Behavior of the Lower Organisms

We have already seen that the position taken by Cerianthus is partly determined by gravity. The sea anemone Sagartia, according to Torrey (1904), usually moves upward when this is possible, and at the same time it tends to keep its body in line with gravity, with the disk above. If while moving on the floor of the aquarium it reaches the perpendicular side, it at once begins to ascend. Since Sagartia creeps by movements of its foot, remaining in the upright position, its ascent on a vertical surface involves bringing the body into an oblique position, in place of the usual perpendicular one. Thus its tendency to creep upward interferes with its tendency to keep its body in line with gravity, and the former prevails. Sagartia may also creep on the under side of the surface film, with head down, so that it is by no means a rigid requirement that the head shall be above. Doubtless many other sea anemones will show a tendency to keep the body in a certain position with reference to gravity.

In the hydroid Corymorpha, according to Torrey (1904 a), there is a decided tendency to take a position with the head (or oral end) upward. When placed in an inverted or oblique or horizontal position, Corymorpha rights itself by a bending of the body, which is due, according to Torrey, not to muscular contraction, as in the sea anemones, but to a change in the turgidity of the large axial entoderm cells. Those on the lower side become more turgid, increasing in volume and thus bending the stem directly upward. Either the entire animal or a piece of the stem, without head or foot, reacts in this manner. Thus the reaction is in this animal comparable to the reaction to gravity in a plant.

But in many species of fixed ccelenterates gravity clearly has little or nothing to do with the usual position. Metridium, Aiptasia, Stoichactis kelianthus, Condylactis passiflora, and many others are found occupying all sorts of positions with reference to gravity, and the same is true of Hydra and various hydroids. In some medusae the movement is partly guided by gravity. Go- nionemus, as we have seen, swims in its "fishing" movements upward to the surface. Yerkes (1903) found that this occurs in the same way when the light comes from below, so that the guiding factor is apparently gravity. This reaction to gravity is of course not constant; it occurs only at intervals and under certain circumstances.

Careful examination will probably show that gravity plays a part in certain episodes of the behavior of most of these animals, even though it may not affect their usual position or direction of motion. Thus, gravity plays a part in the "rejecting reaction" of the actinian Stoichactis, described in Section 5 of the present chapter. The situation " waste-matter-on-the-disk-not-removed-by-the-first-reaction " is responded to by taking such a position with reference to gravity as results in removing the waste ; then the reaction to gravity ceases. Similar transitory reactions to gravity, seeming to serve definite ends, are found in many other animals. Thus, in the hermit crab, according to Bohn (1903), we have such a case. While investigating a shell which it may adopt as a home if fitting, this animal takes a certain position with reference to gravity; namely, with body on the steepest slope of the shell, and head downward. It then turns the shell over (the position mentioned being the most favorable one for this action), and ceases to react with reference to gravity. Other cases of the same sort will be described for the flatworm Convoluta (Chapter XII). Gravity has, of course, many diverse effects on the substance of organisms, and in almost no case has its precise action in directing movements been determined. When an animal is inverted, this may cause a redistribution of the constituents of the body or of the separate cells. Such a redistribution would probably interfere with the usual physiological processes, and might therefore act as a stimulus to a change of position. Again, in freely moving organisms, gravity causes differences in the ease of movement in different directions, and such differences may well determine the direction of motion. Again, a change in the usual position with reference to gravity may induce unusual strains in various

parts of the body, or may shift the weight of the body to parts unaccustomed to bearing it; and these effects might serve as stimuli to cause the animal to take another position. This possibility will be vividly realized by any one who undertakes to rest with a limb doubled in some unusual position beneath him. Again, certain movements with reference to gravity may produce results involving a change of the conditions affecting the organism, and since it is a well-established fact that the results of behavior partly determine future behavior, this fact may determine movements with reference to gravity. There seems to be no a priori reason why each of the relations above mentioned, as well as various others, may not induce reaction in one organism or another, and it seems not difficult to find probable examples of all. We have been assured by various writers that the reaction to gravity must be explained in the same way in all cases, but this is evidently said rather in the capacity of a seer or prophet, than in the capacity of a man of science whose conclusions are inductions from observation and experiment.

