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

On May 31, 2022March 21, 2023 By Dan KillamIn Biology, clamsLeave a comment

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 view of the *Heteropsammia* coral from the side

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.

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 silhouette 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!

Gollum clams

On May 11, 2021May 12, 2021 By Dan KillamIn clamsLeave a comment

Right: Gollum, Middle Earth. Photo credit: Peter Jackson, New Line Cinema. Left: *Congeria kusceri*. Photo credit: Helena Bilandžija

In some ways, living in a cave sounds pretty comfortable. A relatively stable year-round environment and refuge from above-ground predators/competitors make it a place that trogloditic (cave dwelling) animals can develop stable evolutionary forms which persist through long periods of time. Like the deep sea, caves are great places to look for “relict” organisms representative of groups that disappeared long ago on the surface. But living in a cave presents a lot of challenges that require specialized adaptations. The most obvious is the lack of light, the source of energy for photosynthesis supports food webs on the surface. Animals in caves must make a living eating material that flows in from the surface world, like bat gauno or debris from runoff. They can also make a living eating the microbes that directly feed off the rocks of the cave walls. Some caves also have methane or other geologically sourced gases that can serve as a food source, similar to the deep sea, where methane seeps and hydrothermal vents provide fuel for diverse and vibrant ecosystems.

A map of the 15 caves where *Congeria* has been found. Source: Bilandžija et al. 2013

You don’t need to watch Lord of the Rings to see that spending your life in a cave like Gollum requires serious changes to your lifestyle. But that’s exactly where we can find an unusual genus of freshwater mussels called Congeria. Congeria consists of three species found so far only in fifteen caves in the Dinaric Alps, a mountain range in Southeastern Europe stretching from Italy to Albania. These mountains are made from limestone that first formed at the bottom of a shallow tropical sea (picture the Bahamas and you get a good idea of how it would have looked) during the Mesozoic era, the time of the dinosaurs. This limestone (also called karst) was lifted up in the early Cenozoic (after the Cretaceous extinction) by tectonic activity due to the collision of the Adriatic microplate with Europe. This 645 km-long row of mountains is made of a highly soluble rock similar in chemical composition to Tums. Over millions of years, cracks in this karst have been widened by acidic rainwater dissolving away the limestone to make caves. The Dinaric Karst is chock-full of such caves which form a huge maze of interconnected systems deep into the earth (the limestone goes down for kilometers into the crust)!

*Congeria kusceri* shows its white, unpigmented flesh. Photo by Vedran Jalžić

So if you were to put all your cards into evolving to be a cave creature, the Dinaric Karst would be a great place to try it. All sorts of spooky trogloditic creatures are found down there, such as olm salamanders, cave-dwelling isopods (rolly-pollies), and more. But Congeria is of particular interest because it is a remnant of a group of mussels that was once much more prevalent across this area of Europe, once a huge mass of swamps and lakes called Paratethys. Many species of mussels in the same family as Congeria can be found as fossils in rocks covering an area reaching from Switzerland to Lake Aral in Central Asia. But over time, the climate and geography of the area changed and almost all of these species went extinct. It was once assumed that Congeria had itself gone extinct 5 million years ago, as it was only known from fossils.

*Congeria kusceri*. Photo by The Croatian Biospeleological Society

In the 1960s, a team exploring the caves of the Dinaric Karst were shocked to find examples of living Congeria in caves. In many ways, the story was very similar to the discovery of coelocanths in the deep sea, a fish assumed to have gone extinct millions of years ago which was found by accident. These species are remnant twigs of previously lush branches of the tree of life. Such species are sometimes called “relict” taxa, or sometimes “living fossils.” Many biologists prefer not to use that phrase, because while these creatures may closely resemble the forms of their distant ancestors, they often have changed in all sorts of ways not easily visible to the naked eye. Congeria was unknown to us, but spent millions of years evolving to improve its fitness in its cave environment. Such groups thought extinct only to reappear later in the fossil record are also sometimes called “Lazarus taxa.” Like Lazarus in the biblical story, Congeria was thought dead only to reappear much later.

It appears the species making up Congeria were trapped in Paratethys first by the rise and retreat of the Mediterranean Sea and then trapped in caves following the drying up of Paratethys. For the past several million years, they have lived only in the cave systems of the Dinaric Alps. But like Gollum, they were not preserved exactly as they previously lived in the Paratethys. While other freshwater mussels continue to frolic like merry hobbits through the streams of the Dinaric Alps above, Congeria has adapted in all sorts of interesting ways to its life as spelunking animals.

Like other bivalves, Congeria makes a living filter feeding. But in caves, they don’t have access to the photosynthetic plankton food that is the main dietary staple for typical bivalves. Congeria instead feeds on whatever detritus flows its way through the waters of the caves, and it can’t be picky. Bivalves use their gills to catch food when filtering, and Congeria has a particularly bulked up set of gills to supercharge its ability to grab these particles. But the palps, organs to select which particles to actually bring to the animal’s mouth, are tiny to the point of being almost absent. As with Gollum, who was known to gobble down the occasional goblin, Congeria can’t be selective. They have to try to eat whatever comes its way, unlike other bivalves such as my Biosphere 2 clams, which spit out many of the particles they catch as “pseudofeces.”

