Behavior of the Lower Organisms

The testing movements are specially marked under certain conditions. When the active planarian is about to come to rest, it stops and moves the anterior end from side to side, touching any object that may be found in the neighborhood. After thus thoroughly testing the surroundings, the muscles relax and the animal comes to rest. When later the animal resumes its active progression, this begins again with the testing movements of the head. The same testing movements are seen under various sorts of stimulation. On coming to a solid body, the flatworm moves the head about over its surface. If it turns out to be something fit for food, the animal now feeds upon it, otherwise it moves away again. . If while a number of specimens of Planaria are moving in a certain direction, the direction of the light is changed so as to fall upon their anterior ends, they usually turn the head from side to side two or three times, then follow up one of these movements by turning the body till it is finally directed away from the light. These testing movements are also seen when the animal begins to Fig i 6 — Re- drv> an<^ when the water is heated; the worm gives the action of Planaria to impression that it is seeking about for other conditions. drying. After Pearl. Qther features of the reactions to drying and to

temperature changes are of interest from our present standpoint. If the planarian is laid on a glass plate, as soon as the tendency to dry becomes evident the worm curls up closely and thrusts the head under the body (Fig. 136). In this way the exposed surface of the body is made as small as possible, and the sensitive head especially is kept from drying. At intervals the animal straightens out, extends its head as far as possible, and waves it from side to side. If in this way it finds water, it of course moves into it. If it does not find water, it curls up again. After a time, if the drying becomes more decided, the animal attempts to crawl backward. Under natural conditions drying will usually take place at the edge of a pool, and this backward movement carries the animal again into the water. All together, the reaction to drying is not simple and stereotyped, but involves the successive performance of many different activities.

In responses to heat or cold we find a similar train of activities. If the gliding Planaria comes to a region of considerably higher or lower temperature, it waves its head back Zl and forth several times, apparently till it has determined the direction which leads back to the usual temperature, then turns and moves in that direction. Responses of this character usually take place several times before the animal is completely directed toward the region of optimum temperature (see Fig. 137). If the temperature of the water is slowly raised in a uniform manner, so that all parts of the body are similarly affected, then a series of reactions occurs. First the animals become more Fig. 137. - -Behavior of the flatworm in apactive, gliding about rapidly, ex-

proaching the heated end of a trough The lines tencling the head, and turning it show the paths followed. At each of the points ° ° marked by a round spot, the animal stopped and toward One Side Or the Other. The waved its head to and fro, finally following up behavior resembles that of specipoints show the number of trial movements that mens showing the positive rewere made, in each case. After Mast. actjon to weak stimuli. As the temperature rises, the animal begins to contract at intervals, and to turn the head frequently and strongly from side to side, making little progress in advance. The behavior has now the characteristics of the "negative" reaction. As the temperature rises further, the turning ceases, and the animal begins to make rapid, violent contractions, such as occur in "crawling," under other violent stimuli. Later the animal twists its body, as occurs in its righting reaction when placed on its

back; it thus forms a spiral of two turns. Finally it behaves in a manner somewhat similar to that shown when it dries. It rolls the two ends under the body, arching the dorsal surface. In this position the animal rolls over on its back and dies. Thus under a single unlocalized stimulus of gradually increasing intensity, the behavior of the organism passes through a series of stages, closely resembling the reactions given under most diverse conditions. As Mast (1903), to whom these observations are due, expresses it, "the general impression is given that as the thermal stimulus increases, the animal tries, in a sort of 'hit-or-miss' way, every reaction which it has at command in order to get rid of the stimulation."

The "righting reaction" of the flatworm is another example of a response that is not stereotyped in character, but varies greatly. If the animal is turned on its back, it quickly rights itself again. This usually occurs as follows. The animal twists itself into a spiral (Fig. 138, A), Fig. 138. — Righting reactions in the flatworm. After Pearl. A, reaction of entire worm. B, righting reaction of short piece from anterior end of worm, a, b, c, d, e, /, successive steps in the process. C, righting reaction of triangular pieces, a, manner in which the piece is cut. b, a small portion of the thin edge turns so as to bring the ventral surface in contact with the bottom, c, d, this turning increases; by a continuation of the process the whole piece is finally righted, e, /, cross sections through the pieces while turning.

