Resume Reading — The Evolutionary Pull of Ocean Tides


The Evolutionary Pull of Ocean Tides

How animals’ biological clocks turn with the tides.

In winter, the knots come by the thousands to feast on the riches in the intertidal mudflats of the Wash. These medium-size wading…By Hugh Aldersey-Williams

In winter, the knots come by the thousands to feast on the riches in the intertidal mudflats of the Wash. These medium-size wading birds are rather dull and unprepossessing in appearance, white underneath and sandy on their backs. During the breeding season their plumage turns a rich russet, but this happens in the Canadian Arctic and other colder climes where the birds spend the summer, and we seldom see it. In Britain, knots are more remarkable for their sheer numbers.

Vast flocks of them put on a mesmerizing aerial performance over their feeding grounds: here in my county of Norfolk, in the Severn and Thames estuaries, in Morecambe Bay, and in other areas where sufficiently broad stretches of mud are exposed by the tide. The birds then pass the hour or two of high tide hidden in vegetation on slightly higher ground before returning to feed once more. At Snettisham in Norfolk, on the west-facing shore of the Wash, high-tide flights of 45,000 birds have been recorded.

The Rhythm Method: The knot arrives to feed an hour later each day, like clockwork, in tandem with the tides. Andrea Westmoreland / Wikipedia

The knots’ behavior is highly distinctive. Some wader species fly off at intervals as individuals when the tide comes and goes. Others, such as oystercatchers, turn their back on the water as the tide advances, and walk disconsolately, it seems, up the mud slope in time with the rising sea. But knots, perhaps because they cluster too tightly to move in this way, face the rising water and take off at the very last chance they have, when it has risen up their legs and threatens to wet their underfeathers.

I watch as they fly off in a continuous flourish like a magician’s curtain being swept aside. The dense flock swirls and feints like a single aerial organism. Once aloft, the birds first coalesce as an egg-shaped cloud low over the water, before gaining height and taking on ever more extravagant, twisted shapes like a pixelated flamenco dancer. As the ever-changing shape swerves and dives, each of its dots switches between light and dark as the bird’s body banks into a turn, creating a scintillating effect in the smoke-like apparition. All the while, the birds call, queek-eek, their cries piling up on one another to make a deafening, high-pitched white noise.

It is clear that the grunion is engaged in a subtle dance with the tide.

Once it has rested ashore during the hour or so of the highest tide, the knot returns to its task, continually marching down to the tide’s edge as the water recedes, in search of food. The returning flock is less theatrical than the one that rose up into the sky a short while ago, and more urgent. They spread themselves out along the ever-changing edge of the water. These birds are tactile feeders that use their long bills to detect vibrations transmitted through the mud that reveal the presence of buried mollusks. They eat small mussels and cockles but are especially partial to a species of clam known as the Baltic tellin, Macoma balthica, and a small mud snail, Hydrobia ulvae. The tellin lives in the mud of the lower part of the intertidal zone and down below the mean low-water line, where it uses a siphon to draw nutrient material down to it from the wet surface. The mud snail, on the other hand, inhabits the upper reaches of the intertidal zone and feeds on algae—it is also known as the laver spire shell—and organic detritus, such as the decaying remains of sea creatures and fecal matter, from which it extracts protein. This segregation of its principal foods is reflected in the knot’s feeding habits—pecking from the surface for snails in the higher parts of the intertidal zone when the tide is approaching high water or beginning to ebb, but probing and pushing in the mud for tellins in the lower reaches when the tide is out.

Other shorebirds favor different foods and therefore exhibit somewhat different behaviors in relation to the water. Where the knot stays at the edge, the dunlin is happy to wade into the water after its prey. Avocets use their upturned bills to skim very shallow water for rag worms and shrimp. The oystercatcher can break into the harder shells of limpets using its jackhammer of a bill. In the Bay of Fundy, up to 2 million semipalmated sandpipers stop off on their migration to feast on mud shrimp, the location favored because the invertebrates develop earlier there owing to the exceptional tidal range, which in turn guarantees a more reliable food supply.

