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There are certain creatures that, for whatever reason, give me the creeps. I imagine everyone has them. Some people have arachnophobia, I have caterpillarphobia. While fear of some animals makes a certain amount of evolutionary sense--spiders and snakes, for example, can have deadly bites--my own personal phobia can be traced back to a traumatic childhood event involving an older cousin and a slew of very large tomato hornworms. Even typing the words decades later makes me want to rub my hands on my jeans.

But enough about caterpillars. This Halloween I want to share something that isn't nearly as disgusting, but can still creep me out sometimes. Commonly called skeleton shrimps, caprellid amphipods are a type of small crustacean very common in certain marine habitats. They are bizarre creatures, but a close look reveals their crustacean nature. For example, they possess the jointed appendages and compound eyes that only arthropods have.

Female caprellid amphipod (Caprella sp.)
22 October 2017
© Allison J. Gong

Around here the easiest place to find caprellids is at the harbor, where they can be extremely abundant. The last time I went to the harbor to collect hydroids for my class, the caprellids were swarming all over everything. When I brought things back to the lab I had to spend an hour or so picking the caprellids off the hydroids. I don't think they eat the 'droids, but they gallop around and keep messing up the field of view, making observation difficult. They're essentially just a PITA to deal with, and everything is easier after they've been removed.

Caprellid amphipods (Caprella sp.) at the Santa Cruz Yacht Harbor
23 June 2017
© Allison J. Gong

Caprellids are amphipods, members of a group of crustaceans called the Peracarida (I'll come back to the significance of the name in a bit). They have the requisite two pairs of antennae that crustaceans have, and seven pairs of thoracic appendages of varying morphology. Some of these thoracic legs are claws or hooked feet that like to grab onto things. A caprellid removed from whatever it's attached to and placed by itself in a bowl of seawater thrashes around spastically. Only when it finds something to grab does it calm down. Even then, they attach with their posterior appendages and wave around the front half of the body in what I call the caprellid dance: they extend up and forward, and sort of jerk front to back or side to side. It isn't pretty.

A bunch of caprellids removed from their substrate and dumped into a bowl together will use each other as something to grab. This forms the sort of writhing mass that makes my skin crawl. I was nice enough to give them a piece of bryozoan colony to hang onto, but even so they ended up glomming together.

Now, back to the thing about caprellids being peracarids. The name Peracarida means "pouch shrimp" and refers to a ventral structure called a marsupium, in which females brood their young. Males don't have a marsupium, so adult caprellids are sexually dimorphic. When carrying young, a female caprellid looks like she's pregnant. See that caprellid in the top photo? She's a brooding female. That's all fine, until her marsupium itself starts writhing. This ups the creepiness factor again. Here's that same brooding female, in live action:

Crustaceans obviously don't get pregnant the way that mammals do, but many of them spend considerable energy caring for their young. Well, females do, at least. A female caprellid doesn't just carry her babies around inside a pouch on her belly. Although she isn't nourishing them from her own body in the way of mammals (each of the youngsters in the marsupium is living off energy stores provisioned in its egg), the mother does aerate the developing young by opening and closing the flaps to the marsupium. This flushes away any metabolic wastes and keeps the juveniles surrounded by clean water. As the young caprellids get bigger, they begin to crawl around inside the pouch, and eventually leave it. They don't depart from their mother right away, though; rather they cling to her back for a while, doing the caprellid dance in place as she galumphs along herself.

Until the juveniles strike out on their own they form a small writhing mass on top of a female who can herself be part of a larger writhing mass. And the sight through the microscope of all these long skinny bodies jerking around spasmodically can indeed be very creepy. Fortunately not as creepy as caterpillars, or I wouldn't be able to teach my class or go docking with my friend Brenna. And it's a good thing caprellids are small, 'cause if they were any bigger. . . just, no.

 

Although the world's oceans cover approximately 70% of the Earth's surface, most humans interact with only the narrow strip that runs up onto the land. This bit of real estate experiences terrestrial conditions on a once- or twice-daily basis. None of these abiotic factors, including drying air, the heat of the sun, and UV radiation, greatly affects any but the uppermost few meters of the ocean's surface so most marine organisms don't need to worry about them. Despite the apparent paradox of where they live, intertidal organisms are also entirely marine--they cannot survive prolonged exposure to in air or freshwater. So how do they manage to live here?

