Forced Movements, Tropisms, and Animal Conduct

Garrey observed that when the lower halves of the eyes of the robber fly are blackened the position of the legs of the two sides is symmetrical, but the anterior and middle pairs of legs are extended forward to the maximal extent, producing a striking posture in which the anterior end of the robber fly is pushed up and back from the sur¬ face of the table. The body is in opisthotonus with the abdomen concave on the dorsal side, while the head is tilted far up and back (Fig. 21).

FiG. 22.»~Poiition of robber fly when upper halves of both eyes are blackened. Head down, body convex above. (After Garrey.) When walking these robber flies gave the impression of trying to climb up into the air. The wings are frequently somewhat spread ind the animal may push itself up and back until poised vertically on the tips of the wings and abdomen. The tendency to fly is very pronounced in this condition and upon the slightest disturbance the fly soars upward and backward, striking the top of a confining glass dish or completing a circle by looping the lo-op backward. If it falls upon its back it rights itself by turning a backward somersault. Unequal blackening of the lower parts of the two eyes results in a combination of the effecte Just described, with those described for blackening one eye, for the animal also performs circus motions.

With the upper halves of the eyes blackened the attitude is the reverse of that desciihed in the preceding section (Mg. 22). The an¬ terior and middle pairs of legs are flexed. The anterior and posterior ends of the body bend ventrally with the body in emprosthotonus. The head is bent far down. The animal may actually stand on its head, but the abdomen retains its ventral curvature, leaving a considerable angle open between its dorsum and the wing's which normally rest on it.

In both walking and hying it continually keeps close to the table, and upon encountering an obstacle it frequently does a forward somer¬ sault. If it gets on its back it rights itself with greatest dillieulty as its effc'orts simply result in bending the tail and head ventrally until they may form a complete ring. In galvanotropism the same general picture is presented by Palcemonetes and Amhlystoma when the anode is at the head end, the tonus changes involved being identical in the two conditions

These experiments leave no doubt that the primary effect of light consists in changes in the tension of muscles and that the heliotropic reactions which appeared to the older observers as voluntary acts are, in reality forced movements. in the chapter on forced movements after brain lesion the fact was mentioned that a dog which had shown circus movements to the left after lesion of the left cerebral hemisphere shows circus motions to the right when after¬ ward the right hemisphere is injured symmetrically; in¬ stead of being a physiologically symmetrical animal again after the second operation. The explanation is that the new operation is more effective than the old one whose etfect has partly worn off. Garrey has made an obser¬ vation on heliotropism which shows some analogy with this experiment on the brain.

He found that ‘ ‘ robber flies with one eye black¬ ened show the postural conditions in the most pronounced way in the early morning or after being kept for some hours in the dark. Constant exposiire to the light pro¬ duces considerable fatigue of the eye with recovery in the dark. These facts among others suggested the possi- bility of producing a different sensitiveness of the two eyes and corresponding differences in the muscle tonus with asymmetry of position, and in physiological action of the muscles of the two sides of the body when the two eyes were equally illuminated. Such an experiment constitutes a crucial test of the tonus theory of helio- tropism. It succeeded beyond our greatest expectations. Asphalt black was apphed to the right eye of several specimens of Proctacanthus. In two or three days the paint had formed a brittle shell. During this time the blackened eye had become ‘ dark adapted.’ When such a fly is exposed to light, it tilts and circles to the left. If now the brittle shell is cracked off the right eye by care¬ fully pinching with fine forceps, the exposure of this very sensitive eye to light results in a reversal of the whole picture; the fly circles toward the side from which the black was removed. Although the illumination of the two eyes is of equal intensity, what was the normal eye now becomes relatively a darkened eye owing to its lesser sensitiveness. A differential effect results, probably due to a difference in the rate of photochemical cliange in the two eyes. This reversal of the muscle tonus and of forced motions may persist for an hour or two or even longer, until the two eyes become, as they ultimately do, of equal sensitiveness and the fly behaves like a normal animal.

