Oxygen and predators and Cambrian awesomeness (with worms!)

I didn’t plan to write anything today, but damn, Cambrian explosion. And polychaetes. I can’t not. Plus I’m going on holiday soon, so I might as well get something in before I potentially disappear off the internet. (Below: a Cambrian polychaete, Canadia spinosa, via the Smithsonian’s Burgess Shale pages.)

First, a confession.

I’m a bit of a coward about the Cambrian explosion.

Make no mistake, I love it. It’s fascinated me ever since I came across the heavily Stephen Jay Gould-flavoured account in The Book of Life. It’s an event that made the world into what it is today, with its complex ecosystems full of animals eating, cooperating or competing with each other. And it’s one of the great mysteries of palaeontology. What actually happened? What caused it? Why did it happen when it did? Why didn’t it happen again when animal life was nearly wiped out at the end of the Permian?

The problem is, I love it so much that I’m afraid to have an opinion about it. You have no idea how many times I wanted to discuss the big questions, only to shy away for fear of getting it wrong. Which is really kinda stupid, because no one has the one and only correct answer. Whether I’m qualified to comment on it is a different issue, but it wouldn’t be the first subject I comment on that I don’t fully understand.

So, here I take a deep breath and plunge into Sperling et al. (2013).

The abstract started by scaring me. It begins, “The Proterozoic-Cambrian transition records the appearance of essentially all animal body plans (phyla), yet to date no single hypothesis adequately explains both the timing of the event…” To which my immediate reaction was “why the fuck would you want a single hypothesis to explain it?” But luckily, they don’t. They actually argue for a combination of two hypotheses, which they think are more connected than we thought.

But let’s just briefly establish what the Cambrian explosion is.

I want to make this absolutely clear: it’s not the sudden appearance of modern animals out ot nowhere. It could be more accurately described as the appearance of basic body plans we traditionally classify as phyla, such as echinoderms, molluscs, or arthropods, in a relatively short geological period.

Doug Erwin (2011) trawled databases and literature to draw up a timeline of first appearances for animal phyla, and he found that they increase in number gradually over a period of 80 million years (see Erwin’s plot below).


Appearance of “phyla” also doesn’t equal appearance of modern animals, as Graham Budd has been known to emphasise (e.g. Budd and Jensen, 2000). For example, I already mentioned how none of the mid-Cambrian echinoderms recently described by Smith et al. (2013) would look familiar today. In fact, the modern classes of echinoderms, which include sea urchins, starfish and sea lilies, didn’t appear until after the Cambrian. Likewise, while there were chordates (our own phylum), and probably even vertebrates, in the Cambrian, such important vertebrate features as jaws or paired appendages were yet to be invented. (If memory serves, both of those inventions date to the Silurian.)

There is also a discussion to be had about the meaning and validity of concepts like a phylum or a body plan, but let’s not complicate things here. I have a paper to get to! 🙂

With that out of the way…

There is no doubt that something significant happened shortly before and during the Cambrian. Before the very latest Precambrian, fossils show little evidence of movement, of predation, or of the diverse hard parts that animals use to protect themselves or eat others today. All of these become commonplace during the Cambrian, establishing essentially modern ecosystems (Dunne et al., 2008).

There are many explanations proposed to account for the revolution. I’ve not the space (or the courage) to discuss them in any detail. If you’re interested, IIRC Marshall (2006) is a very nice and balanced review. (Link leads to a free copy.) However, we can discuss what Sperling et al. have to say about two of them.

The first hypothesis is oxygen, which likely became more abundant in the ocean towards the end of the Precambrian. That  could explain the timing, but maybe not the nature of the explosion. Oxygen levels impose a limit on the maximum size of animals, but what compels larger animals to “invent” more disparate body plans? (Also, on a side note, many Ediacaran organisms weren’t exactly tiny, so I’m not sure how much of a size limit there is in the first place.)

The second one is animal-on-animal predation (Sperling et al. prefer the term “carnivory”), which can lead to predator-prey arms races and therefore encourage the evolution of innovations like shells or burrowing or jaws that give one party an edge. This is a decent enough basis for body plan innovation, but it applies for any time and place with animals. So if carnivory is the explanation, why did the explosion happen when it did?

Because, Sperling et al. argue, carnivory and oxygen are linked.

