Forced Movements, Tropisms, and Animal Conduct

The following facts may be offered as a proof for this statement.®^® When we put a piece of the stem of Bryo- phyllum calycimtm in a horizontal position it soon bends and gradually assumes the form of a U with the concave side above (Fig. 35). This bending is due to the fact that the cortex on the under side of the stem grows in length while the cortex on the upper side remains unaltered Fio, 35.—^Geotropic curvature of stems of Bryophyllum calycwnm. These stems were -originally straight and suspended in a horizontal position. In rt ten days they bent, becoming concave on the upper side. The black rings, made with India ink, which were originally parallel, remain unaltered on the upper side of the stems, while their distance increases on the lower side, indicating that the curvature is due to an increase in growth on the lower side (of the cortex) of the stem.

Fig. 36.—All stems were originally straight and suspended horizontally. The stems to the r'sht, without leaves, bend much less in the same time than the stems to the left, with two apical leaves: the leaves supplying material for growth to the oortex of the stem on which the bending depends. This material collects in greater masses on the lower side of the cortex than on the upper side (Loeb^^^). This can be demonstrated if we mark the cortex in definite intervals with india ink at the begin¬ ning of the experiment (Fig. 35). After some time the distance between these marks will increase in a certain region of the under side, while it remains constant on the upper side, and this difference causes the bending. This positive increase in length of the under side can only happen; through growth, and this growth of the cortex on the lower side of the stem takes place at the expense of material furnished constantly by the leaves which send it in the direction toward the basal end of the stem. "When we compare the rate of geotropic bending of horizontal stems without leaves and with one or two leaves at the apex, we find that the bending in the latter is much more rapid (Fig. 36), owing to the greater mass of material supplied for the growth of the cortex, and the same is true, if we compare the rate of curvature of stems having a whole axjical leaf attached with that of stems having an apical leaf whose mass has been reduced by cutting off parts of the leaf (Figs. 37 and 38). The writer has shown in other experiments that under equal conditions leaves produce material fit for growth in proportion to their mass. It is, therefore, a safe inference that the influence of the mass of an apical leaf upon the rate of geotropic bending is due to the mass of material it sends into the stem. This material has obviously a tendency to behave like a liquid—^whieh it probably is—and to sink to the lower level. It is, therefore, useless to look for a “gravi¬ tational stimulus.”

What has been demonstrated in this case explains probably also why the apex of many plants when put into a horizontal position grows upward, and why certain roots under similar conditions grow downward^ It disposes also in all probability of the suggestion that tbe apex of a positively geotropie root has “bi^ain functions.” It is cbemicalmass action and not “brain functions” which are needed to produce the changes in growth underlying geotropic curvature.

2. As long as animals are in such a position that their plane of symmetry goes through the center of the earth, the position of their eyes and limbs is symmetrical in regard to their plane of symmetry. If, however, we incline the animal we can bring about forced movements and forced changes of position of the same nature as those caused by injury of one side of certain parts of the brain. Thus we have seen that if we cut the left side of the medulla oblongata in a shark, its two eyes are no longer in a symmetrical position but the left eye looks down and the right eye up, when the shark is kept in a normal posi¬ tion. The same change can be brought about in a normal shark by the influence of gravitation. "When the shark is kept in a position with its right side inclined downward, the right eye is turned upward, the left eye downward. This has nothing to do with light or vision, since it occurs in the dark just as well as in an illuminated room. The abnormal position of the eyes lasts as long as the animal is kept in this abnormal position. The experiment shows that if the plane of symmetry is no longer vertical, forced positions of the eyes can be produced of the same nature as those produced by one-sided injury of certain parts of the brain.

Just as in the case of one-sided injury to the medulla oblongata the changes in the position of the eyes are accompanied by changes in the position of the pectoral fins, so also when we put a normal shark with one side downward or half downward.®*® If the right side of such a fish, is dowa the right pectoral fin is turned more ven- trally, the left fin is turned more dorsally. This means, the tension of the muscles causing the right fin to press down and the left fin to press up is increased. This is the mechanism by which the normal “equilibrium” or more correctly the normal geotropic orientation of the animal is maintained. If the animal should accidentally roll to one side in its normal movements, the tension of the muscles of the pectoral fins would automatically change in such a way as to restore the normal orientation of the animal, whereby the plane of symmetry becomes vertical again. This “maintenance of equihbrium” is therefore a case of automatic orientation by gravitation comparable to the automatic orientation by light.