Many of the sea anemones and medusae do not react to light, so far as known. In other cases a reaction to light is very marked. The relation of the behavior to light is in certain cases exceedingly complex, and very instructive, as showing the numerous factors on which behavior depends. We shall take up especially the reactions of Hydra, and of the medusa Gonionemus. The behavior of Hydra with relation to light has been studied especially by Wilson (1891). Both the green and the brown Hydra are usually found at the lighted side of the vessel containing them. If they are at first scattered, they will in a day or two be found to have moved to the lighted side. If at the side of the dish next the window there are attached light and dark strips of glass, the Hydras collect in the light strips. If different colored lights are used, by placing strips of glass of different colors on the lighted side of the vessel, the Hydras collect in the blue light, while all other colors (except perhaps green, which seems slightly effective) act like darkness. The animals gather in the blue even in preference to the white light, which of course contains all the blue rays. As to the way in which the reaction to light takes place, the following facts were brought out by Wilson. A change from light to dark, or from blue or white light to one of the colors which acts like

darkness, causes the animal to become restless and move about. The motion seems undirected, but as soon as the animal comes into the blue or white light, it becomes less restless, and remains. The behavior is thus far, then, like the reaction to heat; the animal when not lighted simply moves about in various directions, till one of its movements brings it into light. Whether the animal when moving draws back or stops on coming to the boundary of the light, where it would pass into the darkness, as Euglena does, has not been determined. But when the vessel is lighted from one side, the animal moves toward the source of light, and the movement is no longer an irregular wandering, but according to Wilson (1891^.432) is fairly direct. This is like thereaction of Euglena, and it seems possible that in Hydra the reaction is produced in the same manner as in that organism. If this is true, there is a tendency for the moving animal to keep its anterior end directed toward the light, due to the fact that when it turns this end away, the change to relative obscurity at the anterior end causes further movement, till the light again falls on the anterior end. The movements should be studied further to determine this point. Fixed Hydras do not maintain any particular orientation with reference to the light rays, but change their position frequently, in the way illustrated in Fig. 1 14. The green Hydra moves to the lighted side of the vessel more rapidly than the yellow Hydra. This is probably due to the generally more rapid movements of the green species.

In a powerful light the reaction of Hydra, like that of most other positive organisms, becomes reversed. The animals collect in the shadow of leaves or on the bottom. They have not been observed to move directly away from the source of light (Wilson, 1891), so that the reaction is probably an irregular wandering based on the method of trial. Hertel (1904) found that both the green and the colorless Hydra react by contraction when subjected to powerful ultra-violet light. These rays killed the colorless Hydra in about one minute, while Hydra viridis resisted their action for six to eight minutes.

The gathering of Hydras in lighted areas and the movement toward a source of moderate light are of much benefit to the animals in obtaining food. Hydra preys upon small Crustacea and other minute animals, and these gather as a rule at the lighted side of the vessel. By taking a position on this side, the Hydras find themselves in the midst of a dense swarm of organisms and are able to capture much food. When in such situations one frequently finds them gorged with prey. In other parts of the vessel they would have almost no opportunity of obtaining food (Wilson, 1 891).

The relation of the behavior of the medusa Gonionemus to light, as studied by Yerkes (1902 a, 1903), is exceedingly complex; it can by no means be expressed by any simple formula. In examining the matter it will be well to consider first the relation of the light to the amount of activity shown by the animal; then the nature of the activities in constant lights of various intensities; then the effects of changes of illumination. In ordinary daylight, Gonionemus continues its usual activities, swimming about by rhythmical contractions, and pursuing its usual occupation of "fishing" (p. 192). It is not clear that the direction of its movements has any relation to the direction of the rays of light, so long as all conditions remain uniform. If the light comes from below instead of above, Yerkes (1903) found that Gonionemus continues to swim to the top and float to the bottom, as before.

If the light is cut off, the medusa usually comes to rest after one to five minutes. By covering the vessel containing them, it is thus possible to bring the animals to rest for experimental purposes. In continued darkness the animal is much less active than in the light. In strong sunlight the animal becomes very active. At first it swims toward the source of light, thus rising under natural conditions to the surface of the water. Later its reaction changes ; it stops coming to the surface, begins to avoid the light, and swims toward the bottom. It may now persistently strike against the bottom in its efforts to swim away from the source of light. Sometimes in a strong light it places the more sensitive subumbrellar surface against the bottom and comes to rest. At times its activities become, under the action of direct sunlight, uncoordinated; it moves upward in its contraction, downward in its expansion.

