Behavior of the Lower Organisms

IX. STRUCTURE AND HABITS OF ANTS. (In preparation) By W. M. Wheeler The objective processes exhibited in the behavior of the lower organisms, particularly the lower animals, form the subject of the present volume. The conscious aspect of behavior is undoubtedly most interesting. But we are unable to deal directly with this by the methods of observation and experiment which form the basis for the present work. Assertions regarding consciousness in animals, whether affirmative or negative, are not susceptible of verification. This does not deprive the subject of consciousness of its interest, but renders it expedient to separate carefully this matter from those which can be controlled by observation and experiment. For those primarily interested in the conscious aspects of behavior, a presentation of the objective facts is a necessary preliminary to an intelligent discussion of the matter.

But apart from their relation to the problem of consciousness and its development, the objective processes in behavior are of the highest interest in themselves. By behavior we mean the general bodily movements of organisms. These are not sharply distinguishable from the internal physiological processes ; this will come forth clearly in the present work. But behavior is a collective name for the most striking and evident of the activities performed by organisms. Its treatment as subsidiary to the problems of consciousness has tended to obscure the fact that in behavior we have the most marked and in some respects the most easily studied of the organic processes. Such treatment has made us inclined to look upon these processes as something totally different from the remainder of those taking place in organisms. In behavior we are dealing with actual objective processes (whether accompanied by consciousness or not), and we need a knowledge of the laws controlling them, of the same sort as our knowledge of the laws of metabolism. In many respects behavior presents an exceptionally favorable field for the study of some of the chief problems of life. The processes of behavior are regulatory in a high degree. Owing to their striking character, the way in which regulation occurs becomes more evident than in most other fields, so that they present a most favorable opportunity for study of this matter. To

the regulatory aspect of behavior special attention is paid in the following pages. The modifiability of the characteristics of organisms has always been a subject of the greatest importance in biological science. In most fields the study of this matter is beset with great difficulties, for the modifications require long periods and their progress is not easily detectible. In the processes of behavior we have characteristics that are modifiable with absolute ease. In the ordinary course of behavior variations of action are continually occurring, as a result of many internal and external causes. We see quickly and in the gross the changes produced by the environment, so that we have the best possible opportunity for the study of the principles according to which such changes occur. Permanent modifications of the methods of action are easily produced in the behavior of many organisms. When we limit ourselves to the subjective aspect of these, thinking only of memory, or the like, we tend to obscure the general problem involved. This problem is : What lasting changes are producible in organisms by the environment or otherwise, and what are the principles governing such modifications ? Perhaps in no other field do we have so favorable an opportunity for the study of this problem, fundamental for all biology, as in behavior. There seems to be no a priori reason for supposing the laws of modification to be different in this field from those found elsewhere. The matter needs to be dealt with from an objective standpoint, keeping the general problem in mind.

A study of behavior from the objective standpoint will help us to realize that the activities with which we deal in other fields of physiology are occurring in a substance that is capable of all the processes of behavior, including thought and reason. This may aid us to be on our guard against superficial explanations of physiological processes. But the chief interest of the subject of the behavior of animals undoubtedly lies, for most, in its relation to the development of psychic behavior, as shown by man. The behavior of the lowest organisms must form a fundamental part of comparative psychology.

In the special field of the behavior of the lowest organisms the foundations of our knowledge were laid by Verworn, in 1889, in his "Psycho-physiologische Protistenstudien." Binet, in his "Psychic Life of Micro-organisms" (1889), gave a most readable essay on the subject, presenting it frankly from the psychical standpoint. Lukas, in his " Psychologie der niedersten Tiere " (1905), has recently again dealt with the questions of consciousness in lower animals, the treatment of objective processes being subsidiary to this matter.

The present work was designed primarily as an objective description of the known facts of behavior in lower organisms, that might be used, not only by the general reader, but also as a companion in actual laboratory experimentation. This description, comprising Parts I and II of the present work, on the Protozoa and lower Metazoa, respectively, was made as far as possible independent of any theoretical views held by the writer ; his ideal was indeed to present an account that would include the facts required for a refutation of any of his own general views, if such refutation is possible. These designs have involved a fuller statement of details, with sometimes their repetition under new experimental conditions, than would have been necessary if the theoretical discussion had been made primary, and only such facts adduced as would serve to illustrate the views advanced. But the scientific advantages of the former method were held to outweigh the literary advantages of the latter.

