It has been a while since I've spent any time in the intertidal. There isn't really any reason for this, other than a reluctance to venture out in the afternoon wind and have to fight encroaching darkness. There's also the fact that I much prefer the morning low tides, which we'll have in the spring. However, this past weekend we had some spectacular afternoon lows, and although I was working on Friday and couldn't spare the time to venture out, I went out on Saturday and Sunday.
Saturday was a special day, because I had guests with me. A woman named Marla, who reads this blog, contacted me back in the fall. She said she wanted to do something special for her husband's birthday, and asked if I'd be willing to take them to the intertidal. It turns out that Andrew's birthday was around this past weekend, and he had family coming out from Chicago to celebrate. They picked the perfect weekend, because the low tides we had were some of the lowest of the year. So on Saturday I met up with Marla, Andrew (her husband), and Betsy (Andrew's sister) and we all traipsed out to Natural Bridges.
This was our destination for the afternoon:
Taking civilians into the intertidal can be tricky, because they often come with expectations that don't get met. Like expecting to see an octopus, for example. I explain that the octopuses are there, but are better at hiding from us than we are at finding them, but that never feels very satisfactory. This trio, however, were fun to show around. The tide was beautifully low and we had fantastic luck with the weather. It had rained in the morning, but the afternoon was clear and sunny. I congratulated Marla on remembering to pay the weather bill. And the passing stormlet didn't come with a big swell, so the ocean was pretty flat. We were able to spend some quality time in the mid-tidal zone, with occasional forays into the low intertidal.
The typical Natural Bridges fauna--owl limpets, mussels, chitons, anemones, etc.--were all present and accounted for. Of course, there isn't much algal stuff going on in mid-January.
Given the time of year (mid-January) and the time of day (late afternoon), the sun was coming in at a low angle. This was tricky for photographing, both in and out of water. However, sometimes good things happen, as in this photo below:
That's a big kelp crab (Pugettia producta) nestled among four sunburst anemones (Anthopleura sola). Kelp crabs are pretty placid creatures, for crabs, and usually take cover when approached. But this one remained in plain sight, holding so still that I thought it was dead. Even when I hovered directly over it and blocked the sun, it didn't move at all. Then it occurred to me that maybe he was having the sexy times with a lady friend. So I very carefully reached down and gave him a tap on the carapace. He flinched a little, so I knew he wasn't dead, but made no move to get away. And I caught a glimpse of a more golden leg underneath him.
Crabs live their entire lives encased in a rigid exoskeleton, and can mate only during a short window of opportunity after a female molts. Early in the breeding season, a female crab uses pheromones to attract nearby males. When a suitable male approaches, she may let him grab her in a sort of crabby hug. That's what this male kelp crab is doing to his mate. They may remain in this embrace for several days, waiting until the female molts and her new exoskeleton is soft. At that point the male will use specialized appendages to insert packets of sperm into the female's gonopores. The two will then go their separate ways.
We didn't disturb these crabs, and let them go on doing their thing. By now the sun was going down, so we headed back up and were rewarded with a glorious sunset.
The intertidal sculpins are delightful little fish with lots of personality. They're really fun to watch, if you have the patience to sit still for a while and let them do their thing. A sculpin's best defense is to not be seen, so their first instinct is to freeze where they are. Then, if a perceived threat proves to be truly frightening, they'll scoot off into hiding. They can also change the color of their skin, either to enhance camouflage or communicate with each other.
Around here we have a handful of sculpin species flitting around in our tidepools. Sculpins can be tricky to identify even if you have the fish in hand--many of the meristics (things you count, such as hard spines and soft rays in the dorsal fin, or the number of scales in the lateral line) used to distinguish species actually overlap quite a lot between species. The fishes' ability to change color means that skin coloration isn't a very reliable trait. When I was in grad school there was another student in my department who was studying the intertidal sculpins, and she told me that most of the ones we see commonly are either woolly sculpins (Clinocottus analis) or fluffy sculpins (Oligocottus snyderi). I've developed a sort of gut feeling for the gestalt of these species, but I'm not always 100% certain of my identifications.
Anyway, back to the camouflaged sculpins. The ability to change the color of the skin means that sculpins can match their backgrounds, which comes in very handy when there isn't anything to hide behind. Since the environment is rarely uniformly colored, sculpins tend to have mottled skin. Some can be banded, looking like Oreo cookies. The fish in this photo lives in a pool with a granite bottom. The rock contains large quartz crystals and is colonized by tufty bits of mostly red algae. There is enough wave surge for these fist-sized rocks to get tumbled about, which prevents larger macroalgae from colonizing them.
Other shallow pools higher up in the intertidal at Asilomar have a different type of rocky bottom. The rocks lining the bottom of these pools are whitish pebbles that are small enough to be tossed up higher onto the beach. I don't know whether or not these pebbles have the same mineral content as the larger rocks lower in the intertidal, but they do have quartz crystals. The pebbles are white. So, as you may have guessed, are the sculpins!
Other intertidal locations have different color schemes. On the reef to the south of Davenport Landing Beach, you will see a lot of coralline algae. Some pools are overwhelmingly pink because of these algae. Bossiella sp. is a common coralline alga at this location.
What color do you think the sculpins are in these pools?
Give yourself a congratulatory pat on the back if you said "pink"!
Sculpins aren't the only animals to blend in with coralline algae. Some crustaceans are remarkably adept at hiding in plain sight by merging into the background. Unlike the various decorator crabs, which tuck bits and pieces of the environment onto their exoskeletons, isopods hide by matching color.
