Behavior of the Lower Organisms

Now the large Amoeba c stopped, then began to move in another direction (Fig. 21, at 5-6), carrying with it its meal. But the meal — the ball b — now began to show signs of life, sent out pseudopodia, and became very active ; we shall therefore speak of it henceforth as Amoeba b. It began to creep out through the still open canal, sending forth its pseudopodia to the outside (7). Thereupon Amoeba c sent forth its pseudopodia in the same direction, and after creeping in that direction several times its own length, again enclosed b (7, 8). The latter again partly escaped (9), and was again engulfed completely (10). Amoeba c now started again in the opposite direction (11), whereupon Amoeba b, by a few rapid movements, escaped from the posterior end of Amoeba c, and was free, — being completely separated from c (11, 12). Thereupon c reversed its course (12), overtook b, engulfed it completely again (13), and started away. Amoeba b now contracted into a ball and remained quiet for a time. Apparently the drama was over. Amoeba c went on its way for about five minutes without any sign of life in b. In the movements of c the ball became gradually transferred to its posterior end, until there was only a thin layer of protoplasm between b and the outer water. Now b began to move again, sent pseudopodia through the thin wall to the outside, and then passed bodily out into the water (14). This time Amoeba c did not return and recapture b. The two

Amoebae moved in opposite directions and became completely separated. The whole performance occupied about fifteen minutes. Such behavior is evidently complex. An analysis into simple reactions to simple stimuli is difficult if possible at all. We shall return to this matter later. The method of food-taking illustrated in the behavior described is characteristic for Amoebae of the proteus and Umax types. It is sometimes said that these Amoebae take food at the wrinkled posterior end. This, if true at all, is certainly rare; the author has never observed it, though he has seen food taken in dozens of cases. The essential features of the food reaction seem to be the movement of the Amoeba toward the food body (long continued, in some cases), the hollowing out of the anterior end of the Amoeba, the sending forth of pseudopodia on each side of and above the food, and the fusion of the free ends of the pseudopodia, thus enclosing the food, with a quantity of water. The reaction is thus complex; at times, as we have seen, extremely so.

In the process of taking food which we have just described there is no adherence between the protoplasm and the food body. But in A mceba verrucosa and its relatives foreign objects do adhere to the surface of the body, and this adherence is of much assistance in obtaining food. It partly compensates for the lack of pseudopodia in these species. But it is not alone food substances that cling to the surface of the body. Particles of soot and bits of debris of all sorts become attached in the same way. Not all these substances are taken into the body as food, so that adhesion to the surface does not account for food-taking. For this an additional reaction is necessary.

Food-taking in Amoeba verrucosa often occurs as follows: The animal in its progress comes in contact with a small food body, such as a Euglena cyst. This adheres to the surface, and may pass forward on the upper surface of the body to the anterior edge, in the way described on a previous page. At the same time it begins to sink slowly into the body, surrounded by a layer of ectosarc. When it has rounded the anterior edge, the Amoeba passes over it ; then the food body passes upward again at the posterior end and forward on the upper surface. It is now sunk still more deeply into the protoplasm, and by the time it reaches the anterior edge again it has usually passed completely into the endosarc, together with the layer of ectosarc enveloping it. In this way the author has seen Amoeba verrucosa ingest various algas, small flagellates, Euglena cysts, and a small Amoeba of the proteus type. Indifferent particles, such as bits of soot, which are attached to the surface at the same time, are not taken in.

Sometimes the taking of food is in Amoeba verrucosa a much more complicated process than that just described. Rhumbler (1898) has given a very interesting account of the way in which this species feeds upon filaments of algae many times its own length (Fig. 22). The animal settles upon the middle of an Oscillaria filament, envelopes it, and lengthens out along it (a). Then one end bends over (b), so that a loop is formed in the filament (c). The Amceba then stretches out on the filament again, bends it over anew, and the process is repeated until the filament forms a close coil within the Amceba (c to g, Fig. 22). Leidy (1879, P- 86) has given a similar account of the method of feeding on filaments of algae in Dinamceba.

Filaments that have been partly coiled up are often ejected when light is thrown upon the animal (Rhumbler, 1898). Fig. 22. — Amceba verrucosa coiling up and ingesting a filament of Oscillaria. After Rhumbler (1898). The letters a to g show successive stages in the process. We find that the simple naked mass of protoplasm reacts to all classes of stimuli to which higher animals react (if we consider auditory stimulation merely a special case of mechanical stimulation). Mechanical stimuli, chemical stimuli, temperature differences, light, and electricity control the direction of movement, as they do in higher animals. In other words, Amceba has some method of responding to all the chief classes of life conditions which it meets.

