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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.

Five days ago I collected the phoronid worms that I wrote about earlier this week, and today I'm really glad I did. I noticed when I first looked at them under the scope that several of them were brooding eggs among the tentacles of the lophophore. My attempts to photograph this phenomenon were not entirely successful, but see that clump of white stuff in the center of the lophophore? Those are eggs! Oh, and in case you're wondering what that tannish brown tube is, it's a fecal pellet. Everyone poops, even worms!

Lophophore of a phoronid worm (Phonoris ijimai)
18 Septenber 2017
© Allison J. Gong

Based on species records where I found these adult worms, I think they are Phoronis ijimai, which I originally learned as Phoronis vancouverensis. The location fits and the lophophore is the right shape. Besides, there are only two genera and fewer than 15 described species of phoronids worldwide.

Two days after I first collected the worms, I was watching them feed when I noticed some tiny approximately spherical white ciliated blobs swimming around. Closer examination under the compound scope showed them to be the phoronids' larvae--actinotrochs! Actinotrochs have been my favorite marine invertebrate larvae--and that's saying quite a lot, given my overall infatuation with such life forms--since I first encountered them in a course in comparative invertebrate embryology at the Friday Harbor Labs when I was in graduate school.

2-day-old actinotroch larva of Phoronis ijimai
22 September 2017
© Allison J. Gong

The above is a mostly top-down view on an actinotroch, which measured about 70 µm long. They swim incredibly fast, and trying to photograph them was an exercise in futility. They are small enough to swim freely in a drop of water on a depression slide, so I tried observing them in a big drop of water under a coverslip on a flat glass slide. At first they were a bit squashed, but as soon as I gave them enough water to wiggle themselves back into shape they took off swimming out of view.

Here's the same photo, with parts of the body labelled:

2-day-old actinotroch larva of Phoronis ijimai
22 September 2017
© Allison J. Gong

The hood indicates the anterior end of the larva and the telotroch is the band of cilia around the posterior end. The hood hangs down in front of the mouth and is very flexible. At this stage the larva possesses four tentacles, which are ciliated and will get longer as the larva grows. These are not the same as the tentacles of the adult worm's lophophore, which will be formed from a different structure when the larva undergoes metamorphosis.

As usual, a photograph doesn't give a very satisfactory impression of the larva's three-dimensional structure. There's a lot going on in this little body! The entire surface is ciliated, and this actinotroch's gut is full of phytoplankton cells. You can see a lot more in the video, although this larva is also a little squished.

I've been offering a cocktail of Dunaliella tertiolecta and Isochrysis galbana to the adult phoronids, and these are the green and golden cells churning around in the larva's gut. However, good eaten is not necessarily food digested, and the poops that I saw the larvae excrete looked a lot like the food cells themselves. Today I collected more larvae from the parents' bowl and offered them a few drops of Rhodomonas sp., a cryptonomad with red cells. This is the food that we fed actinotrochs in my class at Friday Harbor. We didn't have enough time then to observe their long-term success or failure, but I did note that they appeared to eat the red cells.

I don't know if phoronids reproduce year-round. It would be a simple task to run down and collect a few every month or so and see if any worms are brooding. Now that I know where they are, it would also be a good idea to keep an eye on the size of the patch. Some species of phoronid can clone themselves, although I don't know if P. ijimai is one of them. In any case, even allowing for the possibility of clonal division, an increase in the size of the adult population would be at least partially due to recruitment of new individuals. If recruitment happens throughout the year, it follows logically that sexual reproduction is likewise a year-round activity. Doesn't that sound like a nifty little project?

Besides, it's never a bad idea to spend time at the harbor!

1

If I asked you to draw a worm and designate the front and back ends, you'd most likely come up with something that looks like this:

And you would be entirely correct. A worm, or any creature described as 'vermiform' for that matter, has an elongated, wormlike body. Some worms have actual heads with eyes and sensory tentacles, but many don't. The great many polychaete worms that live in tubes don't have much of a head at all: usually all you can see sticking out of the tube is a crown of tentacles used for feeding. Although even the use of the word 'crown' more than suggests the presence of a head, doesn't it? After all, where else does one wear a crown?

Polychaete worms, Phragmatopoma californica, sticking their 'heads' out of their tubes at Natural Bridges
26 May 2016
© Allison J. Gong

Most worms, including the worm that we imagined above, are bilaterally symmetrical, with bodies elongated along the Anterior-Posterior axis. This means the head is at the anterior end and the rear is the posterior end. For animals that don't have a prominent head, the Anterior can also be defined by the direction of locomotion. Worms crawl with their bellies against the ground, which sets up a second axis of symmetry, the Dorsal-Ventral axis. The third axis of symmetry is the Left-Right axis. These axes should sound familiar, because they apply to our own bodies, as well of those of all other vertebrates and many invertebrates. Because of our upright stance we actually walk with our ventral surface forward, which is a little confusing, but if you don't trust me you can see for yourself by crawling around on hands and knees for a while.