“These experiments are not only incompatible with any ‘avoidance’ idea, for after removal of the black there is nothing to avoid, but they are also incompatible with the conception of ‘habit formation,’ for ‘habit’ in the per¬ formance of the circling movements is of no avail when light is admitted to the darkened eye—the animala circle to that side because the tonus of the muscles is such that they are forced to do so. “All the experiments show that the musele tone is de¬ pendent upon the intensity of the light and that the postures assumed depend upon the relative difference in the light stimulus to the eyes. In animals with one eye completely covered the radii of the circles in which they moved were shorter the more intense the illumination of the normal eye. With one eye partially covered the circles were larger than when completely covered, and in the same way the circles were larger when one eye was covered by a film of collodion or of brown shellac, which admits some light, than when subsequently covered by opaque asphalt black. When one eye was partially cov¬ ered by central application of the black paint the tilting and circling to the opposite side were abolished or re¬ versed by brilliant illumination of the partially blackened eye. These results explain why a positively heliotropic animal with one eye blackened approaches a light by a series of alternating small and large circles, the former being executed when the good eye is illuminated from the source of light, the larger when it is in the shadow.”

We have thus far discussed chiefly positively helio¬ tropic animals, i.e., animals which are compelled to move toward the source of light. The difference between these and negatively heliotropie animals is that the legs on the illuminated side of a negatively heliotropie animal are extended, while those on the opposite side are in flexed position. This has been directly observed by Holmes, who also made sure of the fact that negatively heliotropie animals, when one eye is blackened, turn in circles with the blackened eye toward the center of the circle ; while positively heliotropie animals turn in circles with the unblackened eye toward the center of the circle.

In. unicellular organisms, where cilia act as locomotor organs, it can easily be shown that the orientation by light is of the nature of changes in the position of cilia; this is for instance the case in respect to Volvox. Holmes states for the heliotropic reactions of this organism, that they are due to differences in the activity of the cilia on both sides of the organism and this ex¬ planation agrees with the actual observations of Bancroft on the galvanotropic reactions of Volvox.

In flagellates, the mechanism of locomotion is very complicated and does not consist in an oar-like action of a flagellum as was formerly assumed. Bancroft has shown that in Euglena, as already stated, the flagellum inserted at the anterior end of the organism is bent backward in the form of an inverted U, and that locomotion is brought about by the formation of a loop which travels from the base of the flagellum toward the free end (Fig. 23). The path of the organism which results from this action is a spiral with continual rotation of the organ¬ ism around its longitudinal axis. Bancroft has shown that the behavior of the organism under the influence of light is identical with that in a constant galvanic field.® ^ One-sided illu¬ mination as well as a current going transversally through such an organism cause changes in the position of cilia comparable with those observed in the legs of crustaceans, insects, and vertebrates.

Fig. 23.—Diagram showing the position of the flagellum as seen in a viscid medium, a, when Buglena is swimming forward in a narrow spiral; 6, when swerving sharply toward the dorsal side; e, when moving backward. (After Bancroft.) Wlieii we study the elfects of light on sessile animals Ave find that they behave in a similar manner to sessile plants. When illuminated from one side they bend their heads to the source of light until their axis of symmetry goes through the source of light. In this case the sym¬ metrical photosensitive elements receive equal illumina¬ tion and the symmetrical muscles are under equal tension. Hence the animal remains in this orientation. These sessile animals were the first examples by which the

Spirographis Spallanzani (Fig. 24) is amarine annelid from 10 cm. to 20 cm. long, which lives in a rather rigid yet flexible tube. The latter is formed by a secretion from glands at the surface of the animal. The tube is attached by the animal with its lower end to some solid body, while the other end projects into the water. The worm lives in the tube and only the gills, which are arranged in a spiral at the head end of the worm, project from the tube. The gills, however, are quickly retracted, and the worm withdraws into the tube when touched or if a shadow is cast upon it.