I’m intrigued by their approach. They’re not looking at fossils in this study at all. (I always like it when palaeontology and the biology of the living join forces!) They are looking at oxygen-poor habitats in modern oceans. Specifically, they asked how low oxygen levels affect polychaete worm communities.

Why polychaetes? The authors give a list of reasons. One, polychaetes are really, really abundant on the seafloor, and particularly so in low-oxygen settings. Two, different species feed in almost every conceivable way from filtering plankton through chewing through sediment to flat out devouring other animals, and their feeding mode can usually be guessed even if you haven’t seen that particular species eat. Three, they are actually quite good at handling oxygen limitation. This is important because back in the Precambrian, all animals would have been well adapted to a low-oxygen environment, so a group that can tolerate the same may be the best comparison. (They do note that  a previous study of a single low-oxygen site that took other animals into account came up with similar results to theirs.)

They worked partly with pre-existing datasets that met a set of criteria designed to get a complete and unbiased view of local polychaete diversity. In total, they analysed data from 68 sites together featuring nearly a thousand species of worms. They also had some of their own data.

They categorised their study sites into four levels of oxygen deprivation, and counted numbers of carnivorous individuals and species at each site. They came to the conclusion that lack of oxygen basically makes carnivores disappear. The lowest-oxygen samples contained fewer carnivores on both the individual and species levels, and they were more likely to be devoid of predators altogether (# species plot from the paper below):


There are a couple of different ways in which lack of oxygen could limit predators. For example, the aforementioned size limit is one, because it’s good for a predator to be larger and stronger than its prey. But the biggest factor according to the authors is the energy required for an active predatory lifestyle. While a suspension feeder can sit in one place all day and only move to stuff a food-laden tentacle into its mouth, a predator has to find, subdue and eat its prey, which are all pretty expensive activities. Then it also has to digest a sudden, large meal, whereas the suspension feeder’s digestion works at a low and steady rate. Animals can get energy from a variety of metabolic processes, but by far the most efficient route requires oxygen. And that really sucks when you are a hunter who might need large amounts of energy at short notice.


Although I’m quite intrigued by the study, there are a couple of issues that bother me. For example, as far as I could tell, all of the study sites included in the analyses were low on oxygen. I would have liked to see them compared to “normal” sites, in particular because the trend in predator abundance wasn’t a neat straight upwards line. In fact, the least oxygen-deprived habitats appeared less predator-infested than slightly more oxygen-poor ones. What’s going on there?

In terms of interpretation in relation to the Cambrian, I also would have liked to see a comparison of the oxygen levels at their study sites to what’s estimated for the geological periods in question. I take it they just didn’t have precise enough estimates, because one of the things they discuss in the closing paragraph is the need to measure just how much oxygen went into the oceans during this late Precambrian oxygen increase.

And my semi-silly question is, how does this apply to “predators” who don’t run around chasing after and wrestling with prey? For example, sea anemones might be perfectly happy to eat large creatures. But they don’t really do much. They just sit and wait, and if a poor fish stumbles onto their sticky venomous tentacles, tough luck for it. Or there’s the unknown predator that drilled holes in late Precambrian Cloudina specimens (Bengtson and Zhao, 1992). Cloudina was sessile, the creature didn’t have to chase it… Predators such as these still have to cope with the energy demands of digesting sudden large meals, I suppose, so maybe the energetics idea still applies. And of course, if there’s no oxygen, large prey is less likely to be swimming around bumping into your tentacles.

Is this “the” explanation of the Cambrian explosion? Probably not, says the cynic in me. I highly doubt we’re done with that question. Is it a good explanation? Well, it is certainly evidence-based, and I like it that it tries to take different factors together and in context. What I don’t think it does is explain the uniqueness of the Cambrian. A thousand words or so ago, I mentioned the Permian extinction. That cataclysm very nearly left the earth devoid of animals. Afterwards, there was certainly enough oxygen for predators to thrive in the sea, and indeed they did, from sea urchins to ichthyosaurs. So why didn’t the first 40 million years of the Mesozoic era beget many new phyla the way the first 40 million years of the Palaeozoic did? Is that just an artefact of our classifications or was something really fundamentally different going on?