In evolution, if you don’t use a feature, you often lose it. Organisms can’t afford to be sentimental about organs; if it saves energy and doesn’t cost any survival ability to cut out a particular feature, it will be reduced or lost over the generations. Like other cave animals, Congeria has lost almost all pigmentation since such pigments have no purpose in the absence of light. It also has a highly reduced foot, which is used by other freshwater bivalves to move around and dig in the sediment. In the stable, low energy environment of caves, a muscular foot would be a waste of energy. It has lost its statocysts; balance stones similar in function to our inner ear used by most mollusks to sense which direction is up. Since it settles on any available surface and doesn’t move, it makes sense to strike that item from the energy budget.

*Congeria* living comfortably out of water, one with valves open! Source Glavaš et al. 2017

Most bivalves in the freshwater mussel Dreissenidae family are “r strategists“, meaning they are like guppies or mice, producing and broadcast spawning a huge number of offspring. They don’t put too much energy into each offspring, and hope a certain small percentage of them will survive each year to keep the cycle going. R strategists often don’t live very long. Such a life strategy would be tough to sustain in isolated cave systems, which are a harsh environment in many ways, particularly regarding food supply for baby Congeria. Congeria instead has evolved to be a “K strategist” like humans or elephants. It “broods” its young rather than broadcast spawning. This process, found in other bivalves from extreme environments such as polar regions, involves taking in sperm to fertilize eggs internally. The mother clam then nurtures the embryos to a certain size, first within the gills and then in special pouches in the mantle tissue. This organ is called a marsupium; these clams are like kangaroos! Brooding is much more energy-intensive than broadcast spawning, since the mother is sharing energy with her babies, but the investment ensures that each baby Congeria will reach a larger size before leaving its mother’s shell, giving each one a better chance of surviving long term. In the resource-deprived environment of a cave, a little boost to reach maturity matters! Because real estate is fairly limited in its caves, Congeria can survive in very dense aggregations with over 1,600 individuals per square meter. These mussels are surprisingly selfless and communally living for such a harsh environment.

An acetate peel of the hinge of *Congeria kusceri*, showing annual growth lines used to tell its age. Source: Puljas et al. 2014.

As with Gollum, Congeria has become very long-lived. Individuals have been confirmed to live almost 60 years based on growth lines in its shell, and there are suggestions that they can live much longer. In the relatively predatory-free environment of the caves, Congeria can bet on not being killed before it reaches its prime. Instead, its greatest enemy is the fickle environment of the caves, which are dependent on water flow from the surface. Their shell growth is interrupted during the summer, when the waters of its cave become much less alkaline than at other times of year, depriving them of the calcium they need to build the shell. At other times they might have to survive extended periods being emersed from the water, when levels drop during the dry season or droughts. Most bivalves can only persist for hours in such conditions, but Congeria can survive 2 months out of water! For Congeria, it makes sense to bet on being able to survive as long as it can in the spot it settled, trying to reproduce little by little over a long period of time. In this way, it is not quite like Gollum, as it has evolved to live a long time to improve its ability to reproduce and pass on its genes, rather than out of selfish worship of a ring.

Like Gollum though, Congeria is very unique and fragile. The caves in which it lives are a sensitive environment, vulnerable to overdevelopment and pollution. Manipulation of groundwater has reduced the flow of water through these caves and thus restricted Congeria‘s habitat, wiping it out from areas of some caves. Because its population is inherently restricted by the “small pond” it inhabits, it would not take a big environmental disruption to wipe Congeria off of the map. To that end, Congeria is red-listed as endangered and is protected in most of its native countries. Still, we can only hope that even now there are other populations of Congeria waiting to be discovered, hidden in unexplored caverns deep in the Dinaric Karst.

Recent Science Communication!

On March 26, 2021March 26, 2021 By Dan KillamIn academia, scicommLeave a comment

At Biosphere 2, our science is essentially done in public. Every time I’m in the water checking on our clams and the sensors around them, I’m in view of the public and essentially an attraction for the public to watch. This is a really unique way to do science unlike any of my past experience, when I’ve been out in the field with a collaborator, or in the lab with a laboratory technician. I was initially intimidated by the idea of doing my science with an audience, but I’ve decided to lean into it as a huge opportunity. It is rare that the public gets to see all the steps going into our science; they usually only see the end of the story and not the whole journey leading up to that point. So recently I participated in two new ways of sharing my work while it’s in progress with the public.

The first was a collaboration with Mari Clevin, a videographer with the University of Arizona who made a really nice profile of my crazy clam journey. It was a lot of fun showing her around B2, trying to capture what it’s like to work here. It was fascinating seeing how all her footage and interviews came together into a video, and how she captured the key points of our conversation into a narrative!

The other scicomm event I participated in was a “Research Show and Tell” event run by the PAGES Early Career Network. Early Career Researchers include PhD students, postdoctoral researchers like me, and early career faculty. The ECN is intended to help us band together to share opportunities and plan events relevant to our interests. Among the North American regional representatives for the ECN, we saw a real need for more informal ways to share our research to an advanced audience of our peers. We’re all burned out from Zoom webinars, and on the other side Zoom coffee hours don’t typically provide much opportunity to share scientific content, so there’s a real need for events in the middle. So I was excited to share my research with a group of my peers, touring them around the Biosphere, showing them my clams via pre-recorded video and then having a Q and A to describe the work. It was a lot of fun and you can watch the whole hour-long event below!

Why eating clams sometimes makes us sick (Part 1 of 2)

On February 2, 2020February 2, 2020 By Dan KillamIn clams3 Comments

Image result for oysters — Is eating these a gamble? Science can help improve our odds!

