Behavior of the Lower Organisms

them. Finding no food, the swallowing movements of the manubrium do not occur. Thus "motile touch," as Yerkes (1902 a) calls it, causes the food reaction, while the touch of an object that is at rest causes only a negative reaction. This reaction to a moving object shows clearly the adaptation of the behavior to the natural conditions of life. Usually, when something moves quickly along the tentacles of a medusa, this will be a fish or other small animal, well fitted to serve as food. So the medusa reacts to such a moving thing in such a way as to seize it and bear it to its mouth. If the object turns out not to be good for food, as is rarely the case, there is of course no harm done, and it may be rejected. If the medusa comes in contact with an object that is not moving, this will probably be a stone or plant or other object not fit for food, hence the animal makes no attempt to take it. The behavior is based, at it were, on the probability that any given case will correspond to the usual condition. Movement serves to the medusa as a sign of something living and fit for food, just as it does to hunters among higher animals and even among men.1 It is a most interesting fact that the positive reaction to a moving object is more rapid than to a quiet one, even though the latter is actually food, while the former is not. The reaction time for a moving object was found by Yerkes (1902 a, p. 440) to be about 0.30 to 0.35 seconds, while the reaction time for quiet objects or food is 0.40 to 0.50. This is again directly adapted to usual conditions ; to a moving animal reaction must be rapid, or it is useless.

One can hardly do otherwise than hold that this specialized reaction to moving objects, so appropriate to the natural conditions of the animal, is not a primitive reflex, but must have been historically developed in some way, and that it would not occur if it were not in the long run beneficial. In sea anemones the dependence of the reactions toward food and other agents on the physiological state of the animal, particularly as determined by the progress of metabolism, is very striking.

Finding Food. — Sea anemones remain for the most part quiet, with disk and tentacles outspread, depending for food largely on the accidental contact of moving organisms with these organs. But there are 1 In this, as in other cases, such expressions as "serves as a sign" of course does not affirm a mental sign, concerning which we have no knowledge in animals outside of the self. It signifies merely that movement does, as a matter of fact, cause a reaction which is appropriate to something usually accompanying the motion, so that the behavior is objectively identical with that due in higher animals and man to a stimulus that serves as a sign.

certain active movements which assist in procuring food. In most sea anemones light stimulation of the tentacles, however produced, causes these organs to wave back and forth, just as happens in medusae ; this increases the chances of coming in contact with food. In Sagartia, according to Torrey, the presence of food near one side of the animal, resulting in weak chemical stimulation, gives rise to more definite movements. Part of the tentacles bend toward the food, contracting on the side most strongly stimulated, while others bend toward the mouth. The animal may at times bend its body toward the food, thus securing it. The tendency of the tentacles to bend toward the mouth, as if carrying food, when stimulated in almost any way, is very striking in many ccelenterates. In Sagartia the tentacles when touched bend first toward the side stimulated, then toward the mouth. In the hydroid Corymorpha, according to Torrey (1904 a), the tentacles when thus stimulated bend only toward the mouth. This bending toward the mouth of course serves the function of carrying food, and it seems to have become the reaction to all sorts of stimuli, on the chance, as it were, that it will serve this function, in the given case. The plan of the behavior is that of trial of a reaction that is beneficial under most circumstances.

The Taking of Food. — In the actual taking of food the behavior varies greatly in different sea anemones. In some species ciliary movement plays the chief part in the process,1 though assisted by muscular contractions. In others, bodily movements brought about by muscles are the main factors. Two or three examples will illustrate the principal variations in this matter. The common Metridium marginatum of the east coast of the United States is an example of the species in which ciliary movement is perhaps the chief agent in food-taking. Under usual conditions the tentacles are pointed away from the mouth, and are covered with cilia, which beat toward the tip of the tentacle. Thus small particles falling on the tentacles are carried outward by the cilia and removed from the animal. But if the particle is something fit for food, the behavior is changed. When a bit of crab's flesh is dropped among the tentacles, they contract on the side touched, thus grasping the flesh. They then bend inward, arching over with tips toward the mouth. The cilia, continuing to strike toward the tip, now of course carry the food toward the mouth instead of away from it. In time the meat drops from the tip of the tentacles into or near the mouth.

The inner surface of the oesophagus, or tube into which the mouth leads, is covered with cilia, which beat outward (save in the two grooves at the angles, known as the siphonoglyphes). They thus bear outward 1 For details regarding this for many different species, see Carlgren, 1905. any indifferent particles which may fall in the oesophagus. But when a piece of meat is dropped into the mouth, the cilia at once reverse, now beating inward. They thus carry the food into the digestive cavity of the animal.

