A coral, a worm and some clams walk into a bar…

The tree of life is often portrayed as a neatly branching structure, with each division point cleanly delineated and separated from its neighbors. The truth is that the various twigs of the tree of life often overlap and become tangled in a process we call symbiosis. I’ve talked about symbiosis before on this blog, which falls along a spectrum of wholesomeness. At one end we have mutualism, a partnership where both organisms benefit and achieve more than the sum of their parts. The other extreme is parasitism, when one organism benefits at the expense of the other. Between the two, there is a broad gray area including commensalism, when one organism’s presence doesn’t necessarily cost or benefit the other in any way. The tree of life is crowded and unpruned, and so sometimes the twigs might wrap around each other quietly and without much fuss. We live on a small planet, and have had to get used to living in uncomfortable intimacy with all sorts of creatures, such as the mites that are living on your eyelashes right now.

But things start to get really weird and tangled when the tree of life loops over on itself twice, or three times, or more. “Three-way” symbioses are surprisingly common, and the more you look for them, the more you realize that the tree of life is more of a knot than anything else.

A worm burrow in a coral, with clams included! Note the little “lateral pores” that serve as windows!

A recent paper from researchers in Bremen (Germany) and Saudi Arabia looked at such a three-way symbiosis between a coral, a worm and bivalves found off of Tanzania in East Africa. The relationship between solitary corals (Heteropsammia cochlea and Heterocyathus aequicostatus), a sipunculan worm (Aspidosiphon muelleri muelleri) and the clam Jousseaumiella, is a complex triangle of dependencies that had previously been noticed by other researchers, but never investigated at great depth. The worm lives with multiple tiny clams attached, all inside of a small solitary coral the size of a dime (1 cm long). Is the coral a willing host for this crowded boarding house, or has it been parasitized? Does the worm gain anything from the clams? The researchers sought to find out.

Part of the reason I enjoyed reading this study so much was that it had to take a narrative structure to describe the evolutionary ménage à trois of its focus. So much of modern science has moved away from anecdote to hard data, and while there is plenty of that to find in the study, it turns out that a lot of the study of symbiosis is storytelling. We need to know the setting and the characters.

The corals are small and would be easy to mistake for small bits of reef rubble if you weren’t looking for them!

In this case, the main characters are small solitary corals living in the tropical reefs of the Indo-Pacific. We denote them as solitary to distinguish them from their giant colony-forming compatriots that construct the coral reefs currently threatened by climate change and pollution. But like those giant reef-builders, these solitary corals get much of their food from sunlight through a mutualistic partnership with algae called Symbiodinium. The algae provide the host with sugars and other photosynthetic products, and the hosts give them nutrients and a safe cozy home in their tissue.

You might be thinking, “Wait! Dan just said this was a three-way partnership between a coral, a worm and some clams. So this is actually a four-way partnership between corals, worms, clams and algae?” You’d be exactly right. And I’m happy to say that the plot of this sordid story is about to thicken even further.

The side of the coral. See the little pores?

The Aspidosiphon worm is found in a spiral-shaped burrow inside of the skeleton of the coral. It is a pretty cozy home, with walls made of calcium carbonate by the coral, with breathing holes in the sides to allow the worm to breathe and release waste. The researchers wanted to know more about the structure of the burrow. Was it dug out by the worm using acid or an abrasive motion, like some clams use to dig into coral? So the researchers essentially gave the coral a CT scan to see its 3D internal structure. Inside they found growth features suggesting the coral grew around the worm, as if intentionally providing it a home.

Cross-sectional CT scans of the coral skeleton. In figure D, you can see the silouette of the chambers of the snail shell where the worm made its first home!

Even more crazily, they found evidence that the worm had first settled inside an empty snail shell, like a hermit crab! The coral probably settled on a snail shell as a larva, and grew to engulf the whole snail shell, leaving growing space for the worm inside, with windows and all! So to review, this is now a five-way symbiosis between a dead snail, a worm that moved into its empty shell, the coral (powered by algae) that grew around it and encased the snail shell within its skeleton, and we haven’t even gotten to the clams. How many creatures are hiding stacked in this trench coat? Please bear with me as I explain!

An SEM image of Jousseaumiella. These are less than 1 mm long! Pinhead sized!

