of millions of years prior to their first appearance in the fossil record. The paucity of bilaterian clade fossils during the Ediacaran challenges unavoidably any inference on earlier divergence of bilaterian phyla.

Provisionally, the conundrum of the Cambrian Explosion appears to have been solved by the combination of palaeontological and molecular data, with at least the stem lineages of the major animal clades diverging during the late Cryogenian to Early Ediacaran, and becoming ecologically important in the Late Ediacaran to Early Cambrian (Erwin et al., 2011). A long history of cryptic evolution is implied that is not present in the fossil record. The Cambrian Explosion is, therefore, largely an ecological phenomenon, including the increasing body size and morphological complexity, as well as widespread biomineralisation among animals.

The exact causality has yet to be established, though many hypotheses have been proposed as to what triggered the Cambrian Explosion, that range from environmental, developmental to ecological causes. A joint project by Chinese and Japanese scientists have worked on palaeontological and environmental issues since 2005, and their preliminary progress has been published in a special issue of Gondwana Research 14 (1-2) 2008 and this volume. This cooperative project was planned to be continued in the next 5 years. Therefore, in this paper Zhang et al. give a review on the available triggering mechanisms of the Cambrian Explosion in order to identify the shortcomings of each hypothesis, in particular with palaeontological data, and finally explicate their future research on this topic.

2. Hypothetical triggers

According to Zhang et al. it seems obvious that there must have been a change in something, or a critical level that was favourable for building large, complex bodies and the construction of hard skeletal material. The hypotheses of such evolutionary triggers is able to be split into extrinsic or external environmental factors, such as tectonic settings, climatic conditions, availability of nutrients, level of oxygen content, oceanic conditions, nutrient variability and biotic factors that are intrinsic or internal, genetical and developmental innovations, and ecological causes.

Environmental triggers

According to Zhang et al. of the many triggers that have been proposed the change in oxygenation and the composition change of seawater are the most relevant factors. A number of others, such the tectonic background and deglaciation of Snowball Earth, merely provide mechanisms of the increase in the level of oxygen and the fluctuation of seawater chemistry. There are, of course, other environmental factors, e.g. the level of atmospheric CO₂, pH of seawater, and trace metals, that are of potential importance for the evolution of animals, though the lack of data that are specifically relevant to the Cambrian Explosion does not allow a further discussion of these issues.

Tectonic backdrop

The assembly of Gondwanaland is viewed more or less as a polyphase accretion of what were previously disparate blocks, which was accomplished along 3 major orogenic belts, the East African Orogen (750-620 Ma), the Brasilina-Damara Orogen (630-520 Ma), and the Kuungan Orogen (570-530 Ma) (Li & Powell, 2001; Meert, 2003; Rogers & Santosh, 2004; Campbell & Squire, 2010; Meert, 2011). The Brasilina-Damara Orogen (630-520 Ma), and the Kuungan Orogen (570-530 Ma) took place just prior to and during the Cambrian Explosion. It is suggested by more recent palaeomagnetic and geochronological that the closure of the Clymene Ocean occurred in the Early Cambrian (Tohver et al., 2010, 2012). The Iapetus Ocean opened at around the same time (Grunow et al., 1996), which was followed by the Mawson and Brasiliano Oceans (Meert & Lieberman, 2008). Pannotia, the hypothetical short-lived supercontinent, formed at the latest Neoproterozoic, just prior to the Cambrian radiations (Dalziel, 1997), was comprised of Gondwana and Laurentia adjacent to Amazonia (Li & Powell, 2001). Regardless of the exact model of Gondwana assembly and the debate on the existence on Pannotia, the formations of the supercontinents was just prior to, or nearly synchronous with, the Cambrian Explosion. According to Zhang et al. it was reasonable, therefore, to link biological changes that occurred at this time with tectonic events that resulted in the assembly of supercontinents and oceans opening. Within Gondwana, each collisional orogen extended for several kilometres (Dalziel, 1997; Campbell & Squire, 2020). When the huge trans-Gondwana Mountains were uplifted and eroded it would have had a significant influence on the composition of seawater and the global climate, which provided nutrients, such as phosphorus, to the oceanic realm (Brasier & Lindsay, 2001; Squire et al., 2006) and increased the rate of burial of organic carbon that is believed to have triggered a critical rise in the availability of atmospheric oxygen (Knoll & Walter, 1992; Campbell & Allen, 2008; Campbell & Squire, 2010).

Both oxygen and a nutrient like phosphorus are, of course, necessary for animal life. An increase in primary production may result from the enrichment of phosphorus or other nutrients that are limiting (Howarth, 1988; Tyrrell, 1999), though neither of these linked directly with an increase in biodiversity (number of species) nor with widespread disparity (the number of phyla) as was embodied by the Cambrian Explosion. Contrary to this, there may be a decrease in biodiversity when the continents are assembling, according to the model of Valentine & Morris (1970). Also, the worldwide deposition of phosphate during the Ediacaran-Cambrian might aid in the preservation of fossils at this time, such as the phosphatised biotas from the Ediacaran of South China and the Terreneuvian small shelly fossils around the world (Meert & Lieberman, 2008). It the case of oxygen it is more complicated (see below). Amalgamation and fragmentation are not unique to Precambrian-Cambrian transition (Dalziel, 1997), and there is no evidence that the oceanic concentration of phosphorus in the Neoproterozoic is insufficient for the diversification of animals. The assembly of Gondwana, therefore, provides a tectonic backup (Meert & Lieberman, 2008), and it alone cannot be a driving force in the Cambrian Explosion. A study of the dissolved marine concentrations of phosphate suggested, on the contrary, the concentrations of phosphate were significantly higher than the levels in the Cambrian (Planavsky et al., 2010). 

