Behavior of the Lower Organisms

In ccelenterates we find the same dependence of behavior on the physiological state of the organism that we found so marked in Protozoa. The same organism does not react always in the same way to the same external conditions. In the present group the dependence of behavior on the progress of the internal physiological processes, particularly those of metabolism, stands out strongly. The animal in which material for the metabolic processes is abundant differs radically in its behavior from the hungry specimen. The reaction to a given stimulus depends not alone on the anatomical structure of the animal and the nature of the stimulus, but also upon the way the internal processes are taking place. We cannot predict how an animal will react to a given condition unless we know the state of its internal physiological processes, and often whether a positive or negative reaction will help or hinder the normal course of these processes. The external processes of behavior are an outgrowth and continuation of the internal processes.

The state of the organism as regards its metabolic processes seems indeed the most important determining factor in its behavior. Certain internal metabolic states drive the animal, without the action of any external agent, to the performance of long trains of activity, of exactly the same character as may also be induced by external stimulation. The state of the metabolic processes likewise determines the general nature and the details of the reactions to external stimuli. It decides whether Hydra shall creep upward to the surface and toward the light, or shall sink to the bottom ; how it shall react to chemicals and to solid objects; whether it shall remain quiet in a certain position, or shall reverse this position and undertake a laborious tour of exploration. It decides whether the sea anemone shall react to indifferent bodies, and to food, by the long and complex "food reaction" or the equally long and complex "rejecting reaction." It determines whether Cerianthus shall remain quietly in its tube in the sand, or shall seek a new abode. Innumerable details of behavior are determined in the ccelenterates by this factor.

The same dependence of behavior on the metabolic processes of the organism we have seen in the Protozoa, and especially in the bacteria. Here, however, the change of behavior of a given individual with a change in these processes needs further investigation ; this has been experimentally demonstrated only with reference to respiratory processes in certain green organisms. In higher animals the dependence of the behavior on the state of metabolism is of course most evident.

This dependence of the reaction to stimuli on the relation of external conditions to internal processes is a fact of capital importance, which may furnish us a key to many phenomena that are obscure from other standpoints. The processes of metabolism are not the only ones occurring in organisms, and the relation of external conditions to other internal processes may equally determine behavior. This is perhaps the most fundamental principle for the understanding of the behavior of organisms.

Of a character differing from those just considered are certain other factors which modify behavior in the ccelenterates. Past stimuli received and past reactions given are, as in the Protozoa, important determining factors in present behavior; they may cause either the cessation of reaction to a given stimulus, or a complete change in the character of the reaction. Certain simple conditions produce a tendency in the organism to perform more readily an act previously performed (p. 206). The internal state of the organism may be changed in most varied ways, giving rise to corresponding changes in behavior. These facts give behavior great complexity, as well as great regulative value* even in so low a group as the one now under consideration.

The foregoing chapters attempt to give a connected systematic account of behavior in the Protozoa and the Ccelenterata. These may serve as types of the lower organisms. The necessary spatial limits of the present work render impossible a similar treatment of other groups. We must content ourselves therefore with a survey of some of the main features of behavior in some other invertebrates. We shall take into consideration chiefly the lower groups.

In the action systems of most organisms we find certain well-defined reaction forms, or what are often known as reflexes,1 which make up a large proportion of the behavior. In the groups we have thus far considered, such definite reaction types are seen in the avoiding reactions of infusoria, the definite contractions occurring in response to stimuli in the Protozoa and Ccelenterata, the bending of the tentacles toward the mouth when stimulated by food, in the hydroids and sea anemones, and in many other features of the behavior. It is true, as we have seen, that even these so-called reflexes are usually variable when studied in detail, and their occurrence and combination depend upon a multiplicity of internal as well as external conditions. Yet certain elements of behavior do occur in accordance with a definite type, and this fact is one of much importance. In some lower animals behavior is largely made up of such definite reaction forms. This fact has assumed an overshadowing importance in much recent work on behavior; investigation has taken largely the form of a search for precisely definable reflexes and tropisms, and for conditions under which they occur in the typical way, while other factors in the behavior have been neglected. Since these matters have been so much dwelt upon, we need not take them up in great detail in the present work.