Now back to our worms, hypothetical and otherwise. Consider a worm that is elongated not along its Anterior-Posterior axis, but along its Dorsal-Ventral axis. It sounds strange, but such worms do exist. They are called phoronid worms, and are classified within their own phylum, the Phoronida. They all live in tubes, and the few times I've seen them they have been in pretty dense aggregations. As with most tube-dwelling worms the only part of the body that you can usually see is the crown of feeding tentacles, which in these animals (as well as in the Bryozoa and Brachiopoda) is called a lophophore.

The other day I was at the harbor looking for slugs with my friend Brenna, and spotted these pale tentacles swaying in the current.

Phoronids at the Santa Cruz Yacht Harbor
18 September 2017
© Allison J. Gong

These are the lophophores of an aggregation of phoronids! I'd never seen them at the harbor before, so I was pretty excited about it. They were on the side of a floating walkway, down almost beyond the reach of my outstretched arm. The current caused the lophophores to sway continuously and I was barely able to snap some blurry photos without falling in (I couldn't really see what I was doing and just hoped for the best) when I accidentally caught this one shot. I wanted to have at least one clear-ish shot to submit to iNaturalist. I did manage to scrape off some bits of stuff that I hoped contained intact phoronids, so I could observe them under the dissecting scope at the lab.

And these are some lovely little worms!

The tubes that these phoronids inhabit are more like burrows of slime to which the surrounding sediments adhere. The tube itself isn't anything particularly interesting, but the bodies of the worms are beautifully transparent. One of the coolest things you can see in a living phoronid is its circulatory system. They have red blood that, like ours, contains hemoglobin, so it's easy to see the vessels that run along the length of the worm (which is the Dorsal-Ventral axis, remember) and the two blood rings around the base of the lophophore. If you get the lighting right you can even see the vessels that extend into each tentacle of the lophophore.

Single phoronid worm extending its lophophore
18 September 2017

I was disappointed to see that none of the video clips I took really do justice to these worms. They are so pretty when I look at them through the microscope, and I wish I could capture their beauty. You may at least be able to see blood moving through the larger vessels of the body in this short video.

Seems I need to upgrade my photomicroscopy set-up. Anybody have a few thousand bucks they want to donate to the cause?

I'm keeping the phoronids for as long as I can, although I don't know what to feed them. I had time to take just a quick look at them this morning, and they look fine. Just for kicks I offered them a little phytoplankton to see what they'd do with it and couldn't see if they were reacting at all. Still, they are filter feeders, and if I can adjust the lighting and get a good view of those ciliated tentacles I should be able to see if they are creating a water current that is bringing food to the mouth. Friday is the next day I have time to spend with these animals that I don't get to see very often. Maybe then I'll have something else to report.

For several centuries now, Earth's only natural satellite has been associated with odd or unusual behavior. Lunatics were people we would describe today as mentally ill, who behaved in ways that couldn't be predicted and might be dangerous. The erratic behaviors were attributed to the vague condition of lunacy. These words are derived from the Latin luna, which means 'moon'. The cycles of the moon have long been thought to influence human behavior as well; hence such legends as the werewolf.

We do know that the moon indeed has a very strong influence on aspects of many organisms, primarily through the tides. For example, reproduction in many marine animals is timed to coincide with a particular point in the tidal cycle. Grunion (Leuresthes tenuis, small, silver, finger-shaped fishes) run themselves up onto California beaches at night to spawn following the full and new moon high tides in the early summer months. Corals in the Great Barrier Reef spawn together in the handful of nights after the full moon in November. Animals such as these, which reproduce via broadcast spawning, are the ones most likely to benefit from synchronized spawning; after all, there is no point in spawning if you're the only one doing it. Invertebrates don't have watches or calendars; they keep time by sensing the natural cycles of sun and moon. The moon's strong effect on the tides is a signal that all marine creatures can sense and use to coordinate spawning, increasing the probability of successful fertilization for all.

Last night, Wednesday 6 September 2017, the moon was full. Yesterday at the lab, I noticed that  the large Anthopleura sola anemones living in the corner of my table had spawned.

A male Anthopleura sola anemone that had spawned
6 September 2017
© Allison J. Gong

That diffuse grayish stuff in the right-hand side of the photo is a pile of sperm. I looked at a sample under the microscope, just to be sure. By this time they had been sitting at the bottom of the table for several hours and most of them were dead. But they were definitely sperm:

Whenever I see something unusual like this my first impulse is to see if it's happening anywhere else at the lab. So I started poking around. The aquarists at the Seymour Center told me that some of their big anemones had spawned in the past couple of days; however, since they clean and vacuum the tanks every day all evidence was long gone.