I am often asked if I eat clams. The answer is yes: while I love to observe live clams and appreciate their abilities, I will eat a good clam chowder or plate of grilled scallops if presented with the chance. While I’m generally not a fan of super fishy-tasting foods, I eat bivalves with a clear conscience because farmed mollusks represent a super sustainable way to get protein! However, as many of us have learned the hard way, shellfish can sometimes produce unwanted results later after the meal, if the animals are contaminated with food poison. Eating such “bad” clams can produce a spectrum of food poisoning symptoms ranging from vomiting and diarrhea to memory loss to even paralysis and death.

Humans have known the hazards of eating shellfish for a very long time. It has been suggested that the ban on shellfish present in kosher and halal dietary rules arose as a preventative measure to protect from food poisoning (though eating fish, land animals and even vegetables can poison people in numerous ways as well). Studies of oysters have determined that ancient peoples of modern day Georgia from 5000 years before present selected their season of harvest based partially on knowledge of the seasons when such poisoning was most prevalent in their area.

How and why does this happen, and what can we do to prevent it? It’s a billion-dollar question, because when flare-ups of shellfish food poisoning happen, they are hugely costly to fishermen and the food industry, costing millions of dollars a year in lost business when fisheries are forced to shut down and products are recalled. Such events are increasing in frequency and severity. Which makes it all the more strange that these shellfish poisoning events are not the fault of the bivalves per se, but rather what they’re eating.

Note: people generally get annoyed when you start to point out the body parts of the oyster they’re about to swallow whole. Source

Almost all bivalves are filter-feeders, using their gills to gather small passing food particles, which they then either ingest or discard based on the quality of the food item. Clams are cows crossed with Brita filters, and for many species of clams which we eat, the reason they do all this filtration is to find phytoplankton food. Phytoplankton are microscopic algae suspended by ocean currents that make their living from photosynthesis. They are a hugely plentiful and high-quality food item, making up a huge amount of the biomass available in the ocean. Like plant-life on land, phytoplankton are highly seasonal in their appearance, rising and falling in abundance in periodic “bloom” events.

an image of red tide in Florida — Aerial view of a red tide off the Texas coast. Source: NOAA

But as Spongebob Squarepants taught us, plankton are not always peaceful. Many types of algae produce toxic compounds which may be integrated into the body parts of bivalves that eat them. Scientists call the blooms of algae which produce toxins “Harmful Algal Blooms” (HABs), and such events are growing in frequency and cause huge harm to marine life and sicken thousands of people per year. There are many algae species which cause HABs all around the world, sometimes visible as “red tides,” but not always. When HABs occur, they can lead to mass deaths of higher animals in the food chain that feed on clams such as marine mammals and seabirds. In fact, HABs are at their most dangerous to humans when they catch us by surprise.

https://cdn.coastalscience.noaa.gov/csmedia/2014/02/K-mikimotoi.jpg — Microscope view of the toxic dinoflagellate *Karenia*. Source: NOAA

When humans eat bivalves which have been dosed with such marine toxins, many types of poisoning can occur. Brevetoxin is produced by a type of dinoflagellate phytoplankton Karenia as well as other species, and when humans are exposed, we can suffer from Neurotoxic Shellfish Poisoning, which causes vomiting, diarrhea and even neurological effects like slurred speech. Saxitoxin is produced by a variety of plankton species including dinoflagellates and freshwater cyanobacteria. When ingested in clams (such as the butter clam Saxidomus which gave it its name), fish or other animals, it can cause Paralytic Shellfish Poisoning, a sometimes fatal syndrome which shuts down nerve signaling, leading to temporary paralysis.

So we know it’s bad for humans to ingest these toxins. What is it doing to the clams? Oddly enough, some types of toxins like saxitoxin are not that harmful to the clams or other plankton eating animals, allowing them to accumulate huge amounts in their bodies with little ill effect. Its presence does not seem to influence their feeding behavior much, or their growth after exposure. Its status as a neurotoxin in mammals might be a total chemical and evolutionary coincidence, as researchers suggest that it may actually serve as a signal in some part of the algae’s mating cycle. This also may be the case for brevetoxin, which appears to be produced when Karenia is under environmental stress. But there is not much agreement in the HAB and aquaculture research fields, because there are many types of algae, which may produce their toxins for many reasons, and it is very hard for us to zoom in to the scale of the microbe and out to the scale of the ecosystem at the same time, to find any kind of universal evolutionary role of these toxins. Some researchers insist that some bivalves are influenced negatively by brevetoxin, but only at the juvenile stage during major bloom events. The effects of the toxin may only influence certain species, or only become significant if the toxin reaches the digestive tract of the bivalve. Overall, research into impact of HABs on clams is still a topic of active research, and the idea that the microbes produce these toxins to defend against bivalve predators is definitely not a slam-dunk, easily proven hypothesis. While some clams are negatively affected by the toxins, it is not consistently observed across species in a open-and-shut way, and it can be a subtle effect to observe and quantify scientifically.

The more I read about this stuff, the more shocked I am at the incredible complexity of marine algae and their toxins. I only started reading about them trying how to to understand how they influence bivalves. I was hoping to find some evidence of their effects on bivalve growth that I could apply back in time in fossil shells to understand the historical occurrence of HAB events. It’s important to understand HABs because they hurt people, cost our society a lot of money and if we understand how to avoid them, we can help minimize such impacts in the future as HABs continue to become more common. In my next post, I’ll talk about some of the ways that researchers have come up with to measure and monitor HABs, so that we can eat clams as safely as possible.