In all cases, the birds’ behavior is regulated primarily by the tide. The ritual of the knot—the feeding, the flocking, the roost, the return to the feeding grounds—is repeated, not at the same time, but nearly an hour later each day because it is driven by the cycle of the tides. When, perhaps after several days, the high tide comes in as night is falling, the knots can afford to roost for a little longer and can dispense with the aerial acrobatics, because their predators hunt by day, but they carry on feeding during the nighttime low tide as well as the daytime low tide.

The intertidal zone is a unique habitat, a concentrated band of transition between the ecological communities of the sea and the land. It is an environment of high rewards in terms of food, but also of high stress, owing to exposure to heat and cold, sun and waves. Other habitats tend to be confined to climatic regions. But the intertidal zone is present on every coast, delimited only by the tides. The kind of life it supports is closely replicated all around the world too, notwithstanding differences in climate.

On rocky shores, the division into zones is precisely painted onto every surface, offering pictorial evidence that animal and plant species are rigidly organized into tiers according to their tolerance to immersion in seawater or exposure to the air. On such a shore I find the topmost stratum is essentially terrestrial rock, a clean mid-gray in color, with green moss growing on it, and splotches of guano showing that the rocks are used as regular perches by seabirds. Below this layer is a darker-gray stratum, more precisely delineated at the top than at the bottom. This is the splash zone, exposed to frequent dousing in brine but not to regular immersion; the different color indicates the presence of small algae.

To the lower slopes of this stratum, in places where it is not steep, clings a wrack-type seaweed. Below this is a brown layer comprising more algae and seaweed, which is covered at every high tide. The final layer I can see, toward the low-water mark, shows gray rock once more, with larger marine organisms such as barnacles and limpets and larger seaweeds fastened to it. It is not only these fixed, or sessile, species that exhibit zonation, but also the myriad insects, crabs, shorebirds, and other creatures that scurry up and down in search of food within their own favored limits.

Sea Level Rise: The intertidal zone changes drastically from high tide to low, inviting a wide array of animals in between. Foxy Orange / Wikipedia

The vertical sequence is the same the world over, although the width of the individual bands may vary, and sometimes one layer may be squeezed out altogether because the physical conditions are not right or because of competition between species. In general, however, this hierarchical organization of life acts to reduce such competition. The bands are as rigid as any national border, and may be shifted only by an unfortunate coincidence of events, and then usually only a little, and for a short time. Battering storm waves on a high tide, for example, will temporarily increase the extent of the splash zone, while a spell of drought occurring at neap tides may dehydrate species that normally live near the mean high-water mark.

There is inevitably one other major threat to the intertidal zone, and that is humankind. In many parts of the world, this rich habitat is being severely squeezed. Rising sea levels encroach from the sea side—a more significant factor than it seems: a single millimeter rise in sea level can be responsible for erosion reaching up to a meter inland. Meanwhile, coastal property development eats away at it from the land. If the two meet, sea defenses may be constructed, replacing wide mudflats, a beach, dunes, and marshes with one hard, concrete barrier. A band of habitat once a mile or two in extent is suddenly supplanted by a more or less vertical wall that compresses the intertidal zone into a few yards.

Other creatures have evolved to use the tides in more sophisticated ways. The breeding cycle of the California grunion, for example, is synchronized exclusively to the spring tides, the highest of high tides that arrive at fortnightly intervals on each new and full moon. The grunion is a small, silvery fish about the size of a sardine with ray-like fins. On spring and summer nights, when the tide is high, the fine sandy beaches of southern California where they come to spawn are suddenly covered in thousands of the writhing creatures.

Perhaps our own removal from the tides makes the problem seem harder than it is.