Snowball Earth – the aftermath

It is indicated by increasing evidence that the climate of the Earth was extremely cold during the Neoproterozoic with the result that there were 2 or 3 episodes of global glaciations with ice sheets extending to equatorial latitudes, i.e. Snowball Earth (Kirschvink, 1992; Hoffman et al., 1998; Hoffman & Schrag, 2002). The duration of Snowball Earth has been constrained to between780 Ma and 635 Ma, during which there were 2 warmer periods of interglacials. For the biological world the Snowball Earth was catastrophic, causing biological productivity in the ocean surface waters to collapse for millions of years (Hoffman et al., 1998), though it is suggested by Zhang et al. to possibly have had a role in triggering the evolutionary bursts that followed (Fedonkin, 2003). Many researchers have argued, however, that ultimately it resulted in significant bursts of biological evolution, such as the Ediacaran radiation and Cambrian Explosion (Kirschvink, 1992; Hoffman et al., 1998; Maruyama & Santosh, 2008; Planavsky et al., 2020; Papineau, 2010). Again, Snowball Earth is tied to biological evolution by the nutrient phosphorus and oxygen. Erosion and high rates of chemical weathering during the retreat of the ice sheets has been argued to have led to higher delivery of riverine phosphorus to seawater, and this would have increased rates of primary productivity and burial of carbon that produced significant quantities of atmospheric oxygen. This resulted in the accumulation of atmospheric oxygen that paved the way to macroscopic air-breathing organisms and led to the emergence of animals in the Neoproterozoic-Cambrian interval (Planavsky et al., 2020; Papineau, 2010).

The harsh and fluctuating abiotic conditions, on the other hand, such as the Snowball Earth, may have temporarily increased the degree of altruism that was adaptive, which promoted an increasing degree of terminal (irreversible) differentiation. It is believed that this is of particular relevance to multicellularity of animals as a result of irreversible differentiation, (which is highly altruistic as it imposes a high fitness cost of the individual cell) is more prevalent than in other multicellular eukaryotes (Boyler et al., 2007). Also, Snowball Earth may increase genetic diversity expressed by animals as a result of the effect of extreme climatic stress on heat shock protein 90 (HSP90), which results in mutant signal transduction proteins, that were pre-existing, and developmental pathways were expressed in animals (Baker, 2006). It seems that up to now the aftermath of the Snowball Earth on biological radiation become increasingly evident, though it remains hard to see how fundamentally new levels of developmental and morphological organisation could result from a cold catastrophe (Marshall, 2006).

The Snowball Earth ended at 635 Ma, however, about 100 Myr before the beginning of the Cambrian Explosion. During this 100 Myr what happened with the surface environment of the Earth may be a crucial point. From the Ediacaran to Early Cambrian the steep rise in seawater ⁸⁷Sr/⁸⁶Sr is attributed to elevated weathering rates, which could have led to increased availability of nutrients, organic burial and to the further oxygenation of the surface environments (e.g. Shields, 2007). Following the end of Snowball Earth the evolution of complex macroscopic multicellular organisms, as revealed by the Early Ediacaran Lantian biota (Yuan et al., 2011) that is resent immediately above the Marinoan glaciation of age, and many more Late Ediacaran macrobiotas following the Gaskiers (McCall, 2006; Fedonkin et al., 2007). In terms of the Cambrian Explosion it is, possibly, the continued post-glacial rise of atmospheric oxygen concentration that paved the way for the later animal diversification during the Early Cambrian.

True polar wander

Palaeomagnetic data that imply anomalously high rates of apparent plate motion that characterise the Ediacaran-Cambrian interval, the rotation or translation rates for each palaeocontinents equivalent to or exceeding 10-20 cm/year (See Mitchell et al., 2011, and references), which is in marked contrast to continental movement rates of a few centimetres/year that are more typical (Meert et al., 1993). The true polar wander (TPW) was, therefore, invoked in order to explain the rapid motion of the palaeocontinents during the transition from the Ediacaran to the Cambrian (Kirschvink et al., 1997; Evans, 1998, 2003). An episode of true polar wander which occurred during the Cambrian Explosion of animal life has been suggested (Mitchell et al., 2010). It has been argued (Kirschvink et al., 1997) that wholesale rotation of the lithosphere was likely to have brought about major changes in the circulation of the ocean and, therefore, regional climates, and repeated reorganisations of the global climatic patterns during a TPW event which would have fragmented any large scale ecosystems that had been established, and so generating smaller populations that were more isolated, and this would lead to a higher rates of evolutionary branching among existing groups. A more explicit relationship between a succession of TPW events and the Cambrian Explosion was proposed (Kirschvink & Raub, 2003). According to the argument:

1)    Tropical continental margins and shelf slopes which form as a result of the fragmentation of Rodinia accumulated huge quantities of organic carbon during the Late Neoproterozoic ;

2)    An initial phase of Ediacaran TPW moved these deposits to high latitudes, where these, as well as other additional added organic material were trapped as methane hydrate or permafrost and stabilised until the geothermal gradient moved them out of the clathrate stability field;

3)    A burst of TPW brought these deposits back to the tropics, where they gradually warmed and released to the atmosphere, and therefore induced pulses of global warming.

As the surface temperature of the Earth correlates powerfully with biodiversity, it was suggested (Kirschvink & Raub, 2003) that global warming could have been the driver of the Cambrian explosion that was forced by the decomposition of methane clathrate, which had been induced by an inertial interchange true polar wander event. This hypothesis, as had been noted (Marshall, 2006), did not offer an explanation as to why an increase in biodiversity, per se, should have led to new levels of disparity. Also, the global warming that occurred during the Early Cambrian is not currently supported by geological or geomechanical data, regardless of the likelihood that the methane hydrates were brought from high latitudes to the tropical latitudes without collapse. Also, diversification resulting from physical stress might be suppressed by rapid fluctuations of climate. The finding that the TPW hypothesis contradicts phylogenetic analyses of biogeography from the Early Cambrian is the other problem. Well established endemism is shown by faunas of the Early Cambrian (Lieberman, 2002), which is not likely to have arisen in the rapidly changing geography that is required by the TPW hypothesis (Meert & Lieberman, 2004, 2008).