Turning over algae and finding hidden creatures like these is always fun. For example, I saw these isopods at Pescadero this past summer. See how beautifully camouflaged they are?
Sometimes, when you're not looking for anything in particular, you end up finding something really cool. Last weekend I met up with students in the Cabrillo College Natural History Club for a tidepool excursion up at Pigeon Point. We were south of the point at Whaler's Cove, where a staircase makes for comparatively easy access to the intertidal.
It's fun taking students to the intertidal because I enjoy helping them develop search images for things they've never seen before. There really is so much to see, and most of it goes unnoticed by the casual visitor. Often we are reminded to "reach for the stars," when it is equally important to examine what's going on at the level of your feet. That's the only way you can see things like this chiton:
Mopalia muscosa is one of my favorite chitons. It is pretty common up and down the California coast. However, like most chitons it is not very conspicuous--it tends to be encrusted with algae! This individual is exuberantly covered with coralline and other red algae and has itself become a (slowly) walking bit of intertidal habitat. It is not unusual to see small snails, crustaceans, and worms living among the foliage carried around by a chiton. Other species can carry around some algae, but M. muscosa seems to be the most highly decorated chiton around here. I showed this one to some of the students, who then proceeded to find several others. A search image is a great thing to carry around!
Compared to the rocky intertidal, a sandy habitat can be a difficult place to live. Sand is inherently unstable, getting sloshed to and fro with the tides. Because of this instability there is nothing for holdfasts to grab, so there are many fewer algae for animals to eat and hide in. Most of the life at a sandy beach occurs below the surface of the sand, and is thus invisible to anyone who doesn't want to dig. There's a beach at Whaler's Cove where I've found burrowing olive snails (Olivella biplicata) plowing along just below the surface. I wanted to show them to the students, so I waded in and rooted around. I did find Olivella, but I also found a burrowing shrimp. I think it's a species of Crangon.
Now that is some damn fine camouflage! If the shrimp didn't cast its own shadow, it would be invisible. Even so, it was clearly uneasy sitting on the surface like that. I had only a few seconds to shove the camera in the water and snap a quick photo before the shrimp wriggled its way beneath the sand again.
As I've said before, observation takes practice and patience. To look at something doesn't mean you truly see it. That's why it is so important to slow down and let your attention progress at the pace of the phenomenon you're observing. If the only things that catch your eye are the ones that flit about, then I can guarantee you will never find a chiton in the intertidal. And wouldn't that be a sad thing?
When we stop to marvel at the wonders of the natural world, we usually forget about all the life that is going on that we don't get to see. But there is a lot happening in places we forget to look. For example, any soil is an entire ecosystem, containing a variety of small and tiny animals, bacteria, and fungi. In fact, if a fungus didn't send up a fruiting body (a.k.a. mushroom) every once in a while, most observers wouldn't realize it was there at all. We humans tend to behave as though something unseen is something that doesn't exist, and I admit to the very same thinking with regards to my own kitchen: anything stored way up in cupboards I can't reach, may as well not be there at all.
But there are places where we can witness the life occurring below our feet, and floating docks in marinas and harbors are some of the best. Of course, the trick is to "get your face down where your feet are", a piece of advice about how to observe life in tidepools that applies just as well to investigating the dock biota. Once you get used to the idea of lying on the docks, which can be more or less disgusting depending on time of year and number of birds hanging around, a whole new world literally blossoms before your eyes.
Some of the flower-looking things are indeed anthozoans ('flower animal') such as this plumose anemone:
and this sunburst anemone:
Other animals look like dahlias would look if they were made of feathers. Maybe that doesn't make sense. But see what I mean?
This is Eudistylia polymorpha, the so-called feather duster worm. These worms live in tough, membranous tubes attached to something hard. They extend their pinnate tentacles for feeding and are exquisitely sensitive to both light and mechanical stimuli. There are tiny ocelli (simple, light-sensing eyes) on the tentacles, and even casting a shadow over the worm causes it to pull in its tentacles very quickly. This behavior resembles an old-fashioned feather duster, hence the common name. These were pretty big individuals, with tentacular crowns measuring about 5 cm in diamter. Orange seems to be the most common color at the Santa Cruz harbor.
One of the students pointed down at something that he said looked like calamari rings just below the surface. Ooh, that sounds intriguing!
And he was right! Don't they look like calamari rings? But they aren't. These are the egg ribbons of a nudibranch. They appeared to have been deposited fairly recently, so I went off on a hunt for the likely parents. And a short distance away I caught the nudibranchs engaging in the behavior that results in these egg masses. Ahem. I don't know if the term 'orgy' applies when there are three individuals involved, but that's what we saw.
To give you some idea of how these animals are oriented, that flower-like apparatus is the branchial (gill) plume, which is located about 2/3 of the way down the animal's dorsum. The anterior end bears a pair of sensory organs called rhinophores; they look kind of like rabbit ears. You can see them best in the animal on the left.
When you see more than one nudibranch in such immediate proximity it's pretty safe to assume that they were mating or will soon be mating. Nudibranchs, like all opisthobranch molluscs, are simultaneous hermaphrodites, meaning that each can mate as both a male and a female. The benefit of such an arrangement is that any conspecific individual encountered is a potential mate. The animals pair up and copulate. I'm not sure if the copulations are reciprocal (i.e., the individuals exchange sperm) or not (i.e., one slug acts as male and transfers sperm to the other, which acts as female). In either case, the slugs separate after mating and lay egg masses on pretty much whatever surface is convenient. Each nudibranch species lays eggs of a particular morphology in a particular pattern. Some, such as P. atra, lay eggs in ribbons; others produce egg masses that look like strings of miniature sausages.