Geotropic changes in the position of the eyes are not confined to fishes,they can be demonstrated in a rabbit and in crustaceans as well. In vertebrates the reactions leading to the maintenance of equilibrium are apparently produced in the ear, since they disappear if the acoustic nerves are cut. Moreover, those parts of the brain whose injury brings about such changes in the position of the eye and the fins are parts of the receiving fibers from the acoustic nerve.^®®

It seems that some change in the pressure upon the endings of the auditory nerve is responsible for the effects. There are fine grains of CaCOs—^the otoliths—in the ear of many species pressing on the underlying nerve end¬ ings. If we put the median plane of a fish at an angle of 45° with the vertical, the otohths will no longer press down equally in both ears. The idea first suggested by Delage that it is the pressure of the otoliths upon the nerve endings which is responsible for these reactions receives some support by a weU-known experiment by

Kreidl.^'® A crustacean, Palcemon, loses its otoliths in the process of moulting and the animal curiously enough replaces them by picking up small grains of sand and put- tiag them into its ears. Kreidl kept such crustaceans in jars free from sand but containing tine particles of iron which the crustaceans after moulting put into their ears. He expected that a magnet would now influence the ani¬ mals as powerfuUy as gravitation, and this was the case. When, e.g., he brought a magnet from above and the right near the animal the latter turned to the left and downward. The animal, therefore, behaved as if changes of pressure of the otolith upon the nerve endings determined its geotropic orientation.

The theory meets with two difficulties which, however, are not insuperable. First, removal of aU the otoliths does not interfere with the normal orientation of the ani¬ mal. This might find its explanation in the fact that the eyes act as a substitute. Delage had shown that if the otocysts are removed in crustaceans or cephalopods the animals lose their normal orientation more easily when they swim about excitedly than do normal animals. In order to show the effects clearly, however, it was neces¬ sary to bhnd the animals. Animals which were merely blinded but had their otocysts did not show these disturb¬ ances of equilibrium.^^®

The second difficulty is the fact that animals which possess naturally no otoliths are yet able to show such geotropic reactions, e.g., certain crustaceans like Gelasi- mus and Platyonichus. We may assume that the pres¬ sure of liquids on the nerve endings may have a similar effect as the pressure of the otoliths. The next question is, How does the pressure on a nerve ending bring about changes in the tension of muscles? We suspect that this occurs through a ehauge in mass action in the nerve endings, in analogy to our experiments on the influence of the mass of the leaf on the geotropie curvature of Bryophyllum, hut experimental data are lacking.

3. We observe phenomena of geotropism in animals which have no ears, but this need not surprise us in view of the observations on geotropism in plants, and in hy- droids (Antennularia antennina). The writer^®® had found that a holothurian {Cucumaria cucumis) has a ten¬ dency to creep upward when put on a vertical object until it reaches the highest level, where it remains. When put on a vertical plate of glass or slate, these animals creep untiringly upward if only the plate is turned 180° around a horizontal axis as soon as they have reached the highest point. It could be shown that light and oxygen supply have nothing to do with the phenomenon. Jennings observed that Paramcscia always gather at the highest point of a vertical tube and that they assume this position by active ciliary motion. Lyon ®*® assumes that the body of Paramcecia contains substances of different density whose location is changed by changes in orientation of the organism to the center of the earth and that these changes automatically turn the animal again so that its oral pole is directed upward. It will then continue to swim in this direction.