What are the clams doing in this picture? Jousseaumiella is part of a family of clams called Galeommatidae, which we previously mentioned on this blog in the context of some bivalves found growing in the gills of unfortunate sand crabs. Many members of the Galeommatidae family are parasitic or commensal with other marine organisms. In this case, Jousseaumiella are tiny flat-bodied clams less than 1 mm long, found attached to the body of the worm, squeezed inside the burrow in the coral’s skeleton. It feeds on the worm’s waste and potentially food particles coming through the pores in the sides of the burrow. Not the most dignified existence, but a more mobile home means more opportunities to eat a varied diet similar to that that the worm and coral are seeking out, and the clam also gets protection from predation tucked inside the coral. It is unclear if it benefits the worm directly to have clams attached to it.

A time lapse of the coral+worm moving from the paper’s supplement! It would be handy to navigate to greener pastures, if it became too muddy in a certain place!

It is, however, clear how living inside a coral would be a pretty good deal for the worm, which gets a stable, protective suit of carbonate armor to protect it from predators, and grows to fit it as it gets larger. They are normally found inside of rocks, shells and other hard inanimate objects, but having a living home is a cool upgrade. What is the coral getting out of the deal? The researchers note that the corals are often found in the crevices between other large reef-building corals, in areas of the reef that receive high supplies of nutrients and turbidity (dirt that blocks out light). These sorts of environments aren’t necessarily friendly places for a coral to be, since they reduce the light and therefore the food that the coral can receive from photosynthesis. These crevices also have a lot of variability in other conditions like temperature and water flow. But because the coral has hitched a ride on the back of a worm, it can actually move in the sediment to react to changing conditions and avoid being buried by piles of sediment floating by! The worm can also act as a sort of anchor preventing the worm from sinking in the sediment underneath, which would be a big hazard for the small, stubby coral on its own. The coral seems to go to great pains to make its partner comfortable, not growing its skeleton to cover the pore windows to the outside. The researchers note that as coral reefs worldwide are subject to increasing human-made pollution and climate change, it would be interesting to research whether this complex three-(five?) way symbiosis provides the various participants with an advantage compared to other corals.

So like any good story, this symbiosis features complex, growing characters, a dynamic setting, and still plenty of mystery demanding a sequel! To that end, there are lots of other great three-way symbioses to investigate. Snails which farm fungus that parasitizes plants. Bryozoans living on snail shells that have a hermit crab inside. Gobies serving as lookouts at the entrances of burrows built by shrimp, with a crab freeloader along for good measure. Algae and bacteria teaming up to attack mussels. The list keeps going! I could see this becoming quite a franchise!

Weird Clam Profile: The Heart Cockles

Corculum cardissa (from Wikipedia)

The heart cockle (Corculum cardissa) is so named because of its heart shaped shell. It is native to warm equatorial waters of the Indo-Pacific. While many bivalves sit with the their ventral valve facing down, the heart cockle sits on its side, with one side of both valves facing downward. The valves have adapted to resemble wings and are flat on the bottom, providing surface area that allows the bivalve to “raft” on the surface of soft sandy sediment and not sink. They may also sit embedded in little heart-shaped holes on the tops of corals.

Two heart cockles embedded in the top of a Porites coral. Source: Reefbuilders

A particularly green heart cockle from Singapore. Source: orientexpress on iNaturalist

Heart cockles are a member of a small club of bivalves which partner with symbiotic algae for nutrition created by photosynthesis. Most of the modern photosymbiotic bivalves are in the family Cardiidae, the cockles. The giant clams (Tridacninae) are also in this family and have a similar partnership with the same genus of Symbiodinium algae. This algae is also found in many species of coral.

The dark circles in these microscope images are Symbiodinium. The top is a view of giant clam body tissue. The cells are present throughout the tissue in giant clams. The bottom shows heart cockle “tubules” which contain their symbiotic algae. The algae are restricted to narrow tubes that run through the tissue of the cockle. Source: Farmer et al. 2001

So when you find a live heart cockle, it is often green in color, because of the presence of this algae near the surface of its tissue. Its shell has adapted to be “windowed” (semi-transparent) to allow in light for the algae to harness to make sugars. The algae are housed in networks of tubes within the soft tissue of the cockle. They trade sugars with their host in exchange for nitrogen and carbon from the clam.

As I’ve mentioned before regarding the giant clams, this is a very productive partnership and has evolved separately several times in the history of bivalves. However, we don’t know why almost all examples of modern bivalve photosymbiosis occur in the cockles. Why aren’t the heart cockles giant like the giant clams? What features are necessary to allow this symbiosis to develop? These are the kind of questions I hope to help answer in my next few years of work.