The cause of a reaction — that is, of a change of movement — is in most cases some change in the environment, due either to an actual alteration of the conditions, or to the movement of the animal into new conditions. This is notably true of the reactions to mechanical, chemical, and thermal stimuli. In the reactions to light and the electric current this is not so evident at first view. The Amoeba reacts even though the light or current remains constant. But if, as appears to be true, the stimulation occurs primarily on that side on which the light shines, or on the anode side in the reaction to electricity, then it is true that even in these cases the reacting protoplasm is subjected to changes of conditions. Since the movement of the Amoeba is of a rolling character, the protoplasm of the anterior end and that of the posterior end continually interchange positions. In an Amoeba moving toward the cathode the extended protoplasm at the cathode end is gradually transferred to the anode end, and as this change takes place it contracts. In the reaction to light the protoplasm of the anterior end directed away from the light is gradually transferred in the rolling movement to the lighted side; it then contracts. It is therefore possible that in these cases also it is the change from one condition to another that causes reaction.

It is notable that changes from one condition to another often cause reaction when neither the first condition nor the second would, if acting continuously, produce any such effect. Thus, Amoebae react negatively to tap water or to water from a foreign culture, but after transference to such water they behave normally. Harrington and Learning (1900) show that when white light is thrown on an Amoeba it ceases to move, but if this light continues, the animal resumes movement. To constant conditions Amoeba tends to become acclimatized.

But even constant conditions may induce reaction if they interfere seriously with the life activities of the animal. Under great heat or strong chemicals the protoplasm contracts irregularly and remains thus contracted till death follows. A different example of the production of a reaction by constant conditions is shown in the behavior of Amoebae suspended in the water. Under these conditions, as we have seen, the animal sends pseudopodia in all directions, taking a starlike form. It is evident that the general condition of the organism, as well as an external change, may determine a reaction.

The fact that the nature of the behavior depends on the general condition of the organism is illustrated in another way by the observation of Rhumbler, that Amoebae may begin to take food, then suddenly reject it. This rejection occurs especially after subjection to light. Apparently the light changes the condition of the animal in such a way that it no longer reacts to food as it did. In Amoeba, as in higher animals, the localization of the stimulation partially determines the reaction. The result of stimulation on the right side is to cause movement in a direction different from that produced by stimulation on the left side. In Amoeba the relation of the movement to the localization of the stimulus is very simply determined,

through the fact that it is primarily the part stimulated that responds. This part contracts or extends, thus partly determining the direction of movement. But the localization of the external stimulus is not the only factor in determining the direction of locomotion. Especially in the negative reactions certain other factors are evident, which are of much importance for understanding the behavior. After stimulation at one side or end, the new pseudopodium is as a rule not sent out in a direction exactly opposite that from which the stimulation comes. It usually appears, as we have seen, on some part of the original anterior end of the body, and at first alters the course only slightly. This is evidently connected with the fact that only the anterior end is attached to the substratum, and without such attachment locomotion cannot occur. If the pseudopodium were sent out from the unattached posterior part of the body, it would have to overcome the resistance of the contraction existing there, and would have to find the substratum and become attached to it. The new pseudopodium thus starts out from the region of least resistance, and in such a way that the new movement forms a continuation of the original one, though in a different direction. If the new direction still leaves the anterior part of the body exposed to the action of the stimulus, then a new pseudopodium is sent out in the same way, still further altering the course. This may continue till the original direction of locomotion is squarely reversed.

This is the method of changing the course that is usually seen in the reactions to mechanical (Fig. 9), chemical (Fig. 15), thermal, and electric (Fig. 17) stimuli. From Davenport's figures (Fig. 16) it appears to be likewise the method in the reactions to light. From these facts it is clear that the direction of movement in a negative reaction is not determined entirely by the position of the stimulating agent or the part of the body on which it acts. The moving Amoeba is temporarily differentiated, having two ends of opposite character, while the two sides differ from the ends. These internal factors play a large part in determining the direction of movement ; the present action of Amoeba, even when responding to stimuli, depends, as a result of these temporary differentiations, partly on its past action. The new pseudopodium will be sent out under most circumstances from some part of the anterior end, only under special conditions from a side, and still more rarely from the posterior end. We have here the first traces of relations which play large parts in the behavior of animals higher than Amoeba. Structural differentiations have become permanent in most animals, and as such play a most important role in determining the direction of movement. Further, in practically all animals the past

