The Power of Movement in Plants

by Charles Darwin; Sir Francis Darwin

LOCALISED SENSITIVENESS TO LIGHT, AND ITS TRANSMITTED EFFECTS.

Phalaris Canariensis.—Whilst observing the accuracy with which the cotyledons of this plant became bent towards the light of a small lamp, we were impressed with the idea that the uppermost part determined the direction of the curvature of the lower part. When the cotyledons are exposed to a lateral light, the upper part bends first, and afterwards the bending gradually extends down to the base, and, as we shall presently see, even a little beneath the ground. This holds good with cotyledons from less than .1 inch (one was observed to act in this manner which was only .03 in height) to about .5 of an inch in height; but when they have grown to nearly an inch in height, the basal part, for a length of .15 to .2 of an inch above the ground, ceases to bend. As with young cotyledons the lower part goes on bending, after the upper part has become well arched towards a lateral light, the apex would ultimately point to the ground instead of to the light, did not the upper part reverse its curvature and straighten itself, as soon as the upper convex surface of the bowed-down portion received more light than the lower concave surface. The position ultimately assumed by young and upright cotyledons, exposed to light entering obliquely from above through a window, is shown in the accompanying figure (Fig. 181); and here it may be seen that the whole upper part has become very nearly straight. When the cotyledons were exposed before a bright lamp, standing on the same level with them, the upper part, which was at first greatly arched towards the light, became straight and strictly parallel with the surface of the soil in the pots; the basal part being now rectangularly bent. All this great amount of curvature, together with the subsequent straightening of the upper part, was often effected in a few hours.

Fig. 181. Phalaris Canariensis: cotyledons after exposure in a box open on one side in front of a south-west window during 8 h. Curvature towards the light accurately traced. The short horizontal lines show the level of the ground.

After the uppermost part has become bowed a little to the light, its overhanging weight must tend to increase the curvature of the lower part; but any such effect was shown in several ways to be quite insignificant. When little caps of tin-foil (hereafter to be described) were placed on the summits of the cotyledons, though this must have added considerably to their weight, the rate or amount of bending was not thus increased. But the best evidence was afforded by placing pots with seedlings of Phalaris before a lamp in such a position, that the cotyledons were horizontally extended and projected at right angles to the line of light. In the course of 5½ h. they were directed towards the light with their bases bent at right angles; and this abrupt curvature could not have been aided in the least by the weight of the upper part, which acted at right angles to the plane of curvature.

It will be shown that when the upper halves of the cotyledons of Phalaris and Avena were enclosed in little pipes of tin-foil or of blackened glass, in which case the upper part was mechanically prevented from bending, the lower and unenclosed part did not bend when exposed to a lateral light; and it occurred to us that this fact might be due, not to the exclusion of the light from the upper part, but to some necessity of the bending gradually travelling down the cotyledons, so that unless the upper part first became bent, the lower could not bend, however much it might be stimulated. It was necessary for our purpose to ascertain whether this notion was true, and it was proved false; for the lower halves of several cotyledons became bowed to the light, although their upper halves were enclosed in little glass tubes (not blackened), which prevented, as far as we could judge, their bending. Nevertheless, as the part within the tube might possibly bend a very little, fine rigid rods or flat splinters of thin glass were cemented with shellac to one side of the upper part of 15 cotyledons; and in six cases they were in addition tied on with threads. They were thus forced to remain quite straight. The result was that the lower halves of all became bowed to the light, but generally not in so great a degree as the corresponding part of the free seedlings in the same pots; and this may perhaps be accounted for by some slight degree of injury having been caused by a considerable surface having been smeared with shellac. It may be added, that when the cotyledons of Phalaris and Avena are acted on by apogeotropism, it is the upper part which begins first to bend; and when this part was rendered rigid in the manner just described, the upward curvature of the basal part was not thus prevented.