When a clam gets an offer it can’t refuse

Tridacna maxima in Eilat, Israel

I study the giant clams, bivalves which can grow over three feet long and and are willingly “infected” by a symbiotic algae which they house in an altered stomach cavity. They provide their algae partners with nitrogen, a stable environment and even funnel light in their direction, and the algae happily share the fruit of their labor in the form of sugars. Imagine yourself swallowing algae, storing it in your gut and developing windows in your flesh to let light into your stomach. You’d never have to eat again. This is the growth hack that enables the giant clams to grow to unusual sizes. But it turns out that this lovely, beautiful partnership may not have started so peacefully. The algae may have made an offer the clam couldn’t refuse.

Top left: normal mussel. Top right: heavily infected L-shaped shell opening. Bottom: view of an algae-infected mussel, including close up of pearls. From Zuykov et al. 2018

A team from University of Quebec recently discussed what such a fresh infection looks like in mussels and it ain’t pretty. The mussels basically have their shells and bodies overgrown by parasitic Coccomyxa algae, leaving its flesh bright green and transforming its shell from the classic elongated, acute angled margin typical of Mytilus mussels into a strange L-shaped overhang. The more algae are present in the mussel, the more extreme this deformity becomes. The researchers propose that this is no accident, but that as they move in, the algae also manipulates the biochemical pathway that the mussel uses to create its shell.

Mussels, like all bivalves, create their shells by laying down calcium carbonate in layers at the outer edge of the shell. The calcium is sourced from salts in the water column and the carbon primarily comes from carbonate ions also available in the water. This reaction is easier when the pH of the clam’s internal fluid is higher (less acidic), and that is exactly what the algae may assist with. Algae like all plants take in carbon dioxide to use in photosynthesis, and in doing so they increase the pH of the mussel’s body fluid,

The authors note that the region of shell which experiences abnormal thickening in the infected mussels is also the most exposed to light. The Coccomyxa algae may be causing runaway calcification of shell in the regions that they infect, and even may be directly assisting with the calcification in an additional way through the action of an enzyme called carbonic anhydrase, which is used in both their photosynthesis and in shell production (I won’t get into the nitty gritty of that reaction here). But the calcification of the mussels does appear to be in overdrive, as infected mussels were also observed to make pearls!

The algae’s photosynthesis may be assisting the mussel’s shell formation, though overall these are still quite unhealthy organisms of lower weight than their uninfected brethren. Still, Coccomyxa is known to form symbioses with lichens and mosses, so it could be that with enough generations of collaboration and a bit of evolution, the harmful algal infection could become a much more mutually beneficial partnership. It’s not so far fetched to imagine that an ancestor of today’s giant clams got a bad case of gastritis and decided to make the best of a bad situation. Making a deal with their invaders, they became greater than the sum of their parts and evolved to be the giant hyper-calcifiers we know today.

The Snails that Farm

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Littoraria grazing on Spartina marsh grass. (source)

Us humans really like to talk up our skills at farming. And while it’s true that we have domesticated animals and plants to a degree not seen in other life forms, the act of nurturing and harvesting food is actually not really that special, and is broadly observed throughout the animal kingdom. Perhaps the most iconic invertebrate farmers are insects. Leaf-cutter ants, termites, and some beetles have been observed to actively cultivate fungus by gathering plant material to feed it, growing the fungus, protecting the fungus from competition, and then harvesting the fungus to feed themselves and their young. Ants are also known to keep livestock in the form of aphids, which they lovingly protect and cultivate for the sweet nectar they excrete. Such practices are called “high-level food production” because, like human farmers with their seeds and fertilizer, insects have evolved a highly complex symbiosis with their fungus. The fungus has shaped their behavior as much as the ants cultivate the fungus. 

The marsh periwinkle Littoraria irrorata (source)

Less well understood is the “low-level food production” that may occur more broadly throughout the tree of life. There is less direct evidence of such behavior because it is more indirect and less specialized than high-level food production, but it may be equally advantageous for the cultivator and the cultivated. One study published in 2003 uncovered a simple but powerful relationship between marsh periwinkles of the genus Littoraria and fungus which they cultivate and harvest.

Close-up of a snail’s radula (source)

Marsh periwinkles are small and not particularly charismatic creatures. Like many snails, they are grazers with a shell, a fleshy foot and a rough, abrasive organ called a radula which they use like sandpaper to graze on pretty much whatever they can get into. Snails are not known as picky eaters. But researcher Brian Silliman of Brown University and Steven Newell of University of Georgia noticed that these innocuous snails regularly undertake the risky, low reward activity of grazing above the water on the blades of swamp grass, stripping off the surfaces of the blades of grass. The researchers were confused why the snails would expose themselves to predation and the harmful open air for such a low-nutrition food.


