5. Recovery of marine communities

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The sudden appearance of complex marine life in the Cambrian – commonly known as the ‘Cambrian Explosion’ – is the most spectacular and perplexing phenomenon in the whole fossil record. According to one authority:

At the beginning of the Cambrian Period, within a span of a mere 10 million years, all the major groups of complex animal life, all the phyla, appeared. Ten million years may seem like a vast stretch of time: by most criteria it is a lot of time. But consider that nearly 3 billion years had already gone by since life had left its first traces in the fossil record. And consider, too, that no new phyla are known to have originated since the early Cambrian.

Here again we find a familiar pattern, on a truly grand scale: relatively suddenly, the whole spectrum of invertebrate life, including sponges, brachiopods, arthropods (trilobites, chelicerates and crustaceans), mollusks, plus spineless chordates in the same phylum as the vertebrates, burst on the scene, the world over. By the end of the Cambrian we have records for all the major groups of hard-shelled invertebrate organisms, and some evidence that vertebrates had appeared as well.

What could have caused such a proliferation?

Niles Eldredge, Fossils: The Evolution and Extinction of Species, 1991 (p 189).

The creativity represented by this invasion of novelty was so extravagant that there were more phyla in the Cambrian, at the beginning of the animal record, than at any future time. Only one new phylum emerged after the Cambrian; many went extinct. One locality where the conditions for preservation were exceptionally favourable, Chengjiang in South China, has yielded no fewer than 18 phyla.

What is a phylum?

Organisms are classified according to their similarities, the lowest unit of classification being the species. Species comprise individuals that are the most similar to each other. Usually a small morphological gap separates one species from the next closest species. Species that are the most similar to each other are then grouped into genera, genera into families, families into orders, orders into classes, and classes into phyla.

Such a scheme can reasonably be understood to reflect degrees of genealogical relationship. Over time species multiply and diversify. Species that have only recently diverged are therefore more similar to each other than distantly related species. Gaps between the groups increase as one ascends the hierarchy, while the number of groups decreases: classes, for example, differ from each other more than orders do, and phyla differ from each other more than classes do. But the greater the morphological and molecular differences, the more one needs to ensure that solid evidence supports the assumption of genealogical relationship. Otherwise the gaps may be evidence of non-relationship.

The theory of evolution assumes no limit, regardless. When phyla are grouped into kingdoms and kingdoms into domains (eukaryotes, bacteria and archaea), the assumption is that all organisms are related, no matter how different. Eukaryotes comprise all organisms whose cells contain a nucleus, namely the kingdoms animals, plants, fungi and protists. Archaea are ubiquitous single-celled organisms whose architectural distinctiveness was recognised only in 1977. They are radically different from both bacteria and eukaryotes. The ultimate step is to postulate that these three domains arose from an entity called the ‘last universal common ancestor’, or LUCA. Unfortunately, LUCAs, unlike bacteria and archaea, which still play a vitally important role in the biosphere, do not exist, and whether they ever existed is something evolutionary biologists themselves find hard to swallow. The two domains are genetically so different that any such ancestor, to be an ancestor, would have had to have more genes and metabolic capabilities than either of them, a kind of super-cell whose existence would only aggravate the problem of how the LUCA itself evolved into being.

If there is a limit beyond which genealogical relationship ceases to be plausible, where might that be? In most cases, the largest grouping suggestive of common ancestry is the phylum. Within a phylum, organisms are united by a body plan or architectural design that differs fundamentally from the body plans of other phyla. When phyla are grouped with other phyla, the body plan dissolves and one is left with an uninformative generality. Note that not all phyla are so diverse as to include families, orders and classes. A single species may constitute a phylum all by itself if there are no other species with the same body plan.