To test our belief that the upper part of the cotyledons of Phalaris, when exposed to a lateral light, regulates the bending of the lower part, many experiments were tried; but most of our first attempts proved useless from various causes not worth specifying. Seven cotyledons had their tips cut off for lengths varying between .1 and .16 of an inch, and these, when left exposed all day to a lateral light, remained upright. In another set of 7 cotyledons, the tips were cut off for a length of only about .05 of an inch (1.27 mm.) and these became bowed towards a lateral light, but not nearly so much as the many other seedlings in the same pots. This latter case shows that cutting off the tips does not by itself injure the plants so seriously as to prevent heliotropism; but we thought at the time, that such injury might follow when a greater length was cut off, as in the first set of experiments. Therefore, no more trials of this kind were made, which we now regret; as we afterwards found that when the tips of three cotyledons were cut off for a length of .2 inch, and of four others for lengths of .14, .12, .1, and .07 inch, and they were extended horizontally, the amputation did not interfere in the least with their bending vertically upwards, through the action of apogeotropism, like unmutilated specimens. It is therefore extremely improbable that the amputation of the tips for lengths of from .1 to .14 inch, could from the injury thus caused have prevented the lower part from bending towards the light.

We next tried the effects of covering the upper part of the cotyledons of Phalaris with little caps which were impermeable to light; the whole lower part being left fully exposed before a south-west window or a bright paraffin lamp. Some of the caps were made of extremely thin tin-foil blackened within; these had the disadvantage of occasionally, though rarely, being too heavy, especially when twice folded. The basal edges could be pressed into close contact with the cotyledons; though this again required care to prevent injuring them. Nevertheless, any injury thus caused could be detected by removing the caps, and trying whether the cotyledons were then sensitive to light. Other caps were made of tubes of the thinnest glass, which when painted black served well, with the one great disadvantage that the lower ends could not be closed. But tubes were used which fitted the cotyledons almost closely, and black paper was placed on the soil round each, to check the upward reflection of light from the soil. Such tubes were in one respect far better than caps of tin-foil, as it was possible to cover at the same time some cotyledons with transparent and others with opaque tubes; and thus our experiments could be controlled. It should be kept in mind that young cotyledons were selected for trial, and that these when not interfered with become bowed down to the ground towards the light.

We will begin with the glass-tubes. The summits of nine cotyledons, differing somewhat in height, were enclosed for rather less than half their lengths in uncoloured or transparent tubes; and these were then exposed before a south-west window on a bright day for 8 h. All of them became strongly curved towards the light, in the same degree as the many other free seedlings in the same pots; so that the glass-tubes certainly did not prevent the cotyledons from bending towards the light. Nineteen other cotyledons were, at the same time, similarly enclosed in tubes thickly painted with Indian ink. On five of them, the paint, to our surprise, contracted after exposure to the sunlight, and very narrow cracks were formed, through which a little light entered; and these five cases were rejected. Of the remaining 14 cotyledons, the lower halves of which had been fully exposed to the light for the whole time, 7 continued quite straight and upright; 1 was considerably bowed to the light, and 6 were slightly bowed, but with the exposed bases of most of them almost or quite straight. It is possible that some light may have been reflected upwards from the soil and entered the bases of these 7 tubes, as the sun shone brightly, though bits of blackened paper had been placed on the soil round them. Nevertheless, the 7 cotyledons which were slightly bowed, together with the 7 upright ones, presented a most remarkable contrast in appearance with the many other seedlings in the same pots to which nothing had been done. The blackened tubes were then removed from 10 of these seedlings, and they were now exposed before a lamp for 8 h.; 9 of them became greatly, and 1 moderately, curved towards the light, proving that the previous absence of any curvature in the basal part, or the presence of only a slight degree of curvature there, was due to the exclusion of light from the upper part.

Similar observations were made on 12 younger cotyledons with their upper halves enclosed within glass-tubes coated with black varnish, and with their lower halves fully exposed to bright sunshine. In these younger seedlings the sensitive zone seems to extend rather lower down, as was observed on some other occasions, for two became almost as much curved towards the light as the free seedlings; and the remaining ten were slightly curved, although the basal part of several of them, which normally becomes more curved than any other part, exhibited hardly a trace of curvature. These 12 seedlings taken together differed greatly in their degree of curvature from all the many other seedlings in the same pots.

Better evidence of the efficiency of the blackened tubes was incidentally afforded by some experiments hereafter to be given, in which the upper halves of 14 cotyledons were enclosed in tubes from which an extremely narrow stripe of the black varnish had been scraped off. These cleared stripes were not directed towards the window, but obliquely to one side of the room, so that only a very little light could act on the upper halves of the cotyledons. These 14 seedlings remained during eight hours of exposure before a south-west window on a hazy day quite upright; whereas all the other many free seedlings in the same pots became greatly bowed towards the light.

