Behavior of the Lower Organisms

A large share of the behavior of lower as well as of higher animals j consists of movements either toward or away from certain objects or sources of stimulation. Behavior can thus be largely classified into two great classes: "positive and negative" reactions; movements of "attraction and repulsion," of approach and retreat. To account in a general way for these directed movements certain theories have been proposed, and one of these has become widely accepted. This is the so-called "tropism theory." The word "tropism" has been used in several different senses by different authors, and not always as implying a definite theory (see page 274). But there is a certain theory which is usually implied when tropisms are mentioned; it has become so generally accepted that it is often spoken of as the tropism theory. It will perhaps be more accurate to speak of it as the local action^ theory of tropisms. "Tropisms" has become the keyword for the behavior of lower organisms, and the theory mentioned is supposed to furnish explanation of most of the puzzles found in this field. A theory so generally accepted demands separate special treatment. What is this tropism theory as usually understood in discussions of animal behavior, and how far does it go in helping us to understand the behavior of lower organisms ?

According to this tropism theory the primary feature in the directed movements of lower organisms is the position or orientation of the body with respect to the source of stimulation, and this orientation is brought about by the direct local action of the stimulating agent on that part of the body on which it impinges. The essential points in this theory are then two: first, orientation; second, the production of orientation by local action. These points we may consider separately.

(1) By this tropism theory a stimulus is considered to force the animal to take a certain position with respect to the direction from which the stimulus comes; in this position it is said to be oriented. Usually the organism becomes oriented with anterior end either toward or away from the source of stimulation. This is the essential feature in the action of the stimulus. "The essential point in all directive stimulation is therefore the axial orientation of the cell body, and the central point in the mechanism of this phenomenon, lies in the explanation of this axial position" (Verworn, "General Physiology," 1899^.480). After the animal has thus become oriented it may move forward in the usual way. If it does so, it will of course incidentally move toward or away from the source of stimulation, but this approach or retreat is not an essential or determining part of the reaction. "The really fundamental phenomenon which characterizes these directed movements is always not so much the forward movement as such, as rather a process which may be called a movement of orientation. The organism places its axis in a definite localized relation to the stimulus, which may be photic, thermic, chemical, etc. That is, it places its axis either in the direction of the stimulation or perpendicular to it (diatropism). In the former case the 'anterior' end may be directed 'positively,' toward the source of stimulation, or 'negatively,' away from it. It now appears a matter of course that if forward motion takes place after such orientation, its direction will correspond to the direction of the stimulus" (Driesch, 1903, p. 5, translation).

(2) This orientation is produced, according to this tropism theory, by the direct action of the stimulating agent on the motor organs of that side of the body on which it impinges. A stimulus striking one side of the body causes the motor organs of that side to contract or extend or to move more or less strongly. This, of course, turns the body, till the stimulus affects both sides equally ; then there is no occasion for further turning, and the animal is oriented. "These tropisms are identical for animals and plants. The explanation of them depends first on the specific irritability of certain elements of the body surface, and, second, upon the relations of symmetry of the body. Symmetrical elements at the surface of the body have the same irritability; unsymmetrical elements have a different irritability. Those nearer the oral pole possess an irritability greater than that of those near the aboral pole. These circumstances force an animal to orient itself toward a source of stimulation in such a way that symmetrical points on the surface of the body are stimulated equally. In this way the animals are led without will of their own either toward the source of stimulus or away from it" (Loeb, 1900, p. 7). Holt and Lee (1901, pp. 479-480) bring out this point in the prevailing theory, as applied to light, as follows : "The light operates, naturally, on the part of the animal which it reaches. The intensity of the light determines the sense of the response whether contractile or expansive, and the place of the response, the part of the body stimulated, determines the ultimate orientation of the animal."

How the orientation is brought about according to this theory may be illustrated most simply by considering an organism covered with cilia. For this purpose we may employ the accompanying diagrams, based on those given by Verworn (1895, p. 484), but modified to make them clearer. In Fig. 142 a stimulus is supposed to act from the right side on the organism, as indicated by the arrows, and to cause the cilia of that side to contract more strongly, as is indicated by the heavier shade and greater curving. This must, of course, turn the body to the left, as a boat is turned to the left when the right oar is more strongly

pulled. The animal therefore occupies successively the positions 1,2,3, and 4. In the position 4 both sides are equally affected by the stimulus, so that there is no cause for further turning. The animal has become oriented and its usual forward movements now take it away from the source of stimulation. We have here a case of negative tropism or taxis. Figure 143 illustrates the conditions producing positive tropism or taxis. The stimulus, coming from the right side, is supposed to cause the cilia of that side to beat less strongly backward, or to beat forward. As a result the organism is turned to the right, through the positions 1, 2, 3, 4, till its anterior end is directed toward the source of stimulation. Both sides are now affected alike, and there is no cause for further turning. The animal now moving forward in the usual way of course travels toward the source of stimulation.