In a moderate light coming from one side the behavior of Gonionemus is at times very peculiar. When the conditions are quite uniform, as we have seen, its movements often show no relation to the direction of such a light. But when the light first begins to act, as when a jar containing medusas is placed near a window, they at first swim toward the source of light. The medusas thus gather at the lighted side of the vessel. But after a time, if undisturbed, they cease to react to light, and may scatter throughout the vessel. If there are regions of light and shade, the animals now usually gather in the shaded region. But if they are again disturbed in some way, as by stirring up the water, they swim toward the light again, — later scattering as before, when the conditions become uniform.

Thus the reaction of the animal depends on its physiological state; when excited it moves toward the light, otherwise it is indifferent or gathers in the shade. In the flatworms we find a parallel condition of affairs, but with the relations reversed. It is not unlikely that the tendency of the medusa to go toward the light when disturbed is related to its usual method of life, and has a functional value. The animal when at rest is commonly attached to the vegetation of the bottom. When disturbed by a large animal foraging among the plants, it would move toward the light, hence out into the free water and upward, thus escaping the enemy.

Thus far we have considered the behavior under light of constant intensity. Let us now see the effects of sudden changes in intensity of illumination. Here we find again that the effect of a given change depends on the state of the animal. If the medusa is at rest on the bottom, a sudden marked increase in the intensity of the light usually causes a sudden contraction of the bell. As a result the animal, of course, swims away from its first position. Sometimes, however, an increase of light merely causes an animal that is at rest with the sensitive concave surface up to turn over, so as to bring the sensitive surface against the bottom, where it is little affected by the light. In a case described by Yerkes, increase of light caused regularly this turn with bell up, while decrease caused a return to the "bell down" position.

A decrease of light usually has no effect on a resting Gonionemus. But sometimes it causes contraction, so that the medusa swims away. In such specimens an increase of light usually causes no reaction. Sometimes, however, a given specimen reacts both to increase and decrease of illumination. Thus the reaction of a resting medusa to a change of illumination is variable, depending on the individual. Doubtless in a given individual it varies with the physiological state and past history of the animal.

In the swimming Gonionemus, usually both an increase and a decrease of light cause the animal to expand, cease swimming, and sink to the bottom. Here it usually remains for a time, then resumes activity. If a vessel containing a number of the medusae is divided by a line x-x into two regions, one brightly illuminated, the other shaded, the animals usually behave as follows: A specimen swimming about in the light region crosses in its course the line x-x, passing into the shade. It at once ceases swimming and sinks to the bottom. Here it remains for a short time, then continues to swim about in the shaded region.

If a specimen swimming in the shaded region crosses the line x-x into the light, it likewise sinks to the bottom and remains quiet for a time. Now, upon resuming activity, it swims in such a way as to pass back into the shade. Yerkes is convinced, from analogy with the effects of other stimuli, that this is due to a stronger contraction on the side most intensely lighted — that farthest from the shadow. This would, of course, turn the medusa back into the shade.

Thus in the course of time practically all the medusa? in the vessel will be found in the shaded region. In the behavior of Gonionemus with relation to light there are evidently a number of paradoxical facts. The medusa swims toward the source of light, yet tends to gather in shaded regions. It goes at first toward a source of strong light, later reverses this reaction. It moves toward the source of light when excited, but becomes indifferent when undisturbed. Different individuals react differently to the same conditions, and the same individual reacts differently at different times. We have here an excellent illustration of the fact that the reactions of organisms, even to simple agents, depend on a multiplicity of factors. If we could study the medusa in the natural conditions under which it lives, and if we knew thoroughly the physiological processes taking place within it, we should doubtless find all these peculiarities explained, and should probably discover that its reactions are regulatory. When we carry such an animal to the laboratory and experiment upon it there, it is like removing an organ from the body and studying it in a dissecting dish. We cannot understand its activities without knowing their relations to the rest of the body — to the environmental conditions.