thus causing the ventral surface of the head to face the bottom, where it attaches itself. Then the worm creeps forward, bringing successively more and more of its ventral surface in contact with the bottom, proceeding toward the rear. Thus the spiral is unwound, so that after the animal has traversed a short distance, the entire ventral surface is in contact with the bottom, as usual. But the righting reaction may take place in quite a different way. Pearl (1903) cut the planarian into pieces of such form that it could no

longer twist itself into a spiral. Then some portion of the ventral surface was brought by other means into contact with the bottom, and from this point the remainder of the surface was pulled into contact. In small strips from the head region, the posterior ends are turned under, bringing the ventral side at this point against the bottom, then by pulling from this point, the entire piece was turned over endwise (Fig. 138, B). In triangular pieces from the middle of the animal, one edge was turned under, then the remainder righted from this region, by pulling the rest of the piece over (Fig. 138, C). These modifications bring out the essentially adaptive character of the behavior. The essential point seems to be, to get some portion of the ventral surface, by any means whatever, into contact with the substratum, then by working out from this point, to bring the whole ventral surface into attachment.

From certain points of view the whole behavior of the flatworm may be considered a process of testing all sorts of conditions, retaining some and rejecting others. As we have seen in the section which precedes the present one, the positive reactions of this animal are not due to any specific qualities of stimulation. On the contrary, the animal turns toward weak stimuli of all sorts. Solid bodies, whether fit for food or not, chemicals of all sorts, including the injurious as well as the beneficial, heat, and cold, all induce, when acting but slightly on one side, a turning toward the source of stimulation. The flatworm may thus be said to investigate every slight change occurring in its surroundings. On reaching a region where the agent in question acts more intensely, the positive reaction may either continue or be transformed into a negative one. Thus the turning toward food is not due to the specific qualities which make the substance in question fit for food, but is the result only of this general tendency to move toward all sources of weak stimulation. The flatworm proves all things, holding fast only to that which is good.

In most if not all other invertebrates there occur many "trial movements" similar to those already described. In many recent accounts of the behavior of other invertebrates little mention, it is true, will be found of such movements. This is apparently because attention has been directed by current theories to other features of the behavior, and the trial movements have been considered of no consequence. Often an attentive reading of papers on "tropisms," etc., will reveal parenthetical mention of various "disordered" movements, turnings to one side and the other, and other irregularities, which disturb the even tenor of the "tropism," and are looked upon for some reason as without significance and not requiring explanation. Further, one often finds in such papers accounts of movements which are clearly of the "trial"

character, yet are not recognized as such by the author, on the watch only for "tropisms." In the earlier literature of animal behavior, before the prevalence of the recent hard-and-fast theories, one finds the trial movements fully recognized and described in detail. This is the case, for example, in the classical papers of Engelmann on behavior in unicellular organisms, and, as we have seen in detail, for that of Preyer on the starfish. Moebius, in 1873, gave a lecture on behavior in which examples of this fact are found. Thus, he describes the reaction of a large mollusk, Nassa, to chemical stimuli, as shown when a piece of meat is placed in the aquarium containing them, in the following way : They do not orient themselves in the lines of diffusion and travel toward the meat, but move "now to the right, now to the left, like a blind man who guides himself forward by trial with his stick. In this way they discover whether they are coming nearer or going farther away from the point from which the attractive stimulus arises" (Moebius, 1873, p. 9).

Unprejudiced observation of most invertebrates will show that they perform many movements which have no fixed relation to sources of external stimuli, but which do serve to test the surroundings and thus to guide the animal. This the present author has observed, for example, in studies on the leech, on various fresh-water annelids and mollusks, and in less extended observation on many other animals. As Holmes (1905) has recently pointed out, in a most excellent paper, this is really a matter of common observation on all sorts of animals. The fact that such movements are not emphasized by writers on animal behavior is evidently due to their being considered without significance.

