The Edge of the Sea
(Dr.) Rachel L. Carson
AAAS General Symposium: The Sea Frontier

In recent years I have been dealing with the ecology of the seashore: with the animal and plant communities of the rocky coasts, the beach sands, the marshes and mud flats, the coral reefs and mangrove swamps. I have been thinking about the relations of one animal to other animals, of animals to plants, and of the animal or plant to the physical world about it. Always in such reflections one is made aware of the complex pattern of life. No thread is found to be complete in itself, nor does it have meaning alone. Each is but a small part of the intricately woven design of the whole, for the living organism is bound to its world by many ties, some of them relating to biology, others to chemistry, geology, or physics.

For example: perhaps we discover that an animal we have found year after year in the same place suddenly is found there no more, and eventually it appears that the whole population of this creature has shifted its range; that it has done this, moreover, in response to a change in a single factor of its physical environment -- the temperature of the water.

Or we may find that a certain marine worm is so specialized in its living requirements that it can live in one kind of sand and one only; and moreover, that its very young stages -- the larvae whose age is measured in hours or days -- are able to find and to recognize sand of these particular qualities with a precision that few human students of geology could match.

Or again perhaps we discover a sudden and quite mysterious change in the ability of a marine animal to grow or to reproduce, or in the ability of its larvae to exist in the accustomed places, and perhaps we are led to suspect a subtle change in the biochemical nature of the seawater.

All or any of these things are enough to convince us that we, as biologists, cannot exist in a comfortable ivory tower of our own; that it is quite necessary that we concern ourselves with the related sciences if we are to understand the creatures of the marine world.

The edge of the sea is a laboratory in which Nature itself is conducting experiments in the evolution of life and in the delicate balancing of the living creature within a complex system of forces, living and non-living. We have come a long way from the early days of the biology of the shore, when it was enough to find, to describe, and to name the plants and animals found there. We have progressed, also, beyond the next period, the dawn age of the science of ecology, when it was realized that certain kinds of animals are typical of certain kinds of habitats. Now our minds are occupied with tantalizing questions. "Why does an animal live where it does?" "What is the nature of the ties that bind it to its world?"

One of the physical ties is especially interesting in this, our present period of earth history. It is a force that is omnipresent; no living thing is exempt from its influence. For life in the aggregate is lived within a relatively narrow range of temperature. The fact that our planet Earth has a fairly stable temperature helps to make it hospitable to life. In the sea, especially, temperature changes are gradual and moderate and many animals are so delicately adjusted that they cannot tolerate an abrupt or extensive change in the temperature of the surrounding water. If such occurs they must migrate or die.

Now our climate is changing and we are moving into a warm cycle of unknown duration. Ocean temperatures are slower to reflect the change than the air, but

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there has been a measurable warming of Atlantic coastal waters. The winter temperatures, which may be the critical ones for some marine animals, are less severe. Also, the water is warmer in summer. Records of winter temperatures for the Gulf of Maine (based on an average of records for Boston, Boothbay Harbor, Eastport, and St. Andrews) show an impressive rise. In 1918, for example, surface temperatures during the coldest month of the year averaged about 28°, and in the 1910-1919 decade, temperatures below 32° occurred almost every winter. During the 1930's, however, in only three years of the decade did the water temperatures of the coldest month average below 32°, and this has not happened in any year since 1940. Last winter's coldest month averaged 38°, or ten degrees warmer than the winter of 1918 -- a very substantial increase as sea temperatures go.

It is not surprising that such a change in the oceanic climate should have caused many shifts of distribution among marine faunas. It is well known that the waters around Greenland and Iceland have been invaded by animals from regions to the south. This has been well documented in papers by Jensen and others. Less has been said about corresponding changes in the waters off the east coast of the United States. But many are occurring, and collectively they seem to form a significant picture.

Take, for example, the green crab. This is a member of the family of swimming crabs to which the blue crab also belongs. Once its range was very restricted. S. I. Smith, in Verrill's report on the Invertebrate Animals of Vineyard Sound, gave its distribution as "Cape Cod to New Jersey." More than a quarter of a century later, in 1905, Dr. Mary Rathbun placed its northward limit in Casco Bay. As late as 1930 she reported only one record of its occurrence east of Casco Bay. The 1929 biological survey of Mt. Desert Island did not include it. However, in 1930, two lots of green crabs were collected in the vicinity of Brooklyn, in Hancock County, Maine. These were sent to the National Museum because they had been taken so far beyond the limits of their normal range. Nine years later, Leslie Scattergood found the species at Winter Harbor, and in 1951 he was able to report its eastward spread to Lubec. A few months later he found it on the Maine shores of Passamaquoddy Bay, and Canadian biologists reported it from Oven Head on the eastern shores of this bay the same year. According to the Biological Station at St. Andrews, the green crabs were very abundant on all the flats of Passamaquoddy Bay in the summer of 1953, when they were also found across on the Nova Scotian shores -- in St. Mary Bay in August and in Minas Basin in November. There the record stands for the moment. The spread of the green crab is better documented than that of most species for a practical reason. Its invasion of the soft clam areas of Maine has, in some localities, almost wiped out the industry, for the crab preys so extensively on the young stages that farming of clams can hardly be practiced in its presence.