A typical snail farm, complete with liberally applied fertilizer. Yum.

They discovered that the snails were investing in the future. By stripping away the protective surface of the swamp grass blades and liberally fertilizing the surface of the grass with their droppings, the periwinkles are ensuring that the swamp grass will be infected with an active and very prolific fungal infection. The fungus, unlike the plant it lives on, is of high nutritional value. The researchers demonstrated the active partnership between the snails and fungus by conducting caged experiments where they showed that snails which grazed on grass but not the resulting fungus did not grow as large as snails which were allowed to return and chow down on the fungus. The fungus loves this deal as well. They grow much more vigorously on grass that is “radulated” (rubbed with the snail’s sandpapery radula) than uninjured grass. The fungus grows even faster if the snails are allowed to deposit their poop next to the wounds. The researchers found that this same relationship applies at 16 salt marshes along 2,000 km of the Eastern Seaboard.

The periwinkles don’t really know what they’re doing. They aren’t actively planting fungus and watching proudly like a human farmer as their crop matures. But over millions of years, the snails have been hard-wired to practice this behavior because it works. Snails that abrade a leaf of swamp grass, poop on the wound and come back later to eat the yummy fungus do a lot better than snails which just stick to the safe way of life below the surface of the water. The fungus loves this relationship too. The only loser is the swamp grass, which the researchers unsurprisingly found grows much more slowly when infected with fungus. But marsh grass is the largest source of biomass in swamp environments, and the snails that partner with fungus are able to more efficiently use this plentiful but low-nutrient food source, to the extent that it is now the dominant way of eating for swamp periwinkles on the East Coast of the US, and probably in a lot more places too. The researchers noted that there are likely far more examples of low-level food production that we simply haven’t noticed.

Since this work was published, other teams have discovered that some damselfish like to farm algae, fiddler crabs encourage the growth of mangrove trees, and even fungus get in on the action of farming bacteria. We love to talk up our “sophisticated” high-level food production techniques, but such relationships probably got started at a similarly low level. Our activities as hunter-gatherers encouraged the growth of certain organisms, we stumbled upon them, ate them, kept doing what we were doing and eventually our behavior developed into something more complex. Next time you see a snail munching its way up a blade of grass, consider to yourself whether it knows exactly what it’s doing. Come back later to see the fruits of its labor.

Fossil-Fueled Life

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Thick aggregates of Bathymodiolus mussels on a cold seep site off of Nantucket. Source: NOAA

Humans aren’t the only users of fossil fuels. In many parts of the ocean, natural gas (methane) is constantly bubbling out of the sediment. These areas are known as cold seeps and are often a marker of productive fossil fuel reservoirs in the crust underneath. The name cold seep is somewhat of a misnomer (they are often slightly warmer than surrounding waters), but they are indeed much cooler than the more famous hydrothermal vents, which form due to geothermal activity. They are often found in shallower waters than hydrothermal vents, which generally occur in the deepest regions of the ocean where the earth’s crust is rifting. As with hydrothermal vents, cold seeps provide a unique opportunity for ecosystems to arise which are based on chemical energy, rather than solar-powered photosynthesis like the rest of the biosphere. Unusual life forms harness the chemical energy of the methane and sulfide emitted at these seeps, and many can also be found at the more famous hydrothermal vents.

Crabs feeding on a bed of Bathymodiolus. Source: NOAA

Bathymodiolus mussels, vesicomyid clams, and other bivalves thrive at these seep environments, and have evolved to partner with bacteria in their gills and stomachs which can directly consume and produce energy from the reaction of methane and sulfate continuously being sourced from the seep underneath, creating bicarbonate and sulfide as products. This form of metabolism, chemosynthesis, is distinct from the familiar photosynthesis/respiration that most life-forms at the surface use to create energy. The partnership between a multicellular animal and chemosynthetic bacteria is called chemosymbiosis. These reactions are of course being utilized by all sorts of microbes not partnering with bivalves, but the bacteria that take on metazoan hosts have the advantage of a stable environment and a constant flow of fresh seep gas brought in by the bivalves’ gills. The bivalves feed on the products of the microbe’s hard work. As they are some of the only inhabitants that can tolerate the oxygen-free, toxic environment of seeps, they form dense thick shell beds wherever a seep appears.