actions are, as in Amoeba, important factors in determining reactions to present stimuli. In Amoeba we see in the simplest way the effects of past stimuli and past reactions in determining present behavior. As a result of this interplay of external and internal factors in determining movement, the avoidance of a stimulating agent usually occurs in Amceba by a process which we should call in higher animals one of trial. If the movement were directly and unequivocally determined by the localization of the stimulus, there would be nothing involved that could be compared to a trial. The direct withdrawal of the part stimulated is a factor due immediately to the localization of the external agent. But the sending forth of a pseudopodium in a new direction is not forced by the external agent, but is an outflow of the internal energy of the organism, and the position of this new pseudopodium is, as we have seen, determined by internal conditions. The latter factors are those which correspond to the activities that we call trial in higher animals. If the new direction of movement leads to further stimulation, a new trial is made. Such trials are repeated till either there is no further stimulation, or if it is not possible to escape completely, until the stimulation falls on the posterior end, and the animal is retreating directly from the source of stimulation.

The entire reaction method may be summed up as follows: The stimulus induces movement in various directions (as defined by internal causes). One of these directions is then selected through the fact that by subjecting the animal to new conditions, it relieves it from stimulation. This is our first example of "selection from among the conditions produced by varied movements," — a phenomenon playing a large part, as we shall see, in the behavior of organisms.

The method of reaction above described gives, with different stimuli, two somewhat differing classes of results. In the reactions to mechanical, chemical, and thermal stimuli, different directions are "tried" until the organism is moving in such a direction that it is no longer subjected to the stimulating agent ; in this direction it continues to move. But in the reactions to light and to electricity new directions are tried merely until the stimulation falls upon the posterior end, and the organism is retreating directly from the source of stimulation. There is no possibility of escaping the stimulating agent completely. In the reactions to the two stimuli last mentioned the long axis of the animal must after a time take up a definite orientation with respect to the direction from which the stimulus comes, while in the reactions to other stimuli there is usually no such orientation. This difference is due, not to any essentially different method of reacting in the two cases, but merely to the peculiar distribution of the stimulating agents ; light and electricity act continu-

ously, and always affect a certain side of the organism, while this is not true of the other agents. If an intense stimulus acts on the entire surface of Amoeba at once, the animal contracts irregularly and ceases to move. If the acting agent is very powerful, the Amoeba may remain contracted till it dies ; otherwise it usually soon begins locomotion again. We may classify the various changes in behavior due to stimulation into three main types, which may be called the positive reaction, the negative reaction, and the food reaction; these have already been described in detail. These types are not stereotyped; each varies much in details under different conditions. The movements in these reactions are clearly not the direct results of the simple physical action of the agents inducing them (see Jennings, 1904 g). As in higher animals, so in Amoeba, the reactions are indirect. The effect of external agents is to cause internal alterations, and these determine the movements. It is therefore not possible to predict the movements of the organism from a knowledge of the direct physical changes produced in its substance by the agent in question.

What decides whether the reaction to a given stimulus shall be positive or negative? This question touches the fundamental problem of behavior. The nature of the physical or chemical action of an agent does not alone determine the reaction, for to the same agent opposite reactions may be given, depending on its intensity, or upon various attendant circumstances. If we should make a chemical or physical classification of the agents affecting movement in Amoeba, this would not coincide with a classification based on the reactions given. But the agents which produce a negative reaction are in general those which injure the organism in one way or another, while those inducing the positive reaction are beneficial. Any agent which directly injures the animal, such as strong chemicals, heat, mechanical impact, produces the negative reaction. The positive reaction is known to be produced only by agents which are beneficial to the organism. It aids the animal to find solid objects on which it can move, and is the chief factor in obtaining food. Thus the behavior of Amoeba is directly adaptive ; it tends to preserve the life of the animal and to aid it in carrying on its normal activities.

It may perhaps be maintained that certain reactions are not adaptive ; for example, that to the electric current. The reaction in this case does not tend to remove the organism from the action of the stimulating agent. But it is instructive to imagine in such a case an organism with possibilities of high intelligence — say even a human being — placed under similar conditions, with similar limitations of sense and of locomotive power. Would it give a more adaptive reaction than Amoeba? Evidently, the conditions are such that it is impossible for the animal to escape by any means from the current. Since the stimulation apparently comes most strongly from the anode side, it is natural to move in the opposite direction. The method of the negative reaction is that of a trial of certain directions of movement. This method is in essence an adaptive one, and if it fails in the present case, certainly no better course of action can be suggested.