This is the first time I've seen big Polycera like these. The slugs were about 4 cm long. They eat a bryozoan called Bugula, and there is a lot of Bugula growing at the harbor these days. Maybe that's why there were so many Polycera yesterday. Nudibranchs are the rock stars of the invertebrate world--they are flamboyantly and exuberantly colored, have lots of sex, and die young. They can be very abundant, but tend to be patchy. Quite often an egg mass is the only sign that nudibranchs have been present.
The next time you happen to be at a marina poke your head over the edge and take a look at the stuff living on the dock. Even if you don't know what things are, you should see different textures and colors. With any luck, you'll be pleasantly surprised at the variety of life you find under your feet.
Be honest now. When you think of clams, what comes to mind? If you're like most people, visions of clams steamed in white wine, garlic, and butter might dance in your head. Or perhaps clams in cioppino or a hearty chowder would be your go-to. In any case, I doubt that clams, as actual living creatures, occupy much of your brain. Because let's face it, at first glance even living clams aren't the most energetic and charismatic animals. Most of the really cool things that they do, like suck water through their shells for filter feeding and gas exchange, they do while buried in the mud.
When you think about it, though, just the fact that clams live in the sand or mud while depending on water that may be quite far from them is rather amazing. All animals require oxygen, and for marine animals that oxygen comes from seawater. Animals that move freely through the water have access to a ready supply of oxygen. But clams live more or less fixed lives encased in sediment, and water can be quite far from their bodies. How, then, do they pull water into their shells and across their gills? They use siphons, which can reach up to the surface of the sediment into the water column.
A clam has two siphons--one pulls clean water into the shells and the other expels water from the shells. This arrangement allows for one-way flow across the gills, which serve double duty as both feeding and gas exchange organs. The siphons themselves are somewhat muscular and can open and close, but it's the ciliary action of the gills that create the actual water current. In a living clam the only visible body parts are the siphons, which in some species (e.g., geoducks) are so large that they cannot be entirely withdrawn into the shells.
Of the two siphons in the picture above, can you tell which is the incurrent and which is the excurrent? What do you think is the functional significance of that network of white structures that cover the opening of one of the siphons?
Not only do clams live buried in sediment, but some of them can actually bore into rocks. These boring clams, the pholads, have shells that are morphologically and functionally different from the typical clams you've encountered in cioppino. They are elongated on the anterior-posterior axis and the anterior ends are heavily sculpted and fortified to grind into rock. Of course, they can do this only in areas where the rock is soft--you don't see pholads burrowed into granite, for example.
Fortunately for the pholads, much of the rock in the Santa Cruz area is a soft mudstone, easily eroded and burrowed into. I've seen pholads at intertidal sites from Capitola to Davenport. Both dead pholads and live pholads can be seen, but it takes a careful eye to spot the live ones. Of course, all you'd ever see of a living pholad is the siphons. When the animal dies, though, the shells are left behind. As the mudstone continues to erode the shells can be exposed, just like fossils. And as a matter of fact, the mudstone formations around here are known for their fossil contents. I think, but am not certain, that these empty shells in holes belong to Parapholus californica.
How does a clam burrow into even soft rock? A description of burrowing activity of Parapholus californica can be read here. As you can imagine, it's a slow and continuous process. Fortunately, these clams don't have much else going on and can take their time. In some ways, their lifestyle sounds pretty ideal: hang out in a snug burrow where predators can't get at your soft body and extend your siphons out to bring in clean water for food and oxygen. Sure, when it comes to reproduction the only option available is free-spawning and hoping for the best, but that has proven to be a successful strategy for countless generations of your kind. Aside from the cost of making gametes, it's a pretty low-energy way to produce offspring. Maybe the old saying "happy as a clam" isn't that far off the truth.
Combine the words "gold" and "California" and you automatically come up with the Gold Rush, don't you? After all, California is the Golden State. And while that nickname may be to honor the golden hills of summer or the poppies that are the state flower, it may also be a tribute to the discovery of gold in 1848. For better or worse, the Gold Rush initiated rapid development of this area, and California eventually became the 31st state in 1850.
For me, and I suspect for many people, gold is one of the quintessential colors of autumn. Yet here we are in the middle of winter heading towards spring, and I saw a lot of gold in the forest the other day. I had taken my Ecology students to Rancho del Oso for the first field trip of the semester and set them loose to saunter through the woods and practice noticing (and recording) patterns in nature. Incidentally, I have adopted the word 'saunter' as a replacement for 'hike' for most of my own outdoor adventures. I have always been a slow hiker, and felt that in order to keep up with other people I had to miss seeing what was going on around me. Not to mention the fact that I'm always stopping to take pictures or examine some weird thing on the ground, or in the trees, or wherever. By giving myself permission to saunter along at the pace at which nature occurs, I have time to slow down and observe more carefully, and come away with a much better understanding of the world I've passed through. It certainly doesn't work for everybody, but I've learned that the journey is as important as the final destination, and that has made hiking sauntering much more enjoyable for me.