As an example of the application of the tropism scheme to a muscular organism, we may take Davenport's exposition of the action of light in determining the direction of locomotion of the earthworm. "Represent the worm by an arrow whose head indicates the head end (Fig. 144, A ). Let solar rays SS fall upon it horizontally and perpendicularly to its axis. Then the impinging ray strikes it laterally, or, in other words, it is illuminated on one side and not on the other. Since, now, the protoplasm of both sides is attuned to an equal intensity of light,

that which is the less S illuminated is nearer its optimum intensity. Its protoplasm is in a photO- Low light attuncment tonic conclition. That lar organism, such as the earthworm. After Davenport, condition. Only the darkcapable of normal contraction; the brightly illuminated ones are relaxed. Under these conditions the organism curves toward the darker side; and since its head region is the most sensitive, response begins there. Owing to a continuance of the causes, the organism will continue to turn from the light until both sides are equally illuminated, i.e. until it is in the light ray. Subsequent locomotion will carry the organism in a straight line, since the muscles of the two sides now act similarly. Thus orientation of the organism is effected. The same explanation, which is modified from one of Loeb ('93, p. 86), will account, mutatis mutandis, for positive phototaxis " (Davenport, 1897, p. 209).

From the relations above set forth, it follows that for determination of the direction of movement in accordance with this tropism theory, a stimulus must act upon one portion of the body differently from or more intensely than on other parts. Without such differential action on different parts of the body there is nothing to cause the animal to turn in one direction or another. This tropism schema is made by its upholders the basis for the larger part of the directed activities of the lower animals. "Thus the phenomena of positive and negative chemotaxis, thermotaxis, phototaxis, and galvanotaxis, which are so highly interesting and important in all organic life, follow with mechanical necessity as the simple results of differences in biotonus, which are produced by the action of stimuli at two different poles of the free-living cell" (Verworn, 1899, p. 503). Verworn (1899) and Loeb (1900) have developed the theory as a general explanation for all sorts of directed activities, and many authors have accepted it for reactions to particular stimuli. In recent times, Holt and Lee (1901) have applied it in detail to the responses to light, Loeb (1900, p. 186) and Garrey (1900) to chemicals, Loeb (1897) and Verworn (1899) to gravitation, Mendelssohn (1902 a) to heat and cold.

In the foregoing chapters we have examined the behavior of a considerable number of lower organisms, of many different kinds. How far does this examination support the above theory? How far is the observed behavior due to orientation produced by the local action of stimuli on the different parts of the body? To what extent does this tropism theory aid us in understanding the behavior of these organisms ? In Amoeba there are no permanent body axes ; anterior and posterior ends continually interchange places in the rolling movement, and any part may become at any time the advancing portion. Under these conditions the term "orientation" can have little meaning, and we can hardly say that stimulation causes the body to become oriented in a certain way. But stimulation does determine the direction of motion, and anything like orientation that can be distinguished is a result of the direction of motion, not its cause. Under stimulation the direction of movement is changed first, then in consequence the animal takes an elongated form which furnishes the only possible basis for the use of the term "orientation."

In the fact that to produce directed movement, local action of the stimulus on a certain part of the body is necessary, causing local contraction or extension, the conditions in Amceba agree with the fundamental postulates of the tropism theory. The agreement is most precise in the positive reactions, where the part stimulated is the part that extends and determines the direction of movement. In the negative reactions the agreement with the theory is less complete ; for while the part that contracts is determined by the region stimulated, the extension and consequent direction of movement are, as a rule, not thus determined.