The best-known case of behavior made up largely of such definite reaction forms is that of the sea urchin, as studied by v. Uexkiill (1897, 1897a, 1899, 1900, 1900a). The sea urchin differs from most lower animals in bearing large numbers of motor organs scattered over its entire surface. Most prominent of these are the spines, which are movable, and may be used as legs, or as means of defence. Among the spines are certain peculiar jawlike organs known as pedicellariae (Fig. 133), each borne on a movable stalk. These jaws frequently open and close, seizing foreign objects. The surface of the body between the spines and pedicellariae is covered with cilia. Finally, the body bears five double rows of tube feet, — - fleshy tubular suckers, protruded through rows of holes in the shell. These are important organs of prehension Fig. 133. — One ^ locomotion. All these different sets of organs

from a sea urchin, are interconnected by a network of nerves, one set After v. Uexkiill. iying on the outer surface of the shell, another on the inner surface. These nerves connect with the five radial nerve trunks, which unite to form a ring surrounding the mouth. V. Uexkiill finds that each of these organs (omitting the cilia) has a number of definite reactions or reflexes, which it performs in response to definite stimuli. In these reactions each organ may act as an independent individual. If a piece of the shell bearing but a single spine or pedicellaria is removed, this organ reacts to external stimuli in essentially the same way as when connected with the entire animal. These reflexes change with different intensities and qualities of stimuli, and with certain other conditions, and they are different in diverse sorts of pedicellariae. But each reflex has a very definite character. Thus the sea urchin appears to be made up of a colony of almost independent structures. Each of these structures has reactions of such a character that they perform certain functions that are useful in the life economy of the animal.

Yet these organs are not entirely independent. They are connected by the nervous network in certain definite ways, so that when one of them performs a certain action, others may receive a transmitted stimulus, and may perform the same or a differing action. That is, each organ may receive stimuli not only from the outer world, but also, through the nerves, from other parts of the body. These interconnections are of such a character that they cause the various organs to work in harmony, usually assisting to perform certain necessary functions.

Thus, if debris falls upon the sea urchin, the pedicellariae seize it, break it into bits, and with the aid of the spines and the cilia remove it from the body. Small animals coming in contact with the sea urchin are seized by the pedicellariae and held, till they are grasped by the slowmoving tube feet and spines, and by them carried to the mouth and eaten. When the sea urchin is attacked by an enemy, the spines all bend toward the region of attack, presenting a serried array of sharp points to the advancing enemy. In some species this occurs even when a shadow falls upon the animal. The spines present their points to the shaded side, thus arranging for an effective defence in case the animal which has cast the shadow shall advance to an attack. In some sea urchins, poisonous pedicellariae seize an enemy, usually causing a quick retreat. Further, when the animal is severely stimulated from one side, the reflexes of the spines are so arranged as to carry the animal in the opposite direction. When attacked, the animal is thus effectively defended, while at the same time it flees.

V. Uexkiill emphasizes the independence of these organs, the definite character of their reflexes, and the definiteness of the interconnections between them. These qualities give the characteristic stamp to the behavior of the sea urchin. According to v. Uexkiill, this animal is a "republic of reflexes." Every reflex is of the same rank, and is independent of the others, save for the definite connections that we have mentioned. There is nothing like a central unity controlling the reflexes, according to v. Uexkiill. The sea urchin, he holds, is a bundle of independent organs, and it is only through the arrangement of these organs that a seemingly unified action is produced. "It is only by the synchronous course of the different reflexes that there is simulated a unified action, which really does not exist. It is not that the action is unified, but the movements are ordered, i.e. the course of the different reflexes is not the result of a common impulse, but the separate reflex arcs are so constituted and so put together that the simultaneous but independent course of the reflexes in response to an outer stimulus produces a definite general action, just as in animals in which a common centre produces the action" (1899, p. 390). The difference between the behavior of the sea urchin and that of higher animals is concretely expressed by v. Uexkiill in the statement that when a dog runs the animal moves its legs ; when the sea urchin runs the legs (spines) move the animal.