In a number of recent papers the importance of trial movements in behavior has been more explicitly recognized. Thus, for the earthworm, the recent papers of Miss Smith (Mrs. Philip P. Calvert) (1902), of Holmes (1905), and of Harper (1905) have set this matter in a clear light. Miss Smith showed that in the reactions of the earthworm Allolobophora fcetida to heat and cold, to chemicals, to drying, and to light, "testing movements" play a large part. When stimulated, the earthworm frequently responds by moving the head first in one direction, then in another, often repeating these movements several times. It then finally follows up those movements which decrease the stimulation. Holmes (1905) confirms these results, especially for the reaction of the earthworm to light. His account of the behavior of the earthworm under the action of light coming from one side may be quoted: "It soon developed that what seemed at first a forced orientation, the result of a direct reflex response, is not really such, but that the orientation which occurs and which is often quite definite is brought about in a more indi-

rect manner by a mode of procedure which is in some respects similar to the method of trial and error followed by higher forms" (I.e., p. 99). The precise behavior of the earthworm in becoming oriented to light is described as follows : "As the worm crawls it frequently moves the head from side to side as if feeling its way along. If a strong light is held in front of the worm, it at first responds by a vigorous contraction of the anterior part of the body ; it then swings the head from side to side, or draws it back and forth several times, and extends again. If in so doing it encounters a strong stimulus from the light a second time, it draws back and tries once more. If it turns away from the light and then extends the head, it may follow this up by the regular movements of locomotion. As the worm extends the head in crawling it moves it about from side to side, and if it happens to turn it toward the light it usually withdraws it and bends in a different direction. If it bends away from the light and extends, movements of locomotion follow which bring the animal farther away from the source of stimulus" (I.e., p. 100).

Other observers — Parker and Arkin (1901), Adams (1903) — had observed that when the earthworm is lighted from one side, it by no means always turns directly away from that side ; Adams, however, showed that it turns more frequently away from the light than toward it, thus indicating that the animal has some direct localizing power. This is confirmed by Harper (1905), who shows that in a strong light the earthworm Perichseta commonly turns directly away from the source of light, though if the light is weak, the "trial movements" are seen. Harper gives many other examples of the performance of varied movements under the action of stimuli in this animal, and brings out some of the internal factors on which some of these depend.

Holmes (1905) found that the leech and the larva of the blowfly react to light in essentially the manner which he had found in the earthworm. For the leech the following account is given: "In its progress the leech frequently raises the anterior part of the body and waves it from side to side as if feeling its way. If the animal turns it in the direction of a strong light, it is quickly withdrawn and extended again, usually in another direction. If the light is less strong, it waves its head back and forth several times and sets it down away from the light ; then the caudal end is brought forward, the anterior end extended and swayed about and set down still farther away from the light than before. When the leech becomes negatively oriented, it may crawl away from the light, like the earthworm, in a nearly straight line. The extension, withdrawal, and swaying about of the anterior part of the body enable the animal to locate the direction of least stimulation, and when that is found it begins its regular movements of locomotion. Of a number of random move-

ments in all directions only those are followed up which bring the animal out of the undesirable situation" (I.e., p. 102). In the case of the blowfly larva, Holmes speaks as follows: "Observations which I have made upon the phototaxis of blowfly larvae with the problem of orientation especially in mind soon convinced me that the movements of these forms are directed by light through following up those random movements which bring them away from the stimulus. When strong light is thrown on a fly larva from in front, the anterior end of the creature is drawn back, turned toward one side, and extended again. Often the head is moved back and forth several times before it is set down. Then it may set the head down when it is turned away from the light and pull the body around. If the head in moving to and fro comes into strong light, it is often retracted and then extended again in some other direction, or it may be swung back without being withdrawn. If a strong light is thrown upon a larva from one side, it may swing the head either toward or away from the light. If the head is swung toward the light, it may be withdrawn or flexed in the opposite direction, or, more rarely, moved toward the light still more. If it is turned away from the light, the larva usually follows up the movement by locomotion. Frequently the larva deviates considerably from the straight path, but as it continually throws the anterior part of the body about and most frequently follows up the movement which brings it away from the stimulus, its general direction of locomotion is away from the light. In very strong illumination the extension of the anterior part of the body away from the light is followed by a retraction, since in whatever direction it may extend it receives a strong stimulus and the larva writhes about helplessly for some time. Sooner or later, however, it follows up the right movement.

Occasionally the larva may crawl for some distance directly toward the light, but after a time its movements carry it in the opposite direction. When once oriented the direction of locomotion of the larvae is comparatively straight " ( I.e., pp. 104-105). As Holmes points out, these are only examples of a very general condition of affairs in the lower organisms. We cannot do better, in concluding this brief section, than to quote some of Holmes's general remarks, which show that his observations have led him to essentially the same conception of behavior that we have reached in the present work.