Seawater composition

Salinity, an environmental factor, is of considerable importance for organisms, as it controls and limits the nature of biological activity. The solubility of atmospheric gases, especially oxygen, is strongly affected by salinity. Therefore, the history of the salinity of seawater is crucial for the evolution of life. It has been estimated that the initial salinity of the oceans was 1.5-2.0 times (52.5-70‰) that of the value of the modern ocean, which is ~35‰, or possibly higher, the salinity declined significantly only after the latest Neoproterozoic when giant evaporite basins sequestered huge amounts of salt and brine (Knauth, 1998, 2005). Salinity of 50‰ is the limit above which most forms of macroscopic life, which includes metazoans, cannot tolerate salinities as a result of the high osmolarity in hypersaline conditions that can be deleterious to cells as water is lost to the external medium until the achievement of osmotic equilibrium. It has been speculated (Knauth, 1998, 2005) that the delayed decline in salinity of the ocean may have been a factor in the Cambrian explosion of life. The modelling of ocean salinity, which was developed by using the maximal and minimal estimates of the volumes of existing evaporite deposits, and the use of constant and declining volumes of ocean water through the Phanerozoic, is also suggestive of a major decline in salinity from the Neoproterozoic to the Cambrian (Hay et al., 2006). The salt deposits of the Hormuz region cannot, however, be dated precisely, and the decline that is apparent prior to the Cambrian may be an artefact of the lack of better information (Hay et al., 2006). Also, Zhang et al. suggest that the high salinity hypothesis is challenged by the abundant, diverse eukaryotic life in the Neoproterozoic.

It is indicated, on the other hand, by analyses of primary fluid inclusions from marine halites that date to the terminal Proterozoic (about 544 Ma) and Early Cambrian (about 515 Ma) that CA²⁺ concentrations in seawater increased ~3-fold during the Early Cambrian (Brennan et al., 2004; Berner, 2004). Also, it was indicated by an experimental study of sponge cells that the concentration of CA²⁺ could increase binding forces between their calcium-dependant cell adhesion molecules. Zhang et al. suggest that this, as well as the advent of self-/non-self-recognition systems, that are assumed to have evolved gradually prior to the Cambrian, could have made possible the rise of the animals. It was proposed, therefore, that the coincidence in time of primitive animals that were endowed with self-/non-self-recognition and a surge in seawater calcium during the Early Cambrian triggered the Cambrian explosion (Fernàndez-Busquets et al., 2009). Rapid increase in Ca²⁺ in the seas of the Early Cambrian was accompanied by a decrease in concentrations of sulphate by more than 2-fold (Brennan et al., 2004). This conflicts with the palaeontological data that the intensity of bioturbation increased significantly (McIlroy & Logan, 1999) and matgrounds evolved into mixgrounds (Seilacher, 2007) during the Early Cambrian as a result of sediment mixing by bioturbating organisms resulting in a severalfold increase in sulphate concentration in seawater (Canfield & Farquhar, 2009).

According to Zhang et al. as they were writing this paper a seemingly new hypothesis links the Great Unconformity, which separates continental crystalline basement rock dating to the Precambrian from the much younger Cambrian shallow marine sedimentary deposits in several palaeocontinents, to the Cambrian explosion (Peters & Gaines, 2012). According to this hypothesis, the formation of the Great Unconformity involved the widespread denudation of continents which was followed by extensive reworking of soil, regolith and basement rock, and the enhanced chemical weathering of continental crust during the first marine transgression on a continental scale of the Phanerozoic; these processes would have affected the chemistry of the seawater, such as increases in the concentrations of Ca²⁺ in seawater, and thus triggered biomineralisation in multiple clades, which thereby promoted the Cambrian explosion of marine animals (Peters & Gaines, 2012). A possible mechanism for the increase in concentrations of Ca²⁺ was provided by this hypothesis. Neither the new data of the concentrations of Ca²⁺ is offered, nor is a new explanation of why an increase in the concentration of Ca²⁺ in seawater, per se, should have led to such a major diversification or biomineralisation among metazoans.

Rise of Oxygen levels

It has been proposed for a long time that atmospheric oxygen was a prerequisite for the appearance of animal life in the fossil record (Nursall, 1959; Canfield & Teske, 1996). Increasing levels of atmospheric oxygen have, therefore, been implicated in the marine faunas in the late Precambrian-Cambrian (Cloud, 1976; Runnegar, 1982a, b; McMenamin & McMenamin, 1990: Gilbert, 1996; Canfield et al., 2007). Oxygen is essential for maintaining many metabolic and physiological processes in metazoans, which allows for the effective aerobic respiration, mobility, increase in body size, skeletonisation, and collagen synthesis (in metazoans, holding cells together) and Cholesterin, which makes the cell membranes more rigid. Accumulative levels of toxic reactive species of oxygen (ROS), however, can be dangerous for all organisms. Animals have evolved sophisticated mechanisms in order to cope with ROS which they used for defence (Decker & van Holde, 2011). Of the defensive strategies used 2 are mentioned here.

1)    Cell aggregation, with surface cells protecting interior members from ROS. It is likely, therefore, that the protection against ROS is one of the driving forces in evolution that drove cells towards multicellularity in which oxygen plays a part that is an even larger role in evolution than has been previously been suspected.

2)    Melanisation, which Zhang et al. have suggested may have occurred on the dermal cells of primitive metazoans. It could offer protection and could possibly have formed a defensive cuticle against predation.