A Make-Up Presentation!

On October 23, 2019October 24, 2019 By Dan KillamIn clams

Hi colleagues! Several weeks ago, I was supposed to present a talk at GSA’s annual meeting in Phoenix at the session “Advances in Ocean and Climate Reconstructions from Environmental Proxies”, but I shattered my wrist in a scooter accident the night before and was in emergency surgery during my talk time. So instead I’ve uploaded my talk with voice-over to Youtube! The whole video is about 15 minutes. You can view it above. Feel free to comment on this post or email me if you have questions!

This work is currently in the last stretch of drafting before submission, but I also discuss some ongoing research and am always open if you have your own ideas for collaborations!

Correction: we are working with geophysicists to understand the shell transport mechanism.

These are the references mentioned at the end:

Crnčević, Marija, Melita Peharda, Daria Ezgeta-Balić, and Marijana Pećarević. “Reproductive cycle of Glycymeris nummaria (Linnaeus, 1758)(Mollusca: Bivalvia) from Mali Ston Bay, Adriatic Sea, Croatia.” Scientia Marina 77, no. 2 (2013): 293.

“Glycymeris nummaria (Linnaeus, 1758).” 2019. World Register of Marine Species. 2019. http://www.marinespecies.org/aphia.php?p=taxdetails&id=504509#distributions.

Grossman, Ethan L., and Teh-Lung Ku. 1986. “Oxygen and Carbon Isotope Fractionation in Biogenic Aragonite: Temperature Effects.” Chemical Geology: Isotope Geoscience Section 59: 59–74.

Gutierrez-Mas, J. M. 2011. “Glycymeris Shell Accumulations as Indicators of Recent Sea-Level Changes and High-Energy Events in Cadiz Bay (SW Spain).” Estuarine, Coastal and Shelf Science 92 (4): 546–54.

Jones, Douglas S., and Irvy R. Quitmyer. 1996. “Marking Time with Bivalve Shells: Oxygen Isotopes and Season of Annual Increment Formation.” PALAIOS 11 (4): 340–46.

Mienis, Henk, R. Zaslow, and D.E. Mayer. 2006. “Glycymeris in the Levant Sea. 1. Finds of Recent Glycymeris insubrica in the South East Corner of the Mediterranean.” Triton 13 (March): 5–9.

Najdek, Mirjana, Daria Ezgeta-Balić, Maria Blažina, Marija Crnčević, and Melita Peharda. 2016. “Potential Food Sources of Glycymeris nummaria (Mollusca: Bivalvia) during the Annual Cycle Indicated by Fatty Acid Analysis.” Scientia Marina 80 (1): 123–29.

Peharda, Melita, Marija Crnčević, Ivana Bušelić, Chris A. Richardson, and Daria Ezgeta-Balić. 2012. “Growth and Longevity of Glycymeris nummaria (Linnaeus, 1758) from the Eastern Adriatic, Croatia.” Journal of Shellfish Research 31 (4): 947–51.

Reinhardt, Eduard G, Beverly N Goodman, Joe I Boyce, Gloria Lopez, Peter van Hengstum, W Jack Rink, Yossi Mart, and Avner Raban. 2006. “The Tsunami of 13 December AD 115 and the Destruction of Herod the Great’s Harbor at Caesarea Maritima, Israel.” Geology 34 (12): 1061–64.

Royer, Clémence, Julien Thébault, Laurent Chauvaud, and Frédéric Olivier. 2013. “Structural Analysis and Paleoenvironmental Potential of Dog Cockle Shells (Glycymeris glycymeris) in Brittany, Northwest France.” Palaeogeography, Palaeoclimatology, Palaeoecology 373: 123–32.

Sivan, D., M. Potasman, A. Almogi-Labin, D. E. Bar-Yosef Mayer, E. Spanier, and E. Boaretto. 2006. “The Glycymeris Query along the Coast and Shallow Shelf of Israel, Southeast Mediterranean.” Palaeogeography, Palaeoclimatology, Palaeoecology 233 (1): 134–48.

Thoughts of a clam

On June 2, 2019June 2, 2019 By Dan KillamIn Biology, clams, Uncategorized13 Comments

To us active, dynamic mammals, the humble clam can appear positively…inanimate. Their nervous system is decentralized relative to ours, lacking any sort of brain, and to the untrained eye, it can appear that their only discernible reaction to the outside world is opening or closing. Open = happy, closed = not happy; end of story, right? Some vegans even argue that the clams are so nonsentient that it is okay to eat them and think of them as having no more agency than a vegetable!

You might already have predicted I intend to tell you about just how animate and sentient clams can be. But let’s start out by describing the nuts and bolts of their nervous system. As with many invertebrates, their nervous system is distributed throughout their body as a system of ganglia. Ganglia are clumps of nerve cells which may have local specialization, and transmit messages within neurons using electrical potentials. At the connection between cells (called a synapse), neurotransmitters are used to pass signals to the next cell. Researchers have found that bivalves use “histamine‐, octopamine‐, gamma‐aminobutyric acid‐ (GABA)…like immunoreactivity” in their central and peripheral nervous systems, much like us vertebrates do, and other studies have even found that the response to serotonin and dopamine is localized in nervous tissue linked to different organ systems.