Yet the fixity of these reactions is by no means absolute, even in the sea urchin. As we shall see in the next section, v. Uexkiill discovered a number of definite laws in accordance with which they change, and there is positive evidence of still other modifying factors not easily formulated. In scarcely any other group of lower animals does there appear to be such a multiplicity of these definite units of reaction as in the sea urchin. In the starfish the extension and withdrawal of the tube feet, and the extrusion and withdrawal of the stomach in feeding, may be considered examples. In free-swimming rotifers we find an avoiding reaction similar in all essentials to that of the ciliate infusoria, the animals when stimulated turning toward a structurally defined side. There is the same variability in this reaction that we find in the infusoria. In planarians, the earthworm, and many other worms, reactions of a fairly well-defined character are seen in the turning of the head toward certain stimuli and away from others. These reactions play a large part in the behavior of Planaria, according to Pearl (1903). Weak stimuli of all sorts affecting one side of the body cause the positive turning ; stronger ones, the negative turning.

Such reactions often depend closely on the localization of the stimulus. This may be illustrated from the behavior of the flatworm just mentioned. A weak stimulus at the side of the head, near the anterior tip, causes the head to turn only a little toward the side touched. If the stimulus is farther back, the turning is greater. In each case the turning is so regulated with reference to the point stimulated as to direct the animal very accurately toward the region from which the stimulus came ; this aids it much in finding food. If something touches the flatworm lightly at the middle of the upper surface of the head, the reaction is much modified. The head is sharply raised and twisted, so as to direct the anterior tip toward the stimulating object, and in such a way that the ventral surface will first come in contact with this object as the animal moves forward. Similar regulatory changes occur in the negative reaction. A strong stimulus at the side of the anterior end causes a quick turning away. A similar stimulus at one side behind the middle causes no turning away, but only a movement forward. At intermediate regions there is a combination of the two reactions, the animal gliding forward and at the same time turning away. The farther back the stimulus is given the greater is the tendency to react by moving forward in place of turning away. This change of reaction with a change in the point stimulated is of course regulatory. An intense stimulus at the anterior end is best avoided by turning away, while one near the posterior end is most easily escaped by moving rapidly forward.

In most animals there are found a certain number of these relatively fixed reaction types which are determined by the usual conditions of existence, — gravity, light, temperature changes, contact with solids, etc. We have examined a considerable number of these in the Protozoa and Ccelenterata. In such reactions the organism often turns or bends directly toward or away from the source of stimulation, as in the positive and negative reactions of the flatworm. Reactions of this character are commonly spoken of as tropisms. In the higher animals and man behavior is, of course, largely determined by the same factors. As we have seen in previous chapters and shall find in the following sections of the present one, in neither lower nor higher animals are the reactions with reference to the general forces of nature of a completely fixed and invariable character.1

In more complex animals than those considered in the present volume, definite reaction forms are often combined into complex trains of action which are known as instincts. Recent work has shown that in these instincts there is by no means that absolute fixity of behavior that was formerly assumed to exist. A detailed treatment of this matter would take us outside the field of the present work. In the highest animals and man, definite reaction forms, which may take place in certain organs independently of the rest of the body, are of course found as abundantly as in lower organisms. Such reactions are seen in the reflexes of muscles, etc., which persist even after the muscle has been removed from the body. There is no difference in principle along this line between higher and lower animals. The former possess a much larger number of such definite types of movement, and these doubtless make up fully as large a portion of behavior as in the lower animals.