However, there are other occurrences perhaps equally interesting. For these largely unpublished records I am indebted to a number of biologists, including various members of the Fish and Wildlife Service, John Berrill of McGill University, and Fenner Chase of the National Museum.

With warming water temperatures, the sea herring is becoming scarce in Maine. Whether this is entirely a matter of temperature or whether diseases or other factors enter the picture I suppose no one can say with assurance. But as the herring declines other fish, members of the same family but of more southern distribution, are moving in. Back in the 1880's there was a substantial fishery for the menhaden at East Boothbay and some other Maine ports. Then the fish disappeared from Maine and for many years has been yielding enormous catches in New Jersey, Virginia, North Carolina, and other southern states. But about 1950 the menhaden came back into Maine waters in numbers, followed by Virginia boats and fishermen. Then there is another member of the same family, the round herring. In the 1920's Bigelow and Welsh reported it as occurring from the Gulf of Mexico north only as

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far as Cape Cod. But it was rare anywhere on the Cape, and two that had been caught at Provincetown were preserved in the Museum of Comparative Zoology. Now, however, immense schools of this fish have been appearing in Maine waters for several years, and the fishing industry is experimenting with canning it.

There are negative responses, too. One of the hydroids, a member of the genus *Syncoryne*, is so delicately adjusted to water temperatures that it has been considered by some a key temperature-zone organism. Professor Berrill tells me that 6 years ago this species was common at Ocean Point, near Boothbay Harbor, in June. So was the hydroid *Clava*. But two years later, in 1950, Professor Berrill could find only a trace of *Syncoryne*, and since then none whatever, even in mid-winter. Apparently temperatures on this part of the coast have become too warm for it. The same appears to be true of *Clava*, of which none has been found during the past three years in the Boothbay region.

If we knew the whole story of each of these examples of a change of distribution we should very probably find the focus of our attention shifting to the larval stages of the animals that are involved. Often the adults might perfectly well be able to establish themselves in new areas outside of the normal temperature range of the species, but they cannot do so -- that is, they cannot reproduce and have their young survive -- because the waters are too cold or too warm for the welfare of the larvae. More and more it is becoming clear that the ecology of the adult marine animal is dependent upon the ecology of the larvae.

This fact is reinforced with beautiful clarity in another field of research, that has to do with the relations of the larval forms of some invertebrates to the substratum. This has been the subject of brilliant and significant work by Douglas Wilson at the Plymouth Laboratory.

Many invertebrates, as adults, live either permanently or semi-permanently attached to the sea bottom, where rocks are exposed, or burrow into its covering of sand or mud. If such sedentary animals are to establish new colonies, this must be done by the larvae, for they alone have freedom to swim or even to be carried passively in the currents. The minute and delicate larvae often have a further responsibility, for many species are so specialized that they can inhabit only a certain kind of sea bottom. Sand, for example, is far from being a substance of uniform nature. It is diverse in its geologic origin, its chemical nature, its capacity to support life. One of the small annelid worms from which Douglas Wilson has learned so much about the reactions of larvae lives only in clean, coarse sand, stirred by strong tidal action, and composed mainly of quartz with some intermixture of materials derived from rocks and shells. Such sand occurs only in scattered areas on the shores of the English Channel, and the occurrence of this species of worm is accordingly limited.

To understand, then, how the adults come to live where they do, we must return to a study of those very early stages in the life of each member of the species, when clouds of young -- the potential founders of new colonies -- are launched into the sea with each spawning of the adults. Most of these larvae spend the early days -- or, it may be, weeks -- in the drifting community of the plankton, in the midst of diatoms, dinoflagellates, and other microscopic plants; in the company of minute crustaceans, worms, pteropods, and other permanent members of the plankton; and of hosts of other larvae, that, like themselves, are only temporary drifters and swimmers in the upper layers of the sea. Some of the larvae feed on the plant plankton, some on other larvae. Many are eaten by other members of the animal plankton, or are destroyed by cold or storms. Almost all are delicate, transparent, and minute, fragile as blown glass. Produced in astronomical numbers, they are destroyed with almost equal prodigality; seemingly the larvae are a tenuous link on which to base the security of the chain of existence.