Nerve cells (bright green) highlighted in a larval oyster with fluorescent dye (from Yurchenko et al 2018)

These systems of chemical nerve transmission are truly ancient, likely dating back to the formation of complex animal body plans in the earliest Cambrian. Researchers have great interest in studying these nervous and hormonal signaling systems in mollusks because they can shed light on the relative flexibility and limitations of these systems throughout the animal tree of life. Characterizing these systems can also allow us to understand the mechanisms that bivalves and other animals use to react to environmental stimuli.

poly-gill-detailsem — Electron microscope view of gill cilia, zoomed in 1000x (from Dan Hornbach)

Like humans, bivalves spend a lot of time and effort eating. Most bivalves eat by filtering food from passing water with tiny cilia on their gills. These cilia work to capture food particles and also act as a miniature rowing team moving water along the gill surface. The bivalve needs a way to control this ciliar activity, and researchers found they could directly control the speed at which oysters move their cilia by dosing them with serotonin and dopamine, which respectively increased and decreased activity.

Bivalves also work very hard to make babies. Most bivalves reproduce by releasing sperm and eggs to fertilize externally in the water column. To maximize their chances to find a mate, they typically save up their reproductive cells in gonads for multiple months and release them in a coordinated mass spawning event. It appears that this process is controlled by hormonal releases of dopamine and serotonin. Researchers have determined that serotonin concentrations vary through the year, with mussels in New England using it to regulate a seasonal cycle of feeding in summer, followed storing of that energy for winter. During the winter when food is less available, they use that stored energy to bulk up their gonads in time for reproductive release in spring months, when their larvae have plentiful access to food and oxygen, ensuring them the best chance of survival. In recent decades, aquaculturists have learned to use serotonin injections to induce spawning in cultured clams, to ensure they will have a harvest ready at a certain time of year.

So bivalves are very sensitive to the seasons. How about shorter term sources of excitement? You might have observed this yourself through the clam’s most iconic activity: opening and closing its shell. Clams close their shells with powerful adductor muscles which pull the two valves together. A springy ligament at the hinge pulls the shell open when the muscles relax. Just like us, the clam needs to use nerve cells to signal the muscle to do its thing. In addition, two different sets of ganglia act to control the foot that some bivalves can extend to dig into sand, with one ganglion acting to extend the foot and the other causing it to contract. While clams don’t have a centralized brain with specialized regions for different uses like we have, this represents a sort of specialization of neural systems with a similar result.

Clam licking salt - Imgur — This iconic gif is often shared along with the claim it shows a clam “licking” salt. It is actually using its foot to search for a place to dig. The salt was not needed.

When a certain neuron is used repeatedly, it can form a cellular memory allowing the organism to acclamate (ugh sorry) and moderate its response to a particular stimulus over time. Giant clams, for example, close their shells when their simple eyes detect a shadow overhead. This behavior can protect them from predation. When I conducted some of my PhD research, sampling body fluid of aquarium and wild giant clams with a syringe, I noticed that captive clams didn’t close up in response to my shadow overhead, while wild clams required me to sneak up and wedge their shells open with a wooden block to do my work. I suspected that after exposure to frequent feedings and water changes by aquarists, the clam had “learned” that there was no reason to expend energy closing its shell. Meanwhile, in the process of proving that our sampling technique was not harmful to the animal, I discovered that clams which detected my shadow would quickly reopen within seconds when I hid from them, while those that were stuck by a syringe would stay closed for minutes before opening and beginning to feed again. Makes sense!

Other researchers noticed this phenomenon as well. One group found that giant clams repeatedly exposed to shadows of different sizes, shell tapping and even directly touching its soft tissue began to habituate (become accustomed) to the stress, opening more quickly and staying open longer each time the stimulus occurred. Even more interestingly, they did not transfer that habituation between stress types; for example, the clams that saw a shadow again and again would still react strongly to a different stress like tapping its shell. This suggests the animal can distinguish between different threats along a spectrum of seriousness, with touching of tissue (similar to a fish pecking at its flesh) being the most serious threat with the most dramatic response.

Another study determined that larger giant clams stayed closed longer than smaller ones in response to the same threat. They proposed this was related to the greater risk large clams face as they have more tissue area vulnerable to attack. While the clams might not have made a “conscious” decision in the way we do as thinking creatures, they were able to place their individual risk in context and vary their response. This ability to tailor a response to different risk levels is a sign of surprisingly complex neurology at work.

Inside the Scallop — Close up of the eyes of a scallop. Each is a tiny crystalline parabolic mirror (photo by Matthew Krummins on Wikipedia)

Scallops show some of the most complex bivalve behaviors. This relates back to their unique adaptations, including simple eyes that can resolve shapes and the ability to swim away from danger. Scallops have been found to discern between predator types by sight alone, to the extent that they did not initially recognize an invasive new predatory seastar as a threat. When swimming, they are capable of using this vision to navigate to places where they can hide, such as seagrass beds. It would be very interesting to compare the behavior of scallops in marine protected areas to those that can be freely harvested. Do they vary their behavior in response?

I hope I’ve made clear that while clams are not exactly intellectual powerhouses, their behavior is much more complicated than simply sucking up water and opening or closing their shells. Like us, they inhabit a complex environment that requires a multitude of responses. Their nervous systems have evolved to allow them to survive and adopt nuanced behaviors which they can vary on the fly, and which us “higher” animals are only just beginning to comprehend.