Scientific observation has revealed that the event is precisely attuned to take advantage of the tides. The run occurs mainly on the days immediately after the full or new moon, when the tides are expected to be high, but not quite as high as the very highest spring tide. The high tide on each successive day during this short period will be a little lower, helping to ensure that the new-laid grunion eggs will not be washed away. In fact, the breaking waves of the subsequent tides throw up sand that helps to protect the eggs by burying them gradually deeper. Over the following 11 days or so, the eggs are incubated in the shallow, moist sand. After 11 days, the first big waves of the next spring tide arrive. The waves begin to erode the beach where the eggs lie buried. Soon the eggs are no longer snugly encased in sand but are being shaken about in the waves, which is their signal to hatch into larvae. Typically, the eggs hatch very shortly before the next new or full moon, giving the larvae the greatest chance of making it down the beach and out to sea over the next few spring tides, which will be of increasing height.

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This is not all. If the following spring tides happen not to reach the incubating eggs—for example, because offshore winds reduce the height of the tide—the fertilized eggs are able to delay hatching for two weeks or even four weeks until a more propitious tide comes.

A number of marine species, including whitebait, mummichogs, and Colchester oysters, exhibit a similar, though less marked, synchrony with the spring tides in their breeding cycle. But in the grunion, the adaptation is so fine-tuned that it is considered an evolutionary marvel. From the intricacy of its mating cycle, it is clear that the grunion is engaged in a subtle dance with the tide. The evidence strongly suggests not only that the grunion evolved in this spot, but also that the tidal conditions of its habitat have remained substantially constant ever since.

How do animals “know” what the tide will do? When scientists began to study them, they thought it unlikely that grunions, for example, could have a wholly internal mechanism by which to time their breeding run. Do they then sense the tide directly, or are they responding to other stimuli? Certain things can be deduced. It cannot be moonlight that causes the fish to run ashore, as they do this at high-water springs both on the bright full moon and in the darkness of the new moon. The fact that spawning occurs not on the very highest tides, but shortly afterward, indicates that the behavior is not directly governed by tide height either (something that the grunion might detect as increased water pressure around its body). It has been found that it is agitation in the sea when the next spring tide comes that stimulates the grunion eggs to release their larvae by generating enzymes that dissolve the egg membrane. But wave action cannot be the trigger for the original beaching, or else storms would disrupt the pattern of the spawning runs.

What else is left? Could the stimulus be pure gravitational attraction? Any forces felt by the fish would be minute in comparison with the changes in pressure that they tolerate when swimming at different depths, but gravity cannot be entirely discounted. Whatever triggers the behavior, it seems it is not confined to the single tide when the grunions come ashore to reproduce, since the eggs begin to mature long before they are spawned—and this, too, has been found to happen in concert with moon phases.

The author John Steinbeck writes about this conundrum in The Log from the Sea of Cortez, the record of a specimen-gathering expedition he made to the Gulf of California with his friend Ed Ricketts in 1940. (The Sea of Cortez was the name of his vessel as well as his happy hunting ground.) Ricketts—who provided Steinbeck with the model for the character of Doc in Cannery Row—later wrote a scientific guide to intertidal life based in part on what the two men collected on the trip. Tangling with mangrove roots in their motor launch at high water, and racing against time to gather specimens from the uncovered beds at low tide (like knots), they find an astounding diversity of colorful life in the warm waters: crabs and snails, and creatures with names out of horrible myth, such as the gorgonian, and others, like the serpulids, so obscure that their only name is the exotic-sounding one given to them by science. They see fish that can survive out of water, at least for the period of one tide, and minutely observe how the foreshore is graded with different kinds of life by height and by the time spent immersed in seawater.

Inevitably, they find themselves drawn into speculation on the importance of the tide to this abundance of life, especially since, in Precambrian times, when single-celled organisms began to evolve into more complex forms in the sea, the tides were far greater than they are today, because of the closer orbit of the moon. Steinbeck writes, “The moon-pull must have been the most important single environmental factor of littoral animals.” Their body weight and displacement in the sea would have cycled strongly with the rotation of the earth. “Consider, then, the effect of a decrease in pressure on gonads turgid with eggs or sperm, already almost bursting and awaiting the slight extra pull to discharge.” What Steinbeck finds more remarkable is that so many creatures seem to have carried forward a kind of ancestral memory of this response and fine-tuned it to the far weaker signal of tides now—an effect to which, he believes, even we are not immune. “Tidal effects are mysterious and dark in the soul, and it may well be noted that even today the effect of the tides is more valid and strong and widespread than is generally supposed.”