The way was open for almost infinite pathways of development of special organs, functions and diversity of animals (Decker & van Holde, 2011), once the principle of specialisation of cells was established. Also, it was proposed that the prevailing concentrations atmospheric oxygen may have had a role in the evolution of mechanisms for sensing oxygen (Tayler & McElwain, 2010), which is mediated by hypoxia inducible factor (HIF) and acted by prolyl hydroxylases (PHDs). It has been found that the HIF/PHD system was not present in choanoflagellates or other protists, which suggests that it is unique to metazoans (Leonarz et al., 2011; Rytkönen & Storz, 2011). It is also possible that increasing levels of oxygen in the atmosphere and oceans could have had an indirect effect on biological innovation by increasing the availability of trace elements that are bioessential (Ambar & Knoll, 2002).

The major problem with the suggestion of rising levels being an environmental trigger for the Cambrian explosion is the lack of precise values of oxygen levels prior to and during the diversification of animal phyla. Over the last 25 years geochemical evidence of the rising levels of oxygen during the Late Neoproterozoic has been accumulating, though it remains difficult to distinguish atmospheric from oceanic and global from local redox changes (Shields-Zhou & Och, 2011). It was argued (Canfield & Teske, 1996) that according to sulphur isotope discrimination values the level of oxygen rose above 5% of the present atmospheric level (PAL) during the Precambrian-Cambrian transition. Though it is still difficult to determine if the increase in Δ³⁴S is related to higher oxygen levels or instead to intensive bioturbation (Canfield & Farquhar, 2009). It is shown by the iron content of sediments that shallow waters were typically well oxygenated throughout the later Neoproterozoic (<742 ± 6 Ma) (Canfield et al., 2008), much earlier than the Cambrian explosion, whereas the deep ocean was anoxic and ferruginous prior to and during the Gaskiers Glaciation 580 Ma and that after this glaciation, it became oxic (Canfield et al., 2007; Liet et al., 2010). A very late oxygenation of deep seas was suggested by a recent study, since Cambrian Stage 3 (Wang et al., 2012). Oxygen levels higher than 15% of PAL are required to oxygenate deep sea (Canfield et al., 2007), though persistent anoxia in the oceans in the Neoproterozoic is argued to require levels of oxygen below 40% of PAL (Canfield et al., 2005; Kump, 2008). The atmospheric oxygen level was, therefore, constrained between 15% and 40% of PAL by the Late Ediacaran. Such an estimation that is based on uniformitarian principles was, however, questioned (Butterfield, 2009). He argued that the oceans of the Precambrian, which were stratified, had a turbid anoxic water column dominated by cyanobacteria, differed from their counterparts of the Phanerozoic, that were well-mixed, with a clear-water system that was dominated by eukaryotic algae), and therefore deep sea geochemical signatures were not able to be used as a direct proxy for atmospheric oxygen levels under such no nonuniformitarian conditions (Butterfield, 2009).

Erosion of the supermountains of Gondwana was suggested to have formed more free oxygen than earlier supercontinent amalgamations as a result of the maximum height of the Gondwanan supermountains being greater (Campbell & Squire, 2010). In the Early Cambrian the advent of large, mobile and skeletal animals may have been contemporaneous with the increased oxygenation of the surface environment (Shields-Zhou & Och, 2011), though there is a geochemical study that shows that the oxygen content declined significantly during the Early Cambrian (Komiya et al., 2008). The minimum oxygen requirements for metazoans to support their aerobic metabolism, on the other hand, are constrained loosely. It has been suggested (Catling et al., 2005) that there was quite a broad range from 5% to 50% PAL. The absolute minimum oxygen content that can support metazoans varies between species, and is probably impossible to know for the first animals of diverse metazoan phyla. Extant marine infaunal and epifaunal metazoans are capable of accommodating dissolved oxygen concentration decreasing to the 10s of micromolar. They correspond to ~25% PAL, if these concentrations are extrapolated to equilibrium of the atmosphere with surface water that is cold and well-mixed. However, it is not known when oxygen rose above this level, and geochemical evidence is not known of for a stepwise rise of oxygen levels that correspond to the episodic appearances of bilaterian clades during the Early Cambrian. Also, it needs to be known when a given level of oxygen might select for a given type of physiology or morphology and whether such effects might affect morphological origins, ancestral form, etc. It is difficult, therefore, to determine whether oxygen is a key threshold that must be crossed for the Cambrian explosion to occur.

According to Zhang et al. they are sure that oxygen has an important role in the development of complex, multicellular organisms. Though the widespread distribution of anaerobic chemistry and anaerobic mitochondria, mitochondria that are not dependant on the final mediator of a transfer of an electron to O₂, in most eukaryotic supergroups, which includes the Metazoa, combined with the presence of enzymes that have clear evolutionary links to an anaerobic past, suggests that the ancestors of eukaryotes evolved in a past that was more anoxic (See van der Giezen and Lenton, 2012 and references therein). It has been found that many extant animals are facultative anaerobes, having the ability to live in hypoxic or anoxic conditions (Budd, 2008). Some loriciferans have been found living in conditions that are permanently anoxic, such as sediments (Danovaro et al., 2010). The claim that increasing levels of oxygen were a prerequisite for the evolution of animals is undermined somewhat by the widespread anaerobic pathways across metazoan phylogeny (Mentel & Martin, 2010).

Developmental genes and molecular clock

Large gene regulatory networks (GRNs) control the development of the animal body plan, and evolution of the body plan depends on the architecture of developmental GRNs over deep time (Davidson & Erwin, 2006); Davidson, 2010).

The composition and structural organisation of the GRNs and, therefore, their functions and evolutionary changes are fundamental genetic issues to understand their development and evolutionary and evolution of animals (Carroll et al., 2001; Davidson & Erwin, 2006, 2009; Davidson, 2010). In this context, with regard to the Cambrian explosion, the key questions are which developmental genes define ancestral bilaterians and whether the genes responsible for building morphological complexity of bilaterian clades were in place prior to and during the Cambrian explosion. What accounts for the great differences between major metazoan linages and the long prod of stasis in phylum- and class-level body plans since the Early Cambrians, if the development systems of bilaterians were established prior to their divergence in the Early Cambrian?