The behavior of organisms is largely determined by the relation of the environment to their internal physiological processes. In no field is this so striking as in the relation of behavior to the obtaining of material for carrying on the processes of metabolism. Under this point of view come the reactions of organisms with reference to food, and to the gases necessary for respiration. These reactions in the Ccelenterata we shall take up now. Hydras are usually found in the upper parts of a vessel of water, near the surface. This is not due to a reaction to gravity, but rather to the relative quantity of oxygen in different parts of the water. If an experiment is arranged in such a way that the lower surface of the vessel is free and in contact with air, while the upper is not, the Hydras tend to gather near the lower surface (Wilson, 1891). Collecting in

oxygenated regions is probably brought about through a process of trial, the organisms wandering irregularly till they come into oxygenated regions and there remaining. If the water is allowed to become very foul, all the Hydras soon collect at the very upper surface, often in contact with the surface film itself. Let us now examine the usual behavior of Hydra in obtaining food, as described by Wagner (1905). As we have seen, the undisturbed green Hydra changes its position at intervals, thus in the course of time exploring thoroughly all the region about it. The tentacles of the green Hydra are comparatively short, so that such exploring movements are needed. In the colorless Hydras the tentacles are often excessively long and slender, lying in coils on the bottom, and almost filling the surrounding waters with a network of fine threads. They may reach three or four inches in length. In these species changes of position are less frequent, the great length of the tentacles rendering this unnecessary. When a small animal comes in contact with one of the tentacles, in a typical case a somewhat complicated

reaction OCCUrS. The nematOCVStS of, Fig. 131. — Hydra endeavoring to swal- . . . t • i 1 • 1 l°w a large annelid. Camera drawing. comes in contact are shot out, causing the organism to cease its movements. The tentacle is viscid and clings to the animal. Now the tentacle is bent toward the mouth. At the same time the other tentacles bend in the same direction. If the animal is a large one and is inclined to struggle, the other tentacles seize it, and many nematocysts are shot out and pierce it, so that the organism may become quite covered with these structures. An insect larva which was rescued from a Hydra at this stage is shown in Fig. 132, B. Meanwhile, the mouth becomes widely opened, sometimes before the prey comes in contact with it. When the food reaches the mouth, the tentacles usually release it and are folded slightly back, while the edges of the mouth, or "lips," actively work up over the food, till it is enveloped and passes into the cavity of the body. In this way a Hydra often takes organisms much larger than itself. Figure 131 shows such a case, where a Hydra endeavored to swallow an annelid that was, at a moderate estimate, fifty times its own bulk. The mouth and body were immensely distended, and the worm was about half enveloped. The Hydra seemed then to have reached its utmost limit, and the process stopped.

We now wish to analyze this complicated behavior, determining as far as possible the nature and causes of the different factors which make it up. We may ask first, What is the cause of the discharge of the nematocysts ? Near each nematocyst there is a projecting point, the cnidocil (Fig. 132, el). This has often been compared to a trigger; touching the cnidocil is said to cause discharge of the nematocyst. That is, it is supposed that a mechanical stimulus is the cause of the discharge. But experiment does not bear out this supposition. Hydra may be rubbed roughly with a needle, without causing discharge of the nematocysts.

Hard organisms, such as Os- tracods, may strike against it or run over its surface, brushing against many cnidocils, yet no nematocysts are discharged. On the other hand, various chemicals readily cause discharge of the nematocysts; a solution of methylene blue or methyl green, for example, produces this effect in a marked degree. Apparently, then, some chemical stimulus must be associated with the mechanical stimulus in order to Fig. 132 -Nematocysts and their action in Hydra. cause discharge of the nema. A, portion of a tentacle, showing the batteries of nema- °

tocysts; d., cnidocils. B, insect larva covered with tOCystS. Chemical Stimuli nematocysts as a result of capture by Hydra. of Qne SQrt Qr another wjU doubtless usually be received from the organisms which serve as prey. To what is the remainder of the behavior due? One thing which must be noticed first is that the food reaction depends upon the physiological condition of the animal. Not all Hydras react to suitable food, but only those which have not been recently fed. It is, of course, not surprising that only hungry Hydras should eat. Yet this brings out the important point that the behavior is not an invariable reflex, but depends on the physiological state of the organism.

When the animal eats, are the determining factors of the reaction mechanical stimuli or chemical stimuli? Experiment shows that mechanical stimuli alone do not induce the food reaction. If bits of filter paper, or ostracods with a hard shell, are brought in contact with the tentacles or the mouth of a hungry Hydra, they are not swallowed. But if the filter paper is soaked in meat juice, or if the ostracod is crushed, then they are readily swallowed. A chemical stimulation is a necessary factor in producing the reaction. But under usual conditions the chemical alone — the meat juice — will not produce the food reaction. There must be a combination of chemical stimuli (of the proper character) and of mechanical stimuli before the reaction is induced.