Some organisms have a physiological tolerance for difficult conditions. These tidepool copepods and periwinkle snails, for example, are able to survive in the highest pools in the splash zone, where salinity can be either very high (due to evaporation) or very low (due to rain or freshwater runoff), dissolved oxygen is often depleted due to high temperature, and temperature itself can be quite warm. Sculpins and other tidepool fishes cope with low oxygen levels by gulping air and/or retreating to deep corners of their home pools.

Of course, animals that can locomote have the option of moving to a more favorable location. Other creatures, living permanently attached to their chosen site, aren't quite so lucky. Let's take barnacles as an example.

Nauplius larva of the barnacle Elminius modestus
© Wikimedia Commons

Barnacles have two planktonic larval stages: the nauplius and the cyprid. The nauplius is the first larval stage and hatches out of the egg with three pairs of appendages. It can be distinguished from the nauplius of other crustaceans by the presence of two lateral "horns" on the anterior edge of the carapace. The nauplius's job is to feed and accumulate energy reserves. It swims around in the plankton for several days or perhaps a couple of weeks, getting blown about by the currents and feeding on phytoplankton.

Cyprid larva of a barnacle

After sufficient time feeding in the plankton, a barnacle nauplius metamorphoses into the second larval stage, the cyprid. A cyprid is a bivalved creature, with the body enclosed between a pair of transparent shells. It has more appendages than the nauplius, and these are more differentiated. If the nauplius has done its  job well, then the cyprid also contains a number of oil droplets under its shell. These droplets are of crucial importance, because the cyprid itself does not feed. For as long as it remains in the plankton it survives on the calories stored in those droplets. The cyprid's job is to return to the shore and find a suitable place on which to settle. Somehow, a creature about 1 mm long, being tossed about by waves crashing onto rocks, has to find a place to live and then stick to it.

Returning to the topic of the challenges that marine organisms face when they live under terrestrial conditions, let's see how these barnacles manage. Along the northern California coast we have a handful of barnacle species living in the intertidal. In the higher mid-tidal regions at some sites, small acorn barnacles of the genera Balanus and Chthamalus may be the most abundant animals.

Mixed population of the acorn barnacles Balanus glandula and Chthamalus dalli/fissus at Davenport Landing
27 June 2017
© Allison J. Gong

However, nowhere is a particular pattern of barnacle distribution more evident than at Natural Bridges. Here, the barnacles in the high-mid intertidal are small, and concentrated in little fissures and cracks in the rock.

I think most of these small (~5 mm) barnacles are Balanus glandula:

Small acorn barnacles (Balanus glandula) at Natural Bridges
11 October 2017
© Allison J. Gong

And here's a closer look:

Small acorn barnacles (Balanus glandula) at Natural Bridges
11 October 2017
© Allison J. Gong

If all of the rock surfaces were equally suitable habitat, the barnacles would be distributed more randomly over the entire area. Instead, they are clearly segregated to the cracks in the rock. Each of these barnacles metamorphosed from a cyprid into a juvenile exactly where it is currently located. The cyprid may be able to move around to fine-tune its final location, but once the decision has been made that X marks the spot and the cyprid has glued its anterior to the rock, the commitment is real and lifelong. The barnacle will live its entire life in that spot and eventually die there. It is quite probable that cyprids landed in those empty areas on the rock, but they didn't survive to adulthood.

How did this distribution of adult barnacles come to be?

There is one very important biological reason for barnacles to live in close groups, and that is reproduction. They are obligate copulators, which I touched on in this post, and as such need to live in close proximity to potential mates. But today I'm thinking more about abiotic factors. In a habitat like the hid-mid rocky intertidal, desiccation is a real and daily threat. Even a minute crack or shallow depression will hold water a bit longer than an exposed flat surface, giving the creatures living there a tiny advantage in the struggle for survival. No doubt cyprid larvae can and do settle on those empty areas of the rock. However, they likely die from desiccation when the tide recedes, leaving only the cyprids that landed in one of the low areas to survive and metamorphose successfully. There are other factors as well, such as the presence of adult individuals, that make a location preferable for a home-hunting cyprid. In addition to facilitating copulation, hanging out in a cluster slows down the rate of water evaporation, giving another teensy edge to animals living at the upper limit of their thermal tolerance.

Lower in the intertidal, where terrestrial conditions are mitigated by more time immersed, barnacles and other organisms do indeed live on flat rock spaces. But at the high-mid tide level and above, macroscopic life exists mostly in areas that hang onto water the longest. Pools are refuges, of course, but so are the tiniest cracks that most of us overlook. Next time you venture into the intertidal, take time on your way down to stop and salute the barnacles for their tenacity.