But while some important features of the behavior of Amoeba are thus in agreement with the underlying assumptions of the tropism theory, it is certain that for such organisms alone the theory would never have been proposed. The facts for Amoeba can be formulated in a much simpler way than by bringing in the conception of orientation, — a conception derived from organisms with permanent body axes, and fitting only these. But when we turn to an examination of the behavior of those unicellular organisms having permanent body axes, we find the conditions widely at variance with the assumptions of the local action tropism theory. In the infusoria most of the behavior is quite inconsistent with the theory. The reactions are not determined by the direct action of a localized stimulus in producing greater contraction or extension in that part of the body on which it impinges. The organism responds as a whole, by a reaction involving all parts of the body. It does not necessarily turn directly toward or directly away from the source of stimulation, as would be the case if it reacted in accordance with this tropism theory. The direction of turning is determined by internal factors; the animal turns toward a side which is structurally defined. For inducing directed motion it is not necessary that the stimulus should act differently on different parts of the body. The cause of reaction — that is, of a change in the movements — is usually a change from one condition or intensity to another. Thus the essential point in determining whether reaction shall occur is in most cases the direction of movement — whether this takes the organism (or its most sensitive portion) away from, or toward, the optimum. It is difficult to conceive a type of behavior more completely opposed to the local action theory of tropisms above set forth.

In some cases this method of reaction produces orientation with relation to the direction of some external force, in other cases it does not. The orientation when it occurs is brought about through continued movements that are varied in direction, with final selection of one of these directions. Whether orientation shall or shall not result depends on whether it must result in order that there shall be a cessation of the stimulation which is producing the varied movements. These relations have been set forth in detail in our account of the behavior of Paramecium (Chapter IV, Section 6), so that it is not necessary to take them up here.

To almost all the relations set forth in the preceding paragraphs there is one exception. In the reaction of ciliate infusoria to the electric current we find certain features which agree with the local action tropism theory. These features are so striking and so utterly at variance with everything found in the remainder of the behavior of these organisms that they throw into strong relief the contrast between the usual behavior and the requirements of this tropism schema. Owing to the remarkable cathodic reversal of the cilia (a phenomenon not paralleled under any other conditions), the motor organs of opposite sides or ends of the ciliate infusorian act under the electric current in different ways. The result is behavior partly in accordance with the tropism schema. This furnishes us with a picture of what behavior would be if this schema held throughout. The unity and coordination that are so striking in the remainder of the behavior are here quite lost. Different parts of the motor organs urge the organism in different directions at the same time. The animal seems to be trying to do two opposed things at once (see p. 89). Nothing more ineffective and unpurposive can be imagined than such behavior. But in producing these local effects the electric current is unique among stimuli, and the reaction is as far from the typical behavior of these organisms as can be imagined. The electric current may be used for producing local contractions in man as well as in Paramecium, but such contractions cannot be considered an adequate type of the behavior of mankind. The electric current never acts effectively on the organisms under the natural conditions, so that normally they never show the peculiar behavior produced by it. To all the natural conditions of existence they react in a totally different manner — a manner quite at variance with this tropism schema.

In the bacteria as in the infusoria the behavior is not in accordance with the above-discussed theory of tropisms. The details of the reactions are not so completely known as in the infusoria. But what we know shows that the behavior of these organisms so far as involved in the directed reactions is as follows: When stimulated the bacterium changes its course, moving in some other direction, — a direction determined by its own body structure, and not by the position of the stimulating agent.

Thus we find in the unicellular organisms very little in the behavior that can be interpreted in accordance with this local action theory of tropisms. The latter does not by any means express the fundamental nature of their behavior in directed reactions. These are based chiefly on the performance under stimulation of varied movements, with selection from the resulting conditions, — the "method of trial." In the symmetrical Metazoa we of course find many cases in which the animal turns directly toward or away from a source of stimulation, without anything in the nature of preliminary trial movements. This

is a simple fact of observation, which leaves open the possibility of many different explanations. Is the simple explanation given by the local action theory of tropisms one that is of general applicability to the directed reactions of lower and higher Metazoa ? In considering the evidence on this question, we find that even in symmetrical Metazoa the direction of movement with reference to external agents is by no means always brought about by a simple, direct turning. On the contrary, in many of the Metazoa, trial movements are as noticeable and important as in the Protozoa. This we have illustrated in detail for many invertebrates in the section devoted to this subject (Chapter XII, Section 2). For such behavior the local action theory of tropisms fails to give determining factors.