So, back to the gold. One of the very first thing I noticed when we hit the trail was this brilliant yellow-orange slime mold growing on twigs on the forest floor. This area is a mixed forest of hardwoods (mostly oaks) and various pines. I can't be certain what these sticks hosting the slime mold are, but they may be some kind of pine.
Slime molds are very strange organisms that don't fit into any of the major eukaryotic kingdoms of life (Animalia, Plantae, or Fungi). The current taxonomic position of slime molds is up for debate and far from settled, so I won't go into it here. Like fungi, slime molds feed on dead and decaying plant matter and are part of the decomposer niche of organisms. Also like fungi, most of a slime mold's life is microscopic. In the case of fungi most of the body, called a mycelium, is a network of extremely thin threads called hyphae. The mycelium for most fungi is underground and thus invisible to the casual observer. What we call a mushroom is only the reproductive fruiting body, which pushes to the surface so that spores can be released into the air.
For most of the time, or at least as long as food is plentiful, a slime mold exists as single amoeba-like or flagellated cells that feed on bacteria. These cells are haploid, containing only one set of chromosomes. Sexual reproduction (labelled SYNGAMY in the figure below) occurs when an amoeba-like cell encounters a compatible flagellated cell. I would also be willing to bet that the amoeboid and flagellated cells are triggered to find each other and initiate syngamy when food is scarce, as is the case with many animals.
The result of syngamy in a slime mold is a zygote which develops into a macroscopic stage called the plasmodium. The plasmodium undergoes nuclear division multiple times but cytokinesis doesn't occur, resulting in a large cell bounded by a single plasma membrane and containing many nuclei. In animal tissues we describe this condition as syncytial; I don't know if the same word is used by slime mold specialists, but the concept applies.
One of the things that makes slime molds truly bizarre is their method of locomotion. Using time-lapse videography, you can actually see how the contents of the cell swash back and forth in a process called cytoplasmic streaming. The net result of all this cytoplasmic streaming is the physical movement of the plasmodium into new territory. It's a process much easier to understand if you can see it, so here's a video from KQED's Deep Look series:
As with many fungi, slime molds are difficult to identify if you don't see the fruiting body. The slime mold that we encountered the other day was an immature plasmodium that hadn't yet produced fruiting bodies. The experts who took a look at my observation on iNaturalist agreed that it is likely Leocarpus fragilis, based on location and time of year, but they cannot be certain.
Continuing with our theme of gold, we saw several small blotches of golden jelly growing on tree trunks. These were the Tremella fungi. There are two species of golden Tremella in our region, T. mesenterica and T. aurantia. It seems that differentiation between the species depends on examination of microscopic structures, so I am unable to tell which species this little blob is. However, I will point out that the species epithet aurantia means 'gold', so I really hope that's the name for this blob.
Saving the best for last! Moving away from the creek and into the more enclosed forest we entered the realm of everybody's favorite terrestrial pulmonate gastropod, the banana slug. They were out in full force, chowing down on mushrooms and sliming up the foliage. One of my students picked up a banana slug and let it crawl on her hand for a while, but to my knowledge nobody licked one. All of the banana slugs that I saw were bright yellow with no brown or gray blotches, so I conclude that they were either Ariolimax californicus (the so-called Peninsula banana slug) or A. dolichophallus (the Santa Cruz banana slug, also the school mascot for UC Santa Cruz).
But this is where things get interesting. According to their mitochondrial DNA these two species, A. californicus and A. dolichophallus, do not have overlapping ranges. And the dividing line between them is Rancho del Oso, with A. californicus occurring to the north and A. dolichophallus occurring to the south. So, if Rancho del Oso is the magic line defining the ranges of these two species, what species are the slugs at Rancho del Oso? I think that answering this question will require a much finer scale study. For now, I'm just going to call them Ariolimax sp., because that seems to be the safest option until things get sorted out.
I've written about banana slugs before, but I've never had a chance to photograph them doing the actual nasty. Luckily for me and the students, banana slugs have no shame. I think the entire class got to get a close look and photos of this copulating pair:
This perfect yin-yang symbol is the result of how banana slugs align themselves during copulation. Each hermaphroditic slug has a genital open behind the head on the right side of the body. There's a lot of kinky stuff that happens during banana slug sex, including the chewing off of one partner's penis, but suffice to say that one animal's penis is inserted into the vagina of the other and, well, we don't know how quickly sperm is transferred, but the animals remain locked together for several hours. Yes, HOURS. Ahem. The penis chewing thing doesn't happen every time slugs mate, and biologists are still trying to figure out the function for this unusual behavior.
We have another several weeks (hopefully!) of rainy weather, so there will be lots of time to explore the world of fungi, slime molds, and banana slugs. The combination of rain and lengthening days creates great conditions to revel in the gold of a California winter in the forest.
Every once in a while some random person drops off a creature at the marine lab. Sometimes the creature is a goldfish that had been a take-home prize at a wedding over the weekend (now weddings taking place at the Seymour Center are not allowed to include live animals in centerpieces). Once it was a spiny lobster that spent the long drive up from the Channel Islands in a cooler, and became the Exhibit Hall favorite, Fluffy. This time the objects had been collected off the beach and brought in by somebody who thought they might still be alive.