2

About three weeks ago I collected some mussels from the intertidal, to use both in the lab and in the classroom. A mussel can itself be an entire habitat for many other organisms. Many of the mussels I brought into the lab this last time were heavily encrusted with barnacles and anemones. I wanted to look more closely at one of the anemones so I took the mussel to the microscope. And, as often happens when I look at stuff under the microscope, I got totally distracted by things other than what I intended to.

But for the record, this is the anemone that started the whole chain of events:

A small aggregating anemone (Anthopleura elegantissima). 5 December 2016 © Allison J. Gong
A small aggregating anemone (Anthopleura elegantissima).
5 December 2016
© Allison J. Gong

Below the anemone there's a thick mat of small acorn barnacles (Balanus glandula) and a couple of leaf barnacles (Pollicipes polymerus). They were all alive when I brought the mussel into the lab, and over the weeks a few of them have died. But many of them are still kicking, both figuratively and literally.

Barnacles are most strange animals. Believe it or not, they are crustacean arthropods, somewhat closely related to crabs and lobsters. They live encased within a shelter of calcareous plates, which they can close seal up against predators and desiccation. I've never figured out why they are called "acorn barnacles," as they don't look anything like acorns to me, but in Balanus and such the base of the shelter is glued directly to a rock or some other hard surface. Leaf barnacles are shaped very differently, and have a fleshy stalk between the shelter that houses the main body of the animal and the rock surface.

Small acorn barnacles (Balanus glandula). 5 December 2016 © Allison J. Gong
Small acorn barnacles (Balanus glandula).
5 December 2016
© Allison J. Gong
Close-up view of a leaf barnacle (Pollicipes polymerus). 5 December 2016 © Allison J. Gong
Close-up view of a leaf barnacle (Pollicipes polymerus).
5 December 2016
© Allison J. Gong

To picture what's going on with a barnacle, imagine a shrimp lying on its back, then curl it up and stick the whole thing inside some calcareous plates. The thoracic appendages would be facing up. In barnacles the thoracic appendages are modified to be clawlike feeding structures called cirri. Barnacles are filter-feeders, collecting particles from the water by maneuvering the cirri in a sort of grasping fashion. So in a nutshell, or more precisely a test, a barnacle lies on its back and kicks its legs out to catch food.

Here's what B. glandula looks like when feeding. Note the clearly jointed cirri, with fine hairs that help catch particles. The cirri can be controlled independently, as you can see when they flick towards the center, and the entire apparatus can be rotated quite a bit.

Same deal with Pollicipes.

So that's the feeding part. A little strange, but not as interesting as the barnacles' sex lives. Let's start with some background about sexual function. And get your mind out of the gutter; this is real science stuff! Most of the animals that you're familiar with are described as dioecious (Gk: "two houses"). This means that female and male sexual functions are segregated; in other words, there are male bodies and female bodies. Other animals are described as monoecious (Gk: "one house"), so that a single body has both female and male sexual function. Monoecious animals could also be described as hermaphroditic. Some monoecious animals have male and female function in a single body at the same time; we call these simultaneous hermaphrodites. If a body first functions as one sex and then either acquires or switches to the other sex, we say the animal is a sequential hermaphrodite. Many fishes, including the California sheephead and the anemone fishes of coral reefs, are sequential hermaphrodites. Make sense?

Barnacles are simultaneous hermaphrodites. If you dissect an adult barnacle you will find mature ovaries and testes. This means that every barnacle can be both a mother and a father. The logical assumption is that monoecious animals should just fertilize their eggs with their own sperm. . . however, this generally isn't the case. The whole point of sexual reproduction is to combine the genomes of two individuals, and self-fertilization obviously doesn't accomplish this. So even though there are many hermaphroditic animals, very few of them are self-fertile.

One other weird thing about barnacles, and crustaceans in general, is their sperm. Arthropods have non-flagellated sperm, which means they don't swim (although some of them have amoeboid sperm that can ooze around a little bit). Many marine animals reproduce by broadcast spawning; that is, by throwing their gametes into the water, where fertilization takes place. Fertilization is facilitated by the sperms' ability to swim towards conspecific eggs.

Barnacles, with their non-swimming sperm, generally cannot rely on broadcast spawning to get sperm to egg. They must copulate. How do you suppose they do this? The same way that other animals (e.g., Homo sapiens) copulate, by using a penis or some other structure to transfer sperm from one individual to the body of another. In barnacles the penis's technical name is intromittent organ. The penis is inserted into the test of a neighboring barnacle and sperm is delivered. The receiving barnacle uses the sperm to fertilize its eggs. Unlike the cirri, the penis is unjointed and flexible, the better to seek out and slip into potential mates. You can see the intromittent organ unrolled and poking around.