Can the behavior of Amoeba be resolved throughout into direct unvarying reactions to simple stimuli, — into elements comparable to simple reflexes ? For most of the behavior described in the preceding pages the stimuli can be recognized in simple chemical or physical changes in the environment. Yet there are certain trains of action for which such a resolution into unvarying reactions to simple stimuli seems unsatisfactory. This is notably true for some of the food reactions. In watching an Amoeba following a rolling food ball, as in Fig. 19, one seems to see the animal, after failing to secure the food in one way, try another. Again, in the pursuit of one Amoeba by another, it is difficult to conceive each phase of action of the pursuer to be completely determined by a simple present stimulus. For example, in Fig. 21, after Amoeba b has escaped completely and is quite separate from Amoeba c, the latter reverses its course and recaptures b (at n-13). What determines the behavior of c at this point ? If we can imagine all the external physical and chemical conditions to remain the same, with the two Amoebae in the same relative positions, but suppose at the same time that Amoeba c has never had the experience of possessing b, — would its action be the same ? Would it reverse its movement, take in b, then return on its former course? One who sees the behavior as it occurs can hardly resist the conviction that the action at this point is partly determined by the changes in c due to the former possession of b, so that the behavior is not purely reflex.

Of less interest than the case just mentioned are modifications in behavior due to acclimatization, and to the interference of stimuli. Amoeba may become accustomed to certain things, so as to cease reacting after a time, though the condition remains the same. Thus Verworn (1889 b) found that Amoebae which at first react to a weak electric current may after a time continue their usual movements, without regard to the current. Harrington and Learning (1900), as we have seen, found that white or blue light thrown on Amoeba causes it to cease moving, but if the light is continued, the movements begin again after a time. In- deed, we have recognized above the general fact that change is the chief

factor in causing reaction, so that such acclimatization is a constant, normal factor in the behavior. A change in reaction due to a different cause is seen in Rhumbler's observation of the fact that Amoeba after beginning to ingest food may reject it when subjected to light. Beyond facts of this character, little is known as to the modifiability of reactions in Amoeba. (Works are cited here by giving the author's name followed by the date of publication. The full title will be found in the alphabetical list at the end of the volume. Only the important works are mentioned.)

A. General account of the behavior of Amoeba, giving details of the observations on which the foregoing account is mainly based : Jennings, 1904 e. D. Reactions to unlocalized stimuli, and to localized heat: Verworn, 1889. Bacteria are perhaps the lowest organisms having a definite form and special organs for locomotion. In these characteristics they are less simple than Amoeba and resemble higher animals, though in other ways the bacteria are among the simplest of organisms. Whether they are more nearly related to animals or to plants is a question of little importance for our purposes ; they are usually considered as nearer to plants. Bacteria are minute organisms living in immense numbers in decaying organic matter, and found in smaller numbers almost everywhere.

They have characteristic definite forms (Fig. 23) ; some are straight cylindrical rods; some are curved rods; some are spiral in form; others are spherical, oval, or of other shapes. The individuals are often united together in chains. - Difterent species of bacteria, processes, the flagella or cilia. The flagella may be borne singly or in numbers at one end of the body, or may be scattered over the entire surface. Figure 23 shows the distribution of flagella in a number of species. In most bacteria we can distinguish a permanent longitudinal axis, and along this axis movement takes place. Thus both the form, and in correspondence with it, the movement, are more definite than in Amceba. If the bacterium is quiet, we can predict that when it moves it will move in the direction of this axis; for Amceba such a prediction cannot be

showing the distribution of the flagella. a. Chromatium • okeni, after Zopf ; b, Chromatium photomctriciim, after Engelmann ; c, Spirillum undula, after Migula; d, Vibrio cholera, after Fischer ; e, Bacilli of typhus, after Fischer ; /, Bacillus syncyaneus, after Fischer ; g, Clostridium butyricum, after Fischer. made. In some bacteria the two ends are similar, and movement may take place in either direction. In others the two ends differ, one bearing flagella, while the other does not. In these species the movement is still further determined ; the end bearing the flagella is anterior in the usual locomotion. In none of the bacteria can we distinguish upper and lower surfaces or right and left sides. As the bacterium swims, it revolves continually on its long axis; the significance of this revolution will be considered in our account of behavior in the infusoria.