When sucli tubes with their inhabitants are put into an aquarium which receives light from one side only, it requires, as a rule, a day or more until the foot end of the tube is again attached to the bottom of the aquarium- As soon as this occurs, the anterior end of the tube is raised by the worm until the axis of symmetry of tlie gills falls into the direction of the rays of light (Pig. 24) which enter through the window into the aquarium.^s® When the animal has once reached this position it retains it as

Fig. 25.—The same animals aftet the position of the aquarium to the window was reversed. long as the position of the aquarium and the direction of the rays of light remain the same. When, however, the aquarium is turned 180°, so that the light falls in from the opposite direction, the animal bends its tube during the next twenty-four or forty-eight hours in such a way that the axis of symmetry of its circle of gills is again in the direction of the rays of light (Pig. 25). When the light strikes the aquarium from above, the animals assume an erect position, like the positively heliotropic stems of plants when they grow in the open.

In these phenomena the mechanical properties of the tube play a role. When the animal is taken out of the bent tube, the latter retains its form. This permanent change of form of the tube is appareutly caused through the secretion of new layers on the inside of the tube. The youngest layers of the secretion are more elastic than the old layers, and, moreover, have at first a powerful tend¬ ency to shorten. If such a secretion occurs on one side of the tube only, or more so than on the opposite side, the former must become shorter than the latter, and the result must be a curvature of the tube, that side becoming con¬ cave where the new secretion has occurred.

On this assumption the process of heliotropic curva¬ ture is in this case as follows: when the light strikes the circle of gills from one side only, in these elements certain photochemical reactions occur to a larger extent, than on the opposite side. This results in corresponding altera¬ tions of the sensory nerve endings, the sensory nerves and the corresponding motor nerves, and their muscles. The sense of these changes is such as to throw the muscles connected with the nerves of the gills on the hght side into a more powerful tonic or static contraction than the mu scles on the opposite side of the body. The consequence is a bending of the circle of tentacles, or the head, toward the source of light, which will continue until the axis of symmetry of the circle of tentacles falls into the direction of the rays of light. When this happens, symmetrical tentacles are struck at the same angle (or in other words, with equal intensity) by the rays of light, and therefore the tone of the antagonistic muscles is the same. The result is that the circle of tentacles becomes fixed in this position. The bending of the head produces an increased pressure and friction of the animal against that side of the tube which is directed toward the light, and this pres¬ sure and friction lead to an increased secretion and the formation of a new layer inside the tube.

Fig. 26.—^Polyps of Budendrium, all Rowing toward source of light. The arrow indi¬ cates the direction of the rays of light, which in one case fall in from above, in the other from the left side. sea water. In a day or two new polyps are formed by regeneration and these polyps will bend toward the light until their axis of symmetry is in the direction of the rays of light (Fig. 26). The region at the base of the polyps is contractile and when light strikes the polyps from one

side only, the stem on the side of the light contracts more than on the other side, and this results in a bending of the stem, whereby the polyp is put into the direction of the rays of light. As soon as the axis of the polyp is in the direction of the rays of light (provided there is only one source of light), the tension of the contractile elements is the same all around, and there is no more reason for the organism to change its orientation. It, therefore, re¬ mains in this orientation to the light.

The muscle tension theory of animal heliotropism is, therefore, proved for all classes of the animal kingdom, infusorians, hydroids, annelids, crustaceans, etc. It would be wrong to state that the theory holds only for insects. The reader will have perceived that in the preceding analysis animals are treated as machines whose appar¬ ently volitional or instinctive acts, as e.g., the motion toward the light, are purely physical phenomena. The best proof of the correctness of our view would consist in the fact that machines could be built showing the same type of volition or instinct as an animal going to the light. This proof has been furnished by the well-known inventor, Mr. John Hays Hammond, Jr. The following is a descrip¬ tion of the machine given by one of Mr. Hammond’s fellow-workers who cooperated with him in the develop¬ ment of the machine, Mr. B. F. Miessner.