In some cases the turning movements are directly toward or from certain stimuli. But the question here is, whether this turning is produced by the local action of the agent in question on the part of the body against which it impinges, as is asserted by the theory which we are considering, and illustrated in Fig. 144. In a few instances this is apparently the case. The medusa escapes unfavorable stimulation by contracting most strongly on the side on which the stimulus impinges. In Hydra local stimulation by chemicals, heat, or electricity often produces limited local contraction, causing the animal to bend toward the side stimulated. In various sea anemones the tentacles, and sometimes the body, may bend toward the side stimulated, as this theory demands. Yet this direct contraction plays very little part in the behavior of these animals. In Hydra it is only injurious agents to which the animal responds in this way, and the result is to still further subject the animal to the action of the injurious agent. In order to escape the action of injurious stimuli, Hydra has recourse to behavior of quite a different character, and in its natural life there seems to be no indication that behavior ever occurs in accordance with this theory of direct local action. In sea anemones the direct turning toward the region stimulated is at once supplemented by movements determined in quite a different way, — through the structure of the organism, — the tentacles bending toward the mouth. Without this supplementary reaction the local bending would be of no service. In the hydroid Corymorpha it is only this second method of bending that occurs at all. Throughout the Ccelenterata the part played by trial movements, not directly determined by the position of the stimulating agent, is most striking and important.

In the echinoderms we have, as in Amoeba, organisms which are as a rule without a definite body axis, so far as the direction of locomotion goes; there is usually no permanent anterior, posterior, right, or left. Hence a theory like that of tropisms, based primarily on the position or orientation of the body axis with reference to the direction of the stimulating agent, can find little precise application. Yet it is again in this group that we find behavior that is in certain respects at least in accordance with the tropism theory. For locomotion in a certain direction the stimulus must be localized, acting in a different way on the two sides; this is one of the postulates of the tropism theory. Further, a local stimulation may have at least a partially local effect, and this may result in movement in a certain direction. But as v. Uexkull has well pointed out, the elementary factors here are the typical reaction methods (" reflexes") of the individual organs of the body surface. The tropism, if we attempt to apply the concept at all, is a mere collection of these elementary reactions ; it is not in any sense itself an elementary factor. In other words, the tropism theory would never have been based on the known behavior of the echinoderms, for the facts, even so far as they agree with the fundamental postulates of the theory, can be formulated more directly and simply in another way. The tropism theory is furnished with an apparatus of relations that finds no application to the starfish and sea urchin.

Furthermore, as we have shown in detail, much of the behavior of these animals is based on the method of trial. In such bilaterally symmetrical animals as the flatworm Planaria we have the most favorable possible conditions for action on this tropism theory, and such animals often do turn directly toward or away from sources of stimulation. But when this occurs, is it due merely to the local contraction or extension of the musculature on the side on which the stimulus impinges, or is it a reaction of the animal as a whole ?

This question can be answered only by a thorough study of all the factors in the reaction; such a study is given us for the flatworm by Pearl (1903). The positive reaction of the flatworm — the direct turning toward the source of stimulation — seem to present ideal conditions for explanation on the simple tropism theory. But Pearl, after exhaustive study, concludes that the processes in the reaction are as follows : — "A light stimulus, when the organism is in a certain definite tonic condition, sets off a reaction involving (1) an equal bilateral contraction of the circular musculature, producing the extension of the body; (2) a contraction of the longitudinal musculature of the side stimulated, producing the turning toward the stimulus (this is the definitive part of the reaction); and (3) contraction of the dorsal longitudinal musculature, producing the raising of the anterior end. In this reaction the sides do not act independently, but there is a delicately balanced and finely co-

ordinated reaction of the organism as a whole, depending for its existence on an entirely normal physiological condition" (Pearl, 1903, p. 619). Similar lack of uniformity and simplicity appears in the remainder of the behavior of the flatworm. In few of the lower metazoa has the movement been so thoroughly analyzed as in Planaria. But there seems to be no reason for thinking that in this simple animal these relations are more complex than in most invertebrates.

The recent thorough studies of Radl (1903) on reactions to light in many animals have shown clearly the inadequacy of this theory to account for most of the reactions to this agent. Bohn (1905) has likewise been compelled to reject this theory, on the basis of the results of his thorough studies on the behavior of the animals of the seashore. To the writer it appears that most of the recent thorough work on animal behavior points in the same direction.

