Rocky intertidal fishes

some fish out of water do just fine.

A trip at low tide to one or our rocky intertidal sites always yields an array of pleasures and some treasures. Maybe I’ll see my favorite bright red hermit crab! Or find an Aristotle’s lantern—the feeding apparatus of sea urchins, which may be all that’s left of the innards of a hapless urchin demolished by a crow. Or maybe I’ll catch a whelk in the act of laying eggs. Always fun.

Lurking under rocks and rockweed, I’ll find small, slender fishes. Sometimes called eels, or blennies, they are neither: in our area, they are usually gunnels or pricklebacks, and I will focus here on some that reside in the upper portion of the intertidal zone. They spend their entire lives in the intertidal zone, which means that they are not submerged in sea water for a significant portion of each day. Of course, the higher up in the intertidal zone they are, the longer the non-submerged period, which happens twice a day. Most fish can’t handle that; we even have an expression “like a fish out of water” to describe someone completely out of his or her element.

Gunnels and pricklebacks, however, deal with low tides just fine. They (and many other species of fishes, of many different kinds) are able to breathe air. Air-breathing fishes around the world accomplish this feat in lots of different ways: for example, some use their swim bladders, or various parts of the digestive tract, or special chambers above the gills. Gunnels and pricklebacks can breathe air, using both gills and skin, as they do in water. Their respiration is reported to be just as effective in air as it is in water, although prolonged stress might alter that.

To begin this discussion, let me present some basics about respiration (in either air or water). Respiration is all about 1) getting oxygen into the body and then to the cells where mini-organs called mitochondria do the work of oxidizing carbohydrates and creating energy to run the whole body, and 2) getting rid of carbon dioxide, which is one of the byproducts of oxidizing those carbos, so that the interior of the cells and of the body don’t become too acidic (which interferes with lots of processes). Both gills and skin perform these functions, but the relative roles of those organs differ among species.

Gills of most fishes are long, thin, and delicate, so as to expose lots of surface area for uptake of oxygen and elimination of carbon dioxide. But such gills tend to collapse when out of water. Intertidal fishes make what is called a ‘trade-off: they have gills that are shorter and not quite so delicate, thus reducing their tendency to collapse, but they sacrifice some of the surface area for diffusion of respiratory gases. Shorter, stouter gills also reduce the risk of desiccation in air.

Both gills and skin need to be kept moist in order for oxygen to diffuse in and carbon dioxide to diffuse out. So when the tide is out, these intertidal residents may dip in and out of tiny pools or roll in wet places, for example.

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High cockscomb prickleback. Photo by Bob Armstrong

A common prickleback in our upper intertidal zone is known as the high cockscomb prickleback—named for the prominent ridge on top of its head. That ridge tends to lie flat, however, when this dark fish is not submerged, making confident identification difficult for non-experts, in most field conditions. In this species, females tend to be larger than males (at equal ages), and males compete for mating privileges with females. Large females are especially worth competing for, because they lay more eggs than small females. Eggs are laid under rocks, where the female takes care of them for about a month: coiling around the ball of stuck-together eggs, fanning them to increase flow of oxygenated water, and guarding.

We also see crescent gunnels in the upper intertidal zone. These are sometimes readily identified by the light-colored marks along the sides, but I’m told that some individuals are dark, so discriminating them from other dark species may not be easy in the field. Crescent gunnels have apparently been studied less than high cockscomb pricklebacks, but both parents (but sometimes one or none) often tend the eggs, which are laid under rocks. Most of the other gunnels and pricklebacks in our region are either relatively rare or occupy lower parts of the intertidal zone, and in some of these species, parental care is by the males.

Another small fish is common in the upper parts of the intertidal zone: the tidepool sculpin. As the name tells us, it typically lives in tidepools left by the receding tide. It’s an air-breather too, using the gills, mouth lining, and skin. Sometimes conditions in its home tidepool become low in oxygen or too acidic; this could happen especially at night when all organisms continue to respire and produce carbon dioxide but there is no photosynthesis to use that carbon dioxide. Or sunlight might make the pool too warm. Then these little sculpins often choose to leave their pools, either partially—just exposing the head to air—or fully, resting on nearby weeds or rocks or, occasionally, crawling to another tidepool. They are said to be quite good at homing…returning to their home pond if they are displaced.

This fish is unusual in that males and females copulate and the males’ sperm are deposited inside the female, but the eggs are actually fertilized after they are laid. This is obviously a contrast with most other fishes, in which males and females spawn by releasing sperm and eggs into the water. There is no parental care.

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Crow with a prickleback. Photo by Bob Armstrong

These intertidal fishes face many risks in addition to desiccation and respiratory difficulties. Even though they have escaped the many predators in the open sea, there are opportunistic land-based predators that can find them. For example, ravens and crows fossick about in the rockweed and poke under rocks, sometimes coming up with a prize; mink delve into tidepools or turn over rocks. And we who love to explore the rocky intertidal inevitably do more damage than we would like.