This Orientation Mechanism consists of a rectangular box, about 3 feet long, IVs feet wide, and 1 foot high. This box contains all th& instruments and mechanism, and is mounted on three wheels, two of which are geared to a driving motor, and the third, on the rear end, is so mounted that its hearings can be turned by solenoid electro-magnets in a horizontal plane. Two 5-inch condensing lenses on the forward end appear very much like large eyes. If a portable electric light, such as a hand flashlight, he turned on in front of the machine it will immediately begin to move toward the light and, moreover, will follow that light all around the room in many complex manoeuvre at a speed of about 3 feet per second. The smallest cirelo in which it will turn is about 10 feet diameter; this is due to the Umiting motion of the steering wheel.

Upon shading or switching off the light the '' dog can be stopped immediately, but it will resume its course behind the moving light so long as the light reaches* the condensing lenses in sufficient intensity. In¬ deed, it is more faithful in this respect than the proverbial ass behind the bucket of oats. To the uninitiated the performance of the pseudo dog is very uncanny indeed. The explanation is very similar to that given by Jacques Loeb, of reasons respon§i]?le for the flight of moths into a fl^ame. . . .

The orientation mechanism here mentioned possesses two selenium cells corresponding to the two eyes of the moth, which when influenced by light effect the control of sensitive relays instead of controlling nervous apparatus, as is done in the moth. The two relays (500 to 1,000 ohm polarized preferred) controlled by the selenium cells in turn control electro-magnetic switches, which effect the following operations: When one cell or both are illuminated the current is switched on to the driving motor; when one cell alone is illuminated an electro-magnet is energized and effects the turning of the rear steering wheel. The resultant turning of the machine will be such as to bring the shaded cell into the light. As soon and as long as both cells are equally illuminated in sufficient intensity, the machine moves in a straight line toward the light source. By throwing a switch, which reverses the driving motors, the machine can be made to back away from the light in a most surprising manner. When the intensity of the illumination is so decreased by the increasing distance from the light source that the resistance of the cells approach their dark resistances, the sensitive relays break their respective circuits and the machine stops.

The principle of this orientation mechanism has been applied to the Hammond Dirigible Torpedo for demonstrating what is known as attraction by interference. That is, if the enemy tries to interfere with the guiding station's control the torpedo will be attracted to him, etc.^ Nothing seems to have been published beyond these meagre details, but the writer understands that the active machine has been demonstrated in a number of places in this country. It seems to the writer that the actual con¬ struction of a heliotropic machine not only supports the mechanistic conception of the volitional and instinctive actions of animals but also the writer’s theory of helio- tropism, since this theory served as the basis in the con¬ struction of the machine. We may feel safe in stating that there is no more reason to ascribe the heliotropic reac¬ tions of lower animals to any form of sensation, e.g., of brightness or color or pleasure or curiosity, than it is to ascribe the heliotropic reactions of Mr. Hammond’s machine to such sensations.

It was necessary for us to begin our analysis witli symmetrical animals since as tlie result of tins analysis the conduct of asymmetrical organisms oilers no difliculty. The result of tne asymmetry consists merely, in a change in the geometrical character of the path in which an animal is compelled to move to or from the source of energy. While this path is a straight line in a symmetrical and positively heliotropie organism it is a spiral around this straight line as an axis in an asymmetrical organism, like Euglena. Suppose a positively heliotropic animal to have slightly asymmetrical appendages which give it a tendency to deviate to the left. Let us suppose that the plane of symmetry of the animal goes at the beginning of the experiment through the source of light and that the animal is swimming toward the light. After a few strokes the head of the organism will have deviated slightly to the left on account of the asymmetry in the activity of the appendages. As soon as the median plane of the animal deviates to the left, the left eye is less illuminated than the right one. As a consequence, a difference in the ten¬ sion of the muscles on the two sides of the animal will be produced which will compensate the natural lack of sym¬ metry in the muscles and the animal will cease to deviate further to the left; and this compensating effect of the unequal illumination of the two eyes will continue until the animal is actually oriented in the right way again, i.e.,