A bed of tubeworms and a deep-living octopus in the Arctic. Source: MBARI via BBC

Other chemosymbiotic groups use the hydrogen sulfide byproducts from seeps, which they oxidize into elemental sulfur. The most prominent of these are the vestimentiferan tubeworms, which lack mouth or anus and are totally dependent on the activity of the bacteria that they house in a modified digestive tract. Some of these worms have been found in seeps in extreme environments, such as the truly cold cold seeps of the Arctic. They are less spectacular in appearance than their bright red counterparts from hydrothermal vents, but are believed to live for an extremely long time, depending on the consistency of the seep that they inhabit.


Hesiocaeca methanicola, one species of the poorly understood “ice worms.” Source: NOAA via Wikipedia

At the extreme pressures and low temperatures of the deep ocean, methane can freeze in combination with water molecules, forming structures called clathrates. Much of the deep ocean floor is dusted with deposits of clathrates. Microbes which feed on clathrates are believed to be a food source for grazing polychaete “ice worms.” These unusual organisms can survive up to 96 hours without a whiff of oxygen, an unbelievable feat for a moving, multicellular organism.

Imaginative artist representation of a probe visiting a vent under the ice of Europa. Source

Cold seep environments are perhaps merely one specific manifestation of a vast, poorly understood collection of biota which do not depend on the sun for their energy. We do not yet understand many of the deep ecosystems which may be present within the earth’s crust, in the deep ocean and trapped under polar ice. NASA studies cold seep and hydrothermal environments as the best analog for the conditions life could experience in the frozen oceans of Europa and Enceladus. It is eerie to think that such alien ecosystems  exist merely a few kilometers off of our familiar shores, and were using fossil fuel energy far before humans figured out how to combust it.

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Methane bubbling out of the seafloor off of the Virginia coast. Source: NOAA


The Many Homes of Hermit Crabs

My boy Harry, a purple pincher (Coenobita clypeatus) inhabiting a tapestry turban snail (Turbo petholatus) shell. These seem to be his favorite kind, even though they do not come from his native Caribbean.

Hermit crabs (superfamily Paguroidea) are most famous for using snail shells as their home, having evolved a soft, spiral abdomen to be able to use them for protection. But they are more flexible about their choice of abode than you might expect.

This crab was likely preserved buried alive in sediment. Note how it uses its claw as a protective trap door sealing the opening of the ammonite shell. Source: Jagt et al, 2006

Different groups of shelled organisms have risen and fallen in abundance through geological time. During the time of the dinosaurs, ammonites (relatives of modern squid and octopus) were among the most common marine organisms, and hermit crabs were there to recycle their shells when they died.

Each tiny pore (zooid) in this bryozoan contained a tiny tentacled organism. Together they grew in a shape that made for a nice hermit crab house (image 5 shows a cross section where the crab’s abdomen would fit). Source: Taylor and Schindler 2004

Mollusks aren’t the only contractors for hermit crabs. Some hermits utilize the skeletons of colonial organisms like bryozoans as a home. Bryozoans are filter-feeding colonial animals made up of thousands of tiny tentacled organisms living in the pores of a shared skeleton. The extinct bryozoan Hippoporidra lived in symbiotic partnership with hermit crabs, growing around a gastropod shell to attract a hermit crab partner. This was an example of mutualism: by providing a home for a crab, the bryozoan would be transported to new environments with plentiful food particles to eat, and also would be protected from their arch-enemy, nudibranchs (sea slugs). Some modern day hermits, such as Manucomplanus varians of the Gulf of California, have evolved very similar partnerships with live staghorn corals.

Manucomplanus varians at Monterey Bay Aquarium

Not all hermit crabs live in hard houses. Some deep sea forms partner with anemones, with the stinging tentacles serving as an effective defense.

Source: Okeanos Explorer

The recently discovered green-eyed hermit crab, which also lives in deep water, lives in a glued-together mass of sand created by tiny anemones, which continue to grow the structure to fit the crab as it increases in size.

The green-eyed hermit crab was found over 200 m deep off of South Africa. Source: Lannes Landschoff via Eurekalert 

Unfortunately, hermits adapted for gastropod shells are unable to find adequate homes in some areas, due to overharvesting of shells for the tourist trade as well as an excess of plastic trash. These crabs make do with whatever items that they can find. Plastic is not an ideal home material for hermits. Bottlecaps and narrow tubes do not allow the crab to fully retract for protection and leach chemicals which may harm the crab. The crabs also nibble on their shells as a source of calcium, which is obviously not possible with plastic.

Coenobita purpureus, a land hermit crab on Okinawa. Source: Shawn Miller

But hermits continue to impress me with their flexibility and ingenuity in their search for homes. For a hermit crab, home is where the abdomen is.