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Pugnacity, and the need to regrow limbs

My friend Peter Macht is the aquarium curator at the Seymour Marine Discovery Center. He is responsible for all of the live (i.e., wet) exhibits and has a team of student and volunteer aquarists who help him care for the animals in the hall and behind the scenes. Peter and I go way back together, to years before the Seymour Center opened in 2000. Back then the only public space at Long Marine Lab was called the Shed Aquarium because it was, literally, in a wooden shed. I do miss the marine lab the way it was then, when I knew everybody who was there and it was a quieter and more peaceful place to work. However, we've come a long way, baby, and the Seymour Center is in just about every way imaginable, a huge improvement over the Shed Aquarium.

For one thing, there are two large exhibits in the Seymour Center, each of which would occupy about half the volume of the old Shed Aquarium. One of these tanks, the Sandy Seafloor tank, has housed many different animals over the years: surf perches, sand dabs, sharks, rays, señoritas, and various invertebrates. My personal favorite continues to be the burrowing sea star Astropecten, although she hasn't been on exhibit for several years now. The current inhabitants are a close second favorite, even though when they first arrived I didn't expect them to be nearly as fascinating as I've found them.

Pleuroncodes planipes is a little red crab commonly called the pelagic crab or the tuna crab. For once the common names reveal something about the biology of the animal--these crabs spend their lives in the water column over the continental shelf, at least as youngsters, and are one of the favored food items of tunas. They are usually found in the waters of southern California and Mexico, but during the El Niño event of 2015 they washed onto the beaches around Monterey Bay in humongous numbers; they also did so during the ENSO event of 1982-1983.

Front view of a living pelagic crab, P. planipes. 22 November 2016 © Allison J. Gong
Front view of a living pelagic crab, P. planipes.
22 November 2016
© Allison J. Gong
Lateral view of a living pelagic crab, Pleuroncodes planipes. 22 November 2016 © Allison J. Gong
Lateral view of a living pelagic crab, Pleuroncodes planipes.
22 November 2016
© Allison J. Gong

Although they resemble crayfish, Pleuroncodes is a crab. They are anomuran crabs more closely related to hermit crabs and porcelain crabs than to "regular" brachyuran crabs such as shore crabs and rock crabs. The way you tell the difference between anomuran and brachyuran crabs is to count the number of thoracic walking legs, keeping in mind that the claws are included as walking legs: anomurans have four pairs while brachyurans have five pairs. You can see in the picture of the lateral view that this crab has three pairs of stick-like legs and one pair of chelipeds (claws).

Being arthropods, red crabs molt periodically. Peter has been collecting data on frequency of molts for individual crabs since the spring of 2016. Doing so requires isolating crabs in separate containers, to keep track of which crab molts when and also to prevent the crabs from ripping apart a freshly molted compadre, which they do with great enthusiasm. It is not unusual to see one or more of the inhabitants of the Sandy Seafloor tank missing a leg.

Here's one of Peter's tables containing crabs in baskets:

Individual red crabs (P. planipes) in separate baskets. 22 November 2016 © Allison J. Gong
Individual red crabs (P. planipes) in separate baskets, for their own safety.
22 November 2016
© Allison J. Gong

It's just as well that these guys have extraordinary regenerative capabilities, as they are eager to rip each other's legs off. With most crabs that I've observed in the lab limb regeneration is a gradual process, with the new leg growing a bit with each successive molt. Chelipeds, even with their increased size and complexity, seem to regrow faster than the other walking legs, likely reflecting their importance to the animal's lifestyle.

Pelagic crab (P. planipes) and its molt. 22 November 2016 © Allison J. Gong
Pelagic crab (P. planipes) and its molt.
22 November 2016
© Allison J. Gong

Peter told me last week that he'd seen one of his isolated crabs regenerate an entire cheliped with a single molt, going from nothing to an almost-full-size functional limb essentially overnight. This seemed very unlikely to me, but Peter said he'd seen the before (the empty molt) and after (the actual crab) together in the same container. Unfortunately the crabs end up demolishing and eating their molts within a couple of days, so the evidence doesn't stick around very long.

Sometimes, though, you get lucky. When I was at the lab yesterday morning Peter told me that he'd seen another of his crabs molt, and that it had grown a missing cheliped since the previous day. And this time he could show me the proof. Voilà!

A pelagic crab (P. planipes) with its molt. Note that the molt has only one cheliped, while the crab itself has two. 22 November 2016 © Allison J. Gong
A pelagic crab (P. planipes) with its molt. 
22 November 2016
© Allison J. Gong

Note that the molt has only one cheliped, the left, while the crab itself has two. How cool is that? The crab's right cheliped is a bit smaller than the left, as might be expected of a regenerating limb, but it's definitely intact and functional. It was pretty exciting to see evidence of wholescale limb regrowth taking place in such a short period of time, which must be incredibly energetically expensive. On the other hand, chelipeds are extremely important for defense, and there is obvious selective pressure to regrow them as quickly as possible should a crab be unfortunate enough to lose one.

Peter gave me permission to examine the molt more closely, so I took it back to the lab where the lighting is better. And surprise! The right cheliped apparently didn't grow from nothing overnight. If you look really hard at the photo above, you can just barely see a ghostly transparent sheath where the missing arm would be. Hmm. This was not at all what I expected. Did I really see that?

It turns out that, yes, that is exactly what I saw.

Ventral view of the right side of a molt of the a pelagic crab (P. planipes).
22 November 2016
© Allison J. Gong

See that translucent tiny limb up front? That's a little cheliped! And it had been there at least six months, as this crab's last recorded molt was in April. Why hadn't anyone seen it before? I think because this limb was so small that the crab kept it tucked underneath the carapace, where it wouldn't be seen from the dorsal (top) side.

In the course of one morning I got taken for quite a roller coaster ride. Peter reminded me that he'd seen a crab apparently regrow a missing appendage in a single molt cycle . . . and had just found a crab whose molt showed exactly that . . . and then that molt ended up including a claw after all. What fun!

Now, why is that little claw so transparent? An arthropod's exoskeleton is made of a material called chitin, with varying degrees of calcification depending on species. The large marine crustaceans (e.g., crabs and lobsters) have heavily calcified exoskeletons, while insects have much more lightweight, less-calcified exoskeletons. As a crab prepares to molt, one of the things its body does is resorb some of the minerals that it had deposited in the soon-to-be-discarded exoskeleton, so they can be re-used in the new one. If you find a discarded molt on the beach, pick it up and note how little it weighs; you'd be surprised at how flimsy it is.

Here's my hypothesis. I think that this little cheliped, because it was newly regenerated before this most recent molt, was only lightly calcified. The crab may have used it, but it wouldn't have been much use for defense. Then, the next time the crab molted the claw was shed along with the rest of the exoskeleton, and the limb was significantly larger. This crab now possesses a complete pair of chelipeds again. After examining the molt I returned it to the crab, which has probably torn it to pieces and eaten already. It's a way for the animal to recover some of the nutrients it allocated into building the exoskeleton in the first place.

Kind of a neat trick, isn't it?

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