We must then conclude from our examination of the facts that for the lower organisms taken into consideration in the present work, the local action theory of tropisms is of comparatively little value for interpreting behavior. This theory uses and attempts to make of general application certain elements here and there observable in the behavior of some organisms. But in many organisms even these elements are almost completely lacking, and in no organism that we have taken up does this theory adequately express the nature of behavior. The tropism as applied to animal behavior in the sense we have considered, is not an elementary factor ; it is only a more or less artificial construction, made by combining certain elements of behavior and omitting others that are of most essential significance. It makes use of certain simple phenomena that actually exist, but elevates these into a general explanation of directed behavior, for which they are utterly inadequate. The prevalence of this local action theory of tropisms as a general explanation of behavior in lower organisms is based only on an incomplete knowledge and an insufficient analysis of the facts of behavior.

In the foregoing pages we have criticised a certain definite theory of tropisms, this being the theory most commonly implied when the word is used in a precisely defined way. But the term "tropism" is often used in a looser sense. By some writers the word is applied merely to the general phenomenon that the movements of organisms show definite relations to the location of external agents. In this sense the word implies no theory, and is not open to criticism on the basis of observed facts. It is, of course, equally applicable to the behavior of man and

that of lower organisms; in this sense the botanist Pfeffer (1904, p. 587) consistently remarks that a man who bends toward a lighted window shows phototropism as does a plant. The use of the word in this purelydescriptive sense is often convenient, but we need to keep in mind the fact that the word thus used involves no explanation, and includes phenomena of the most heterogeneous character. By some writers the word " tropism " is restricted to the bending or inclination of a fixed organism, while the movements of free organisms under the influence of external agents are called taxis. This distinction is a purely descriptive one.

Some writers reserve the term " tropism " (or taxis) for those reactions in which the organism takes up a well-defined orientation with relation to the line of action of some external agent. Other reactions, in which orientation is not a feature, are variously designated as kinesis (Engelmann, 1882 a; Rothert, 1901 ; Garrey, 1900), as -pathy (Davenport, 1897; Yerkes, 1903 b; and others), as -metry (Strasburger, 1878; Oltmanns, 1892), and by various other names, depending on the method by which the author in question considers them to be brought about. On this basis the reactions of infusoria to water currents, gravity, the electric current, and to light coming from one side would be called tropisms or taxis; while the reactions to chemicals, osmotic pressure, heat and cold, and mechanical stimuli would be designated by some other term.

An immense number of technical terms have been devised for application to the phenomena of behavior in the lower organisms. A systematic exposition of a very complete set of such terms will be found in the paper of Massart (1901). The "Plant Physiology" of Pfeffer (1904) likewise deals extensively with this matter. A proposed new terminology applying to many of the features of behavior is set forth by Beer, Bethe, and v. Uexkull (1899). A number of other references to this matter will be found in the literature list at the end of the present chapter.

As to the value of giving technical names to every distinguishable act that an organism performs, opinions will differ. So far as the names are purely descriptive, expressing nothing more than some observed action of the organism, it is difficult to see any very great advantage in their use. To say that an organism shows phobism (Massart), is merely to say that it moves backward; to say that it reacts by dorsoclinism (Massart), is the same as to say that it reacts by turning toward the dorsal side. To most readers the latter expressions are more intelligible than the former, and they are equally accurate and complete. Such purely descriptive terms embody no results of scientific analysis. Their use is therefore merely a question of convenience or taste on the part of the

writer. They are doubtless at times convenient and may perhaps be used to advantage. So far as the terms involve a certain explanation of the phenomena, their use requires that the writer shall accept that explanation for the phenomena in question, otherwise their use gives rise to misconception. This makes many of the terms unavailable, save in a very restricted degree. The study of behavior seems hardly to have reached as yet the stage where a hard and fast nomenclature can be used to advantage. To the present writer, after a longcontinued attempt to use some of the systems of nomenclature devised, descriptions of the facts of behavior in the simplest language possible seems a great gain for clear thinking and unambiguous expression. If investigators on the lower organisms would for a considerable time devote themselves to giving in such simple terms a full account of behavior in all its details, paying special attention to the effect of the movements performed on the relation of the organism to the stimulating agent, this would be a great gain for our understanding of the real nature of behavior, and some theories now maintained would quickly disappear. Less attention to nomenclature and definitions, and more to the study of organisms as units, in their relation to the environment, is at the present time the great need in the study of behavior in lower organisms.