The movements of the bacteria are not unordered, but are of such a character as to bring about certain general results, some of which at least are conducive to the welfare of the organism. If a bacterium swimming in a certain direction comes against a solid object, it does not remain obstinately pressing its anterior end against the object, but moves in some other direction. If some strong chemical is diffusing in a certain region, the bacteria keep out of this region (Fig. 24). They often collect about bubbles of air, and about masses of decaying animal or plant material. Often they gather about small green plants (Fig. 25), and in some cases a large number of bacteria gather to form a welldefined group without evident external cause.

How are such results brought about ? To answer this question, we will examine carefully the behavior of the large and favorable form, Spirillum1 (Fig. 23, c). Spirillum is a spiral rod, bearing a bunch of flagella at one end. In a thriving culture a large proportion of the individuals bear flagella at both ends and can swim indifferently in either direction. It is said by good authorities that such specimens are preparing to divide. When Spirillum comes against an obstacle, it responds by the simplest possible reaction, — by a reversal of the direction of movement. In specimens with flagella at each end the new direction is continued till a new stimulation causes a new reversal. In bacteria with flagella at only one end, the movement backward is continued only a short time, then the forward movement is resumed. Usually when the forward movement is renewed, the path followed is not the same as the original path, but forms an angle with it ; the bacterium has thus turned to one side. Whether this turning is due to currents in the water or other

1 There are several species of Spirillum found in decaying organic matter. The species have not been clearly determined in most of the work on behavior, and this is not of great importance, as the behavior is essentially the same in character throughout. accidental conditions, or, as is more probable, is determined in some way by the structure of the organisms, has not been discovered. In the infusoria, as we shall see, the latter is the case. The reversal of movement of course carries the organism away from the agent causing it. We find that the same reaction is produced when the bacterium comes to a region where some repellent chemical is diffusing in the water. This is well shown when a drop of jr per cent NaCl is introduced with a capillary pipette beneath the cover-glass of a preparation swarming with actively moving Spirilla. The bacteria at first keep up their movement in all directions, but on coming to the edge of the drop of salt solution the movement is reversed. Hence none of the bacteria enter the drop, and it remains empty, like the chemicals in Fig. 24.

Fig. 24. — Repulsion of bacteria by chemicals. A. Repulsion of Chromatium ivcissii by malic acid diffusing from a capillary tube. After Miyoshi (1897). B, Repulsion of Spirilla by crystals of NaCl. a, Condition immediately after adding the crystals; b and c, later stages in the reaction. After Massart (1891). They react in this way toward solutions of most acids and alkalies, as well as toward many salts and other chemicals. A drop of these chemicals remains entirely empty when introduced into a preparation of Spirilla.

This simple reversal of movement is the method by which avoidance of any agent takes place ; in other words, it is the method of the negative reactions in bacteria. Bacteria also collect in certain regions, as we have seen, — about air bubbles, green plants, food, etc. ; they have thus what are called "positive reactions" as well as negative ones. What is the behavior in the formation of such collections? One finds, rather unexpectedly, that the positive reaction is produced in essentially the same way as the negative one, — by a simple reversal

of movement under certain conditions. If we place water containing many Spirilla on a slide, allowing some small air bubbles to remain beneath the cover-glass, we find after a time that the bacteria are collecting about the bubbles. The course of events in forming the collections is seen to be as follows: At first the Spirilla are scattered uniformly, swimming in all directions. They pass close to the air bubble without change in the movements. But gradually the oxygen throughout the preparation becomes used up, while from the air bubble oxygen diffuses into the water. After a time therefore the bubble must be conceived as surrounded by a zone of water impregnated with oxygen. Now the bacteria begin to collect about the bubble. They do not change their direction of movement and swim straight toward the center of diffusion of the oxygen. On the contrary the movement continues in all directions as before. A Spirillum swimming close to the bubble into the oxygenated zone does not at first change its movement in the least. It swims across the zone until it reaches the other side, where it would again pass out into the water containing no oxygen. Here the reaction occurs ; the organism reverses its movement and swims in the opposite direction. If the specimen has flagella at each end, it continues its reversed movement until the opposite side of the area containing the oxygen is reached ; then the movement is reversed again. This is continued, the direction of movement being reversed as often as the organism comes to the outer boundary of the zone of oxygen within which it is swimming.1 Thus the bacterium oscillates back and forth across the area of oxygen. Specimens having flagella at but one end swim backward only a short distance after reaching the boundary of the area, then start forward again.