But we are still left with the question of how it is that these creatures respond to the tides. They do not go around with tide tables; they do not superfluously relate tide to time as we do. So either they must have some kind of built-in tidal clock, or they must directly sense some primary or secondary property of the tide, which might include the pressure or rate of flow of water, or its change in temperature or salinity.

Perhaps our own removal from the tides makes the problem seem harder than it is. It is, after all, no miracle that animals are sensitive to time. We ourselves are slaves to the circadian rhythm, as our alarm clocks and news bulletins daily remind us. Why should a circatidal rhythm be any odder than a circadian one? Of course, the circadian rhythm has the obvious cues of bright sunlight alternating with utter darkness. But this is what is obvious to us. What cues might be just as obvious to marine creatures very different from ourselves? We find a 24-hour cycle perfectly natural, but might not these animals find a period of 12-and-a-bit hours just as natural, especially if their survival depends on it?

Solar control of the daily and yearly rhythms of life on land is relatively well understood (and of course inescapably familiar in ordinary human experience). But an explanation of the rhythmic mechanisms of marine life is only just beginning to emerge. Circadian rhythms are regulated by genes that provide chemical feedback. This means that the rhythm is maintained in a “free-running” fashion even in the absence of external stimuli such as changing light levels or temperatures. Similar free-running rhythms are seen in sea creatures, but it has been arguable whether these biological clocks are truly tide related or are versions of the circadian clock tweaked by the processes of natural adaptation to operate at a different rate.

In 2013, however, geneticists at the University of Leicester obtained evidence to suggest that a dedicated circatidal biological clock does exist. Researchers led by Charalambos Kyriacou worked with the speckled sea louse, a familiar denizen of intertidal sandy beaches that bears the deceptively alluring name Eurydice pulchra. By disrupting the expression of genes responsible for circadian timekeeping, and showing that the animals nevertheless maintained their normal tidal behavior, they established that the tidal rhythms are driven independently by a circatidal clock. The lice have biological clocks of both kinds: a circadian clock that governs such matters as the production of pigments in the body, and the circatidal clock that regulates their swimming activity in response to the 12-hourly cycle between successive high tides.

As for the longer cycle of spring and neap tides (the word “circa-lunar” is used to distinguish this period from the circatidal response to each tide), there is new evidence to explain animal responses to this too, from similar experiments at the Max F. Perutz Laboratories of the University of Vienna. The Austrian researchers used ragworms for their subjects. This was one of the first species observed to spawn on a cycle attuned to the spring tides and is considered a living fossil, with a physiology, behavior, and habitat unchanged over millions of years. Unlike the grunion, it does not spawn on every spring tide at the right time of year, but only monthly, on the spring tides at the new moon. This behavior suggests that the animal’s circalunar clock may be entrained to moonlight, or rather the absence of moonlight, and not to the hydrodynamic factors that might be important for the grunion. Biochemical reactions catalyzed by lunar light may play a role in this programming. All known biological clocks are linked ultimately either to the sun or to the moon.

I was entirely unaware of the dependence of the ragworm on the lunar cycle when I picked one out of the mud one day, while observing the tides on the north Norfolk coast. I saw gulls and curlews come and go that day too, but I would have had to stay for many more days in order to appreciate all these animals’ obeisance to the tides. It is surely a mark of how much our own lives are ruled by the black and white of day and night that we are so insensitive to these different rhythms, and it is only now that science is beginning to comprehend them.

Hugh Aldersey-Williams is the author of many books, including Anatomies, The Periodic Table, and The Most Beautiful Molecule, a finalist for the Los Angeles Times Book Prize. He lives in Norfolk, England.

Reprinted from The Tide by Hugh Aldersey-Williams Copyright © 2016 by Hugh Aldersey-Williams. With permission of the publisher, W.W. Norton & Company, Inc. All rights reserved.

Lead image collage credits: Andrew Smidth; USFWS / Richard Crossley / Wikipedia; Miwok / Flickr

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