Invertebrates can be classified into around 35 basic body plans, ignoring extinct phyla. In the context of Darwinian evolution ‘basic body plans’ are not predicted. Darwinian evolution postulates that life starts with minimal complexity and becomes more complex only gradually, whereas, at both the morphological and molecular level, all animals are complex, even those at the beginning of their fossil record. This is because animals move, and locomotion requires a locomotor system (muscles, ligaments, tendons and the like), a nervous system capable of sensing the environment, energy produced by digestive and respiratory systems, an excretory system and (almost invariably) a brain. So far as the fossils allow us to determine, the phyla that have eyes now had eyes then, and some eyes were extremely complex. The stalked eyes of one arthropod consisted of over 2000 lens facets – 2000 images is a lot for a brain to have to put together. The genetic programs that constructed all this complexity were of course no less complex; it is implausible to suppose they could have been the products of mutations haphazardly accumulating one by one.

Furthermore, species diversify over time, as we have noted, and if incremental evolution correctly describes the process, genera, families and so on should appear in the fossil record in the same order as their hierarchical order. Degrees of difference between the various types of organism should start off small and gradually increase. One of the great mysteries of the Cambrian Explosion is that virtually all the animal phyla appear at the beginning of the animal fossil record. As palaeontologist Douglas Erwin put it,

The fossil record suggests that the major pulse of diversification of phyla occurs before that of classes, classes before that of orders, and orders before families. … The higher taxa do not seem to have diverged through an accumulation of lower taxa.

Evolution 41, 1177–1186 (1987)

When, for example, molluscs first appear, they are already split into the classes Gastropoda, Bivalvia and Cephalopoda (represented today by whelks, scallops and octopuses), and the cephalopods already had jet propulsion and eyes (probably camera eyes). Cambrian brachiopods – a type of shellfish – encompassed eight classes: Lingulata, Phoronata, Craniata, Chileata, Obolellata, Kutorginata, Strophomenata and Rhynchonellata. And so with the other phyla. These radical pre-programmed re-organisations within the basic plan must have taken place in the Precambrian. Evolutionary history after the Cambrian was merely variation on already existing themes: the origination of orders and a few further classes within the phyla and of many new species within the already established classes.

Why the Precambrian ocean might have been hostile to animal life

Of course, if we abandon the presupposition of interrelatedness and instead suppose that the body plans were present from the start, what we are left with is the problem of timing. A long stretch of time preceded the Cambrian, during which bacteria, algae and ‘acritarchs’ (unidentifiable plankton) are well attested. Although they eluded fossilisation, animals also must have existed. Ancestors of the Cambrian brachiopods, onychophora, chelicerates, crustaceans, molluscs, cnidarians, comb jellies, echinoderms, graptoloids, flatworms, roundworms, segmented worms, radiolarians, loricifera and chordates, not to mention the phyla that later became extinct, must have existed somewhere and in some form for at least as long as bacteria and algae did.

According to the biblical tradition, the original ocean lay beneath the land (see The antediluvian world). Lakes may have existed at ground level, but since all terrestrial surfaces were destroyed in the Cataclysm, the only aquatic creatures likely to have survived would have been those living at some depth, in the dark. Indeed, a great variety of animals and other organisms still live below the 200 metre-deep photic zone.

Following the Cataclysm, seafloor spreading, and thus the generation of ocean crust, was orders of magnitude faster than now, because heat-producing radioactive elements were more abundant and because their rate of decay was higher. Consequently the seas were much warmer. Some estimates suggest average temperatures in the Archaean were in excess of 60 °C. Submarine volcanism spewed out large volumes of dissolved iron, manganese and sulphur, and made all but the surface layer of the ocean poisonous to animal life. Oxygen generated by photosynthesising cyanobacteria made the surface habitable. Since oxygen solubility decreases with temperature and dissolved iron reacts with oxygen to form insoluble iron oxide, oxygen was prevented from diffusing or circulating downward, so most of it escaped to keep levels high in the atmosphere. Marine animals were probably confined to the poles.