There are some accounts of behavior in various lower animals in wrhich only these definite reaction forms are described and only those conditions are dealt with in which these appear in the typical way. Such accounts have given rise to a widespread impression that behavior in the lower animals differs from that of higher forms in that it is of a fixed, stereotyped character, occurring invariably in the same way under the same external conditions. This impression is in a high degree erroneous. These definable reaction forms are usually in themselves variable within wide limits, as exemplified in the avoiding reaction of infusoria. But even if this were not true, the criteria for judging as to the fixity or modifiability of behavior are to be derived from the study of the conditions that induce reaction, that determine which of several possible reactions shall occur, and that determine the order and combination of reactions. Such a study shows that in lower as well as in higher animals varied internal conditions and changes are of the greatest importance in determining behavior, the animal by no means behaving always in the same way under the same external conditions. With this aspect of the matter we shall deal in the two following sections.

1 See, for example, the section on reactions to gravity in ccelenterates, Chapter XI. In the foregoing section we have dealt with the fact that stimulation often causes the performance of actions that are of a definite, typical character, such as are often called reflexes. But this by no means exhausts the problem of behavior, as our account of the matter in unicellular animals and in Ccelenterata has shown us. Indeed, we find it not to be the rule that an animal when stimulated performs a single definite movement, then returns to its original state. On the contrary, stimulation is usually followed by varied movements, and the animal may continue active long after the external agent has ceased to impinge upon it. The continued varied movements subject the organism successively to many different conditions, external and internal. In one of these conditions the animal remains through a cessation of the changes in activity. It may thus be said to select certain conditions through the production under stimulation of varied movements. We have seen many examples of this type of behavior in the groups thus far considered.

Behavior of this character is very general in lower animals. We shall in the present section give a number of examples, taken from diverse classes of invertebrates. As we have seen, the echinoderms furnish perhaps the best examples of organisms in which the behavior is made up largely of more or less independent "reflexes." Yet in the same group we find that much of the behavior is of the type now under consideration. There is, of course, no opposition between the two, the different "reflexes" forming the variables out of which behavior of the present sort is made up. The pedicellarke of the sea urchin have, as we have seen, a number of these definite reflexes. When the entire animal is suddenly and strongly stimulated, by mechanical shock, by a chemical, or by light, the pedicellariae respond, not by a single definite reflex, but by beginning to move about in all directions (v. Uexkiill). They seem to feel and scrape the entire surface of the body, seizing anything with which they come in contact, and this behavior may continue for an hour or more after stimulation has ceased. Similar effects are often produced in the spines by a general stimulus. They wave about, their tips describing circles, and this may continue for a long time. Such reactions are seen also in the tube feet. When the sea urchin or starfish is suspended in the water or is placed on its back, the tube feet extend and wave back and forth, as if searching for something to which they might attach themselves.

On a more extensive scale, the "righting" reaction of the starfish is a notable example of behavior that is not stereotyped, but is flexible and variable. The usual course of this reaction is as follows: After the starfish has been placed on its back, it extends its tube feet and moves them about in all directions. At the same time the tips of the arms become twisted, so that some of the tube feet are directed downward. In this way, after a time, some of the feet become attached to the bottom. These begin to pull on the arm to which they belong, turning it farther over and bringing other tube feet into contact with the bottom; these now assist in the process. If two or three adjacent rays become thus attached, the other rays cease their searching, twisting movements, and allow themselves to be turned over by the activities of the tube feet of the attached rays. If two or more opposite rays become attached to the bottom in such a way that they oppose each other, then one releases its hold, and allows the turning to be accomplished by the opposing rays. It is evident that the reaction is an example of the performance of varied movements under stimulation, with selection from the conditions resulting; from these movements. Certain features in this reaction are of special interest. At first all the tube feet and rays try to find an attachment. When certain ones have succeeded, this is in some way recognized by those parts whose action would oppose the movement, for these cease their attempts, or even release the hold already attained. In some way the physiological state corresponding to "success" in certain rays is transmitted to the other rays, and they change their behavior accordingly.