But when the Hydra is very hungry — when it has starved for a long time — then a suitable chemical stimulus acting alone will produce the food reaction. Placed in a solution of extract of beef the very hungry Hydra opens its mouth widely and takes in the fluid. What seems very remarkable is that a solution of quinine produces this effect as well as does extract of beef (Wagner, 1905). Thus the food reaction is throughout dependent upon the physiological condition of the Hydra. Hydras that are not hungry will not eat at all ; moderately hungry specimens will take the solid food (chemical and mechanical stimuli) ; very hungry ones take liquid food (chemical stimulus alone). Hungry Hydras show still further modifications in their behavior, compared with those that are not hungry. As we have previously seen, they frequently contract and change to a new position and even move about from place to place. Wilson (1891) records a remarkable cycle of behavior in hungry yellow Hydras. Hydras usually remain, as we have seen, in the upper layers of the water, on account of the oxygen there found. But when the Crustacea on which the animals feed have become very scarce, so that little food is obtained, Hydra detaches itself, and with tentacles outspread sinks slowly to the bottom. Here it feeds upon the debris composed of dead organic matter which collects at the bottom, often gorging itself with this material. It then moves toward the light, and at the lighted side again upward to the surface. Here it remains for a time, then sinks again and feeds upon the material at the bottom. This cycle may be repeated indefinitely, requiring usually some days for its completion.

The food reactions have been studied most carefully in Gonionemus. In this animal, as we have seen, there is a definite set of " fishing" movements, having the function of obtaining food. These movements are of course not direct reactions to food, but are, so far 'as food is concerned, spontaneous movements of the animal. If food is brought near a resting medusa, this sets the animal to moving. If a piece of fish is placed at one side of the medusa, it does not move directly toward the food, according to Yerkes (1902 a). After a few seconds the tentacles nearest the food begin to move about irregularly, and this gives

them a chance to find the food if it is very near. If they do not find it, "there soon follows a general contraction or series of contractions of the bell, which may take the animal either toward or away from the source of the stimulus." Thus the medusa is induced by the presence of food to swim about, and it usually in this way sooner or later comes in contact with the food (Yerkes, 1902 a, p. 438). The behavior is throughout not a definitely directed action, but an excellent example of the method of trial — of what we call searching, in higher animals.

When the tentacles actually come in contact with food, they contract and twist about each other in such a way as to hold it. The group of contracting tentacles then bends toward the mouth, and that portion of the margin of the bell bearing them contracts, drawing them nearer the mouth. The manubrium bends toward the food, placing the mouth against it, and the food is enveloped by the lips and swallowed. What are the determining factors in this behavior? Doubtless, as in Hydra, internal conditions play a part in determining the reaction to food bodies, but this matter has not been studied in the medusa. As to external factors, Yerkes (1902 a) has brought out the following: In Gonionemus the entire food reaction may be produced by chemicals alone. If with a pipette a strong infusion of fish meat is applied to the tentacles, they twist and contract, bending toward the mouth, while the manubrium as usual bends toward the tentacles stimulated. Solutions of common inorganic chemicals do not produce this result ; the tentacles merely contract from them, remaining straight. If the infusion of fish meat is made very weak, the animal begins the food reaction, contracting and twisting the tentacles ; but the reaction goes no farther. In rare cases Yerkes (1902 a, p. 439) found that the animal begins the food reaction when a very weak inorganic chemical, such as an acid, is applied to it. But this quickly ceases, before it has gone far. The medusa in such cases makes what we call in higher animals a mistake, but changes its behavior as soon as it discovers the mistake.

Mechanical stimuli of a certain sort may likewise produce the food reaction. With regard to this we find in Gonionemus certain peculiar and most suggestive relations. If riie tentacles come in contact with some quiet object, or are touched with a rod or a needle, they merely contract, remaining straight, as when they are affected by inorganic chemicals. The response is clearly a negative reaction, not a food reaction. But if the tentacles are touched in a peculiar way, by drawing the rod quickly across them, they behave differently. They quickly react and twist, just as when they touch a piece of meat. Then they bend toward the mouth, the margin bearing them contracting inward as usual, while the manubrium bends toward