Meanwhile, the muscles surrounding the mouth, and those of the oesophageal tube, contract in such a way as to produce swallowing movements, which aid in ingesting the food. These swallowing movements may begin while the food is still held by the tentacles, showing that the stimulation from the food has been transmitted. In Aiptasia annulata there are cilia which act in the same manner as in Metridium, but the chief role in food-taking is played by movements of the tentacles and oesophagus. If a small object comes in contact with a tentacle, it adheres to the surface, and the tentacle contracts strongly, the entire animal usually contracting at the same time. Then the tentacle bends over and places the food with considerable precision on the mouth. The adjacent tentacles likewise bend over and are applied to the food body, holding it down against the mouth. The latter then opens, the lips seizing the food, while the tentacles may release it and bend away. The swallowing of the food is mainly due to the activities of the lips and oesophagus. In this animal a bit of food may be completely enclosed within ten seconds of the time it touches a tentacle.

In the large sea anemone Stoichactis helianthus, cilia seem to play no part in the taking of food. In this animal the disk may be 10 to 15 cm. in diameter. If a piece of crab meat is placed on the disk of a hungry specimen, the tentacles immediately surrounding it begin suddenly to wave back and forth. This movement stops for a few seconds, then begins again. All the tentacles that come in contact with the food bend over against it and shrink, so as to hold it down against the disk. Now that portion of the disk bearing the food begins to sink inward, the mouth begins to open, and the walls of the oesophagus protrude from the mouth as large bladderlike lobes. The region between the mouth and the food contracts, the tentacles which it bears collapsing and almost completely effacing themselves. By this contraction the mouth and food are caused to approach each other, the intervening region almost disappearing. The oesophageal lobes increase in size, becoming 3 or 4 cm. long and half as thick; they extend toward the food, finally reaching it. The mouth may, in the way described, be transferred from the centre of a disk 10 cm. in diameter to within 1 cm. of the edge. Now the oesophageal lobes extend over the food, while the tentacles progressively withdraw from it, till the food is lying on the contracted part of the disk, completely covered by the oesophageal lobes. Now that part of the disk below the

food withdraws, by an extension and displacement of the mouth, till there is nothing beneath the food body, and it is pressed by the oesophageal lobes into the internal cavity. The lobes then withdraw and the mouth closes. The determining factors in the food reaction are partly internal, partly external, the variations of the former playing perhaps the most important part. Many of the sea anemones are voracious, taking food until the body forms a distended sac. But in most species, if not all, the behavior changes decidedly as the animal becomes less hungry, and after a time it refuses to take food, even removing it if the food is applied to the disk. The changes in reaction as hunger decreases seem less marked in those species in which the food is taken mainly by ciliary action.

Specimens that have not been fed for a long period frequently swallow indifferent bodies, such as pellets of paper, grains of sand, and the like. This has been observed in Aiptasia (Jennings, 1905 a), Sagartia (Torrey, 1904), Metridium (Allabach, 1905), and in a number of Mediterranean anemones (Nagel, 1892). In Stoichactis the taking of such indifferent bodies is rare, but sometimes occurs. In Sagartia and Metridium such indifferent bodies cause a reversal of the beat of the oesophageal cilia, just as is occasioned by actual food. All together, it is clear that in hungry specimens of various sea anemones mechanical stimuli acting alone may cause the food reaction.

In some cases chemical stimuli acting alone produce the food reaction. If filtered crab juice is applied to the tentacles of Metridium, they arch over toward the mouth. If the juice reaches the mouth, the cilia of the oesophagus are reversed, striking inward, just as when a piece of meat is present. The swallowing movements of the oesophagus may likewise take place under chemical stimulation. Parker (1905) has lately found that certain inorganic chemicals, containing potassium, will cause the cilia to reverse and beat inward ; this is the case for example, with KC1 and KN03. But the reversal which takes place under the action of meat juice is not due to the potassium salts which it contains, for it requires a concentration of the potassium salt to produce this result that is much greater than that existing in meat juice. In Adamsia, according to Nagel (1892), the tentacles react to sugar in the same way as to meat juice; this is not true for Metridium and Sagartia.