Fortunately there are several A. sola anemones in other labs that aren't cleaned as regularly as the public viewing areas. One of the animals in the lab next door to where I have my table had also spawned. . .

Female Anthopleura sola
6 September 2017
© Allison J. Gong

. . . and this one is a female! What looks like a pile of fine dust is actually a pile of eggs.

Eggs of Anthopleura sola
6 September 2017
© Allison J. Gong

And the eggs are really cool. See those spines? They are called cytospines and apparently deter predation. Other species in the genus Anthopleura (A. elegantissima and A. xanthogrammica) are known to have spiny eggs, so it appears that this is a shared feature. Now, if only I could get my hands on eggs of the fourth congeneric species--A. artemisia, the moonglow anemone--that occurs in our area, I'd know for certain, at least for California species. I examined the eggs under higher magnification, but due to their opacity I couldn't tell if the had been fertilized. Most appeared to be solid single undivided cells; they could, however, be multicellular embryos.

All told, of the anemones that had obviously spawned, 1 was female and 4 were male. I sucked up some of the eggs and put them in a beaker of filtered seawater. I doubt that anything will happen, but I may be in for a pleasant surprise when I check on them tomorrow.

We humans are accustomed to thinking of sexual function as being both fixed and segregated into bodies that we designate as either Female or Male. And while we, as a species, generally do things this way, in the larger animal kingdom sexual function doesn't always follow these rules. Many animals are monoecious, or hermaphroditic, having both male and female sex organs in the same body. Not only that, but lots of animals change from one sex to the other. As in so many aspects of biology, the way humans do things may be thought of by us as "normal," but it isn't the most interesting way.

Take, for example, the slipper shell Crepidula adunca. This is a small limpet-like creature that lives on the shell of a larger snail. Around here the usual host is a turban snail, either Tegula funebralis or T. brunnea.

Slipper shell (Crepidula adunca) on its host, the turban snail Tegula brunnea, at Pigeon Point
1 May 2017
© Allison J. Gong

There are several species in the genus Crepidula, including C. fornicata, which lives on the Atlantic coast of North America. The species epithet gives an inkling of how reproduction occurs in at least these two species of the genus.

Sometimes C. adunca is found in stacks. I've never seen a stack taller than three individuals, but C. fornicata occurs in stacks of about six. The animal at the bottom of the stack is always the largest, and a given turban snail can play host to more than one stack at a time.

Two stacks of Crepidula adunca on the turban snail Tegula funebralis, at Pigeon Point
28 June 2017
© Allison J. Gong

As you might guess, it isn't mere happenstance that these stacks of C. adunca occur. It turns out that this unusual living arrangement is key to both sexual function and eventual reproduction in this species. The individual on the bottom of the stack (i.e., the oldest) is always a female; those at the top of the stack (i.e., the youngest) are males. However, every stack begins with a single individual, and the default sex in newly settled C. adunca is male. An experiment conducted at Friday Harbor in Washington State1 showed the change from male to female began when the snails reached a size of 7 mm, and all animals larger than 10 mm were female. Animals that begin life as male and transform into females are described as protandrous hermaphrodites. How common is this phenomenon? Not uncommon among fishes, actually. Clownfishes in the genus Amphiprion are protandrous. Remember how in the beginning of the moving Finding Nemo, Nemo's mom dies? Well, in real life Nemo's dad would have become his new mom!

In any case, all C. adunca begin adult life as males. If they live long enough to reach about 7 mm in length, they might get to become females. Crepidula adunca's unusual living arrangement also facilitates reproduction. Unlike most limpet-like gastropods, C. adunca isn't a broadcast spawner. Rather, it copulates, as hinted at by the species epithet of its congener C. fornicata. A female slipper shell with a male on her back has a convenient source of sperm with which to fertilize her eggs:  the male reaches into her mantle cavity and transfers sperm to her. Given the constraint of copulation, a female cannot mate until she carries at least one male on her back, and a male cannot reproduce unless he settles atop a female. Once the eggs have been fertilized, they develop within the mother's mantle cavity until she pushes them out as little miniatures of herself.

Crepidula adunca on the turban snail Tegula brunnea, at Davenport Landing
27 May 2017
© Allison J. Gong

Cool little animals, aren't they? They remind us not to think of ourselves as The Way Things Are Done. We have a lot to learn from creatures that are not like us, and it's stories like these that ensure I will never lose my appreciation and love for the marine invertebrates.

 


1 Collin, R. 2000. Sex Change, Reproduction, and Development of Crepidula adunca and Crepidula lingulata (Gastropoda: Calyptraeidae). The Veliger 43(l):24-33.

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