We will now turn to the trials with caps made of very thin tin-foil. These were placed at different times on the summits of 24 cotyledons, and they extended down for a length of between .15 and .2 of an inch. The seedlings were exposed to a lateral light for periods varying between 6 h. 30 m. and 7 h. 45 m., which sufficed to cause all the other seedlings in the same pots to become almost rectangularly bent towards the light. They varied in height from only .04 to 1.15 inch, but the greater number were about .75 inch. Of the 24 cotyledons with their summits thus protected, 3 became much bent, but not in the direction of the light, and as they did not straighten themselves through apogeotropism during the following night, either the caps were too heavy or the plants themselves were in a weak condition; and these three cases may be excluded. There are left for consideration 21 cotyledons; of these 17 remained all the time quite upright; the other 4 became slightly inclined to the light, but not in a degree comparable with that of the many free seedlings in the same pots. As the glass-tubes, when unpainted, did not prevent the cotyledons from becoming greatly bowed, it cannot be supposed that the caps of very thin tin-foil did so, except through the exclusion of the light. To prove that the plants had not been injured, the caps were removed from 6 of the upright seedlings, and these were exposed before a paraffin lamp for the same length of time as before, and they now all became greatly curved towards the light.

As caps between .15 and .2 of an inch in depth were thus proved to be highly efficient in preventing the cotyledons from bending towards the light, 8 other cotyledons were protected with caps between only .06 and .12 in depth. Of these, two remained vertical, one was considerably and five slightly curved towards the light, but far less so than the free seedlings in the same pots.

Another trial was made in a different manner, namely, by bandaging with strips of tin-foil, about .2 in breadth, the upper part, but not the actual summit, of eight moderately young seedlings a little over half an inch in height. The summits and the basal parts were thus left fully exposed to a lateral light during 8 h.; an upper intermediate zone being protected. With four of these seedlings the summits were exposed for a length of .05 inch, and in two of them this part became curved towards the light, but the whole lower part remained quite upright; whereas the entire length of the other two seedlings became slightly curved towards the light. The summits of the four other seedlings were exposed for a length of .04 inch, and of these one remained almost upright, whilst the other three became considerably curved towards the light. The many free seedlings in the same pots were all greatly curved towards the light.

From these several sets of experiments, including those with the glass-tubes, and those when the tips were cut off, we may infer that the exclusion of light from the upper part of the cotyledons of Phalaris prevents the lower part, though fully exposed to a lateral light, from becoming curved. The summit for a length of .04 or .05 of an inch, though it is itself sensitive and curves towards the light, has only a slight power of causing the lower part to bend. Nor has the exclusion of light from the summit for a length of .1 of an inch a strong influence on the curvature of the lower part. On the other hand, an exclusion for a length of between .15 and .2 of an inch, or of the whole upper half, plainly prevents the lower and fully illuminated part from becoming curved in the manner (see Fig. 181) which invariably occurs when a free cotyledon is exposed to a lateral light. With very young seedlings the sensitive zone seems to extend rather lower down relatively to their height than in older seedlings. We must therefore conclude that when seedlings are freely exposed to a lateral light some influence is transmitted from the upper to the lower part, causing the latter to bend.

This conclusion is supported by what may be seen to occur on a small scale, especially with young cotyledons, without any artificial exclusion of the light; for they bend beneath the earth where no light can enter. Seeds of Phalaris were covered with a layer one-fourth of an inch in thickness of very fine sand, consisting of extremely minute grains of silex coated with oxide of iron. A layer of this sand, moistened to the same degree as that over the seeds, was spread over a glass-plate; and when the layer was .05 of an inch in thickness (carefully measured) no light from a bright sky could be seen to pass through it, unless it was viewed through a long blackened tube, and then a trace of light could be detected, but probably much too little to affect any plant. A layer .1 of an inch in thickness was quite impermeable to light, as judged by the eye aided by the tube. It may be worth adding that the layer, when dried, remained equally impermeable to light. This sand yielded to very slight pressure whilst kept moist, and in this state did not contract or crack in the least. In a first trial, cotyledons which had grown to a moderate height were exposed for 8 h. before a paraffin lamp, and they became greatly bowed. At their bases on the shaded side opposite to the light, well-defined, crescentic, open furrows were formed, which (measured under a microscope with a micrometer) were from .02 to .03 of an inch in breadth, and these had evidently been left by the bending of the buried bases of the cotyledons towards the light. On the side of the light the cotyledons were in close contact with the sand, which was a very little heaped up. By removing with a sharp knife the sand on one side of the cotyledons in the line of the light, the bent portion and the open furrows were found to extend down to a depth of about .1 of an inch, where no light could enter. The chords of the short buried arcs formed in four cases angles of 11°, 13°, 15°, and 18°, with the perpendicular. By the following morning these short bowed portions had straightened themselves through apogeotropism.