These white objects are egg masses of the California market squid, Doryteuthis opalescens, that had been cast onto the beach at Davenport. Sometimes the masses are called fingers or candles, because they're about finger-sized. Each contains dozens of large eggs. Squids, like all cephalopods, are copulators, and after mating the female deposits a few of these fingers onto the sea floor. Many females will lay their eggs in the same spot, so the eggs in this photo represent the reproductive output of several individuals. The cephalopods as a group are semelparous, meaning that they reproduce only once at the end of their natural life; salmons are also semelparous. After mating, the squids die. Not coincidentally, the squid fishing season is open right now, the idea being that as long as the squids have reproduced before being caught in seines, little harm is done to the population. Most of the time the squids are dispersed throughout the ocean, and the only time it is feasible to catch them in large numbers is when they gather to mate.
These egg masses look vulnerable, but they're very well protected. The outer coating is tough and leathery, and the eggs must taste bad because nothing eats them. I've fed them to anemones, which will eat just about anything, and they were spat out immediately.
The eggs were brought to the Seymour Center because the person who brought them in thought they might make a good exhibit. I happened to be there that day and got permission to take a small subset of the bunch so I could keep an eye on them. And they did and still do make a good exhibit.
16 April 2018: I obtain squid eggs!
At this stage it is impossible to tell whether or not the eggs are alive. The only thing to do was wait and see.
30 April 2018: After waiting two weeks with apparently no change, I decided it was time to look at the egg fingers more closely again. Lo and behold, they are indeed alive! Look at the pink spots in the individual eggs--those are eyes. And if you can see the smaller pink spots, those are chromatophores, the 'color bodies' in the squids' skin that allow them to perform their remarkable color changes.
9 May 2018: A week and a half later, the embryos definitely look more like squids! Their eyes and chromatophores have darkened to black now. The embryos are also more active, swimming around inside their egg capsules. You can see the alternating contraction and relaxation of the mantle, which irrigates the gills. Squids have two gills. More on that below.
At this point the squid fingers began to disintegrate and look ragged. They became flaccid and lightly fouled with sediment.
14 May 2018 (today): Almost a month after they arrived, my squid eggs look like they're going to hatch soon! I didn't see any chromatophore flashing, though.
In the meantime, some of the eggs on exhibit in the Seymour Center have already started hatching. The first hatchlings appeared on Friday 11 May 2018. The hatchlings of cephalopods are called paralarvae; they aren't true larvae in the sense that instead of having to metamorphose into the adult form, they are miniature versions of their parents.
Peter, the aquarium curator at the Seymour Center, allowed me to take a few of the paralarvae in his exhibit and look at them under the scope. The squidlets are about 3mm long and swim around quite vigorously. Trying to suck them up in a turkey baster was more difficult than I anticipated. But I prevailed!
You can actually see more of what's going on in a video:
The cup-shaped layer of muscular tissue that surrounds the squid's innards is the mantle. When you eat a calamari steak, you are eating the mantle of a large squid.The space enclosed by the mantle is called the mantle cavity. Because the paralarvae are transparent you can see the internal organs. Each of those featherlike structures is a ctenidium, which is the term for a mollusk's gill. The ventilating motions of the mantle flush water in and out of the mantle cavity, ensuring that the gill is always surrounded by clean water.
And now we get to the hearts of the matter. At the base of each gill is a small pulsating structure called a branchial heart ('branch' = Gk: 'gill'). It performs the same function as the right atrium of our own four-chambered heart; that is, boosting the flow of blood to the gas-exchange structure. So that's two hearts. Between the pair of branchial hearts is the systemic heart, which pumps the oxygenated blood from the gills to the rest of the squid's body. This arrangement of multiple hearts, combined with a closed circulatory system, allows cephalopods to be much more active swimmers and hunters than the rest of their molluscan kin.
I expect that my fingers will hatch very soon. If and when they do, it will be a challenge getting them to eat. I've never tried it myself, and cephalopods are known to be difficult to rear in captivity. But I'm willing to give it a shot!
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.
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.
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.
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.
One of the defining characteristics of the Phylum Mollusca is the possession of a shell, which serves both as a protective covering and an exoskeleton. We've all seen snails, and some people may have noticed that snails often withdraw entirely into their shells and even have a little door that they can use to seal up the opening of the shell. That little door is called the operculum. Opercula occur in non-molluscan animals, too, such as some of the tube-dwelling polychaete worms and some of the thecate hydroids. Snail opercula come in lots of different shapes, depending on the aperture of their owner's shell.
Given the enormous morphological diversity within the Mollusca it shouldn't be surprising that their shells vary immensely in prominence and shape. In fact, molluscan shells demonstrate quite beautifully the relationship between form and function. The benthic and most familiar molluscs, the gastropod snails, generally have coiled shells. Notable exceptions to this generality are the marine opisthobranchs (nudibranchs and sea hares) and the terrestrial slugs. And for the most part snail shells look recognizably like snail shells, even though some are plain coils, others may be flattened (e.g., abalones), and still others may be crazily ornamented. Aquatic animals crawl around in water, which helps to support the weight of heavily calcified shells. Terrestrial snails, on the other hand, live in a much less dense medium (air) and have lighter, less calcified shells. The trade-off for a more easily transportable shell is that air is also very drying, and a thinner shell provides less protection from desiccation.
I should state for the record right now that I'm not talking about the many molluscs that don't have shells at all, or that have much reduced shells.