4. It is known since Knight’s experiments that cen¬ trifugal force can act like gravitation and we must assume that the centrifugal force leads to an alteration in the distribution of the sap or of other substances in the cell. This leads to differences in the rate of chemical reactions and may account for the phenomena of orientation under the influence of centrifugal force. When an animal, e.g., a shark or a pigeon, is rotated on a turntable, during rotation a nystagmus is observed in the motions of the eyes and sometimes also of the head. If the rotation is not too rapid the eyes move slowly in the same plane but in an opposite direction from the rotation of the turntable, until they form a maximum angle with their normal position in the head; then they rapidly swing back and the whole phenomenon is repeated. This phe¬ nomenon is called nystagmus. It depends upon the nerve endings in the semicircular canals, but is not dependent upon the motion or pressure of the lymph in the canals,*®®. ®^®. ®*® since the cutting out of the canals in the shark or the plugging up of the canals in the pigeon leaves the phenomenon unaltered. When after some rota¬ tion the motion of the turntable suddenly stops, a nystag¬ mus of the eyes or head in the same plane but in the oppo¬ site direction as during the rotation is observed.

Maxwell has shown that if Phrynosoma is rotated on a horizontal plane with constant velocity and the eyes of the animal are closed, compensatory motions of the head are produced as soon as the angular velocity exceeds a certain value which was 8 seconds for a rotation through an angle of 45°. The experitnents on forced, movements show that we have three groups of forced movements, (1) right to left and left to right (circus movements); (2) forward move¬ ment, and (3) backward movement. The latter is not always possible. A fourth group, the rolling motions around the longitudinal axis may be omitted here in order to simplify the discussion.

The forced movements, called forth by the galvanic current, supported the idea that the nervous elements determining these motions must have a definite orientation and that this orientation bears some simple relation to the direction of motion caused by their activity. The experiments on the effect of blackening different parts of the eye indicate that the different parts of the retinse of positively heliotropic insects are connected in a simple way with the main centers of the three types of forced movements: namely, the left eye is connected with the brain center causing motions from right to left (and the right eye with the center for the opposite motion); the lower halves of the retina with the forward movements, the upper halves with the backward movements.

We know through the work of Ewald Hering that each illuminated element on the human retina determines a definite motion of the two eyes which move as if they were a single organ, and that this motion is a function of the location of the illuminated element in the retina. This fact induced the writer to suggest in his first publication on tropisms that the act of focussing in our vision was simply a phenomenon of hehotropism. “The general principle of orientation of organisms to light is also mani¬ fested in our act of binocular vision which results auto¬ matically in such an orientation of the two retinae that the image of the luminous point falls upon the two fovese centrales of the retinae” (which are symmetrical ele¬ ments). In other words, when an object causes us to turn our eyes to it we are dealing with a phenomenon of forced (heliotropic) movement. In order to prove this it is neces¬ sary to show that a moving retina image can produce forced movements determined by the direction of motion of the luminous object. The difficulties inherent in the proof for such a statement lie in the general prejudice that the motions of an animal are directed to a purpose and it is, therefore, necessary to devise experiments which exclude the assumption of an interest on the part of the animal in the motion.

The writer observed years ago that when a fly is put on a rotating disk it rotates in the opposite direction from the disk. When the motion of the turntable ceases these compensatory motions of the fly stop also and none of the after effects mentioned at the end of the previous chapter are noticed.^®® This suggested that the so-called compensatory motions of insects on the turntable have a different origin from that of vertebrates. The phenom¬ enon was explained by Eadl, who proved that the com¬ pensatory motions of insects on the turntable are pro¬ duced in the eye and that they are due to the fact that the eye tries automatically to fix the same object.^^’’ This agrees with the observation of Lyon who had already