In the next trial much younger cotyledons were similarly treated, but were exposed to a rather obscure lateral light. After some hours, a bowed cotyledon, .3 inch in height, had an open furrow on the shaded side .04 inch in breadth; another cotyledon, only .13 inch in height, had left a furrow .02 inch in breadth. But the most curious case was that of a cotyledon which had just protruded above the ground and was only .03 inch in height, and this was found to be bowed in the direction of the light to a depth of .2 of an inch beneath the surface. From what we know of the impermeability of this sand to light, the upper illuminated part in these several cases must have determined the curvature of the lower buried portions. But an apparent cause of doubt may be suggested: as the cotyledons are continually circumnutating, they tend to form a minute crack or furrow all round their bases, which would admit a little light on all sides; but this would not happen when they were illuminated laterally, for we know that they quickly bend towards a lateral light, and they then press so firmly against the sand on the illuminated side as to furrow it, and this would effectually exclude light on this side. Any light admitted on the opposite and shaded side, where an open furrow is formed, would tend to counteract the curvature towards the lamp or other source of the light. It may be added, that the use of fine moist sand, which yields easily to pressure, was indispensable in the above experiments; for seedlings raised in common soil, not kept especially damp, and exposed for 9 h. 30 m. to a strong lateral light, did not form an open furrow at their bases on the shaded side, and were not bowed beneath the surface.

Perhaps the most striking proof of the action of the upper on the lower part of the cotyledons of Phalaris, when laterally illuminated, was afforded by the blackened glass-tubes (before alluded to) with very narrow stripes of the varnish scraped off on one side, through which a little light was admitted. The breadth of these stripes or slits varied between .01 and .02 inch (.25 and .51 mm.). Cotyledons with their upper halves enclosed in such tubes were placed before a south-west window, in such a position, that the scraped stripes did not directly face the window, but obliquely to one side. The seedlings were left exposed for 8 h., before the close of which time the many free seedlings in the same pots had become greatly bowed towards the window. Under these circumstances, the whole lower halves of the cotyledons, which had their summits enclosed in the tubes, were fully exposed to the light of the sky, whilst their upper halves received exclusively or chiefly diffused light from the room, and this only through a very narrow slit on one side. Now, if the curvature of the lower part had been determined by the illumination of this part, all the cotyledons assuredly would have become curved towards the window; but this was far from being the case. Tubes of the kind just described were placed on several occasions over the upper halves of 27 cotyledons; 14 of them remained all the time quite vertical; so that sufficient diffused light did not enter through the narrow slits to produce any effect whatever; and they behaved in the same manner as if their upper halves had been enclosed in completely blackened tubes. The lower halves of the 13 other cotyledons became bowed not directly in the line of the window, but obliquely towards it; one pointed at an angle of only 18°, but the remaining 12 at angles varying between 45° and 62° from the line of the window. At the commencement of the experiment, pins had been laid on the earth in the direction towards which the slits in the varnish faced; and in this direction alone a small amount of diffused light entered. At the close of the experiment, 7 of the bowed cotyledons pointed exactly in the line of the pins, and 6 of them in a line between that of the pins and that of the window. This intermediate position is intelligible, for any light from the sky which entered obliquely through the slits would be much more efficient than the diffused light which entered directly through them. After the 8 h. exposure, the contrast in appearance between these 13 cotyledons and the many other seedlings in the same pots, which were all (excepting the above 14 vertical ones) greatly bowed in straight and parallel lines towards the window, was extremely remarkable. It is therefore certain that a little weak light striking the upper halves of the cotyledons of Phalaris, is far more potent in determining the direction of the curvature of the lower halves, than the full illumination of the latter during the whole time of exposure.