The bivalve molluscs (mussels, clams, oysters, etc.) live inside a pair of shells. They are sedentary animals, living either attached to a hard surface or buried in sand or mud. Not being able to run from predators (although some scallops can swim!), their only defense is the toughness of their shells and the strength of the adductor muscles that hold the shells closed. Most bivalves feed by sucking water into the shells through an incurrent siphon, using their gills to filter food particles from the water, and expelling the water through an excurrent siphon. To do so they must open their shells enough to extend their siphons, or at least expose inhalant and exhalant openings, to the water current surrounding them.
So, snails have one shell and bivalves have two. Some of the most interesting molluscs, in terms of shell morphology, are the chitons. The Polyplacophora (Gk: 'many plate bearer') have a shell that is divided into eight dorsal plates. This makes them immediately distinguishable from just about any other animal.
Chitons live from shallow water to the deep sea, but the majority of species live in the intertidal. This is a high-energy habit characterized by the bashing of waves as the tide rises and falls twice daily. Any organism living here must be able to hang on for dear life or risk being swept away to certain death. Chitons are certainly well equipped to survive in this habitat. They have a low profile, offering minimal resistance to the waves. Rather than stand tall and face the brunt of the wave energy, chitons cling tightly to the rocks and let the waves wash over them.
The chiton's shell, divided into eight articulating plates, gives the animal a much more flexible shell than is found in any other mollusc. This allows them to conform to the topography of the rocks, giving them an even lower profile than, say, a limpet of the same overall shape and size.
While most chitons are pretty sedentary, at least during the low tides when we can see them, some of them can move pretty quickly when they want. So what, exactly, motivates a chiton to run? One species, Stenoplax heathiana, lives on the underside of rocks in the intertidal; it comes out at night to forage on algal films and retreats back under its rock with the dawn. I've seen them at Pistachio Beach, where I turned over rocks and watched them run away from the light. This video is shot in real-time; the chitons are really running fast!
When the eight shell plates are visible it's easy to identify a chiton as a chiton. But not all chitons are quite so obliging with their most chiton-ish characteristic, and one is downright misleading.
Below is Katharina tunicata, one of the largest chitons on our coast. Its shell plates are barely visible, as they are almost entirely covered by the animal's mantle, the layer of tissue that covers the visceral mass and encloses an open space called the mantle cavity in which the gills are located. In chitons, the mantle extends onto the dorsal side of the animal and is called the girdle. Katharina's girdle is smooth and feels like wet leather.
The largest chiton in the world is the gumboot chiton, Cryptochiton stelleri, and it lives on our coast. This beast is about the size of a football, reaching a length of 30 cm or so. It lives mostly in subtidal kelp forests, but can be found in the very low intertidal, which is where I usually see it. At first encounter it's hard to figure out what this animal is. It certainly doesn't look like a chiton.
If anything, it looks like a mostly deflated football, doesn't it? Turning it over to look at the underside doesn't help much, either, although this photo does give an idea of how big the animal can get:
Cryptochiton goes one beyond Katharina and covers its plates entirely. Just looking at the animal you'd have no idea that there are eight plates underneath the tough reddish-brown mantle, but you can feel them if you run your finger along the midline of the dorsum. Living subtidally as it does, Cryptochiton doesn't have the ability to cling tightly to rocks that its intertidal relatives do, and it tends to get washed off its substrate and cast onto the beach during storms. I've never seen one on the beach that wasn't very dead. Once a friend and I were trudging back up the beach after working a low tide, and encountered a dead softball-sized Cryptochiton. I mentioned that it would be nice to have a complete set of shell plates from one of these animals. My friend always carries a knife in her pocket, so we started an impromptu dissection right there on the beach. It didn't take long to learn that the mantle of a gumboot chiton is really tough and difficult to cut through with a pocket knife. And even once we got through the mantle, dissecting the plates from the underlying tissue wasn't going to happen with the tools we had with us. Besides, the stench was godawful even with our unusual tolerance for the smell of dead sea things. We abandoned that corpse.
Many beachcombers have found white butterfly-shaped objects in the sand, but not known what they are. They are definitely calcareous and feel like bone, but what kind of animal makes a bone shaped like this? Turns out this object is one of the shell plates from C. stelleri. They wash up frequently, never attached to their neighbors so they provide no clue as to what organism they came from.
In order to obtain a complete set of Cryptochiton plates, I'd have to start with an intact chiton corpse. I did happen upon another dead Cryptochiton on a beach somewhere I was allowed to collect organisms, and I brought it back to the marine lab. I remember spending a smelly afternoon cutting the plates out of the corpse and removing as much of the tissue as I could, then feeding the plates to various hungry anemones to take care of the rest. Some of the plates got a little broken during the extraction process, but I do have my very own full set!
Some day I will figure out a way to mount those plates permanently.
One final question to ponder. Does a chiton have one shell, or eight shells?
This past Monday I did something rare for me: I returned to the same intertidal site I had visited the previous day. I enjoyed myself so much the first time that I wasn't able to refuse an invitation to go out there again. The site, Pigeon Point, is one of my favorites, especially in all of its spring glory as it is now. It has always been a hotspot especially for macroalgal diversity, and so far this year appears to be living up to its reputation. The day before I collected several reds that I got to spend the next two days trying to identify.
On Monday I was less overwhelmed by obsessed with algae and able to focus more on the animals, and was delighted to find a small cluster of Thylacodes squamigerus, the strange and fascinating vermetid snail. Nearby one of the vermetid snails was a yellow nudibranch (Doriopsilla albopunctata) and one of the common turban snails (Tegula funebralis). The chance proximity of three different gastropods brought to mind the incredible diversity of this group of molluscs.