demonstrated previously tliat the compensatory motions of inseots on a turntable stop when their eyes are black¬ ened.^^® Such forced motions, due to the influence of the motion of the retina image, can be demonstrated in the Californian lizard Phrynosoma hlainvilli, which is an ideal object for such experiments and in this animal it is possible to separate these effects from the compensa¬ tory motions caused by centrifugal force. It was accidentally observed by the writer that when the hzard Phrynosoma is kept at the window of a moving train with its eyes toward the window, a nystagmus of the head of the lizard ensues, the head moving slowly in a direction opposite to that of the moving train, as if to keep its eyes fixed on the objects outside—^telegraph poles and trees, etc. The head moves until it is bent maximally, when it is brought baok into its normal position with a quick jerky movement, and then follows again the appa¬ rent motion of the objects outside, and so on. These nys- tactie motions last for hours, in fact as long as the animal is kept with its head toward the window. As soon as it is turned around so that it cannot see the objects outside, the nystactic motions of the head cease. When the animal is put on a turntable and rotated slowly, vigorous com¬ pensatory movements can also be observed during rota¬ tion. If, however, the eyes of the hzard are closed during rotation these movements are considerably diminished though they do not cease entirely. They are also consider¬ ably diminished when the animal with its eyes open is rotated on a turntable surrounded by a high gray cylinder of cardboard which excludes the possibility of images of outside objects moving on the retina. We can also produce compensatory motions of the head if the animal

is kept quiet and objects are moved in front of it, the eyes following tbe moving object. it is of interest to separate the nystagmus or compen¬ satory motions of eyes and bead caused by the orienting effect of a moving retina image from those caused by the orienting effect of centrifugal force and this can be done easily in Phrynosoma. "When the lizard is rotated very slowly on a turntable with its eyes closed, only very slight compensatory motions of the head and body are observed during rota¬ tion, while very powerful compensatory motions are pro¬ duced when the motion of the turntable is suddenly interrupted after a rotation lasting about thirty seconds.

When, however, the same experiment is made with the eyes of the lizard open the reverse is observed. The compensatory motions of the animal during rotation are exceedingly vigorous, while the compensatory motions of the auiTnal after the interruption of the rotation are shght. When the eyes of the animal are closed we are dealing only with the geotropic effect of passive rotation; when the eyes are open the orienting influence of the moving retina image is added algebraically to the orienting effect of centrifugal force upon the ear. These two influences act in the same sense during rotation and therefore are additive; while after the rotation they act in the opposite sense to each other. When we rotate the body of an animal passively to the right, during rotation the objects have an apparent motion to the left and the eyes and head of the animal are compelled to follow these moving objects, i.e., to the left. The geotropIc effect of passive rotation of the animal to the right also causes a motion of the eyes and head to the left and hence both effects are additive.

When a human being has been rotated passively to the 1-ight for some time, at the interruption of the passive motion the eyes move slowly to the right and return rapidly to the left. Only the slow motions give rise to the sensation of an apparent motion of the objects and hence after the sudden stopping of a passive rotation to the right the objects seem to such a person to move to the left. The geotropio after etfect, after passive rota¬ tion to the right, consists in inducing passive compensa¬ tory motions to the right, i.e., in the opposite sense of the orientation caused by the apparent motion of the visual objects. Hence in the after effect the orienting effect of the retina image and the centrifugal effect weaken each other.

were formerly described as rheotropism in fish are due to the orienting effect of moving retina images. The reader is familiar with the fact that many fish when in a lively current have a tendency to swim against the current. This phenomenon was believed to be due to the friction of the water. Lyon showed that fish orient themselves just aa well when they are put into a closed glass bottle, which is dragged through the water, although in this case they are not under the influence of any fric¬ tion from the current. When the bottle is not moved the fish swim in any direction inside the bottle. It is obviously the motion of the retina images of the objects on the hank of the brook which causes the “rheotropic” orientation of fish. When driven backward by the current or when dragged backward in a bottle through the water, the objects on the bank of the river seem to move in the opposite direction. The animal being compelled to keep

the same object fixed, an apparent forward motion of the fixed object changes the muscles of the fins in such a sense as to cause the animal to follow the fixed object automatically. When such rheotropic fishes were kept in an aquarium and a white sheet of paper with' black stripes was moved constantly in front of the aquarium the fish oriented them- Fig. 39. —Influence of motion of the hand of an observer on the direction of the motion of a swarm of sticklebacks in an aquarium. The arrows indicate the direction in which the hand was moved. The swarm of fish moves always in the opposite direction in which the hand is moved. (After Garrey.)

selves against the direction in which the paper and its stripes moved. The phenomenon was more marked in young than in older specimens. All the phenomena of rheotropism ceased in the dark or when the fish were blind. Wheeler has observed a phenomenon of anemotrop- ism, namely that certain insects have a tendency to put the axis of their body in the direction of and against the wind. He considers this analogous to the phenomenon of rheotropism in fishes. The cause is also in all probability the tendency toward fixation of the moving retina image.