In confirmation of the above results, the effect of thickly painting with Indian ink one side of the upper part of three cotyledons of Phalaris, for a length of .2 inch from their tips, may be worth giving. These were placed so that the unpainted surface was directed not towards the window, but a little to one side; and they all became bent towards the unpainted side, and from the line of the window by angles amounting to 31°, 35°, and 83°. The curvature in this direction extended down to their bases, although the whole lower part was fully exposed to the light from the window.

Finally, although there can be no doubt that the illumination of the upper part of the cotyledons of Phalaris greatly affects the power and manner of bending of the lower part, yet some observations seemed to render it probable that the simultaneous stimulation of the lower part by light greatly favours, or is almost necessary, for its well-marked curvature; but our experiments were not conclusive, owing to the difficulty of excluding light from the lower halves without mechanically preventing their curvature.

Avena sativa.—The cotyledons of this plant become quickly bowed towards a lateral light, exactly like those of Phalaris. Experiments similar to the foregoing ones were tried, and we will give the results as briefly as possible. They are somewhat less conclusive than in the case of Phalaris, and this may possibly be accounted for by the sensitive zone varying in extension, in a species so long cultivated and variable as the common Oat. Cotyledons a little under three-quarters of an inch in height were selected for trial: six had their summits protected from light by tin-foil caps, .25 inch in depth, and two others by caps .3 inch in depth. Of these 8 cotyledons, five remained upright during 8 hours of exposure, although their lower parts were fully exposed to the light all the time; two were very slightly, and one considerably, bowed towards it. Caps only .2 or .22 inch in depth were placed over 4 other cotyledons, and now only one remained upright, one was slightly, and two considerably bowed to the light. In this and the following cases all the free seedlings in the same pots became greatly bowed to the light.

Our next trial was made with short lengths of thin and fairly transparent quills; for glass-tubes of sufficient diameter to go over the cotyledons would have been too heavy. Firstly, the summits of 13 cotyledons were enclosed in unpainted quills, and of these 11 became greatly and 2 slightly bowed to the light; so that the mere act of enclosure did not prevent the lower part from becoming bowed. Secondly, the summits of 11 cotyledons were enclosed in quills .3 inch in length, painted so as to be impermeable to light; of these, 7 did not become at all inclined towards the light, but 3 of them were slightly bent more or less transversely with respect to the line of light, and these might perhaps have been altogether excluded; one alone was slightly bowed towards the light. Painted quills, .25 inch in length, were placed over the summits of 4 other cotyledons; of these, one alone remained upright, a second was slightly bowed, and the two others as much bowed to the light as the free seedlings in the same pots. These two latter cases, considering that the caps were .25 in length, are inexplicable.

Lastly, the summits of 8 cotyledons were coated with flexible and highly transparent gold-beaters’ skin, and all became as much bowed to the light as the free seedlings. The summits of 9 other cotyledons were similarly coated with gold-beaters’ skin, which was then painted to a depth of between .25 and .3 inch, so as to be impermeable to light; of these 5 remained upright, and 4 were well bowed to the light, almost or quite as well as the free seedlings. These latter four cases, as well as the two in the last paragraph, offer a strong exception to the rule that the illumination of the upper part determines the curvature of the lower part. Nevertheless, 5 of these 8 cotyledons remained quite upright, although their lower halves were fully illuminated all the time; and it would almost be a prodigy to find five free seedlings standing vertically after an exposure for several hours to a lateral light.