As originally written, this descriptive portion of the work was more extensive, including, besides the behavior of the Protozoa and Ccelenterata, systematic accounts of behavior in Echinoderms, Ro- tifera, and the lower worms, together with a general chapter on the behavior of other invertebrates. The work was planned to serve as a reference manual for the behavior of the groups treated. But the exigencies of space compelled the substitution of a chapter on some important features of behavior in other invertebrates for the systematic accounts of the three groups last mentioned. The accounts of the Protozoa and of the Ccelenterata as representative of the lowest Metazoa remain essentially as originally written.

After this objective description was prepared, the need was felt for an analysis of the facts, such as would bring out the general relations involved. Part III is the result. Thus the conclusions set forth in Part III are the result of a deliberate analysis of the facts presented in a description which had been made before the conclusions had been drawn. The selection of facts set forth in the descriptive parts of the work has therefore been comparatively little affected by the general theories held by the writer. The loss of unity toward which this fact tends has perhaps its compensation in the impartiality which it helps to give the descriptions.

The writer is conscious of the necessarily provisional nature of most general conclusions at the present stage of our knowledge, and the analysis given in Part III is presented with this provisional character fully in mind. The reader should approach it in a similar attitude. Since the book is written primarily from a zoological standpoint, it would be appropriate in some respects to entitle it " Behavior of the Lower Animals." But the broader title seems on the whole best, since the treatment of unicellular forms involves consideration of

many organisms that are more nearly related to plants than to animals. The figures have been drawn for the present work by my wife. Figures not credited to other authors are either new or taken from my own previous works. The author is much indebted to the Carnegie Institution of Washington for making possible a year of uninterrupted research, devoted largely to studies preliminary to the preparation of this work and to its actual composition. He is further indebted for the use of a number of figures first published by the Carnegie Institution.

3. Features of General Significance in the Behavior of Amoeba 19 Behavior of Infusoria; Paramecium Structure; Movements; Method of Reaction to Stimuli Behavior of Paramecium (continued) Special Features of the Reactions to a Number of Different Classes of Stimuli 5. Orienting Reactions, to Water Currents, to Gravity, and to Centrifugal Force . 73 6. Relation of the Orientation Reactions to Other Reactions 78 Behavior under Two or More Stimuli ; Variability of Behavior ; Fission and Conjugation ; Daily Life ; General Features of the Behavior

5. Features of General Significance in the Behavior of Paramecium .... 107 B. Causes of the Reactions, and Effects produced by them . . . ,108 Literature 109 Action Systems. Reactions to Contact, to Chemicals, to Heat and Cold D. Reactions to Light in Other Infusoria Reaction to Gravity and to Centrifugal Force modifiability of behavior in infusoria, and behavior under Natural Conditions. Food Habits 2. Conditions required for Retaining a Given Position : Righting Reactions, etc. . 192

10. Independence and Correlation of Behavior of Different Parts of the Body . . 227 2. Reaction by Varied Movements, with Selection from the Resulting Conditions . 238 3. Modifiability of Behavior and its Dependence on Physiological States . . . 250 Literature 259 Comparison of the Behavior of Unicellular and Multicellular Organisms 260 Is the Behavior of the Lower Organisms composed of Reflexes? . . 277 1. The Causes and Determining Factors of Movements and Reactions . . . 2S3

(1) Activity does not require Present External Stimulation . . 283 (3) Changes in Activity depend on Changes in Physiological States . 286 (4) Reactions to External Agents depend on Physiological States . 286 (5) The Physiological State may be changed by Progressive Internal (7) The Physiological State may be changed by the Activity of the (8) External Agents cause Reaction by changing the Physiological (9) The Behavior of the Organism at any Moment depends upon its