Deep or shallow divergence

It has been found that the developmental genes were established prior to the divergence of bilaterian clades. The finding that many developmental bilaterian genes are present in simpler organisms that are morphologically simple reinforces the suggestion that the original role of these genes and regulatory networks was in the formation of specialised cell types in specific body regions, though not necessarily in the production of complex morphology (Erwin & Davidson, 2002). The advent of developmental genes was, therefore, a component that was a necessary, though not sufficient, component of the Cambrian radiation of bilaterian lineages (Erwin et al., 2011). What then is the genetic basis that underlies the morphological diversification of bilaterian forms? According to Zhang et al. the key issue is in the timing and level of gene expression.

It is suggested by the earliest use of haemoglobins to arrive at molecular estimates that the initial radiation of the animal phyla occurred at least 900 Ma – 1.0 Ga (Runnegar, 1982c). Subsequent estimates of the times of metazoan divergence that were based on molecular clock vary as new studies have been reported, ranging from several hundred million years prior to the Cambrian explosion to close to the base of the Cambrian (see Blair, 2009 for a complete review). According to Zhang et al. it was believed that some of the younger dates had been affected by severe methodical biases (Blair, 2009). It was suggested by the most recent dating study (Erwin et al., 2011) that the common ancestor of all metazoans arose about 800 Ma,, the split between the deuterostomes and protostomes occurred at around 680 Ma, and stem lineages leading to most extant bilaterian clades had evolved by the close of the Ediacaran. Most crown group bilaterian phyla were estimated, however, to have diverged during the later Ediacaran through to the Cambrian, which is largely consistent with the fossil record (Erwin et al., 2011). It is also indicated by the phylogenetic distribution of different oxygen transport proteins (OTPs) (haemocyanin, globin and haemerythrin), which is a prerequisite for the development of shells and hard carapace, also indicates that there was an early divergence of bilaterian clades, with OPTs evolving before the appearance of shelly fossils, though following the divergence of phyla (Decker & van Holde, 2011). The molluscan haemocyanin evolved 700 Ma, or possibly earlier, and it was estimated that the origin of arthropod haemocyanin was between 600 and 700 Ma.

The deep divergence of bilaterian phyla, at least in stem lineages, has been supported by a majority of molecular clock studies, though it is suffering from a couple of challenges:

1)    The cold climate during the Late Cryogenian was not favourable for the diversification of animals,

2)    It remains unclear whether oxygen content was sufficiently high for the bilaterians by the Cryogenian.

The paucity of fossils of bilaterians in this period is the greatest challenge, with bilaterians being completely absent prior to the Gaskiers Glaciation. Possible animal embryo fossils from the Doushantou Formation, which dated to the Ediacaran, have been reinterpreted recently as non-metazoan Holozoa (Butterfield, 2011; Huldtgren et al., 2011). Zhang et al. suggest that most putative metazoans from biotas of Ediacaran type are very likely to be within the scope of cnidarian-grade organisms below the split of the protostomes and the deuterostomes (Erwin, 2009), with the exception of Kimberellomorpha, which could possibly be molluscans commonly associated with radiating trace fossils (Fedonkin, 2003). It has been accepted widely that trace fossils are strong evidence for the presence of bilaterian animals in the Ediacaran, whereas the bilaterian nature of early trace fossils has been questioned by the finding that large amoeboid protists leave macroscopic traces at the bottom of the deep ocean (Matz et al., 2008). The earliest putative evidence of bioturbation by bilaterians that is known of dates to ~555 Ma. The Kimberellomorpha is the only body fossil that is relatively convincing, which is coeval with the earliest-known bioturbation. However, according to Zhang et al. a small group makes neither diversity nor disparity. That early bilaterians were small, soft-bodied animals, and therefore were not often fossilised, is the explanation that has been most commonly attempted, though microscopic fossils of protists and prokaryotes have been recognised as early as the Archaean and Lagerstätten of macroscopic soft-bodied fossils have been known of that dated to the Ediacaran. It is also possible that the early bilaterians were not significant ecologically, and were therefore quite rare. The deep divergence of bilaterians can only be testified to by the discovery of diverse body fossils prior to and during the Ediacaran.

Many of the genes and subcircuits of the GRNs underlying the building of body plans may, alternatively, remained untapped over millions of years. Phyla of basal metazoans diverged morphologically during the Late Ediacaran and the phyla of bilaterians diverged in the Early Cambrian, as indicated in the fossil record (Shu et al., 2014-in this issue). The genetic makeup of Urbilateria is complex, though they were small and morphologically simple. A minority of molecular studies do, however, support the shallow divergence model. Possibly, oxygen levels as well as other environmental factors, such as the concentration of Ca²⁺ in seawater, until they crossed a critical threshold in the Early Cambrian and favourable ecosystems were well established, which therefore caused a widespread biomineralisation and increase in morphological complexity, body size, diversity, and disparity among bilaterian lineages. This model is, approximately, reconciled by palaeontological data, though it is still rare to find unequivocal body fossils of metazoans in deposits from the Ediacaran. This view is also challenged by animals from the Early Cambrian that were considerably diverse and had morphology that was complex. According to Zhang et al. it is hard to imagine all of these arising from a single ancestral form in the brief period from about 550-520 Ma.