The cotyledons of Avena, like those of Phalaris, when growing in soft, damp, fine sand, leave an open crescentric furrow on the shaded side, after bending to a lateral light; and they become bowed beneath the surface at a depth to which, as we know, light cannot penetrate. The arcs of the chords of the buried bowed portions formed in two cases angles of 20° and 21° with the perpendicular. The open furrows on the shaded side were, in four cases, .008, .016, .024, and .024 of an inch in breadth. Brassica oleracea (Common Red).—It will here be shown that the upper half of the hypocotyl of the cabbage, when illuminated by a lateral light, determines the curvature of the lower half. It is necessary to experimentise on young seedlings about half an inch or rather less in height, for when grown to an inch and upwards the basal part ceases to bend. We first tried painting the hypocotyls with Indian ink, or cutting off their summits for various lengths; but these experiments are not worth giving, though they confirm, as far as they can be trusted, the results of the following ones. These were made by folding gold-beaters’ skin once round the upper halves of young hypocotyls, and painting it thickly with Indian ink or with black grease. As a control experiment, the same transparent skin, left unpainted, was folded round the upper halves of 12 hypocotyls; and these all became greatly curved to the light, excepting one, which was only moderately curved. Twenty other young hypocotyls had the skin round their upper halves painted, whilst their lower halves were left quite uncovered. These seedlings were then exposed, generally for between 7 and 8 h., in a box blackened within and open in front, either before a south-west window or a paraffin lamp. This exposure was amply sufficient, as was shown by the strongly-marked heliotropism of all the free seedlings in the same pots; nevertheless, some were left exposed to the light for a much longer time. Of the 20 hypocotyls thus treated, 14 remained quite upright, and 6 became slightly bowed to the light; but 2 of these latter cases were not really exceptions, for on removing the skin the paint was found imperfect and was penetrated by many small transparent spaces on the side which faced the light. Moreover, in two other cases the painted skin did not extend quite halfway down the hypocotyl. Although there was a wonderful contrast in the several pots between these 20 hypocotyls and the other many free seedlings, which were all greatly bowed down to their bases in the direction of the light, some being almost prostrate on the ground.

The most successful trial on any one day (included in the above results) is worth describing in detail. Six young seedlings were selected, the hypocotyls of which were nearly .45 inch, excepting one, which was .6 inch in height, measured from the bases of their petioles to the ground. Their upper halves, judged as accurately as could be done by the eye, were folded once round with gold-beaters’ skin, and this was painted thickly with Indian ink. They were exposed in an otherwise darkened room before a bright paraffin lamp, which stood on a level with the two pots containing the seedlings. They were first looked at after an interval of 5 h. 10 m., and five of the protected hypocotyls were found quite erect, the sixth being very slightly inclined to the light; whereas all the many free seedlings in the same two pots were greatly bowed to the light. They were again examined after a continuous exposure to the light of 20 h. 35m.; and now the contrast between the two sets was wonderfully great; for the free seedlings had their hypocotyls extended almost horizontally in the direction of the light, and were curved down to the ground; whilst those with the upper halves protected by the painted skin, but with their lower halves fully exposed to the light, still remained quite upright, with the exception of the one which retained the same slight inclination to the light which it had before. This latter seedling was found to have been rather badly painted, for on the side facing the light the red colour of the hypocotyl could be distinguished through the paint.

We next tried nine older seedlings, the hypocotyls of which varied between 1 and 1.6 inch in height. the gold-beaters’ skin round their upper parts was painted with black grease to a depth of only .3 inch, that is, from less than a third to a fourth or fifth of their total heights. They were exposed to the light for 7 h. 15 m.; and the result showed that the whole of the sensitive zone, which determines the curvature of the lower part, was not protected from the action of the light; for all 9 became curved towards it, 4 of them very slightly, 3 moderately, and 2 almost as much as the unprotected seedlings. Nevertheless, the whole 9 taken together differed plainly in their degree of curvature from the many free seedlings, and from some which were wrapped in unpainted skin, growing in the same two pots.

Seeds were covered with about a quarter of an inch of the fine sand described under Phalaris; and when the hypocotyls had grown to a height of between .4 and .55 inch, they were exposed during 9 h. before a paraffin lamp, their bases being at first closely surrounded by the damp sand. They all became bowed down to the ground, so that their upper parts lay near to and almost parallel to the surface of the soil. On the side of the light their bases were in close contact with the sand, which was here a very little heaped up; on the opposite or shaded side there were open, crescentic cracks or furrows, rather above .01 of an inch in width; but they were not so sharp and regular as those made by Phalaris and Avena, and therefore could not be so easily measured under the microscope. The hypocotyls were found, when the sand was removed on one side, to be curved to a depth beneath the surface in three cases of at least .1 inch, in a fourth case of .11, and in a fifth of .15 inch. The chords of the arcs of the short, buried, bowed portions formed angles of between 11° and 15° with the perpendicular. From what we have seen of the impermeability of this sand to light, the curvature of the hypocotyls certainly extended down to a depth where no light could enter; and the curvature must have been caused by an influence transmitted from the upper illuminated part.