Variability and flexibility are the essence of such behavior. This is well illustrated by study of repetitions of the righting reaction in the starfish. It is by no means always the same arm or combination of arms that initiates and finally brings about the turning. The essential point is to get started in some way, then to continue on the basis of the start made. Preyer (1886) studied this behavior in the starfish with great care. He says : " Neither in one [species] nor the other is the method of turning always the same. I have likewise seen Aster ias glacialis, which was several times in succession turned on its back without change in the outer conditions, right itself sometimes in one manner, sometimes in another. The spirals of the twisted arms do not work each time in corresponding directions, but at first the neighboring arms often oppose each other. But soon the correction takes place, in that the attached feet stop those that are disturbing the turning, and the wrongly twisted radii straighten out again. . . . The variability of form in starfish that are righting themselves is great, and no species rights itself in only one way. . . . But here, too, it is true that no Astropecten rights itself twice in succession in exactly the same way. An adaptation to the sur-

face of attachment always occurs, and according as this is convex, concave, smooth, rough, or inclined, is the turning process made easier or more difficult, and brought about in this manner or that" (1886, pp. 107- 108). Sometimes the animal turns a somersault; sometimes it extends all its arms upward, taking the "tulip" form and toppling over on one side — and so on through many variations. Even the main features of the typical reaction may be omitted or changed, the turning taking place by means quite different from the usual ones. Thus, Astro pecten aiirantiacus usually rights itself by means of its tube feet, but sometimes turns without using the tube feet at all. Lying on its back, it lifts the central disk high, resting on the tips of three or four of the arms. Then it turns two of the arms under, while lifting the others upward, so that it now falls with ventral side down. During this action the tube feet are moved about in a lively way, and when the turning is nearly completed the tube feet of the upper radii which are approaching the substratum are pushed far out, as if preparatory to meeting the bottom.

When a portion of the feet were prevented from acting, by subjecting them to alcohol or other drugs, Preyer found that the starfish righted itself by means of the remaining ones, and by bending and twisting its arms. Pieces of the arms may right themselves, and this again occurs in many different ways. The thorough study of the movements and reactions of the starfish made by Preyer (1886) shows that the righting reaction is typical of the entire behavior. If the starfish is suspended just below the surface of the water with ventral side up, by threads attached to the tips of its arms, it performs varied movements, until in the course of time it turns over, just as in the usual righting reaction. If a short rubber tube was slipped over one of the arms of a brittle star, to its base, Preyer found that this caused the animal to perform many varied movements, till by one of them the tube was removed. Sometimes the animal merely moved rapidly forward, dragging the arm bearing the tube behind it till the tube was scraped off. Sometimes the animal placed one or two of the other arms against the tube and forced it off. In other cases the covered arm was dropped from the body (as often happens in brittle stars). Again, sometimes the arm bearing the tube was lifted and waved back and forth, till the tube was in this way displaced. Thus Preyer observed five different ways in which the tube was finally removed; as he remarks, "If one method does not help, another is used." It may, of course, be maintained that in all these cases the removal of the tube was in a sense accidental. But this is precisely the essential point in much of the behavior of lower organisms. When stimulated

they perform varied movements, till one of these "accidentally" removes the source of stimulation. How this may develop into more directly regulatory reactions we shall consider in the next section. The same qualities are shown in certain experiments of Preyer in which he attempted to confine the starfish by means of large, flat-headed pins. These were placed in the angles between the rays, close against the disk, and driven into the board on which the starfish lay. They thus held it down without injury. The starfish in the course of time escapes from the pins, but only after much effort. The animals try successively various methods, " now they seek to force themselves through, now to climb over the top, now to push through by turning on one side." In scarcely any two cases does the process of escape occur in the same way, according to Preyer. The behavior is as far as possible from that of invariable reflexes always occurring in the same way under the same external conditions.