The bilaterian developmental GRNs were established prior to the diversification of body plans. Once Kimberella was accepted as a true bilaterian, then the establishment of developmental systems predated the Cambrian explosion by at least 10 Ma. Though the developmental system, which enabled the divergence of the bilaterian body plans, is a prerequisite, it is not sufficient for the Cambrian explosion (Marshall, 2006; Erwin et al., 2011). If the invention of toolkit genes per se was not the trigger for the Cambrian explosion, then what was? According to Zhang et al. it is being increasingly appreciated that the Cambrian explosion was an ecological phenomenon and environmental triggers indispensable.

Ecological causes

The case for ecological explanations is now increasing, since environmental changes at the close of the Proterozoic and opening of the Phanerozoic form the essential backdrop of the Cambrian explosion, and it is very likely the genetic complexity was established long before the construction of an ecosystem that was dominated by metazoans (see discussion above), (Carroll, 2005; Conway Morris, 2006; Budd, 2008; Erwin et al., 2011; Erwin & Tweedt, 2012). The Cambrian explosion is seen by many as an ecological phenomenon, which consisted to a large extent on a cascade of knock-on events that emerged from multicellularity and mobility (E.g. Budd, 2008). Following the appearance of the first animals the interactions between different types of organisms as well as with environments would lead to ecologies that more were complex. The complex ecologies were subject to continuing expansion and feedback, and this resulted in the evolution of metazoan-dominated ecosystems since the Early Cambrian (Conway Morris, 2006). Of the many ecological hypotheses that have been proposed as drivers, none of them is able to satisfy geological, palaeontological and molecular records. While some theories are well-suited to explaining why there was a rapid increase in diversity and disparity, they fail to explain why the “explosion” happened when it did (Marshall, 2006). Some have even considered consequences as causes, e.g. increase of bioturbation and the advent of macrophageous predators, thereby falling into the trap chicken-egg problem.

Extinction of Ediacaran biotas

The most significant episodes of adaptive radiation in the history of metazoan evolution have often been preceded by mass extinction events. Ecologically dominant species can be removed by extinction events and thereby makes the resources the removed species had previously utilised making them available to surviving species. Following mass extinction events many clades diversified rapidly, the most famous case being the diversification of many mammal and bird clades following the end Cretaceous extinction event (Losos, 2010). Therefore extinction of Ediacaran macrobiotas (Narbonne, 2005) and Cloudina-Namacalathus assemblage (Amthor, 2003) could open up new possibilities for metazoans, as was the case with the dinosaurs, which opened the way for mammal and bird clades (Knoll & Carroll, 1999; Amthor et al., 2003). However, as has been noted (Marshall et al., 2006; Erwin et al., 2011), standard models of radiation involved diversification for clades that were pre-existing, e.g. the evolution of land vertebrates, and is not able to explain the polyphyletic nature, morphological and ecological breadth, or the extended duration of the Cambrian explosion.

Cropping

This ecological theory was developed by Stanley (1973, 1976). It argued that in terms of diversification, pre-Cambrian systems were self-limiting, because systems in the absence of cropping by herbivores; when advanced heterotrophy arose it would initiate systems of diversification that were self-propagating; therefore, the almost simultaneous origin and explosive radiations of heterotrophic protists, metaphytes and metazoans were inevitable. The increases in diversity under the influence of cropping could be explained by this theory, though it was not directed against the uniqueness of the Cambrian explosion in terms of timing and nature. The Cambrian explosion is far more than the increase in biodiversity. Also, the evolution of heterotrophic protists began much earlier (Porter, 2011), and herbivorous metazoan fossils, such as Kimberella were present in biotas of the Ediacaran about 555 Ma. The question is what delayed the occurrence of bilaterian clades.

Phytoplankton-zooplankton diversification

In modern marine ecosystems the vast majority of production is comprised of phytoplankton. Very few large animals are capable of grazing on even relatively large net phytoplankton (2-200 μm). The microscopic world of marine primary productivity is linked to the macroscopic world of large animals by zooplankton which repackage unicellular phytoplankton as particles that are rich in nutrients some 10-100 times as large. Repackaging by herbivorous mezozooplankton (0.2-20 mm) represents a key link in marine metazoan food chains (Butterfield, 1997, 2001). In the Early Cambrian the phytoplankton (acritach) underwent a major diversification, which is in marked parallel with the Cambrian radiation of metazoans. Oceans would have been dominated by picoplankton (0.2-μm) prior to the evolution of planktic metazoans (Butterfield, 2009). The diversification of zooplankton might have been stimulated by this sudden diversification, which in turn might stimulate the evolution of large metazoans through food supply. The ecological significance of zooplankton during the Early Cambrian is not clear, however, because of the sparseness of zooplankton fossils of this age (Butterfield, 1997, 2001; Vannier et al., 2007). In addition, the diversification of acritachs, as a component of the Cambrian explosion, may also require a trigger. It has been suggested that the expansion of animals into the water column in the Early Cambrian might have been responsible for driving the evolution of large net-phytoplankton (Butterfield, 2009). So a chicken-egg problem arises. Was the evolution of zooplankton caused by the diversification of phytoplankton, which in turn stimulated the radiation of animals? Alternatively, was the increase of net-phytoplankton in size and diversity caused by the ecological expansion of planktic metazoans? According to Zhang et al., at this point they adopt a simpler solution, considering the diversification of phytoplankton as a consequence, rather than the cause of the Cambrian explosion.