The lower halves of five young hypocotyls were surrounded by unpainted gold-beaters’ skin, and these, after an exposure of 8 h. before a paraffin lamp, all became as much bowed to the light as the free seedlings. The lower halves of 10 other young hypocotyls, similarly surrounded with the skin, were thickly painted with Indian ink; their upper and unprotected halves became well curved to the light, but their lower and protected halves remained vertical in all the cases excepting one, and on this the layer of paint was imperfect. This result seems to prove that the influence transmitted from the upper part is not sufficient to cause the lower part to bend, unless it be at the same time illuminated; but there remains the doubt, as in the case of Phalaris, whether the skin covered with a rather thick crust of dry Indian ink did not mechanically prevent their curvature.

Beta vulgaris.—A few analogous experiments were tried on this plant, which is not very well adapted for the purpose, as the basal part of the hypocotyl, after it has grown to above half an inch in height, does not bend much on exposure to a lateral light. Four hypocotyls were surrounded close beneath their petioles with strips of thin tin-foil, .2 inch in breadth, and they remained upright all day before a paraffin lamp; two others were surrounded with strips .15 inch in breadth, and one of these remained upright, the other becoming bowed; the bandages in two other cases were only .1 inch in breadth, and both of these hypocotyls became bowed, though one only slightly, towards the light. The free seedlings in the same pots were all fairly well curved towards the light; and during the following night became nearly upright. The pots were now turned round and placed before a window, so that the opposite sides of the seedlings were exposed to the light, towards which all the unprotected hypocotyls became bent in the course of 7 h. Seven out of the 8 seedlings with bandages of tin-foil remained upright, but one which had a bandage only .1 inch in breadth, became curved to the light. On another occasion, the upper halves of 7 hypocotyls were surrounded with painted gold-beaters’ skin; of these 4 remained upright, and 3 became a little curved to the light: at the same time 4 other seedlings surrounded with unpainted skin, as well as the free ones in the same pots, all became bowed towards the lamp, before which they had been exposed during 22 hours.

Radicles of Sinapis alba.—The radicles of some plants are indifferent, as far as curvature is concerned, to the action of light; whilst others bend towards and others from it.[^[6]] Whether these movements are of any service to the plant is very doubtful, at least in the case of subterranean roots; they probably result from the radicles being sensitive to contact, moisture, and gravitation, and as a consequence to other irritants which are never naturally encountered. The radicles of Sinapis alba, when immersed in water and exposed to a lateral light, bend from it, or are apheliotropic. They become bent for a length of about 4 mm. from their tips. To ascertain whether this movement generally occurred, 41 radicles, which had germinated in damp sawdust, were immersed in water and exposed to a lateral light; and they all, with two doubtful exceptions, became curved from the light. At the same time the tips of 54 other radicles, similarly exposed, were just touched with nitrate of silver. They were blackened for a length of from .05 to .07 mm., and probably killed; but it should be observed that this did not check materially, if at all, the growth of the upper part; for several, which were measured, increased in the course of only 8–9 h. by 5 to 7 mm. in length. Of the 54 cauterised radicles one case was doubtful, 25 curved themselves from the light in the normal manner, and 28, or more than half, were not in the least apheliotropic. There was a considerable difference, which we cannot account for, in the results of the experiments tried towards the end of April and in the middle of September. Fifteen radicles (part of the above 54) were cauterised at the former period and were exposed to sunshine, of which 12 failed to be apheliotropic, 2 were still apheliotropic, and 1 was doubtful. In September, 39 cauterised radicles were exposed to a northern light, being kept at a proper temperature; and now 23 continued to be apheliotropic in the normal manner, and only 16 failed to bend from the light. Looking at the aggregate results at both periods, there can be no doubt that the destruction of the tip for less than a millimeter in length destroyed in more than half the cases their power of moving from the light. It is probable that if the tips had been cauterised for the length of a whole millimeter, all signs of apheliotropism would have disappeared. It may be suggested that although the application of caustic does not stop growth, yet enough may be absorbed to destroy the power of movement in the upper part; but this suggestion must be rejected, for we have seen and shall again see, that cauterising one side of the tip of various kinds of radicles actually excites movement. The conclusion seems inevitable that sensitiveness to light resides in the tip of the radicle of Sinapis alba; and that the tip when thus stimulated transmits some influence to the upper part, causing it to bend. The case in this respect is parallel with that of the radicles of several plants, the tips of which are sensitive to contact and to other irritants, and, as will be shown in the eleventh chapter, to gravitation.