How does a scallop swim?

On February 13, 2019February 13, 2019 By Dan KillamIn clams5 Comments

uelx7yhbixf01 — Scallops spooked by divers’ lights and fleeing en masse to filter somewhere else

The ocean is a place of constant dynamic movement. Fish use their fins to push water away from themselves, and because every action has an equal and opposite reaction, they therefore move forward. Some cephalopods use jet propulsion, constricting their mantle cavity to push water out through siphons, allowing them to jet forward like a deflating balloon. And other life forms sail the seas on constantly moving currents , indirectly harnessing the power of the sun and earth.

Bivalves are a fairly sedentary bunch by comparison. While most bivalves have a planktonic larval form, when they settle they are constrained to a fairly small area within which they can burrow or scramble around with their muscular feet.

graybountifulgopher-size_restricted

But some bivalves have evolved to move at a quicker rate. The most famous swimming bivalves are the scallops, which have evolved to use jet propulsion, similar to their very distantly related cephalopod relatives. But unlike the cephalopods, scallops evolved to use their hinged shells to aid this process!

wyjgzzw — Notice the expelled water disturbing the sediment below the scallop as it “claps” its way forward!

Many filter-feeding bivalves use their shell valves as a biological bellows to pull in water for the purposes of sucking in food, or even to aid in digging, but scallops have developed another use for this activity, to enable propulsion. Scallops draw in water by opening their valves to create a vacuum which draws in water to their sealed mantle cavity. They then rapidly close their valves using their strong adductor muscles to pull them together, which pushes the water back through vents in the rear hinge area, propelling the scallop forward.

esn6uyb — Don’t panic if a scallop swims toward you. They can see, but not super well. This one is just confused.

Using this strategy, scallops can evade predators and distribute themselves to new feeding sites. It’s a surprisingly effective swimming technique, with the queen scallop able to move 37 cm/second, or over five body lengths per second! Michael Phelps would have to swim at nearly 35 km/h to match that relative speed (his actual highest speed is around 1/3 of that). I’m sure sustaining that speed would be tiring for Mr. Phelps, though, and it’s the same for scallops, only using their swimming for short-distance swims.

(video from Supplemental Materials of Robertson et al. 2019)

A recent paper from a team in Switzerland just came out describing an effort to engineer a robot which imitates the scallop’s elegant and simple swimming method. The resulting totally adorable “RoboScallop” closely imitates the design of a scallop, using a pair of hinged valves with rear openings to allow the movement of water backward. The internal cavity is sealed by a rubber membrane draped across the front so that all water is forced through these rear vents when the Roboscallop snaps shut.

Diagram from the Roboscallop paper (from Robertson et al. 2019)

As seen in the diagram above, the rhythm and relative velocity of opening vs closing is important to make sure the RoboScallop actually moves forward. If the scallop opened as quickly as it closed, it would just rock back in forth. It instead opens slowly so that it does not draw itself backward at the same rate that it can push itself forward. The researchers had to do quite a bit of calibration to get these rates right (equating to about 1.4 “claps” per second), but once they did, they ended up with a RoboScallop that can generate about the same force of forward movement (1 Newton) as a real scallop (1.15 Newtons), and similar rates of speed.

This paper really fascinated me because it is merely the latest in a long line of successful engineering projects imitating the ingenuity of evolution. Other marine robots have been made which emulate the locomotion of fish, manta rays, sea snakes and other forms of swimming. And now we have a clam! Let me know when I can buy one to play with in my pool.

Mystery of the “spurting” mussels

On November 21, 2018November 11, 2019 By Dan KillamIn Biology, clams2 Comments

If you’ve read any of my posts, you should realize by now that clams are pretty weird. Some catch live prey. Some have algae in their bodies that they “farm” for food. Some can bore into hard rock. Some sail the seas on rafts of kelp. Clams live in a competitive world and have had hundreds of millions of years of time to evolve to try out all sorts of weird, unlikely ways of life.

unio_crassus3_a_mrkvicka — *U. crassus* in a Slovenian river (Alexander Mrkvicka)

The thick shelled river mussel (Unio crassus) is known from many rivers and streams of Central Europe. As this is a very well-studied region of the world, many generations of academics have noted an unusual, seemingly inexplicable behavior undertaken by these mussels at certain times of year.

20_u-crassus_2 — *U. crassus* propped up on its foot (UCforLife)

Using its muscular foot, U. crassus pulls itself to the edges of the streams and rivers it lives in until it is partially exposed to air. It orients itself at a right angle with the surface of the stream with its siphons (two little snorkels coming out of the shell) facing out towards the water. Like all bivalves, U. crassus can act as a bellows by opening and closing its shell to pull in and push out water through those siphons. It has one siphon above the water and one below, and it proceeds to suck in water and spray it into the center of the stream using the power of its suction. The water can travel over a meter away and they continue this spurting about once a minute, sometimes for hours.

squirt — Squirting water into the stream! (Vicentini 2005)

Needless to say, this is a very strange and unlikely behavior to observe in a mussel. It is exposing itself to potential dessication or suffocation from exposure to air. It is vulnerable to predation from terrestrial mammals and birds. There has to be a very powerful benefit from this behavior to outweigh those risks. And why squirt water into the air?