As sea anemones become less hungry they usually cease to react to such indifferent bodies as grains of sand, pellets of paper, etc., though they still take crab meat readily. In Metridium and Sagartia bits of paper no longer cause the reversal of the oesophageal cilia, by which particles are carried to the mouth, while crab meat still produces this effect. In Aiptasia annulata the tentacles no longer carry pellets of paper to the mouth, but bend backward along the column and drop them. In the Stoichactis that is'not very hungry such indifferent bodies are removed by the rejecting reaction described on page 202.

As the sea anemones become still less hungry the reaction to even such food bodies as pieces of crab meat becomes changed. The reaction gradually becomes slower and less precise. In a hungry specimen of Aiptasia the food reaction is rapid, often requiring but ten or fifteen seconds. But after several pieces of meat have been taken, the reaction occupies a much longer period. The tentacles touched by the food may not react for several seconds, then they bend in a languid way toward the centre of the disk, while the adjacent tentacles may not react at all. The food body is not placed so accurately on the mouth as before. At a later stage food applied to the tentacles induces no reaction at all, or a withdrawal of the tentacles, while if it is applied directly to the mouth it is very slowly swallowed. In Stoichactis at this stage food is often carried toward the mouth, then after or even before it reaches the mouth the reaction is reversed and the food is rejected. If two pieces of meat are applied at once to the disk of Stoichactis when in this condition, one may be swallowed while the other is rejected. Often in Aiptasia one piece may be rejected, while the immediately following piece is swallowed. The animal seems in a condition of most unstable equilibrium, so that the reactions are most inconstant and variable. No one could suppose, in studying the behavior of a sea anemone in this condition, that the behavior of such organisms is made up of invariable reflexes, always occurring in the same way under the same external conditions.

As the animal becomes satiated, the food reaction ceases completely. Pieces of crab meat placed on the disk of a Stoichactis in this state are removed by the rejecting reaction already described. Aiptasia either does not react at all when food is applied to the tentacles, or the tentacles contract and bend backward — a negative reaction. Some anemones are exceedingly voracious, seeming to take food as long as it is mechanically possible for them to do so. This seems to be the case, for example, with Metridium, where the changes in reaction as the animal becomes filled with food are almost lacking. It may feed till the body cavity becomes so completely filled as to cause disturbance of function. As a result the entire mass of food is sometimes disgorged undigested. After this has occurred, Metridium will often take food as before. But in most sea anemones the taking of food ceases before any such disturbance has been produced.

The rejection of food is not determined merely by the mechanical fulness of the digestive cavity, but is evidently due to the effects of food on the internal processes. An Aiptasia (species undetermined), studied by the present author, continued to take filter paper till the body was a swollen sack, and pieces of the paper were repeatedly disgorged. But new pieces, and even those that had just been disgorged, were readily swallowed when applied to the disk. But when specimens of this Aiptasia were fed considerable quantities of meat, they refused to take either more meat or paper.

The reactions of well-fed sea anemones differ in many other ways from those of hungry specimens. They are much less inclined to react to stimuli of all sorts. A disturbance in the water, or a touch with a needle, that would produce a strong contraction in the hungry animal, often causes no reaction whatever in the satiated specimen. A much stronger solution of any given chemical is required to produce contraction than in the well-fed individual. If we should attempt to determine the strength of a given chemical that caused contraction in Aiptasia, we should get totally different results, according as we employed specimens that were very hungry, or only moderately hungry, or thoroughly satiated.

Another factor influencing the food reactions of the sea anemone is fatigue, and the effects due to this are easily mistaken for phenomena of a different character. If the tentacles of a certain region of the disk of Metridium are given many pieces of food, one after the other, they refuse after a time to take the food, though the other tentacles will still take food readily. In taking food very large quantities of mucus are produced, and it is not surprising that many rapid repetitions of this process exhaust the tentacles. If they are allowed to rest five to ten minutes, they usually take food as at first.

As the fatigue conies on, the tentacles first cease to react to weak stimuli, such as are produced by plain paper, or paper soaked in meat juice ; later to strong stimuli, such as that produced by meat. If meat and paper are given in alternation, the tentacles will thus at first take both ; then they come to refuse the paper, while the meat is still taken. Later they come to refuse the meat also. The reaction to food varies also with certain other conditions. In Metridium and Aiptasia the following is often observed: A specimen refuses to take bits of filter paper, though it still takes meat. After it has thus refused paper, two or three pieces of meat are given in succession, and taken readily. Now the bit of paper is placed again on the disk, and it too is swallowed. Clearly, the uninterrupted taking of a number of pieces of meat changes the physiological condition in some way, preparing the animal for the taking of any object with which it comes in contact. One cannot fail to note the parallelism with what occurs in higher animals under similar conditions.