Bioturbation

The Cambrian explosion is manifested by explosive radiation of bilaterian phyla in the Early Cambrian, as well as substrate revolution during the Ediacaran-Cambrian transition, which was the result of advents of burrowing bioturbation into the sediment depths (Seilacher & Pflüger, 1994; Bottjer et al., 2000). Therefore it was assumed that bioturbation had a key role in the evolution of early metazoan life (Meysman et al., 2006). Microbial mats that were well-developed with poorly developed vertically oriented bioturbation were characteristic of the seafloor of the Ediacaran. The substrates that were mat-bound (aka matgrounds) produced a stable, sharp water-sediment interface that had little interaction with bottom water. The seafloor sediments of the Early Cambrian, referred to as mixgrounds, were bioturbated heavily by burrowing organisms, which resulted in sediment ventilation, and changes in redox gradients. It was suggested (Bottjer et al., 2000) that substrate revolution had significant evolutionary and ecological impact. It was assumed, accordingly, that benthic faunas needed to adapt to the bioturbated mixgrounds that were newly emerging, thereby triggering the Cambrian explosion (Thayer, 1979; Bottjer et al., 2000; Meysman et al., 2006). In contrast to this, it was also suggested that the infaunal habits were a strategy to escape the menace of predation that had evolved (Seilacher, 2007). Zhang et al. suggest that the effect of bioturbation would have been profound (Thayer, 1979; Meysman et al., 2006; Erwin & Tweedt, 2012). However, infaunal bioturbators were required by the substrate revolution to destruct the matgrounds, with the result that the chicken and egg problem arises again (Levinto, 2001). The question then arises was the Cambrian explosion caused by substrate revolution or did the substrate revolution drive diversification of bilaterian clades, including the bioturbators? Zhang et al. suggest it is evident that the advent of bilaterian bioturbators is a consequence rather than a cause.

Advent of macrophageous predation

The most commonly proposed ecological trigger of the Cambrian explosion is the predator-prey pressure (Evans, 1912; Hutchinson, 1961; Vermeij, 1990; Bengtson, 2002; Peterson et al., 2005: Erwin et al., 2011. A rapid increase in body size by natural selection would result from the rise of predation, and novel defensive mechanism such as biomineralisation to form shells, or developing new structures or capabilities that allowed movement into new habitats (Levinton, 2001; Erwin et al., 2011). In the Middle Neoproterozoic the rise of macrophageous single-celled organisms might have led to the appearance of biomineralisation of skeletons in protists about 750 Ma (Porter, 2011), though according to Zhang et al. it did not trigger the widespread biomineralisation in metazoans, most likely because animals had not evolved by this time. It appears reasonable to assume the advent of macrophagous predators near the end of the Neoproterozoic, therefore, stimulated the spectacular radiation of animals (Peterson et al., 2005), while the fossil evidence for the presence of macrophagous predators is not certain. Cloudina, a skeletonised tubular fossil,                                                                                                                                                                                           from the Ediacaran, preserved boring holes which were considered to be predatory traces (Bengtson & Yue, 1992; Bengtson, 2002; Hua et al., 2003), though they are also likely to have been nonpredatory in origin, as there are many microbial borers that are capable of drilling holes. Body fossils that are thought likely to be macrophagous predators first appeared in the fossil record in the Early Cambrian. The first appearance of protoconodonts in the Fortunian Stage (Kouchinsky et al., 2012), were interpreted as teeth and grasping spines of chaetognaths (Szaniawski, 2002), and therefore represented the earliest known candidates for bilaterian predators. The first appearance of definite large predators, such as anomalocarids, was in Cambrian Stage 3, about 520 Ma, which postdates significantly the biomineralisation of the metazoans. There is currently no known evidence for macrophagous predators earlier than the Early Cambrian. Again, the advent of macrophagous predators still requires a trigger. It is reasonable to assume that their invasion lagged, as predators stand high above the primary producers in trophic level. It is apparent that predator-prey relationships are an essential component of the Cambrian explosion, though not an ecological trigger.

Roughening of fitness landscapes

The concept of fitness landscapes from genetics to the morphogenesis is applied by this hypothesis (Marshall, 2003, 2006). It has been demonstrated by computer simulations that the roughening of fitness landscapes could lead to increases in diversity and disparity of land plants, and not necessarily requiring new developmental genes (Niklas, 2004). The number of needs the organism must satisfy controls the roughness (Niklas, 1994, 1997, 2004), rather than the degree of interaction between the genes, as is the case of genetic fitness landscapes (Kauffman, 1993). The needs of the organisms are, however, often frustrated, which leads to conflicting solutions, so that the overall design for an organism is not often achieved (the principle of frustration) (Marshall, 2006). It is the degree of frustration, therefore, that determines the roughness of the fitness landscape (corresponding to diversity and disparity), i.e., as the number of frustrated needs is increasing the fitness of the landscapes are roughening. There were very few bilaterians in the biotas of the Ediacaran, which shows fitness landscapes that are rather smooth (Marshall, 2006). The faunas of the Early Cambrian, on the contrary, contained about 20 bilaterian body plans, which show very rough landscapes (Marshall, 2006). It was accordingly suggested (Marshall, 2006) that roughening was the primary driver of the Cambrian explosion. This theory depicted nicely the Ediacaran-Cambrian evolutionary transition, as well as providing a good explanation of the diversification of body plans without invoking the invention of toolkit genes. However, it invoked the ecological interactions between organisms, especially the arms race (predation pressure) as a roughening mechanism, which stated ”There were myriad predators to contend with, and a myriad number of ways to avoid them, which in turn led to more specialised ways of predation as different species developed different avoidance strategies, etc.” This hypothesis therefore suffers from the same problem as the predator-prey hypothesis (see above). Simply, in the Early Cambrian the roughening of fitness landscapes is a consequence of evolution.

Geosphere-biosphere feedbacks

According to this hypothesis, this is based on an Earth system model for the long-term carbon cycle by introducing 3 different types of biosphere: prokaryotes, eukaryotes, and complex multicellular life, each of which is characterised by different global temperature tolerance windows. The nonlinear feedback between productivity that is temperature dependent of multicellular life and their biotic enhancement of silicate weathering could lead to the drops in temperature to the optimum value of 15^oC for complex multicellular life productivity by about 540 Ma. It was assumed, therefore, that an earlier appearance of complex life could have been initiated by the Neoproterozoic Snowball Earth events and that the Cambrian explosion might have been mainly driven by extrinsic environmental causes, i.e., cooling of the Earth that was gradual (von Bloh et al., 2003). It appears this hypothesis did not touch the essence of the Cambrian explosion. Also, no geological evidence has been found of this cooling event. There is at least 1 study which suggested that the surface temperature of the Earth declined dramatically in the Paleoproterozoic reaching values similar to those of the Phanerozoic by 1.2 Ga (Knauth, 2005).