Now think about the ramifications of these constraints. Barnacles live their entire post-larval lives permanently cemented to a rock. They also have non-motile sperm so sperm transfer can occur only by copulation. If the key to reproductive success is to mate with as many other individuals as possible, what do you suppose natural selection has done? That's right: barnacle anatomists, including the great Charles Darwin himself, have noticed that barnacles have incredibly long penises. In fact, compared to overall body size, barnacles have the longest penises in the animal kingdom, up to 15 times the length of the body! That's what you call bragging rights. Not all barnacle species are so amply endowed, however. The same leaf barnacle that I observed today (P. polymerus) has recently been reported to be a spermcaster; their penises are shorter than body length, and they release sperm that are captured by their downstream neighbors.

Wonders never cease.

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?

ORGANISM OF THE MONTH: Pugettia producta, the kelp crab

For a few months now, I've had a pet kelp crab running around in one of my seawater tables. I don't remember where I collected it, or even whether or not I collected it at all; quite often crabs and other animals arrive as hitch-hikers on kelp that we bring into the lab to feed urchins, and I end up with many cool critters in my care that way. However she got here, this crab has been rather a pain in the butt during her stay with me. For at least a couple of weeks she got stuck in the drain of the table and would not come out despite three experienced marine biologists (including yours truly) trying to persuade her by altering water flow and offering food bribes. Then she disappeared from the table drain and I assumed that she had gone all the way through to the floor drain, where she could live quite happily for all eternity. Then she suddenly showed up again in one of my urchin baskets. When she came back up from the drain and how long she'd been hiding, I'll never know.

Wondering why I keep referring to this crab as "she"? It's because I know for certain that she's a female. Here's the secret to how you can determine the sex of brachyuran crabs (most of the common crabs: kelp crabs, shore crabs, rock crabs, even Dungeness crabs): You look at the shape of the abdomen, which is curved forward on the underside of the body. See here:

Abdomen of female Pugettia producta. 16 October 2015. © Allison J. Gong
Abdomen of female kelp crab (Pugettia producta)
16 October 2015
© Allison J. Gong

The abdomen is the broad flat upside-down-U-shaped panel that covers about half the width of the ventral surface. Female crabs brood their embryos under the abdomen, hence the broad shape. Male crabs of the same species have a much narrower, pointed abdomen.

Since her escapade with the drain the crab has been more, shall we say, co-operative. She's still free to scurry around at will in the table, but I haven't found her doing anything objectionable such as tormenting urchins or trying to get down the drain again. She has also been eating well.

Until this past week, that is. On Monday she accepted a piece of food but then abandoned it without even tasting it. On Wednesday she fled from the food, which I took to mean that she was getting ready to molt. Like all arthropods, crustaceans molt their exoskeletons every so often. The decapod crustaceans I'm most familiar with tend to off their feed for a few days before molting, and usually the actual shedding of the exoskeleton occurs at night. Then we show up the next day and voilà! like magic there's a new, bigger crab in the table.

Ms. Kelp Crab stopped eating on Monday of this week. Today (Friday) I didn't get to the lab until about noon, and one thing I noticed in the table was an empty carapace. Sure enough, she had molted. It took a little hunting to find the crab herself, but she wasn't really hiding and her new exoskeleton had already hardened. I'm pretty sure she'll eat on Monday.

Kelp crab (Pugettia producta) and carapace of its molted exoskeleton. 16 October 2015 © Allison J. Gong
Kelp crab (Pugettia producta) and carapace of her molted exoskeleton
16 October 2015
© Allison J. Gong

Living in a rigid exoskeleton means that a crustacean can increase in body size only in the time period between when an old exoskeleton is shed and the new one hardens up. I'm always curious about exactly how much crabs grow when they molt. So today I measured the crab and her old carapace at the same place, halfway between the two points on the lateral edges of the carapace. Huzzah for empirical data! The old carapace measured 27.6mm across, and the new one 33.8mm, for an increase in width of 6.2mm or 22.5%. Mind you, this is simply the increase in one linear dimension of the crab's body. To obtain a more accurate measurement of body size increase, I'd have to have weighed the crab immediately before her molt and after it. Still, it does give an estimation of how much bigger a body part can get when a crab molts.

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