I ain’t Jon Snow, but when it comes to the Cambrian, I still feel like I know nothing…



Bengtson S & Zhao Y (1992) Predatorial borings in Late Precambrian mineralized exoskeletons. Science 257:367-369

Budd GE & Jensen S (2000) A critical reappraisal of the fossil record of the bilaterian phyla. Biological Reviews 75:253-295

Dunne JA et al. (2008) Compilation and network analyses of cambrian food webs. PLoS Biology 6:e102

Erwin DH (2011) Evolutionary uniformitarianism. Developmental Biology 357:27-34

Marshall CR (2006) Explaining the Cambrian “explosion” of animals. Annual Review of Earth and Planetary Sciences 34:355-384

Smith AB et al. (2013) The oldest echinoderm faunas from Gondwana show that echinoderm body plan diversification was rapid. Nature Communications 4:1385

Sperling EA et al. (2013) Oxygen, ecology, and the Cambrian radiation of animals. PNAS 110:13446-13451

Fanworm fandom

In all my meanderings so far, I have never talked about my work in more than vague references to my connection to biominerals. Well, today won’t be the day I really start, but I would like to introduce the animals I work with. Because they are beautiful, awesome, and I love them (except when they’re sabotaging my experiments :-P). They are fan worms.

“Fan worm” is a bit of a loose term, and I’m still not entirely sure what group of worms it is/isn’t supposed to apply to. The group of fan worms I’d like to talk about today is family Serpulidae. (Call them “serps”. They won’t mind.)

Serpulidae are, if the latest phylogenetic research is to be believed, a subgroup of another “family”, the Sabellidae or feather duster worms (Kupriyanova and Rouse, 2008). All sabellids are sedentary filter-feeders. They live in tubes, putting a feathery crown of tentacles out into the water to catch their microscopic food. This is the fan in fan worm, and it’s all that most people ever see of these gorgeous creatures. It’s also today’s excuse to post some Nick Hobgood Christmas tree worms from Wikipedia, although their crazy spiralling tentacle crowns are not all that fan-like. (Bottle brush worms? :D)

These guys in the photo are mostly buried in a coral colony, with only their tentacle crowns sticking out.

Ancestrally, sabellid tubes are made of hard particles like sand and shell fragments glued together with mucus secreted by the worm. Serpulids are special in that they make their own hard material – calcium carbonate – instead of picking stuff up from the environment.

Serpulid tubes can have a highly organised structure that betrays sophisticated tube-building mechanisms (Vinn et al., 2008). Incidentally, some of them are pretty awesome if you look close enough. Below are the rather bland-looking tubes of Ditrupa arietina lying on the seafloor (from ten Hove and Kupriyanova [2009]). Then an electron microscope image of the outer tube layer showing the cool jigsaw-like cross sections of the calcareous rods it’s made of (Olev Vinn via Wiki Commons).


The general anatomy of the animal inside the tube is demonstrated quite nicely in the photograph below, from ten Hove and Kupriyanova (2009):


This is Serpula vermicularis, the species that gave its name to the family. The head end, obviously, is the one with the tentacles. Below it is a rather elegant thorax wearing a jacket of skin flaps (technically, “thoracic membranes”), with a wide collar folding down over the top. The collar builds the tube: when the worm wants to expand its home, it pokes its head out, wraps its collar over the rim, and deposits a new layer of material from glands under the collar.

The weird funnel-shaped thingy sticking out Serpula‘s head above is called an operculum. It’s another speciality of (most) serpulids, functioning in defence against predators. It’s used to close off the tube, but – at least in my species – it’s also a sacrifice body part that pops off at a predetermined point if you tug or prod it too hard. A bit like a lizard’s tail. (Or a sea cucumber’s guts, because gross examples are always better.) Also like the lizard’s tail, the operculum regrows easily, but unlike lizards, serps can regenerate a perfect new operculum. Some serps, including mine, have upgraded their defences further by reinforcing the operculum with calcium carbonate. A calcified body part that you can make develop on demand. What more can you dream of? 😉

Serpulids are found all over the world. Most of the 300+ species live in the sea, all the way from tidal rock pools to deep sea vents. There are a few that can handle brackish water, and there’s a single species that somehow found its way into freshwater-filled limestone caves along the Adriatic coast. According to Kupriyanova et al. (2009), this little explorer is closely related to the brackish-water species, so serps probably only figured out how to deal with lower salinity once.

They are nowhere near as famous as corals, but a few serpulid species are prolific reef builders. Ficopomatus enigmaticus (one of the brackish serps) can grow in roundish reefs made of generations of worm tubes. Although the individual tubes are only a few cm long, reefs can reach several metres across.

