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THE SELECTION OF RANDOM MOVEMENTS AS A
FACTOR IN PHOTOTAXIS.
By S. J. HOLMES. Contributions from the Zoological Laboratory of the University of Michigan, No. 91.
It is customary to explain the phototactic movements of organisms as dependent upon a sort of forced orientation which is brought about by the fact that when the two sides of the body are stimulated unequally they give unequal muscular responses which result in turning the animal until both sides are stimulated to the same degree, when the creature moves either towards or away from the light in the direction of the rays. But however satisfactory this explanation may be for the phototactic movements of most organisms, there are several cases where locomotion is directed by the rays of light which cannot be accounted for in this way. It is well known that earthworms, leeches, and the larvæ of house-flies, blow-flies and many other insects have a strong tendency to shun the light and collect in the darkest regions they can reach. These forms have been cited as affording typical illustrations of negative phototaxis. The often precise orientation of these organisms to the direction of the rays very naturally disposes one to explain their phototactic movements as taking place according to the scheme just mentioned. No one has attempted to work out in detail the exact mode of response in any of these forms, although the fact of their orientation to the direction of the rays of light has been described by several different observers. A variety of explanations may be offered according to the gener
The descriptive part of this paper with the exception of a few minor changes was read before the section of Animal Morphology of the International Congress of Arts and Sciences at St. Louis, Mo., Sept. 21, 1904.
al theory we have referred to. It might be assumed, in the earthworm, for instance, that light causes a greater contraction of the longitudinal muscles on the less illuminated side, or that it inhibits the action of the longitudinal muscles on the side that receives the greater stimulus, or that both these effects are combined.
The attempt was made to get some clue to the method of orientation by carefully watching the movements of the animals under the influence of light. It soon developed that what seemed at first a forced orientation, the result of a direct reflex response, is not really such, but that the orientation which occurs and which is often quite definite is brought about in a more indirect manner by a mode of procedure which is in some respects similar to the method of trial and error followed by higher forms.
The response of the earthworm to light has been noted by several observers HOFMEISTER, DARWIN,? GRABER, YUNG, Hesse,' PARKER and ARKIN, Smith,' and ADAMS. While all parts of the surface of the earthworm are sensitive to light the directive influence of light, as PARKER and ARKiN have shown, is greatest at the anterior end of the body and diminishes towards the posterior end. The negative reaction of the earthworm becomes less as the intensity of the light is diminished, and in very weak light the reaction, according to Adams, becomes slightly positive. The directive influence of light was tested by Parker and Arkin and by Adams by placing the worm at right angles to the direction of the rays and noting the number of times it extended its head towards or away from the
'HOFMEISTER, W. Die bis jetzt bekannten Arten aus der Familie der Regenwürmer, Braunschweig, 1845.
?DARWIN, C. The Formation of Vegetable Mould through the Action of Worms, with Observations of their Habits, New York, 1900.
GRABER, V. Grundlinien zur Erforschung des Helligskeits und Farbensinnes der Thiere, Leipzig, 1884.
'YUNG, E. Compt. Rend. Trav. Soc. Helv. Sci. Vat. 1892, p. 1275 Hesse, R. Zeit. wiss. Zool. 1896, 61, 393. Parker and ARKIN. Am. Jour. Physiol. 1901, 4, 151. SMITH, A. C. Am. Jour. Physiol., 6, 459. *ADAMS, G. P. Am. Jour. Physiol., 9, 26.
light, or simply straight ahead. In all except very weak light the number of negative reactions was found to exceed the posi tive ones, the proportion being greater, as a rule, the more intense the illumination (Adams). In these investigations attention was mainly centered upon the direction of the response, the directive influence of light falling on different regions of the body, and the effect of light of different intensities. The mechism of the reaction was not especially considered.