One further point mentioned by Preyer is of great interest. He says that when the experiment is repeated with the same individual, the time required for escape becomes less. The number of useless movements, "superfluous twistings, feelings about, and forward and backward motions," becomes less the oftener the individual has been placed in such a situation. If this is true, we have in so low an animal as the starfish regulation through the selection of conditions produced by varied movements passing into a more directly regulatory action; in other words, what is commonly called in higher animals intelligence. There seems to be no reason for doubting Preyer's observations on this point, but on account of their great importance they should be repeated and verified or refuted.

Many other illustrations of behavior of the general character set forth above could be presented from the valuable work of Preyer (1886). It has become the fashion to neglect and even speak slightingly of the work of Preyer on the behavior of the starfish. This seems to be due to the tendency observable in recent scientific literature to represent all such matters as extremely simple and reducible to separate well-known mechanical factors, and to avoid all experiments tending to reveal the fallacy of this view. Preyer was not afraid to open his eyes by properly designed analytical experiments to the complexity and regulatory character of the behavior. Such thorough and detailed studies of animal behavior as that of Preyer on the starfish are rare at the present time ; his work stands in this respect in most refreshing contrast with some of the superficial work recently put forth. The excellent work of Romanes (1885) had already, before Preyer, brought out many examples of the style of behavior we have illustrated above.

In many free-swimming Rotifera the chief methods of movement and reaction are similar even in details to those of the free-swimming infusoria, which we have already described. Like the infusoria, these rotifers swim by means of cilia, revolve on the long axis, and swerve toward one side (usually dorsal), as they progress. The cilia produce a current passing from in front to the mouth and ventral side, thus allowing the animals to test the conditions in advance. To most effective stimuli these rotifers react, as do the infusoria, by swerving more than usual toward one side, — usually the dorsal side. Thus the spiral becomes much wider, and the animals are pointed successively in many different directions and subjected to many different conditions. In time they may thus reach conditions which relieve them of the action of the stimulating agent. Thereupon the reaction ceases, so that the animals continue in the direction which has thus been reached. All the general features of the reactions are essentially like those of infusoria, so that we need not enter into details. The reactions to mechanical stimuli, to chemicals, to heat and cold, to light, and to electricity are known to occur in the way just • 'a I34i — Pla" sketched, in a number of species. Orientation to

After Woodworth. light and to the electric current takes place in the same way as the orientation to light in Euglena and Stentor. It is interesting to observe that in the Rotifera, owing to the concentration of the cilia at one end of the animal, there is no such incoherence and lack of coordination in the reaction to the constant electric current, as is found in infusoria. The rotifer (Anurcea cochlear is) becomes oriented with anterior end to the cathode by the same method as in reactions to light and other agents.

In many rotifers the reaction plan just described forms only one feature of the activities, so that the behavior, taken all together, may be exceedingly complex. There is much opportunity for further study of the reactions of this group. But so far as known, much of the behavior may be expressed as follows: When stimulated, the animals perform continued and varied movements, the variations often taking place in a systematic way. These movements necessarily subject the animals to varied conditions, one of which is finally selected, through the fact that it removes the cause of stimulation.

Much of the behavior of the flat worm Planaria (Fig. 134), as studied Fig. 135. — Side view of moving Planaria. After Pearl. A, body; B, mucus; C, cilia; D, substratum. by Pearl (1903), may be summed up under the same formula set forth in the preceding paragraph. Varied movements which subject the animal to many different conditions, are seen even in the unstimulated specimen. As the flatworm glides along by means of its cilia, the head is held upward (Fig. 135) and moved frequently from side to side, while its margins wave up and down, and are extended and contracted. The flatworm thus seems to "feel its way" with its head. Sometimes these feeling movements become much accentuated, the animal almost or quite stopping, then raising the whole anterior part of the body and waving it about in the water. These movements of course serve to test the environment on each side ; in other words, they subject the sensitive anterior end to varied conditions.