Thanks to Dr. K. L. Martin, Pepperdine University, for helpful references and consultation.

Intertidal discoveries…

…include kleptoparisitism

On the next-to-the-lowest tide in late April, some friends and I explored the intertidal zone not far from town. We soon catalogued all the usual beasts, but several observations really caught my fancy.

Three tiny, bright red hermit crabs (very cute!) guarded their protective periwinkle shells with their big claws. We counted over seventy small king crabs, all less than an inch in carapace width. There were lots of five-armed sea stars, but one had only three arms and one had only two arms, with no signs of regeneration. So we wondered about the feeding success of these crippled stars, with so few arms for pulling open clams; how does their diet differ from that of intact stars, and how long does it take to get enough nutrition to regenerate those missing arms?

Among all the small fishes that lurked under boulders were two large crescent gunnels, at least eight inches long. They were so dark that the crescent marks on the backs were hard to see; these individuals were reddish on the lower parts of head and body and were probably males. The heads of two flatfish lay on a low ledge. The bodies of both fish behind the gills had been gnawed off, leaving a ragged margin. Someone had feasted well—probably otters, which commonly eat these fishes tail-first, and crabs may also have picked off a few bits.

The biggest puzzle was a heap of fuzzy-looking snails piled up on a mound of mostly indistinguishable material. We had no idea what this was, so I asked an expert and did some reading. Here is what I learned: These snails are known as Hairysnails (currently classified as Trichotropis cancellata). The shell bristles with hairs, and experiments have shown that the hairs deter some, but not all, predators. This snail lives in the North Pacific, usually sub-tidally, so the very low tide on this day was fortuitous for us.

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Photo by Kerry Howard

Hairy snails are sequential (protandrous) hermaphrodites: as they mature they are male first and then gradually turn into females as they grow. Bigger snails produce larger clutches of eggs, increasing their reproductive output, while size is less important to male reproductive success, so for this species it pays to start reproducing (as a male) when small and producing eggs, lots of them, when large. During the transition time, they can sometimes function as both sexes at the same time—researchers have seen pairs of snails in which both snails are being male and female simultaneously.

The feeding habits of Hairysnails are fascinating. They can feed on small organisms suspended in the water but, more interestingly, they are kleptoparasites—stealing food particles right out of the mouths of tube worms (they are rarely seen parasitizing other potential hosts). The tube worms feed by catching plankton on their waving tentacles and funneling the prey to their mouths, and the snails just cling to the side of the tube and reach out with an extended lower ‘lip’ to snap up incoming prey. The snails that we saw were all clinging to a conglomeration of tube worms, ready to snatch food particles when the tide came up again.

Worms thereby suffer a reduced growth rate, but the sneaky, thieving snails grow much better—up to eighteen time faster than when simply suspension feeding. Small, immature snails, including those that are only a millimeter in size, gain the most in growth from their kleptoparasitism, but larger ones are also able to reproduce better. In most places, there is only one kleptoparasitic snail on a given tube worm, but occasionally there are two or even three, potentially in competition for stolen prey.

Hairysnails mate and lay eggs in winter, and in that season the adults generally leave their hosts and occupy themselves with reproductive activities. Males come back to stealing from tube worms when they are done mating, but females tend their batches of eggs for a while, and thus return to their hosts later than the males do. Small snails, less than about five millimeters in size, do not leave their hosts seasonally, but continue to thieve and grow.

Kleptoparasitism, in reference to stealing food from another animal, is widespread in the animal kingdom. Birds are perhaps the best studied: frigatebirds, jaegers and skuas, and some terns are well-known for harassing other birds that have caught a fish, making the victim drop the fish for the pirate to grab. In Berners Bay, we watched young glaucous-winged gulls, acting like teen-age hoodlums, chase other gulls until the prey was dropped. We sometimes see eagles forcing another eagle or an osprey to drop its fish. Among insects, cuckoo-bees lay their eggs on the pollen balls made by queen bumblebees for their own larvae and thus are stealing food from the bumblebee larvae. Web-building spiders may lose their prey to other spiders or to flies. Hyenas sometimes harry lions at a kill until the lions depart, letting the hyenas take much of the lions’ prey; and sometimes lions steal from hyenas. Those are just a few examples, but researchers say that kleptoparasitism occurs in every major taxonomic group of animals. Humans are not exceptions!

Sometimes the concept of kleptoparasitism is broadened to include the stealing of any useful item from another animal. So male bowerbirds that swipe alluring objects from each other, in order to decorate their own bowers, are kleptoparasites. So, too, are penguins robbing each other of stones used in their nests or tree swallows forcing a chickadee to give up its nest for the swallows’ use. Again, humans are not exceptions!

Thanks to Dr. Aaron Baldwin, ADFG, for sharing some of his extensive knowledge of marine invertebrates and providing literature references.