(10) Physiological States change in Accordance with Certain Laws . 289 (6) Summary of the External Factors which produce or determine C. Selection from the Conditions produced by Varied Movements . . . 302 Relation of Behavior in Lower Organisms to Psychic Behavior . . . 328 A. Factors in Regulation in the Behavior of Lower Organisms . . . 339 The typical Amoeba (Fig. i) is a shapeless bit of jelly like protoplasm, continually changing as it moves about at the bottom of a pool amid the debris of decayed vegetation. From the main protoplasmic mass there are sent out, usually in the direction of locomotion, a number of

lobelike or pointed projections, the pseudopodia (Fig. 1, ps.). These are withdrawn at intervals and replaced by others. Within the mass of protoplasm certain differentiations are observable. Covering the outer surface there is usually, though not always, a transparent layer containing no granules; this is called the ectosarc (Fig. i, ec). Within this the protoplasm is granular, and contains bits of substance taken as food, vacuoles filled with water, and certain other structures. This

granular protoplasm is known as the endosarc (Fig. i, en.). Within the fluidlike endosarc we find two welldefined structures. One is a disklike or rounded, more solid body, The other is a spherical globule of water, which at intervals collapses, emptying the contained water to the outside. This is the contractile There are many different kinds of Amoebae, varying in their appearance and structure. For our purposes it will be sufficient to distinguish

moving Amcebae, of nearly constant form, usually having wrinkles on the surface, and with the thick ectosarc much stiffened, so that it does not appear fluid in character. The commonest representative of this type In its usual locomotion the movement of Amoeba is in many respects comparable to rolling, the upper surface continually passing forward and rolling under at the anterior end, so as to form the lower surface. This may best be seen by mingling soot with water containing many Amcebae. Fine granules of soot cling readily to the surface of Amcebae of the verrucosa type, and more rarely to Amcebae of other types. Such particles which are clinging to the upper surface move steadily forward till they reach the anterior edge. Here they are rolled over and come in contact with the substratum. They then remain quiet till the Amceba has passed across them. Then they pass upward again at the posterior end, and

Fig. 4. — Paths of two particles attached to the outer surface of Amoeba. That portion of the paths that is on the lower surface is represented by broken lines. The two particles were seen to complete the circuit of the animal five or six times in the paths shown. (The Amceba was of course progressing; no attempt is made to represent this in the figure.) is repeated as long as the particles cling to the surface. Single particles have been seen to pass thus many times around the body of the animal. Diagrams of the movements of the particles clinging to the surface are shown in Figs. 4 and 5.

It is not only the outermost layer of the ectosarc that thus moves forward. On the contrary, the whole substance of the Amoeba, from the Fig. 5. — Diagram of the movements of a particle attached to the outer surface of Amceba verrucosa, in side view. In position 1 the particle is at the posterior end; as the Amceba progresses, it moves forward, as shown at 2, and when the Amoeba has reached the position 3, the particle is at its anterior edge, at x. Here it is rolled under and remains in position, so that when the Amceba has reached the position 4, the particle is still at x, at the middle of its lower surface. In position 5 the particle is still at the same place x, save that it is lifted upward a little as the posterior end of the animal becomes free from the substratum. Now as the Amceba passes forward, the particle is carried to the upper surface, as shown at 6. Thence it continues forward, and again passes beneath the Amceba.

outer surface to the interior of the endosarc, moves steadily forward as a single stream, only the part in contact with the substratum being at rest. At times small particles are at first attached to the outer surface, then gradually sink through the ectosarc into the endosarc. Throughout the entire process of sinking inward the movement is steadily forward. It is clear, then, that Amceba rolls, the upper surface continually passing across the anterior end to form the lower surface. The anterior edge is thin and flat and is attached to the substratum, while the posterior

Fig. 6. — Diagram of the movements in a progressing Amceba in side view. A,. anterior end; P, posterior end. The large arrow above shows the direction of locomotion: the other arrows show the direction of the protoplasmic currents, the longer ones representing more rapid currents. From a to x the surface is attached and at rest. From x to y the protoplasm is not attached and is slowly contracting, on the lower surface as well as above, a, b, c, successive positions occupied by the anterior edge. As the animal rolls forward, it comes later to occupy the position shown by the broken outline.

end is high and rounded, and is not attached to the substratum. A very good idea of the character of the movements of Amceba may be obtained in the following way: Pin two edges of a handkerchief together, so as to make a flat cylinder. Within this place some heavy objects that will fill part of the cylinder, and lay the whole on a flat surface. Now pull forward the upper surface of the cloth near the anterior edge, a little at a time, bringing it in contact with the substratum. If this process is continued, the handkerchief rolls slowly forward with thin anterior edge and high posterior portion, — the weight within dragging behind. The lower surface is at rest while the upper surface moves forward. In all these respects the movement is like the locomotion of Amoeba. A diagram of the movement of Amceba as it would appear in side view is given in Fig. 6.