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But the larvae are not entirely without resources of their own, as we are discovering now from the work of Wilson and a few others. It seems that they have a fair amount of control over their own destinies, especially in that critical moment of life when they assume the form of the adult. Our early conception of this metamorphosis of the larva has been shown to be false for so many forms that there is some reason to believe we have been generally in error. We used to believe that this drastic change of form, from the larval to the adult stage, occurred at a certain moment in the life of the larva; and that it occurred at this moment whether or not the larva was at that time in surroundings suitable for taking up the adult existence. From these beliefs it would follow that a very large percentage of larvae would be lost because of being on unfavorable ground when the moment of metamorphosis arrived. However, thanks largely to the work of Wilson, we now have a new conception of this crisis in the life of the larva. In many forms, at least, we know that the larva has the ability to recognize the sands or muds of the type inhabited by its parents, that it may test out one area after another and may postpone its own metamorphosis for a considerable period of time, changing to the adult form only when a suitable substratum is found. A few sentences from one of Wilson's reports, on the tube-building polychaete, *Owenia fusiformis*, make this clear:

> "When a month old it can change suddenly, in a few seconds, from an object of elegance and beauty into an ugly little worm... busily engaged in swallowing the remains of its... larval organs. But, and this is the point, it will rarely do so successfully unless it be provided with sand of a suitable sort... There is a period of about a week at any time during which it will metamorphose in contact with the sand in which the adult lives. The quick reaction to contact with such sand is strongly reminiscent of a chemical experiment; to a clean dish containing swimming larvae, sand is added, and almost at once there is a precipitate of worms."

From Wilson's experiments on this and other forms, we may visualize what happens when such a larva is ready for the choice of its adult home. Through its changing reactions to light it has perhaps already turned away from the surface waters and lives within the currents of water that flow over the sea bottom. Now and then it may drop down to the underlying bottom and enter the sand. But if the sand is found to be unsuitable -- if it lacks the sought-for qualities -- the larva emerges from it and enters again the slow drift of the currents, allowing itself to be carried on to new areas where, perchance, it will find that which it requires. When it does, the response is immediate; the larva settles down, and metamorphosis proceeds.

In learning this much, science has taken a long step forward. There are still many questions that recur. What is the link between the delicate larva and its specialized physical environment? To what quality in the environment does it respond? What is the external stimulus that sets in motion those processes within the larva, transforming and remolding its tissues into the likeness of the adult?

One by one, these questions are being posed in the form in imaginatively contrived experiments. Wilson at first tested the possibility that the larvae react to sand grains of a certain size and shape. He concluded that although the grade of sand has some influence, it is not decisive. Then he considered whether a substance, possibly of organic nature, might be given off into the water by the native-type sands, attracting the larvae toward it. But it soon became clear that the larvae do not react, either negatively or positively, until they come into contact with the sand. In his most recently reported work, Wilson favors the theory that some organic material present on the surface of the sand grains causes them to attract or to repel the larvae. Further work along these lines is being done. In the meantime, it is established beyond question that some - perhaps most -

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species of marine bottom invertebrates have an inherited ability to recognize their
own habitat when, as larvae, they first come into contact with it.

This fascinating subject is related to another that is in the forefront of
biological thinking today. This is the subject of the so-called "ectocrines" --
the products of metabolism that are liberated into the sea water by marine organisms.
As yet no conceptions and no conclusions in this field are final; the subject lies
on the misty borderlands of advancing knowledge. And yet almost everything that
in the past we have taken for granted, or labeled as insoluble problem, bears re-
newed thinking about in the light of what we know, or what we think is probable,
about these substances of far-reaching effect.

In the sea there are mysterious comings and goings, both in space and time:
the movements of migratory species, the strange phenomenon of succession by which,
in one and the same area, one species appears in profusion, flourishes for a time,
and then dies out, only to have its place taken by another and then another, like
actors in a pageant passing before our eyes. And there are other mysteries. The
phenomenon of "red tides" has been known from early days, recurring again and again
down to the present time -- a phenomenon in which the sea becomes discolored because
of the extraordinary multiplication of some minute form, often a dinoflagellate,
and in which there are disastrous side effects in the shape of mass mortalities
among fish and some of the invertebrates. Then there is the problem of curious and
seemingly erratic movements of fish, into or away from certain areas, often with
sharp economic consequences. When the so-called "Atlantic water" floods the south
coast of England, herring become abundant within the range of the Plymouth fisheries,
certain characteristic plankton animals occur in profusion, and certain species of
invertebrates flourish in the inter-tidal zone. When, however, this water mass is
replaced by Channel water, the cast of characters undergoes many changes.