Recolonisation of shallow seas beyond the poles would not have been possible until:
  • the coastal waters were no longer toxic (e.g. because of hydrogen sulphide)
  • oxygen levels at the seafloor were high enough
  • the seas had cooled sufficiently
  • animal stocks had begun to recover and spread out from their cold-water refuges

These conditions developed in the course of the late Proterozoic. Prior to that stage almost the only signs of life on the seafloor were layered microbial mats, called stromatolites. A fossil dating to c. 600 Ma might be a sponge (Yin et al. 2015). Stromatolites became less common as the seas became more oxygenated. Higher in the water column, plankton and microplankton also began to recover. Another fossil dating to c. 600 Ma has been identified as a scyphozoan jellyfish (van Iten et al. 2014).

What appeared next, however, around 570 Ma, was not the Cambrian animals but a strange assortment of soft-bodied multicellular organisms known as the Ediacaran Biota. They occur at this time in many parts of the world, from the Ediacara Hills of Australia to Charnwood Forest in England, initially in deep-water settings. Around 555 Ma they migrated into shelf environments (Boag et al. 2018). Some were unattached; some, having a frond-like appearance, were fixed to the seafloor by holdfasts and connected to each other by filaments up to metres long, possibly suggesting that they reproduced by cloning. It is not clear that any were ancestral to later organisms, and most forms became extinct before the Cambrian. One fossil that has been interpreted as an animal – a very strange one – is the bilaterally symmetrical, leaf-like Dickinsonia, on the grounds that it was associated with the remains of cholesterol, a molecule otherwise found only in animals. The argument is slightly circular, since Dickinsonia might be evidence that cholesterol is not found only in animals. It had no discernible legs, eyes, mouth or gut, and it does not resemble any Cambrian animal. On the other hand, there is evidence that it could shift position.

Then, towards the end of the Proterozoic, burrowing organisms began to penetrate the sediment, leaving the first trace fossils in the form of horizontal meanderings and, less commonly, vertical burrows, even U-shaped ones. Small body fossils have also been discovered, such as the stumpy Ikaria, 1-1.5 mm wide, and the elongate Yilingia, up to 2.6 cm wide. Their arrival is of huge significance, for unlike nearly all Ediacaran organisms, these organisms moved of their own accord. They were true animals.

Click on image for larger viewAssociated with the explosion of animal life was the “Cambrian substrate revolution”, in which barren seafloors (substrates) were turned into habitable space for almost the full range of seafloor-dwelling organisms. The story is as much one of colonisation as of evolution. Appearing as if from nowhere, worms, molluscs, trilobites and so on were all benefiting from the recovery of marine animal life further down the food chain. Faecal pellets dropped by zooplankton attracted animals that now had sufficient oxygen to graze and burrow on the seafloor. As they consumed the droppings, they churned up the sediment, aerated it and fertilised it. Their actions, in turn, prepared the ground for other burrowers to live in and feed off still greater depths of sediment.

Why the ancestors of the Cambrian fauna were not fossilised

Evidently the organisms which brought about this revolution did not come into being ex nihilo. Nor is it plausible that some of the Ediacaran organisms might have been their ancestors. The interval between their first appearance and the Cambrian Explosion, a mere 40 Ma, was far too short for slight, successive modifications to have brought about the necessary across-the-board transformations – one might as well believe in natural magic. Other explanations for their apparent absence are: (1) the animals were too few in number to have made a mark on the fossil record, (2) they lacked fossilisable hard parts, such as bones, or shells, and (3) they were mobile rather than sessile, swimming at the surface as far from potential burial as it was possible to be. Some change in global conditions must have happened in the Cambrian to trigger, in nearly every phylum, a fundamental change in behaviour and physiology.