There is a general agreement among those who have studied the behavior of coelenterates that the different parts of the body show remarkable independence in their reactions. The tentacles of the sea anemones and medusae react to most stimuli in essentially the same manner when cut off from the body as when attached. The isolated tentacles of Gonionemus react to meat juice by contracting and twisting, as in the usual food reaction, while to inorganic chemicals they react by a straight contraction, as in the negative reaction of the medusa (Yerkes, 1902 b, p. 183). In Sagartia (Torrey, 1904) and Metridium (Parker, 1896) the separate tentacles react to meat juice by bending toward the side which formerly looked toward the mouth. Thus each tentacle must contain within itself the apparatus necessary for its usual reactions.

The fact that the tentacles have their own reactions independently of the rest of the body is illustrated in a curious way in Loeb's experiment on heteromorphosis in Cerianthus (Loeb, 189 1). He succeeded in causing tentacles to develop at one side of the animal, forming a group not associated with a mouth. These tentacles reacted to food as usual, seizing upon it, and bending over with it in the direction in which, under normal conditions, a mouth would be found. Here it was pressed down for a time, then released.

Like the tentacles, other parts of the body may react independently. Yerkes (1902 b) cut off the manubrium of Gonionemus and pinned it by its base to the bottom of a dissecting dish. It now bent toward food, seized upon and swallowed it, just as in the uninjured medusa. Many experiments with similar results are described in the work of Romanes (1885). Parker (1896) isolated a small bit of the ciliated epithelium of the oesophagus of Metridium. He found that this reacted to meat juice by a reversal of the ciliary stroke, just as happens in the uninjured animal. In Actinia, Loeb (1891) found that if the head is cut off, the lower part of the animal will take food through the oesophageal opening. If the animal is cut in two, even the open lower end of the upper half will take food, just as will the mouth.

For experiments of this kind, the bell of the medusa has become, through the work of Romanes (1885), a classical object. Separating the margin of the bell, containing the chief portion of the nervous system, from the central part, has been a favorite experiment. Romanes found that in the Hydromedusse the margin continues to beat rhythmically, while the centre usually ceases its spontaneous movement. But this was not due to any actual inability of the centre to initiate movement, for Romanes found that when it was stimulated in various ways, it contracts rhythmically. This occurred in the centre of the bell of Sarsia when placed in certain chemicals, notably in weak acids, and in a glycerine solution (Romanes, 1885, pp. 190-197). Rhythmical contractions have likewise been observed by Loeb (1900 a) in the isolated centre of Gonionemus when placed in a pure solution of sodium chloride. Thus it is clear that not only the margin, containing the greater part of the nervous system, but also the centre of the bell, has the power of contracting rhythmically.

These and many other experiments have shown that each part of the body has in the ccelenterates certain characteristic ways of reacting to stimuli, and that it may react in these ways even when separated from the rest of the body. Its reactions may be determined within itself. But from this the conclusion cannot be drawn that the behavior of these animals consists entirely of the separate and independent reactions of these parts to external stimuli. While each part may react independently, each may also react with reference to influences coming from other parts of the body. Thus, the tentacles may react, not only to external stimuli directly impinging upon them, but also, in many ccelenterates at least, to stimuli that are transmitted from other parts. A strong stimulus on the body or on a single tentacle causes a contraction of many tentacles. In some cases this contraction of the other tentacles appears to be due to a direct spreading of the muscular contraction. One fibre pulls on another, setting it in action, until the pull reaches the base of the tentacle. This pull then acts as a direct stimulus, causing the tentacle to contract, in the same way that would occur if it were mechanically stimulated from outside. This is the way in which Torrey conceives of the matter in Sagartia. If this is the correct explanation, there is of course nothing comparable to nervous transmission — passage of a wave of stimulation independently of a wave of contraction — in these cases.