The Gastropoda are the largest group within the phylum Mollusca, and can claim a fossil record that dates back to the early Cambrian, some 540 million years ago. They have been extremely successful throughout that long time and are the only molluscan group to have established lineages in both freshwater and on land (of the other molluscs, only the bivalves have made it into freshwater, with the remaining groups restricted to the sea). As you might expect, this evolutionary history has given rise to a mind-boggling array of body types and lifestyles. Let's investigate this diversity by taking a closer look at the three gastropods in the photo above.
Gastropod #1 (Thylacodes squamigerus): Very few people, on seeing this animal for the first time, would guess that it's a snail. Most would say that it's a serpulid worm. The tube is calcareous, as it is for serpulid worms, and winds around over rocks in the intertidal.
A close look at the opening of the tube, however, reveals snail-like rather than worm-like features. Thylacodes even has a snail's face, although I'll admit it isn't easy to see if you don't know to look for it. And despite crawling under a ledge with my camera, I didn't get the best view of a face. In this photo, however, you can at least see one of the cephalic tentacles:
Living in a tube cemented onto a rock means that Thylacodes can't go out and find food. It must instead catch food and bring it in. Thylacodes does so by spinning threads of sticky mucus that are splayed out into the water, where they capture plankton and suspended detritus. The threads are then reeled in and everything--mucus and food--is eaten by the snail. Thylacodes tends to occur in groups, and individuals within an aggregation contribute threads to a communal feeding net, which presumably can catch more food than the sum total of all the snails' individual efforts.
Pretty unexpected for a snail, isn't it?
Gastropod #2 (Tegula funebralis): The black turban snail is probably one of the most common and commonly overlooked animals in the intertidal. People don't see them because these snails are, literally, everywhere from the high- down into the mid-intertidal. They are routinely stepped over as visitors rush to the lower intertidal, and ignored again as these same visitors leave the seashore. I love them. I keep them in the lab as portable lawnmowers for the seawater tables. They are incredibly efficient grazers, keeping the algal growth down. Plus, I think they're cute!
If there's such thing as a 'typical' marine snail, T. funebralis may very well be it. This little snail exemplifies several of the traits we use to define the Gastropoda: it lives in a coiled shell, it uses a radula for scraping algal film off rocks (yum!) and is torted. The shell is easy enough to understand, as everyone has seen a snail at some point, even if it was a terrestrial snail. The radula and torsion, however, may take a little explaining.
Many molluscs have a radula, a file-like ribbon of teeth that can be stuck out of the mouth and used for feeding. In gastropods the radula can be a scraping organ (as in Tegula and other herbivores such as limpets), a drill (as in the predatory moon snails, which drill holes into unsuspecting clams and then slurp out their soft gooey bodies), or a poison dart (as in the venomous cone snails). The radula of a grazer such as Tegula bears many transverse rows of sharp teeth, which are regularly replaced in a conveyor belt fashion as they are worn down. This assures that the teeth being used are always nice and sharp. Remember the radula marks made by the owl limpet (Lottia gigantea)?
Those zig-zaggy marks are made by the scraping of the radula as the limpet crawls over her farm. Tegula funebralis makes the same type of pattern in my seawater tables. All of that white territory is area that had been scraped clean of algae in about a day. Tegula is a very industrious little snail! And they're not shy, either. I don't have to wait a day or so for them to get acclimated when I bring the back to the lab. I can move them around from table to table and after a few seconds they poke their heads out and start cruising around. I've learned from watching them over the years that they seem to have an entrained response to the rising and falling of the tides, even after I bring them into the lab. For the first few weeks of captivity, every morning when I first get to the lab I find that several Tegula have climbed up the walls. I think they're crawling up when the tide is high. I really should look at that more carefully. They never go too far, but sometimes they do drop onto the floor and I find them by stepping on them. Fortunately they are hardy creatures and the floor is always wet with seawater so as long as I find them within a day and plunk them back into the table they're fine.
Now on to torsion. Torsion is difficult to explain, but let me try. The word 'torsion' refers to the twisting of the nerve cord and some internal organs that occurs during larval development of gastropods. Here's how it works. Imagine a closed loop, like a long piece of string with the ends tied together. Lay the loop down on a table and it is just a simple loop. Pick up one end of the loop, twist it counterclockwise 180°, and lay it down again. Now you have a figure-8, right? That's not exactly what happens in the living snail, but you get the picture.
Tegula and other snails have an elongated body that is coiled and crammed to fit inside the shell. If you could take Tegula's body and stretch it out without breaking it (impossible to do, BTW), you'd see the figure-8 configuration of the nerve cord. Other internal organs are re-arranged by torsion, too. As a result, both the gill(s) and the anus now open into the mantle cavity which has been relocated over the head. This arrangement is ideal for keeping the gill(s) irrigated, but not so good for hygienic reasons. Fortunately, the mantle cavity itself is angled so that water flows through it in a more-or-less unidirectional manner, passing over the gill before the anus. Tegula and other marine snails undergo torsion while in the larval stage, and remain torted as adults. This is not the case in other gastropods, as we'll see next.
Gastropod #3 (Doriopsilla albopunctata): Everybody loves the nudibranchs, because their brilliant colors make them easy to love. Unlike the oft-undetected Thylacodes squamigerus and the ignored Tegula funebralis, many of the nudibranchs are somewhat easy to spot in the field because of their flamboyance. This is a crappy picture, but you get the point.