Some researchers proposed that the mussels were traveling to shore to harvest from the more plentiful food particles deposited there. But why would they face their siphons away from the shore then? Other workers suggested that it was a way to reduce heat stress through evaporation, though that also seems unlikely, considering the water is warmest in the shallows. The question persisted for decades in the minds of curious malacologists.

squirttop — Top-down view of spurting behavior (Vicentini 2005)

In 2005, Heinrich Vicentini of the Swiss Bureau for Inland Fisheries and Freshwater Ecology decided to try settle the question of why these mussels spurt. He observed several dozen of the mussels crawl to the edge of the water and diligently begin squirting into the streams. In the name of science, he put himself in the path of these squirts, caught the water and used a hand lens to observe that the squirted water was full of mussel larvae (glochidia).

Lifecyle of U. crassus (Rita Larje via UCforLife)

U. crassus falls in the order Unionida, a group of freshwater mussels distinguished by a very unusual method of reproduction. They are parasites! Because they can’t swim well enough to colonize upstream against the current, they need to rely on fish to hitch a ride. Some have evolved elaborate lures to convince fish to take a bite, then allowing them to release their larvae, which attach to the fish’s gills like binder clips and ride all the way upstream. Once they have reached their destination, they detach and grow up into more conventional burrowing mussels. It’s a weird, creepy and wonderfully brilliant strategy that enabled the mussels to invade the inland rivers which would otherwise be inaccessible to them.

5_anodonta-glochidia-on-roach — Loach (type of freshwater fish) gills with unionid larvae attached (UCforLife)

The mussels appear to be spurting out not only water, but their babies. They gain a couple of advantages from this. For one, their larvae can distribute further than would be possible from the bottom of the creek. Instead, they are released at the center of the surface of the stream, where they can be carried for a much longer distance by the current before they settle at the bottom. In addition, the splash of water on the surface may mimic the behavior of insects and other fish food falling in the water. A curious minnow might venture to investigate the source of the splash, where it would promptly breathe in a cloud of larvae that get stuck on its gills. A pretty rude surprise, but a brilliant trick to give the baby mussels the best chance of surviving.

So again, clams prove themselves to be far more clever and interesting than they might initially seem. U. crassus and other members of the Unionida are an ancient and globally distributed lineage which have evolved all sorts of weird and wonderful ways to maintain their river lifestyle. Unfortunately, rivers are some of the most widely damaged environments in the world. A majority of freshwater mussel species worldwide including U. crassus are endangered by habitat loss, overharvesting and pollution. But more research into their unusual biology can help us understand ways we can enhance their conservation, with the hope of providing more habitat for them to recover populations in the future. New projects in Sweden and other countries aim to recover habitat for their larvae to settle along 300 km of rivers, and research the fish species which their larvae prefer to hitch a ride on. With more work, we can hopefully ensure that the streams of Europe will harbor little mini super-soakers for millennia to come.

The clams that sail the seas on rafts of kelp

On October 19, 2018October 19, 2018 By Dan KillamIn Biology, clams3 Comments

The streamlined shells of *Gaimardia trapesina*. Source: New Zealand Mollusca

Bivalves are not known as champion migrators. While scallops can swim and many types of bivalves can burrow, most bivalves are primarily sessile (non-moving on the ocean bottom). So for many bivalves, the primary method they use to colonize new territories is to release planktotrophic (“plankton-eating”) larvae, which can be carried to new places by currents and feed on other plankton surrounding them. Many bivalves have broad distributions because of their ability to hitchhike on ocean currents when they are microscopic. They don’t even pack a lunch, instead eating whatever other plankton is around them. But once they settle to grow, they are typically fixed in place.

Not all bivalves have a planktotrophic larval stage, though. Larvae of lecithotrophic bivalve species (“yolk-eaters”) have yolk-filled eggs which provide them with a package of nutrition to help them along to adulthood. Others are brooders, meaning that rather than releasing eggs and sperm into the water column to fertilize externally, they instead internally develop the embryos of their young to release to the local area when they are more fully developed. This strategy has some benefits. Brooders invest more energy into the success of their offspring and therefore may exhibit a higher survival rate than other bivalves that release their young as plankton to be carried by the sea-winds. This is analogous to the benefits that K-strategist vertebrate animals like elephants have compared to r-strategist mice: each baby is more work, and more risky, but is more likely to survive to carry your genes to the next generation.

Brooding is particularly useful at high latitudes, where the supply of phytoplankton that is the staple food of most planktrophic bivalve larvae is seasonal and may limit their ability to survive in large numbers. But most of these brooding bivalves stay comparatively local compared to their planktonic brethren. Their gene flow is lower on average as a result, with greater diversity in genetic makeup between populations of different regions. And generally, their species ranges are more constricted as a result of their limited ability to distribute themselves.

gtrap2 — A bunch of *G. trapesina* attached to kelp. Notice the hitchhiking clams have in turn had hitchhiking barnacles attach to them. Freeloaders on freeloaders! Source: Eleonora Puccinelli

But some brooding bivalves have developed a tool to have it all: they nurture their young and colonize new territories by sailing the seas using kelp rafts. The clam Gaimardia trapesina has evolved to attach itself to giant kelp using long, stringy, elastic byssal threads and a sticky foot which helps it hold on for dear life. The kelp floats with the help of gas-filled pneumatocysts, and grows in the surge zone where it often is ripped apart or dislodged by the waves to be carried away by the tides and currents. This means that if the clam can persist through that wave-tossed interval to make it into the current, it can be carried far away. Though they are brooders, they are distributed across a broad circumpolar swathe of the Southern Ocean through the help of their their rafting ability. They nurture their embryos on specialized filaments in their bodies and release them to coat the surfaces of their small floating kelp worlds. The Southern Ocean is continuously swirling around the pole due to the dominance of the Antarctic Circumpolar Current, which serves as a constant conveyor belt transporting G. trapesina across the southern seas. So while G. trapesina live packed in on small rafts, they can travel to faraway coastlines using this skill.