Despite their morphological differences, one surprising thing that nearly all marine invertebrate phyla have in common, above a certain size, is that they start off as larvae: tiny, usually soft-bodied swimmers. Only after metamorphosing into an entirely different form do they restrict themselves to life on the seafloor. Sponges, worms (encompassing several phyla), molluscs, cnidarians (e.g. corals), brachiopods and loricifera (microscopic sediment-dwellers resembling stalk-filled vases) all have a larval stage. Some larvae go through more than one stage. Barnacles, for example, go through two. The first, called the nauplius, has a thin calcareous shell, a single eye and goes through five moults – itself a remarkable phenomenon – before transforming into the cypris, whose role is to look for a suitable place to settle. Having made its choice, it cements itself to the surface and metamorphoses into the barnacle adult, hedged round with calcareous plates.

In general, metamorphosis occurs, not when a larva reaches a certain age, but when neurosensory cells in the larva detect a specific environmental cue and stimulate the release of chemicals into the nervous system (Ueda et al. 2016). These then activate a cascade of signals which induce the larva to settle and begin the transformation into an adult. Signalling systems differ from one family to another, but in most of them internally synthesised nitric oxide plays a key role. Metamorphosis is repressed when the neurosensory cells maintain high levels of of the gas, and promoted when synthesis of nitric oxide drops.

Metamorphosis is pre-programmed transformation of the individual. To suppose that such programming could have arisen from ‘numerous, successive, slight modifications’ (Darwin’s phrase), each occurring by chance, is to fly in the face of the message that is actually presented. How could the hypothetical modifications each have constituted an advantage in relation to a transformation that was all or nothing? Anything along the way would not have been viable. The transition is kept as brief as possible precisely because the organism during that time is not viable. Even if a long series of evolutionary steps had given rise to the adult form, how could the transition subsequently ever have been telescoped into a few hours? Species evolution and the development of an individual are separate things. By definition, natural selection leaves the previous steps behind, because they are less ‘fit’. In species that metamorphose, the larval stage is not left behind (notwithstanding that some echinoderms and sea squirts, amongst others, have lost the larva stage).

Larvae enable sessile and burrowing animals to colonise areas beyond their immediate habitat. The ability to colonise long-range is of course of no little significance in relation to the Cambrian Explosion, when the same types of substrate-dependent organisms appeared more or less simultaneously across the world. Animals did not get fossilised in the Precambrian, we may surmise, because the subsurface environment was giving them cues that inhibited larvae from settling and metamorphosing, for example because oxygen concentrations were too low and pH too high (Robinson 2016). Unlike their modern equivalents, they must have been able to reproduce. In this respect, a modern analogue might be certain species of salamander, which become sexually mature as larvae and do not metamorphose. If adult forms evolved incrementally from larval forms, larvae would have had to be able to reproduce.

… [under revision]

Recolonisation

Marine organisms appeared successively – first primary producers, then zooplankton, seafloor-dwelling herbivores and immobile filter-feeders, then swimming and seafloor-dwelling carnivores and deposit-feeders, finally large predators. In the Cambrian marine life was mostly restricted to habitats near the seafloor; by the Ordovician almost the entire water column was filled with organisms. This is the true meaning of the order of fossils. Organisms higher up the food chain depended on those lower down and were not programmed to reproduce as numerously. In all its diversity marine life was designed as a complex community.

Food webs in the Cambrian were ‘remarkably similar’ in structure to modern food webs (Dunne et al. 2008). Fundamentally, marine food chains changed little over time, just as, fundamentally, the organisms that composed them changed little. The disparate organisms that appeared in the Cambrian were linked by food chains, not evolutionary chains. There is no evidence that zooplankton evolved from bacteria, or that worms, molluscs, sponges and so on evolved from zooplankton.

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Darwin’s theory of evolution requires the evidence of ‘numerous, fine, intermediate fossil links’. He imagined that in the vast ages before the Cambrian the world must have ’swarmed’ with living creatures. But what we find is revolution, not evolution: an explosion of life forms as continental platforms began to be colonised by recovering populations from elsewhere – presumably, from shallow-marine polar regions. Starting with bacteria and climaxing with sharks, it was an ecological progression, something that occurred over thousands of years, not three thousand million.

Next: The first steps from sea to land