Ecosystem engineering

This refers to the modification of the abiotic environment by aspects that affect strongly other organisms by forming, modifying or destroying the niches of other species (Jones et al., 1994, 1997; Wright & Jones, 2006; Erwin & Tweedt, 2012). Organisms that engineer ecosystems interact nonlinearly and generate positive feedbacks that enhance diversity (Altieri et al., 2010). The role of positive ecological feedbacks during the Ediacaran-Cambrian transition based on the first appearance of genetic diversity patterns of various metazoan clades, was analysed (Erwin & Tweedt, 2012) and the results of this analysis revealed that during the Early Cambrian the feedback increased substantially, principally through bioturbation (ventilating the sediment), pumping by sponges (modifying the chemical condition of the water column) and the appearance of a number of structural engineers, such as archaeocyathid reefs (enhancing the complexity of the habitat). They suggested, therefore, that the ecological expansion during the Early Cambrian was driven, in part, at least, by ecosystem engineering (Erwin et al., 2011; Erwin & Tweedt, 2012). As they noted, at present it is difficult to determine whether the expansion of ecosystem engineering was merely a component of the establishment of marine ecosystems dominated by metazoans or it was a significant driver of this event (Erwin & Tweedt, 2012). Also, in the Early Cambrian infaunas as well as epifaunas were involved in the Cambrian explosion. The increase of bioturbation and the appearance of archaeocyathid structure engineers are better understood as consequences of the Cambrian explosion. Zhang et al. agree with Erwin & Tweedt (2012) that during the Ediacaran ecosystem engineering, in spite of the small degree, might be crucial for the Cambrian Explosion, in particular, engineering effects of sponges because they definitely appeared in the Ediacaran (Gehling & Rigby, 1996; Clites et al., 2012). Sponge fossils from the Ediacaran are, however, actually rare. Therefore, their engineering effects are somewhat speculative as the ecological feedbacks require abundance.

Conclusions

It is suggested by the fossil record and molecular results that the basic developmental system of bilaterian animals was in place in the Urbilateria at least 555 Ma, regardless of whether the Urbilateria had a simple or complex morphology. The GRNs that are responsible for controlling the development of an animal are shared widely among metazoan linages. Zhang et al. suggest the assembly, reassembly, and redeployment of subcircuits of the GRNs are responsible for the morphological diversification of bilaterian clades. The Cambrian explosion still requires environmental triggers as the developmental prerequisites were already present in the ancestral taxon (Gould, 2002). The most common environmental triggers that have been proposed are the oxygenation and change in the composition of seawater, particularly the oxygenation, as it allows the most components of the Cambrian explosion, such as body size increase, widespread biomineralisation, and ecological strategies that are metabolically expensive, such as burrowing and predation. The explosive diversification of complex multicellular organisms as exhibited by the macrobiotas of the Early Ediacaran and the subsequent stepwise increase of atmospheric oxygen levels that linked to the weathering of the trans-Gondwana Mountains that finally caused the Cambrian explosion. The seawater composition change, e.g. the increase in concentration of Ca²⁺, may also contribute to widespread biomineralisation in lineages of the metazoans. The Cambrian explosion itself, at least partially, is an expansion of lineages of bilaterians; therefore, the ecological events that were initiated by this event cannot be invoked as ecological triggers. The positive feedbacks of ecosystems of the Ediacaran, particularly by the sponge engineering, may have contributed to the formation of the well-mixed, clear water system that was typical of the oceans in the Phanerozoic, and thereby paved the way for the Cambrian explosion. But the potential feedback of sponges has been challenged by the rarity of sponge fossils in the Ediacaran. According to Zhang et al. the Cambrian explosion may have been triggered by environmental perturbation near the boundary between the Ediacaran and Cambrian, and subsequent amplification by ecological interactions within the reorganised ecosystems (Knoll & Carroll, 1999).

Outlook for future research

Zhang et al. suggest that if the Cambrian explosion was ecological expansion of bilaterian clades, some of the bilaterian ancestral groups, including Urbilateria, may have already been in existence at least in the Late Ediacaran, regardless of deep or shallow divergence. Analogy with the evolution of vertebrates can make this inference: birds and mammals became ecologically significant since the Cainozoic, though their ancestors appeared in the Triassic and Jurassic. Ancestral forms of the faunas from the Early Cambrian are most likely to be found in exceptional preservations in the Late Ediacaran, even if they were small or soft-bodied. The Lagerstätten of the Burgess Shale type and phosphorous chert deposits are well known for exquisitely preserved soft-bodied fossils and microorganisms they contained. Searching for ancestral forms of faunas in exceptionally preserved fossil beds from the Early Cambrian is a major task of the future palaeontological work of Zhang and his team.

They suggest that environmentally, oxygenation and seawater composition change appear to be more closely relevant to the Cambrian explosion. Precise data is still lacking, however. The increase during the Ediacaran-Cambrian transition was suggested by the tectonic events that were occurring at this period, though it is yet to be confirmed by geochemical studies. It is not clear when the oxygen level crossed the threshold that minimally meets the demand of large animals. Changes in the salinity and concentrations of many important ions (such as Ca, Mg and trace metals) of the oceans during the critical time interval are also working targets for their chemical colleagues.

Sources & References

Zhang, X., et al. (2014). "Triggers for the Cambrian Explosion: Hypotheses and problems." Gondwana Research 25(3): 896-909.