While typically all the currents are forward in a progressing Amoeba, any portion of the protoplasm may be excluded temporarily from the currents. This is especially common at the posterior end or tail, which is often composed of quiet protoplasm, covered with wrinkles or papillae But the substance of the tail is in the course of time drawn into the currents and passes forward. In the formation of pseudopodia the movement is much like that at the anterior end of the body. If the pseudopodium is in contact with the substratum, the upper surface moves forward while the lower surface is at rest. If the pseudopodium is sent forth freely into the water, its entire surface moves outward, in the same direction as the tip. These movements have been determined by observing the motion of particles attached to the outer surface of extending pseudopodia.

In some Amoebae, according to Rhumbler (1898, 1905), the external protoplasmic currents turn backward at the sides of the anterior end, so that there is produced a fountainlike arrangement, an internal current forward, external currents backward. Such currents resemble those due to local decrease of surface tension in a drop of inorganic fluid. FiG. 7. — Currents in a drop of fluid when the surface tension . - . . is decreased on one side. A, the currents in a suspended drop, OCT OI tne SUTiace

when the surface tension is decreased at a. After Berthold. B, fllni is Dulling more axial and surface currents in a drop of clove oh in which the , . ' , surface tension is decreased at the side a. The drop elongates Strong!) , It tnere- and moves in the direction of a, so that an anterior (a) and a fore dl'a^S the SUT- drop away from the point of lowered tension. The result is that currents pass on the surface in all directions away from this point (Fig. 7).

At the same time the inward pressure is decreased in the region of lowered tension, while elsewhere the pressure remains the same. Hence the internal fluid of the drop is pressed out toward the region where the film is weakened ; a current flows in the central part of the drop toward this point. This current may produce a projection at the point of lowered tension, provided the surface currents do not carry the fluid back as fast as it is brought forward.

It was long supposed that the movements of all sorts of Amoebae were of this character. As a natural conclusion, it was commonly held that locomotion and the formation of pseudopodia in Amoeba are due to a local decrease in surface tension at the region of forward movement. As our account shows, most Amoebae do not move at all as do liquid drops whose movements are produced through changes in surface tension.1 Rolling movements with all currents forward cannot be produced experimentally through local changes in the surface tension of a drop of fluid. It is necessary, therefore, to abandon the surface tension theory for those Amoebae that move in the way shown in Fig. 6. If the theory is still maintained for the Amoebae with backward currents, this involves holding that the movements are due to fundamentally different causes in different Amoebae ; this is the view maintained by Rhumbler (1905).

While most Amoebae roll as they progress, different species differ greatly in special features of their movements. The species of the verrucosa type (Fig. 3) move slowly and change form very little, not sending out pseudopodia. Those of the Umax type (Fig. 2) move more rapidly and change form more frequently, but they rarely send out pseudopodia. Finally, in the proteus type (Fig. 1) the form is excessively changeable, many pseudopodia extending and retracting. Many Amoebae show what might be called specialized habits in their usual movements. For example, Amoeba angulata and Amoeba velata usually send forth at the anterior edge a pseudopodium which extends freely into the water and waves back and forth, serving as a feeler or antenna

Fig. 8. — Amwba velata, showing the antennalike anterior pseudopodium projecting freely into the water. After Penard (1902). 1 According to Rhumbler (1905), such movements are most readily seen in a species of Amoeba living parasitically in the intestine of the cockroach. Whether the currents on the upper surface are actually backward, where the interior currents are forward, as is required if the movements are to be explained by local decrease of surface tension, has not been shown.