"The role played by the trial and error method in the behavior of the lower organisms has, as yet, elicited but little comment, owing probably to the fact that attention has been centred more upon other features of their behavior. It may have been considered by some investigators as too obvious for remark, since any one who attentively observes the conduct of almost any of the lower animals for ten minutes can scarcely fail to see the method exemplified. If he were watching a chick pecking at a variety of objects and giving signs of disgust when it had seized a nauseous substance, he would doubtless regard the process as one of trial and error, whatever name he might apply to it. A study of the conduct of much lower organisms would disclose many cases almost equally evident. The lives of most insects, crustaceans, worms, and hosts of lower invertebrate forms, including even the Protozoa, show an amount of busy exploration that in many cases far exceeds that made by any higher animal. Throughout the animal kingdom there is obedience to the Pauline injunction, ' Prove all things, hold fast to that which is good '" (I.e., p. 108).

The well-known behavior of hermit crabs in finding suitable shells in which to live and in changing shells which have become unsuitable shows a systematic application of the method of trial extending to the details of the behavior. This is well brought out in the excellent analysis of this behavior given by Bohn (1903). Behavior of higher animals based on the selection of the results of varied movements — the "method of trial and error" — plays, as is well known, a large part in recent discussions of that subject. The work of Thorndike (1898) on behavior in the cat, and the books of Lloyd Morgan (1900), in which this matter is dealt with, are, of course, well known, and require no discussion on our part. The fact that behavior of this character plays a large part in higher, as well as in lower, organisms, is of the greatest interest, as showing that this method is one of fundamental and general importance. But with the details in higher animals we are not here concerned.

3. MODIFIABILITY OF BEHAVIOR AND ITS DEPENDENCE ON PHYSIO- LOGICAL States In the section preceding the present one we have described many cases of behavior in the lower invertebrates in which the animal, under the action of constant external conditions, passes from one form of behavior to another. All such cases are illustrations of the fact that behavior depends upon internal, physiological conditions, as well as upon external stimuli. Since under the same external conditions the action changes, the animal must itself have changed, otherwise it could not now behave differently from before. It is clear that the continuance of a stimulus, or the performance of a certain action, may change the physiological state of the animal so as to induce new reactions.

In some cases the varied actions performed under stimulation have been spoken of as random movements (Holmes, 1905). The word "random," of course, implies only that these movements are not defined by the position of the stimulus; it does not signify that the movements are undetermined. The principle of cause and effect applies to these movements as well as to others. But the causes lie partly within the animal; each phase of the movement aids in determining the succeeding phase. The earthworm may turn to the right at a given instant merely because it has just before turned to the left. Reactions in which a succeeding phase is determined by a previous one have sometimes been called chain reflexes (Loeb, 1900; Driesch, 1903). If this term is used, it needs to be kept in mind that in most cases the succeeding phase is not invariably and irrevocably called up by the preceding one, as is implied by this term. On the contrary, the relation between the two is extremely variable. One type of action may be repeated many times before the second type comes into play, and the order of the different actions is by no means always the same. Thus the preceding phase is only one factor in deciding what shall be the present action. The latter depends upon the entire physiological state of the organism, which is determined by various factors. Illustrations of this are seen in the righting reaction of the starfish and many other animals ; in the series of reactions by which Stentor responds to a mass of carmine grains in the water (p. 174); in that by which Stoichactis gets rid of waste matter lying on thedisk (p. 202), and the like.

The diverse physiological states of lower organisms have been little studied. This is partly because it is rarely possible to observe them directly; it is only through their effects upon action that they become evident. Thus the real data of observation are the actions ; if we considered these alone, we could only state that a given organism reacts under the same external conditions sometimes in one way, sometimes in another. This would give us nothing definite on which to base a formulation and analysis of behavior, so that we are compelled to assume the existence of changing internal states. This assumption, besides being logically necessary, is, of course, supported by much positive evidence drawn from diverse fields, and there is reason to believe that in time we shall be able to study these states directly. Before we can come to a full understanding of behavior, we shall have to subject the physiological states of organisms to a detailed study and analysis, as to their objective nature, causes, and effects.

