When a clam gets an offer it can’t refuse

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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.

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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.

Behold, my new favorite creature

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Porcellanopagurus nihonkaiensis wearing a bivalve shell (Source)

Some of you may be aware that I harbor great affection for hermit crabs. I own terrestrial Caribbean hermits. Your mental image of hermits may feature a wardrobe of gastropod (snail) shells, which are by far the most common mollusk contractor they use to construct their homes, but as I’ve discussed, they actually have great flexibility in their choice of abode. It turns out that there is yet another option which hermits take advantage of as a mobile home: the flat shells of bivalves and limpets!

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What a cutie, wearing a limpet like a hat (source)

Porcellanopagurus nihonkaiensis is a species of marine hermit found off the coast of Japan. It uses the relatively flat, unenclosed shells of clams (and also limpets) for protection. Though lacking the 360 degree protection afforded by a snail shell, bivalve shell valves can be more plentiful in the marine environment, and being able to utilize a different shell frees them from competition with other hermit species which are specialized to work with snail shells.

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Without the shell! From Yoshikawa et al, 2018

Hermits typically have a long, soft coiled body which fits in where the snail’s body once was, using “uropodal endopods” (little feet at the end of their bodies) to hold themselves in the shell. Some species like Porcellanopagurus, however hold a bivalve or limpet shell on their backs, which still provides protective cover for their bodies. One recent study talked about their method of acquiring and holding the shell. They actually took a cute little series of pictures showing how the crab picks up a shell it with its front claws, places it on its back and then holds it in place with their fourth pair of legs. So now I’ve found a creature that combines my beloved clams and hermit crabs in one fun package. Gonna have to keep an eye out if I ever dive off of Japan!

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Play by play of how they pick up and carry away their new home (in this case a limpet shell) (source)

Hard shells aren’t actually that hard to make (yet)

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One of the Antarctic bivalve species featured in this study. Source

Like all organisms, bivalves have a limited budget governing all aspects of their metabolism. If they put more energy into feeding (filtering the water), they can bring in a bit more food and therefore fuel more growth, but sucking in water takes energy as well, particularly if there isn’t enough food to be filtered out. Bivalves also periodically have to grow gonadal material and eggs for reproduction, expand their body tissue (somatic growth) and of course, grow their shells (made of of a mineral called carbonate). All of these expenditures are items in a budget determined by the amount of energy the bivalve can bring in, as well as how efficiently they can digest and metabolize that energy.

If a bivalve is placed under stress, their scope for growth (the max amount of size increase per unit time) will be decreased. Because they’re cold-blooded, bivalves are limited by the temperature of their environment. If temperatures are low, they simply can’t sustain the chemical reactions required for life at the same rate that endotherms like us can. They also may have to shut their shells and stop feeding if they’re exposed by the tide, or are tossed around by a violent storm, or attacked by predators or toxins from the algae that they feed on.

When their budget is lower, they have to make painful cuts, much like a company lays off employees if their revenues are lower. The question is which biological processes get cut, and when? My first chapter (submitted and in review) has settled temperature being the primary control on seasonal shell growth. Bivalves at high latitudes undergo annual winter shutdowns in growth, which create the growth bands I use to figure out their age, growth rate, etc. We’d be a lot closer to accurately predicting when bivalves suffer from “growth shutdowns” if we had hard numbers on how much energy they actually invest in their shells. A new study from a team led by Sue-Ann Watson of James Cook University attempts to do just that.

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Diagram relating the growth bands of Antarctic soft-shelled clam with a chart showing the widths of those bands. Source

Collecting a database of widths for the annual growth rings of bivalve and gastropod (snail) species from many latitudes, Watson and her team were able to get a global view of how fast different molluscs grow from the equator to the poles. Because the unit cost of creating carbonate is determined by well-understood chemistry, they were able to create an equation which would determine the exact number of Joules of energy used for every bivalve to grow their shells.

They still needed a total energy budget for each species, in order to the percent of the energy budget that each bivalve was investing in their shells. They drew on a previous paper which had calculated the standard metabolic rates for each species by carefully measuring their oxygen consumption. We could do the same for you if you sat in a sealed box for an extended period of time while we measured the exact amount of oxygen going in and CO2 going out. Dividing the amount of energy needed to grow the shell by the total amount of energy used in the organism’s metabolism would give us a percent of total energy that the bivalve dedicates to adding growth layers to its shell.

That number is…not very large. None of the bivalves or gastropods they looked at put more than 10% of their energy into shell growth, and bivalves were the lowest, with less than 4% of their energy going into their shell. Low-latitude (more equatorward) bivalves have the easiest time, putting less than 1% of their energy into growth but getting way more payoff for that small expenditure. High-latitude polar bivalves have to work harder, because the lower temperatures they experience mean the reactions needed to create their shells are more expensive. In addition, most of that energy is going into the protein-based “scaffolding” that is used to make the shell, rather than the crystals of carbonate themselves. Organisms right now don’t have to put a whole lot of effort into making their protective shells, which could explain why so many organisms use shells for protection. That is good, because if shells wereΒ  already breaking the bank when it came to the bivalves’ growth budget, they wouldn’t have a lot of room to invest more energy in the face of climate change. Unfortunately, as the authors note, these budgets may need to change in the face of climate change, particularly for bivalves at the poles. As the oceans grow more acidic due to human CO2 emissions, growing their shells will start to take up more of their energy, which is currently not a major part of their budget.

A cold-water ecosystem dominated by Antarctic scallops. Source

Right now, the cold waters of the poles are refuges for organisms that don’t deal well with shell crushing predators. As polar regions warm, such predators will begin to colonize these unfamiliar waters. Polar bivalves may encounter the double whammy of needing to spend more energy to make the same amount of shell, but also find that it is no longer enough to protect them from predators that easily crack open their protective coverings.

I found this study to be an elegant and thoughtful attempt to fill in a gap in our current understanding of how organisms grow and how energy budgets are influenced by environmental variables like temperature. I instantly downloaded the paper because it answered a question that has long been on my mind. Maybe can sneak its way into my manuscript during the review process!