A very pretty demonstration of the orienting effect of moving retina images was discovered by Garrey in sticklelDacks.^’^® Wken a swarm of such fish was kept iu an aquarium it was noticed that all the fish were oriented with the long axes parallel and that the whole school swam in a course parallel, but in a direction opposite, to that of the moving observer. If the observer remains station¬ ary opposite the aquarium and moves an object, prefer¬ ably white, which is held in the hand, the little fish at once respond by moving slowly and oppositely to that of the moving object. They can be thus made to move up or down or to the right or left (Fig. 39).

By experiments which space forbids us to report in detail Barrey has reached the conclusion that the motion of a near object causes an apparent motion of the whole horizon in the opposite direction and this apparent motion the fish tries to compensate by the motions of its body. This brings the observations on the stickleback into har¬ mony with the general influence of moving retina images, consisting in a compensatory motion of the fish. We have already referred to the fact that the influence of a moving retina image is capable of compensating the forced movement of a dog after a one-sided lesion of the cerebral hemispheres.

OuE orientation in space is determined by three groups of tropistic influences, two of which we have already dis¬ cussed, light and gravitation. The third one is pressure on certain nerve endings of the skin. When the tactile influences on the skin of the soles of the feet are weakened (as is the case in locomotor ataxia), the patient finds it dif&cult to stand and walk in the dark. When he can use his eyes the difficulty is diminished, since the orienting effect of the retina image can compensate the tactile de¬ ficiency; just as we have seen that the effect of the loss of the ears in crustaceans can be compensated by the orienting influence of the eyes.

The role of tactile influences on the orientation of ani¬ mals is most clearly demonstrable in starfish, flatworms, and many other animals, when put on their backs. The ffni.mfl.1s “right” themselves, i.e., they turn around until the ventral surfaces or their feet are pressed against solid objects again. As the writer pointed out long ago,^®® gravitation has nothing to do with the phenomenon, since starfish will stick to solid surfaces with their tube feet even if by so doing their backs are permanently turned to the center of the earth. Unless the nerve endings on the sole of their tube feet are pressed against a solid surface the animals are restless and the arms move about until the feet are again in contact vsdth solid bodies. This phe¬ nomenon of orientation the writer called stereotropism.

still lacking and we must be satisfied with, a few descriptive remarks. Certain animals show a tendency to bring their body completely into contact with solid bodies, e.g., by creeping into crevices. "Without further experimental test this might appear as an expression of negative heliotropism, but it can be shown that this assumption would be wrong. Amphipgra is a positively heliotropic butterfly which, in spite of its positive heliotropism, shows the peculiarity that it creeps into crevices when given an opportunity. Such animals were kept in a box at the bottom of which was a square glass plate resting with its four corners on supports just high enough to allow the animals to creep under the glass plate. After some time every AmpMpgra was found under the glass plate. This happened also when the glass plate was exposed to full sunshine, while the rest of the box was in the shade.^®'^

The same stereotropism is found in female ants at the time of sexual maturity. When such animals are put into a box containing folded pieces of paper or of cloth, after some time every individual is found inside the folds. This happens also when the boxes are kept in the dark.*®^ The same form of stereotropism is found in many species of worms. When earthworms are kept in jars with vertical walls they are found creeping in the corners where their body is as much as possible in contact with solid bodies. It is this tropism which compels the animals to bniTow into the ground.

Maxwell®** kept Nereis, a form of marine worms, which burrows in sand, in a porcelain dish free from sand. Into the dish glass tubes were put, whose diameter was of the order of that of the worms. After 24 hours every tube was inhabited by a worm who made it its permanent abode. They even remained in the tube when exposed to sunlight which rapidly killed them. We find the opposite, negative stereotropism, in many pelagic animals, e.g., larvae of the barnacle or of other crustaceans, which avoid contact with solids. The phenomenon is liable to interfere with heliotropic experiments.