Doriopsilla albopunctata is one of several species of yellow dorid nudibranchs lumped together under the common name 'sea lemon'. Instead of the long fingerlike processes (cerata) that adorn the backs of the aeolid nudibranchs such as Hermissenda spp., the dorids have smooth or papillated backs that may be decorated with rings or spots. Dorids also have a set of branchial plumes on the posterior end of the dorsum; the number and color of these gills can often be used to distinguish similar species. Doriopsilla albopunctata has a smooth yellow back with little white spots, hence the species epithet (L: 'albopunctata' = 'white pointed'), and white branchial plumes.
Nudibranchs are gastropods, although in a different group from Thylacodes and Tegula. The marine slugs, of which the nudibranchs are the most commonly encountered, are in a group called the Opisthobranchia, whose name means 'gill on back' and refers equally to the cerata of aeolids and the branchial plume of dorids. In fact, these animals lack the typical molluscan gill that the snails have. They do have a radula, however, and crawl around on a single foot exactly like Tegula does.
An adult nudibranch's body is elongated, unlike the coiled body of Tegula, and has no apparent signs of having undergone torsion. However, examination of larval nudibranchs shows that they do undergo torsion just like any other respectable gastropod. The weird thing is that some time during the transition from pelagic larva to benthic juvenile they de-tort, or untwist their innards so that their internal anatomy matches their external shape. Instead of having to poop on their own heads, nudibranchs have an anus that is sensibly located at the rear (no pun intended) of the body.
Torsion is one of those biological curiosities whose evolutionary origin is shrouded in mystery. How did such anatomical contortions evolve? Why do gastropods, and only gastropods, undergo torsion? And why do some gastropods tort as larvae, only to detort as they become adults? There are scientific hypotheses about the benefits of torsion, particularly to the larval stages, but nobody knows for sure. After all, none of use were there to watch when it happened.
This is just a tiny taste of the diversity of the Gastropoda. I think it's cool to see three such different gastropods in a small spot of the intertidal. And no doubt there were more that I didn't see. That's one of the joys of working in the intertidal: that I so often see things I wasn't even trying to find.
Before Christmas I was invited to speak at one of the monthly public talks hosted by the Seymour Marine Discovery Center. I'm always happy to be asked to speak to students or the public, so my default answer to these requests is "Yes!" Usually for this kind of presentation I get to choose the topic, but this time my name came up because one of the Seymour Center staffers came up with "bees, banana slugs, and bat stars" so that's what I was given to work with. When my brain took hold of this topic and these very disparate animals, the common theme that came to mind was . . . wait for it . . . reproduction. So yes, this is going to be another sex talk.
What this means is that I need to provide some information on the talk and photos so that the Seymour Center can start publicizing the event, which is in March. Banana slugs are still in the mix, and I don't have any pictures of them, so this afternoon I took advantage of a break between storms to go hiking in the forest and look for slugs. I'd been feeling a little cabin fever for the past few days because of the rain and my own recovery from bronchitis which sapped all of my energy, so I was grateful for an excuse to leave my desk and get outside for a bit.
I headed out to the Forest of Nisene Marks State Park, knowing that where there are redwood trees there should also be banana slugs, especially after all the rain we've had recently. You know how when you're looking for something you can't find it, and when you're not looking for it you see them all over the place? That's how this hike began. It turns out that looking for banana slugs under a deadline makes them very hard to find. And I did have a deadline, as I'd promised to have the blurb and photos for my talk ready today.
After about half an hour of slowly meandering along the trails and getting distracted by all the fungi that popped up after the rains, I did see a banana slug:
That is such a gastropod face! Banana slugs are really cool (and ectothermic, too) animals. One of my buddies in grad school kept one for a pet in our office bullpen; we called it Terry, because slugs are hermaphrodites and deserve androgynous names. Terry really liked eating mushrooms and lettuce.
Banana slugs, and all of the terrestrial snails and slugs, are pulmonate ("lung") gastropods. Most of their marine relatives, with whom I spend so much quality time in the lab and in the field, are prosobranch ("gill in front") gastropods. The nudibranchs and sea hares, which are so photogenic and conspicuous, are opisthobranch ("gill on back") gastropods. As these names imply, the prosobranchs and opisthobranchs possess gills (although they are very different kinds of gills) and thus live in water. The pulmonates don't have gills; they live on land and breathe air. [There are aquatic pulmonates, too. Only a few are marine, and most live in fresh water. They have to come to the surface to breathe.]
So, what is the lung of a banana slug? It's actually the mantle cavity, that oh-so-molluscan feature, that in prosobranchs contains the gill(s). In the pulmonates, the mantle cavity is highly vascularized, as you'd expect from any gas-exchange surface, and opens to the outside by a hole called a pneumostome.
Here's the pneumostome of my first banana slug of the afternoon:
The pneumostome is always on the right side of the animal's mantle. You can actually watch it open and close as the slug breathes.
I found a second slug about an hour into the hike.
See? No pneumostome on the left side.
If I'd had the time, I would have put the slugs together to see if they'd mate. It is a sex talk I'm prepping for, after all. Heck, what would be even better would be to find two slugs already in copulo. No such luck today, though. What's good about not finding everything that I was looking for today is that it gives me incentive to keep going out to search for it. And in the meantime, I've got to start studying up on local fungi. I saw so many different kinds of mushrooms today that now I'm motivated to fill in this particular gap in my knowledge. Might as well take advantage of the El Niño rains, right?