pic_w-msc-197185 — The broad circumpolar distribution of *G. trapesina*. Source: Sealifebase

The biology of G. trapesina was described in greater detail in a recent paper from a team of South African researchers led by Dr. Eleonora Puccinelli, who found that the clams have evolved to not bite the hands (kelp blades?) that feed them. Tests of the isotopic composition of the clams’ tissue shows that most of their diet is made up of detritus (loose suspended particles of organic matter) rather than kelp. If the clams ate the kelp, they would be destroying their rafts, but they are gifted with a continuous supply of new food floating by as they sail from coast to coast across the Antarctic and South American shores. But they can’t be picky when they’re floating in the open sea, and instead eat whatever decaying matter they encounter.

shell-gaimardia-trapesina — Falkland Islands stamp featuring *G. trapesina*. Source.

The clams are small, around 1 cm in size, to reduce drag and allow for greater populations to share the same limited space of kelp. Their long, thin byssal threads regrow quickly if they are torn, which is a useful skill when their home is constantly being torn by waves and scavengers. Unlike other bivalves, their shells are thin and fragile and they do not really “clam up” their shells when handled. They prioritize most of their energy into reproduction and staying stuck to their rafts, and surrender to the predators that may eat them. There are many species that rely on G. trapesina as a food source at sea, particularly traveling seabirds, which descend to pick them off of kelp floating far from land. In that way, these sailing clams serve as an important piece of the food chain in the southernmost seas of our planet, providing an energy source for birds during their migrations to and from the shores of the Southern continents.

Killer Clams

On July 22, 2018July 22, 2018 By Dan KillamIn Biology, clams1 Comment

Some shells of the carnivorous genus *Cardiomya*. Notice the protuberance off one side, making space for the overdeveloped siphon they use to capture prey (Machado et al. 2016)

You might think of clams as rather pacifistic creatures. Most of them are; the majority of bivalves are filter-feeding organisms that suck in seawater and eat the yummy stuff being carried by the currents. This mostly means phytoplankton, tiny single-celled photosynthetic plankton which make up most of the biomass in the world’s oceans. Most bivalves could be considered exclusively herbivorous, but as I’ve learned happens throughout evolutionary biology, there are exceptions to every rule. We already talked about parasitic bivalves that have evolved to hitch a ride on other hapless marine animals. But there is an even more sinister lineage of bivalves waiting in the sediment: yes, I’m talking about killer clams.

View of the oversized siphon (Machado et al. 2016)

Carnivory in bivalves has evolved multiple times, but the majority of known carnivorous bivalves fall within an order called the Anomalodesmata. Within that order, two families of clams called the Poromyidae and Cuspariidae have a surprising number of species which are known to eat multicellular prey.

Screenshot_2018-07-22 Clams.png — Evil clams are also the star of my favorite Spongebob episode

Now, you can rest easy because there are no clams that eat people. You’re safe from the Class Bivalvia, as far as we know. But if you were a small crustacean like a copepod, isopod or ostracod, you would be quite concerned about the possibility of being eaten by a poromyid clam in certain regions of the world. These clams lie in wait in the sediment like a sarlacc, with sensory tentacles feeling for passing prey and a large, overdeveloped siphon ready to suck up or engulf their helpless targets.

Until we catch the feeding behavior of poromyids on video, these whimsical artist’s depictions will have to do (Morton 1981).

Because they spend their lives under the sediment, these clams aren’t very well studied, and the first video of them alive was only taken in recent years. In addition, many of these killer clams live in deeper water, where their murderous lifestyle provides an advantage because food supplies can be much more sparse than in the sun-drenched shallow coastal zone. Much like the venus flytrap and carnivorous plants have arisen in response to the low nutrient supply of boggy swamp environments, the ability to eat alternative prey is valuable to the killer clams in all sorts of unconventional environments.

The siphon which these clams use to suck up their prey is a repurposed organ. In most other bivalves, the siphon is usually a snorkel-like organ which enables the clam to safely remain buried deep in the sediment and still breathe in oxgyen and food-rich water from open water above. But for the poromyids, the siphon is instead a weapon which can be used like a vaccum cleaner hose, or even be enlarged to engulf hapless prey. The poromyids have also evolved to have a much more complex, muscular stomach than any other bivalves. It takes a lot more energy to digest multicellular food, while most other bivalves simply just feed from the single-celled food they catch on their gills, expelling the other un-needed junk as “pseudofeces.”

*Dilemma*, another strange carnivorous bivalve which eats marine isopods (pill bugs), found from deep waters off the the Florida Keys, Vanuatu and New Zealand (Leal 2008)

Hopefully soon we will have video of this predatory activity in action. But until then, you can imagine that somewhere on earth, tiny copepods foraging on the surface of the sediment pass by a strange field of squishy tentacles. Suddenly, out of nowhere a hellish giant vacuum hose appears in view and sucks them in like Jonah and the whale. Then it’s just darkness and stomach acid. What a way to go!