If the earthworm is more likely to turn away from the light than towards it, it might be concluded that the light exercises a direct orienting effect upon its movements, but this does not necessarily follow. When exposed to a very strong light (the beam of a projection lantern passed through an alum cell was used) the earthworms experimented with showed the following type of reaction. The light in the first place stimulates the animal to activity, calling forth the regular movements of locomotion. Waves of contraction of the circular muscles pass from behind forward; the anterior end of the body is extended and set down; waves of contraction of the longitudinal muscles follow those of the circular ones and pull the posterior part of the body forward. As the worm crawls it frequently moves the head from side to side as if feeling its own way along. If a strong light is held in front of the worm it at first responds by a vigorous contraction of the anterior part of the body; it then swings the head from side to side, or draws it back and forth several times, and extends again. If in so doing it encounters a strong stimulus from the light a second time it draws back and tries once more. If it turns away from the light and then extends the head it may follow this up by the regular movements of locomotion. As the worm extends the head in crawling it moves it about from side to side, and if it happens to turn it towards the light it usually withdraws it and bends in a different direction. If it bends away from the light and extends, movements of locomotion follow which bring the animal farther away from the source of stimulus.
The experiments of PARKER and ARKIN show that the head of the worm in crawling is more apt to turn away from the light
as it extends than towards it. It is probable, although not expressly stated, that account was taken of the first decided turn that was made. If one watches carefully the movements of a worm that is placed at right angles to a strong beam of light it will be seen that the head frequently moves from side to side before extension takes place. These movements may be very slight and ordinarily would escape attention. There is often a similar movement during the process of extention. Frequently the head is bent over towards the light during the first part of the extension and then bent the other way and extended farther, or again it may be waved back and forth several times. Slight trial movements in all directions are continually being made. The reason why the worm makes more turns of a dicided sort away from the light than towards it is largely because the little trials that bring the worm nearer the light are not followed up. Many of the turnings that would naturally be counted as negative are preceded by a slight positive turn followed by a stronger negative one. In order to ascertain whether the negative reaction was manifested at the very beginning of the response the following experiment was tried. A worm was allowed to crawl on a wet board. When it was crawling in a straight line it was quickly lowered into the beam from a projection lantern so that its body would lie at right angles to the rays. The exposure to the light was made in each case when the worm was contracted, and the first detectible movement of the head to one side noted. In the two specimens employed the first detectible turn was away from the light 27 times and towards the light 23 times. After a few extensions the worm in nearly all cases soon turned and crawled away from the light. The first detectible movement of the earthworm seems, therefore, to be nearly as likely to be towards the light as away from it. Tne slight preponderance of negative turns may be due to the fact that some of the smaller trial movements were overlooked, to a slight direct orienting effect of the rays, or merely to chance. A decided turning such as was probably counted in PAKKER and Arkin's experiments may represent a first trial, or a result of perhaps several very small trials. It is easy to
see that in strong illumination extensions towards the light are checked while those that bring the worm away are followed up, but this is not so obvious in light of weaker intensity. Whether the negative reaction takes place entirely by the selection of random movements is hard to determine with certainty, but there is no doubt that this factor plays a very large part in the process.
Experiments performed by Miss RHODES and myself three years ago upon the phototaxis of leeches showed that the method of orientation in these forms is, in principle, the same as that of the earthworm. When specimens of Glossiphonia are placed in strong light their locomotor reflexes are set in action. The mode of progression in Glossiphonia differs from that of the earthworm, although in certain fundamental respects the same. The anterior part of the body is extended, the mouth which acts as a sucker is attached, and then the posterior part of the body is brought forward and fastened by the sucker at its caudal end. Then the anterior part of the body extends again and the other movements follow as before. In its progress the leech frequently raises the extended anterior part of the body and waves it from side to side as if feeling its way. If the ani. mal turns it in the direction of a strong light it is quickly withdrawn and extended again, usually in another direction. If the light is less strong it waves its head back and forth several times and sets it down away from the light; then the caudal end is brought forward, the anterior end extended and swayed about and set down still farther from the light than before. When the leech becomes negatively oriented it may crawl away from the light, like the earthworm, in a nearly straight line. The extension, withdrawal and swaying about of the anterior part of the body enable the animal to locate the direction of least stimulation, and when that is found it begins its regular movements of locomotion. Of a number of random movements in all directions only those are followed up which bring the animal out of the the undesirable situation.
The phototactic reactions of the larvæ of the Muscidæ have