In Aiptasia annulata, on the other hand, a light stimulus on the tip of one of the long tentacles induces a sudden quick contraction of the entire body. This contraction appears to the eye to take place over the entire body at once, and it is so rapid as to suggest strongly the operation of a conducting nervous system. The well-known experiments of Romanes (1885, p. 76) demonstrated completely that in medusae there is such a wave of stimulation independent of a wave of contraction, and that this wave of stimulation coming from other parts of the body causes the tentacles to contract. By cutting off the margin of Aurelia in the form of a long strip and stimulating one end, he could cause a

wave of stimulation to pass to the opposite end. This wave of stimulation was followed, if the stimulus was intense, by a wave of contraction ; if the stimulus was weak, the wave of stimulation passed alone. This wave caused the tentacles along the margin to contract as it reached them. Furthermore, we have seen above that the reaction of the tentacles or of other parts of the body to a given stimulus depends upon the general physiological state of the body, as determined by the progress of metabolism. Certain tentacles may, through the activity of totally different tentacles, in another region of the body, in supplying material for the metabolic processes, come to react to a given stimulus in a manner entirely different from their former reactions.

The tentacles are therefore not to be compared exclusively to independent organisms associated in a group, but they form parts of a unified organism. While they may react when isolated, they react also under the influence of other parts of the body. We have of course the same condition of affairs in the muscles and various other organs of vertebrates. They may react when isolated, but, like the tentacles of the medusa, they likewise react to influences coming from other parts of the organism.

The same is true for the manubrium and for other parts of the body. While the isolated manubrium of Gonionemus may react by bending toward food, it shows the same reaction when certain of the tentacles are stimulated by an object moving rapidly across them. The varied reactions of the manubrium to influences affecting other parts of the body are shown most clearly in the experiments of Romanes described on page 201. In Hydra, when the tentacles have seized food, the mouth often begins to open long before the food has reached it. In Metridium, according to Parker, when the tentacles are touched by food, the oesophagus frequently shows peristaltic contractions, and the sphincter of the mouth closes. It is clear that there is a definite coordination and unity in the behavior, brought about by a transmission of stimuli from one part of the body to another. The difference between these organisms and higher animals is in this respect only one of degree. In the ccelenterates a large share of the behavior is due to the independent reactions of the different organs to the external stimuli, and the transmission of influences from one part of the body to another takes place slowly and without such precision as we find in higher animals.

The part played by the nervous system in unifying the body we need not take up here, as it has been thoroughly analyzed in the brilliant work of Romanes (1885), and has been further discussed by Loeb (1900). The essential conclusion to be drawn from the experiment::! results seems to be as follows : The nervous system forms a region in which the physiological changes resulting in activity take place more readily and rapidly than in other parts of the protoplasm. These changes occur in the nervous system more readily both as a result of the action of external stimuli, and under the influence of changes in neighboring parts of the body. Hence parts containing the nervous system are more sensitive to external stimulation than other parts of the body, and they serve to transmit stimulation more readily. Furthermore, the spontaneous changes occurring in the protoplasm, which result in the production of rhythmical contractions, are more pronounced and rapid in the nervous system than elsewhere, so that the rhythmical contractions usually begin in parts containing nerve cells. But the difference between nerve cells and other cells is only quantitative in character. The peculiar properties of the nerve cells are properties of protoplasm in general, but somewhat accentuated.

Comparing the behavior of this low group of multicellular animals with that of the Protozoa, we find no radical difference between the two. In the ccelenterates there are certain cells — the nerve cells — in which the physiological changes accompanying and conditioning behavior are specially pronounced, but this produces no essential difference in the character of the behavior itself. As in the Protozoa, so here, we find behavior based largely on the process of performing continued or varied movements which subject the organism to different conditions of the environment, with selection of some and rejection of others. We find the same changes in behavior under a continued intense stimulus, determined by changes in the physiological condition of the animal. We find at the same time many reaction movements of a fixed character, dependent largely on the structure of the organism, as we do in bacteria and infusoria. Many of these specific responses to specific stimuli are so definitely adapted to the precise conditions under which the organism lives that we can hardly resist the conclusion that they have been developed in some way under the influence of these conditions, as a result of the fact that they are beneficial to the organism. Such, for example, is the quick though complicated grasping and feeding reaction by which Gonionemus responds to a moving object. Possibly such determinate reactions have arisen through fixation of movements which were originally reached by a process of trial, — a possibility to which we shall return in our general analysis of behavior.

In the Ccelenterata we find also, as in Amoeba, a certain number of responses due to the simple, direct reaction (by contraction) of the part affected by a local stimulus. Where such simple and perhaps primitive reactions are advantageous to the organism, they are preserved as important factors in behavior, as in the negative reactions of medusae. Where they are not advantageous to the organism, they are replaced, supplemented, or followed by more complicated reactions, so that they form a comparatively unimportant feature in the behavior of most of these animals.