In these and other phenomena, the question recurs, and, unanswered, recurs
again: Why? Here and there we perceive the first faint glimmerings of what may be
the truth.

It appears that some, at least, of these things may in some measure be explained
as the effects of substances present in the sea water -- substances produced by one
kind of organism as a by-product of its own metabolism, but exerting a powerful
influence on another. A somewhat analagous and better known effect is that of
antibiotic substances on bacteria. Apparently the ectocrines of the sea may be
either harmful or beneficial in their effects. Of this much, however, science now
seems certain: The nature of any mass of water, and its possible influence for good
or ill upon the creatures it surrounds, are strongly influenced by the metabolism
of those forms that, at an earlier point in time, lived within this same water.

It is interesting to trace the growth of an idea -- a voice here, another there,
and finally someone begins to put it all together, invents a terminology, and a
new field of research is recognized. Probably it is only within the past decade
that there has been much talk among biologists about external metabolites or
ectocrines; yet this, also, seems to be one of the new-old subjects, for we can
identify its embryonic beginnings in the literature of at least 70 years ago. In
1885 Pearcey reported in a Scottish journal his observation that herring are scarce
in waters inhabited by certain diatoms, and that animal plankton also are scarce
in such waters. About a quarter of a century ago, Johnstone, Scott, and Chadwick
expressed their opinion that plankton communities influence each other, and that
"there are what we may call group symbioses on the great scale, so that the kind
of plankton which we may expect to be present in a certain sea area must depend,
to some extent, on the kind of plankton that was previously present." Early in the
thirties, Allee made the significant statement that "aggregations of aquatic
organisms condition the medium surrounding them by the addition of secretions and

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excreations, the nature of which forms one of the important problems of mass
physiology."

While the existence of such organic substances in the sea now is generally
recognized, there is little direct evidence as to their chemical nature or their
precise role in the life processes of marine animals. Certain lines of investigation
lead us back to the inshore waters and to the attached marine algae that grow in the
coastal zone. These may be a source of very important ectocrines. If the possi-
bilities now dimly foreseen are confirmed, these substances produced in coastal
waters may act as catalytic agents to set off whole cycles of life in the sea. These
waters are the habitat of the brown meadows of rockweeds, the dusky forests of the
kelps, and the more fragile algae of pale green hue and delicate texture. These
attached plants can live only as deep as light can penetrate and so are excluded
from most of the open ocean.

In recent reports from the Goteborg Laboratory in Sweden we find that where the rockweeds *Fucus* and *Ascophyllum* are growing, the water acquires a property that stimulates the growth of the sea lettuce, *Ulva*, and also of *Enteromorpha*. From other work we know that the sea lettuce itself produces a substance that apparently is needed for the growth of certain diatoms in artificial media.

This is a plant-to-plant relation, but the ectocrines of the algae seem also to
be concerned in an animal-plant relationship. In Japan, Miyazaki found that he
could stimulate the spawning of oysters with a substance extracted from sea lettuce.
This leads to a fascinating field of speculation. If indeed it is confirmed that
ectocrines released into the sea by coastal vegetation induce both the flowering
of the diatoms and the spawning of certain marine animals, a very neatly fitting
chain of circumstances would result. The larval stages of many invertebrates, in-
cluding oysters, feed on diatoms. The eggs of most lamelli-branchs develop into
free-swimming plantonic larvae within a few days, so that one and the same stimulus
could produce the young animals and the plants that will serve as their food.

A link between plant metabolites and animal reproduction is suggested by other
observations. Rapidly maturing herring concentrate around the edges of patches of
plant plankton, although the fully adult herring may avoid them. It has been
suggested that "water-borne metabolities" influence the change of sex that regular-
ly occurs in the mollusk *Crepidula*. The spawning adults, eggs, and young of some
animals have been reported by Wimpenny to occur more often in dense phytoplankton
than in sparse patches. Others associate spawning of the copepod *Calanus* with dense
phytoplankton. Recent research in the physiology of plant pigments seems significant
in this connection, suggesting that the carotenoid pigments have a definite effect
on sex and reproduction of animals.

So, even in the waters of the sea, we are brought back to the fundamental
truth that nothing lives to itself. The water is altered, in its chemical nature
and in its capacity for inducing metabolic change, by the fact that certain organ-
isms have lived within it and by so doing have transmitted to it new properties
with powerful and far-reaching effects. This is a field for imaginative and
creative studies of the highest order, for in it we are brought face to face with
one of the great mysteries of the sea.