The most noticeable and therefore best-known physiological states of lower animals are those which depend upon changes in metabolism. The reactions of the starfish and the planarian to many chemical and mechanical stimuli depend, like those of the sea anemone, on the progress of metabolism. Hungry animals react positively to possible food, while satiated ones react negatively to the same stimuli. This most significant relation is, of course, almost universal in organisms ; it shows directly the dependence of behavior on the relation of external agents to internal processes.

V. Uexkull has made precise studies of certain physiological states and of the factors on which they depend, in the sea urchin and a number of other lower animals. In the sea urchin, some of the pedicellarise will not close in response to a mechanical stimulus, save in case this has been preceded by a chemical stimulus. The latter changes the physiological state of the protoplasm (muscle or nerve), so that it now reacts to a stimulus which before would have had no effect. The spines of the sea urchin usually bend toward a spot on the surface of the body that is mechanically stimulated, as by a needle. But if this stimulus has been preceded by the action of a chemical, the spines now reverse the reaction and bend away from the region stimulated. Many such changes in physiological state are brought by v. Uexkull under the heading of changes in tonus of the muscles or nerves. Steady tension, such as is produced in certain muscles by pressing a spine of the sea urchin to one side, decreases the tonus, so that the muscles are no longer so tense as before. Such muscles react more readily to stimuli than do those of higher tonus. Sudden jarring produces the opposite effect, the muscles pull harder and react less readily than before. Decrease of tonus caused by tension is transmitted in some way to neighboring spines, so that after a certain spine has been pressed to one side, all those about it bend in the same direction and react more readily than before. These changes in physiological state play a large part in determining the behavior of the sea urchin under natural conditions.

Besides such changes, there are in the sea urchin others that are less easy to formulate, and that have not been analyzed. V. Uexkull found that the set reflexes of the spines and the changes in tonus mentioned above impose on the sea urchin a behavior that under most conditions seems stereotyped and predictable. This leads the author named to contrast the sea urchin as a "republic of reflexes" with higher animals in which the behavior is unified. But the difference is only one of degree. If the sea urchin is placed on its back, the usual reflexes and their stereotyped interrelations would not restore the animal to the natural position, but merely cause it to walk forward while lying on its back. As a result, we find a physiological state induced that causes a thoroughgoing change in the behavior of the spines. They now move in such a way as to turn the sea urchin again on its ventral surface. As v. Uexkiill says, the behavior of the spines is variable and capable of adapta-

tion ("variabel und anpassungsfahig," 1900, p. 98). This adaptation, under unusual conditions, of the movements of the spines to the needs of the organism as a whole, seems to remove all difference in principle between the behavior of the sea urchin and that of higher animals. Many illustrations of varied physiological states could be given from an analysis of the behavior of the starfish in the righting reaction, and in the various experiments devised by Preyer (see p. 239).

In the flat worm Planaria the work of Pearl (1903) shows that the behavior depends largely upon the physiological state. In this animal the following different states determining behavior may be distinguished : — 1. Conditions of hunger and satiety, determining the reactions to food in a regulatory way. 2. A resting or "sleeping" condition. The animal is often found lying quietly under rocks, the muscles relaxed. In this condition it fails to react to weak stimuli, but strong stimulation induces the negative reaction, followed by continued activity.

3. The condition of normal, undisturbed activity. The animal now responds to weak stimuli of all sorts by the positive reaction, turning toward the side stimulated, while strong stimuli cause the negative reaction. 4. A condition of heightened activity, in which the worm makes many "testing" movements with the head, and reacts positively to most stimuli, whether strong or weak. In this condition the planarian makes the appearance of actively seeking something, and of following up any source of stimulation which it finds.

5. An "excited" condition, produced by stimulating the animal strongly and repeatedly. In this condition the animal moves about violently and reacts negatively to most stimuli to which it reacts at all. 6. Possibly due to an accentuation of the condition last described is a change of reaction observed by Pearl when one side of the head of an excited specimen is stimulated by repeated blows. At first the animal turns farther and farther away from the side stimulated. Then suddenly it jerks strongly backward, and turns far in a direction opposite its previous turning — that is, toward the side stimulated. "The reaction appears as if, after the animal had tried in vain to get away from an uncomfortable stimulus by its ordinary reaction, it finally tries a wild jump in the opposite direction" (Pearl, 1903, p. 580).