until its plane of symmetry goes through the source of light. All that the inherited or accidental asymmetry does is to cause the animal to move in a path which is not a mathematically straight line; hut this deviation will be marked only in a case of very pronounced or excessive asymmetry. We have already described the behavior of a dog whose left cerebral hemisphere has been injured and who has a tendency to deviate to the left. When such a dog is shown a piece of meat it moves toward it in a fairly straight line, its tendency to deviate to the left being compensated by the orienting effect of the retina image of the piece of meat. If the dog deviates to the left, the piece of meat is apparently dislocated to the right of the dog and this dislocation alters the tension of the muscles on the two sides of the animal in such a way as to make it turn back to the right. In this way the dog reaches the piece of meat in a fairly straight line, though with a greater amount of labor, since the tendency to deviate to the left is constantly compensated automatically by a stronger contraction of the muscles turning the animal to the right.

The writer showed many years ago that many insects have a tendency to creep upward, and that this is due to an orienting effect of gravity upon the animal. When a perfectly symmetrical insect is put on a vertical stick it walks upward in a straight line. What will happen when such an animal is made asymmetrical? Q-arrey has per¬ formed this experiment by using flies in which one eye was blackened. As we have seen, such organisms are rendered asymmetrical not only i» regard to the eyes but also in regard to their apparatus of locomotion, since in one side of the body the tension of the flexors, in the

legs of the other side the tension of the extensors pre¬ vails. As a consequence the fly has a tendency to move in circles with the intact eye toward the center. G-arrey has shown that when a fly with one eye black¬ ened is put on a vertical stick, it still walks upward, but in Fia. 27.—Fly withi one (right) eye blackened can creep only in a spiral on a vertical stick, while normally it creeps in a straight line. (After Garrey.) spirals around the stick (Fig"- 27), instead of in a straight line. The asymmetry of loco¬ motion changes only the geo¬ metrical nature of the path in which the animal moves, from a straight line to a spiral, but does not alter the forced move¬ ment character of the reaction.

Bancroft has pointed out that when in a positively helio- tropic amphipod one eye is blackened and the legs of the same side are cut off, the ani¬ mal’s path would be a combina¬ tion of a circus motion induced by the blackening of the eye and of a rolling motion around its longitudinal axis. Both effects combined would result in the animal swimming in a spiral path, and if the animal is positively heliotropic it would swim in such a path toward the

light. This is the pa^h which aquatic, asymmetrical posi¬ tively heliotropic organisms, such as the flagellate But this locomotor mechanism (of Euglena) is imperfect, it forces the organism to move in a spiral, and always to turn toward a structurally determined side. There are many organisms which swim in spirals and become oriented by turning toward a structurahy defined side. Jen¬ nings and Mast include all such orientations under trial and error and contrast them with the direct orientation of such animals as the amphipods in which the turning may be either toward the left or the right. Let us now consider whether the orientation of Euglena is more like the selection of random movementSi (which we would all agree mav justifiably be called '' trial and error-''), or whether it is more like the orientation of the terrestrial amphipods studied by Holmes.

I think that all students of behavior including Jennings and Mast believe that in the case of these amphipods we have direct heliotropic orientation. If the right eye of such a positively heliotropic amphipod be covered with asphalt varnish it will execute circus movements towards the left. The usual explanation is that the main nervous connection is between the eye on one side and the legs on the opposite side of the body. The light shining on the uncovered eye brings about a condition of in¬ creased muscular tonus in the legs of the opposite side, which is not present in the legs connected with the covered eye. Consequently the right legs push more strongly and the amphipod turns towards the left.