F. enigmaticus is an invasive species. Hitchhiking from their European homeland on boats and spawning wherever they felt happy enough, the worms have spread across the warm, shallow, brackish waters of the world. Below, their reefs are shown polka dotting the Mar Chiquita lagoon over in Argentina (photos: Alejandro Bortolus, in Schwindt et al. [2001]). Note the scale bar!


F. enigmaticus reefs have a pretty big ecological impact in their new territory. Their filter-feeding makes the water less murky (Bruschetti et al., 2008), which is good for the seafloor community, not so great for the phytoplankton that caused the murkiness. The reefs provide hiding places for native predators, changing the composition of the seafloor community (Schwindt et al., 2001), and they can also serve as resting stops and hunting grounds for birds (Bruschetti et al., 2009).

And finally, let’s talk a bit about serpulid babies, because baby worms are the best. I don’t know about other serps, but my species has very stylish BABY PINK EGGS. The moment you remove an adult worm from its tube, it panic-spawns all over the place. If you mix the pink eggs with the boring white sperm in some seawater, by the next day the dish will be full of tiny, zipping white balls. (At this point you’d better feed them, since unlike some other baby polychaetes, they don’t get a lot of food from mum. In nature, they’d swim off and live in the plankton, hunting tiny algae until they are ready to settle.)

In another day or two, the little balls grow quite a bit and turn into textbook examples of the type of larva known as the trochophore. If you’re good to them and give them enough food, they’ll keep growing like crazy. You can always see whether they’re hungry or not, since they are transparent and the colourful algae they like to eat show through their skin. This one, from McDougall et al. (2006) via Wiki Commons, was clearly well-fed when it fell victim to science:

They look all hairy around the broadest part – those are the cilia they use to swim. They are very good at swimming! Within a couple of weeks, they’ve transformed into a more mature form with three newfangled segments and a lovely pair of eyes, like this other one from the same paper:

They are now sniffing along the bottom, looking for a place to settle. When they find a spot they like, they lie down, secrete a tiny tube (made of just mucus at first), and metamorphose into transparent baby worms complete with an operculum and everything. This is what Pomatoceros lamarckii looks like mid-metamorphosis (again from McDougall et al.):


At this point, they are a bit ugly, but don’t worry, the ugly wormling stage doesn’t last long. I’ll finish off with one of my own photos what they turn into:


These are slightly over three weeks old, and they have tiny, iridescent tentacles and minute, transparent opercula. Their now-calcified baby tubes are just a few mm long.

Aren’t they lovely? 😀



Bruschetti M et al. (2008) Grazing effect of the invasive reef-forming polychaete Ficopomatus enigmaticus (Fauvel) on phytoplankton biomass in a SW Atlantic coastal lagoon. Journal of Experimental Marine Biology and Ecology 354:212-219

Bruschetti M et al. (2009) An invasive intertidal reef-forming polychaete affect habitat use and feeding behavior of migratory and locals birds in a SW Atlantic coastal lagoon. Journal of Experimental Marine Biology and Ecology 375:76-83

Kupriyanova EK & Rouse GW (2008) Yet another example of paraphyly in Annelida: molecular evidence that Sabellidae contains Serpulidae. Molecular Phylogenetics and Evolution 46:1174-1181

Kupriyanova EK et al. (2009) Evolution of the unique freshwater cave-dwelling tube worm Marifugia cavatica (Annelida: Serpulidae). Systematics and Biodiversity 7:389-401

McDougall C et al. (2006) The development of the larval nervous system, musculature and ciliary bands of Pomatoceros lamarckii (Annelida): heterochrony in polychaetes. Frontiers in Zoology 3:16

Schwindt E et al. (2001) Invasion of a reef-builder polychaete: direct and indirect impacts on the native benthic community structure. Biological Invasions 3:137-149

ten Hove HA & Kupriyanova EK (2009) Taxonomy of Serpulidae (Annelida, Polychaeta): The state of affairs. Zootaxa 2036:1-126

Vinn O et al. (2008) Ultrastructure and mineral composition of serpulid tubes (Polychaeta, Annelida). Zoological Journal of the Linnean Society 154:633-650

Superfood shelf. Just-fucking-what.

After feeding every stupid health scare ever with its “free from” labels, Tesco has reached a new low. Or maybe it reached it long ago and my brain just refused to see it.

The damn place has a SUPERFOOD SHELF now. Because salad can’t just be healthy, it has to be SUPER healthy.



I have to go and do some real science now.