[6] Sachs, ‘Physiologie Végétale,’ 1868, p. 44.

CONCLUDING REMARKS AND SUMMARY OF CHAPTER.

We do not know whether it is a general rule with seedling plants that the illumination of the upper part determines the curvature of the lower part. But as this occurred in the four species examined by us, belonging to such distinct families as the Gramineæ, Cruciferae, and Chenopodeae, it is probably of common occurrence. It can hardly fail to be of service to seedlings, by aiding them to find the shortest path from the buried seed to the light, on nearly the same principle that the eyes of most of the lower crawling animals are seated at the anterior ends of their bodies. It is extremely doubtful whether with fully developed plants the illumination of one part ever affects the curvature of another part. The summits of 5 young plants of Asparagus officinalis (varying in height between 1.1 and 2.7 inches, and consisting of several short internodes) were covered with caps of tin-foil from 0.3 to 0.35 inch in depth; and the lower uncovered parts became as much curved towards a lateral light, as were the free seedlings in the same pots. Other seedlings of the same plant had their summits painted with Indian ink with the same negative result. Pieces of blackened paper were gummed to the edges and over the blades of some leaves on young plants of Tropaeolum majus and Ranunculus ficaria; these were then placed in a box before a window, and the petioles of the protected leaves became curved towards the light, as much as those of the unprotected leaves.

The foregoing cases with respect to seedling plants have been fully described, not only because the transmission of any effect from light is a new physiological fact, but because we think it tends to modify somewhat the current views on heliotropic movements. Until lately such movements were believed to result simply from increased growth on the shaded side. At present it is commonly admitted[^[7]] that diminished light increases the turgescence of the cells, or the extensibility of the cell-walls, or of both together, on the shaded side, and that this is followed by increased growth. But Pfeffer has shown that a difference in the turgescence on the two sides of a pulvinus,—that is, an aggregate of small cells which have ceased to grow at an early age,—is excited by a difference in the amount of light received by the two sides; and that movement is thus caused without being followed by increased growth on the more turgescent side.[^[8]] All observers apparently believe that light acts directly on the part which bends, but we have seen with the above described seedlings that this is not the case. Their lower halves were brightly illuminated for hours, and yet did not bend in the least towards the light, though this is the part which under ordinary circumstances bends the most. It is a still more striking fact, that the faint illumination of a narrow stripe on one side of the upper part of the cotyledons of Phalaris determined the direction of the curvature of the lower part; so that this latter part did not bend towards the bright light by which it had been fully illuminated, but obliquely towards one side where only a little light entered. These results seem to imply the presence of some matter in the upper part which is acted on by light, and which transmits its effects to the lower part. It has been shown that this transmission is independent of the bending of the upper sensitive part. We have an analogous case of transmission in Drosera, for when a gland is irritated, the basal and not the upper or intermediate part of the tentacle bends. The flexible and sensitive filament of Dionaea likewise transmits a stimulus, without itself bending; as does the stem of Mimosa.

[7] Emil Godlewski has given (‘Bot. Zeitung,’ 1879, Nos. 6–9) an excellent account (p. 120) of the present state of the question. See also Vines in ‘Arbeiten des Bot. Inst. in Würzburg,’ 1878, B. ii. pp. 114–147. Hugo de Vries has recently published a still more important article on this subject: ‘Bot Zeitung,’ Dec. 19th and 26th, 1879.

[8] ‘Die Periodischen Bewegungen der Blattorgane,’ 1875, pp. 7, 63, 123, etc. Frank has also insisted (‘Die Naturliche wägerechte Richtung von Pflanzentheilen,’ 1870, p. 53) on the important part which the pulvini of the leaflets of compound leaves play in placing the leaflets in a proper position with respect to the light. This holds good, especially with the leaves of climbing plants, which are carried into all sorts of positions, ill-adapted for the action of the light.

Light exerts a powerful influence on most vegetable tissues, and there can be no doubt that it generally tends to check their growth. But when the two sides of a plant are illuminated in a slightly different degree, it does not necessarily follow that the bending towards the illuminated side is caused by changes in the tissues of the same nature as those which lead to increased growth in darkness. We know at least that a part may bend from the light, and yet its growth may not be favoured by light. This is the case with the radicles of Sinapis alba, which are plainly apheliotropic; nevertheless, they grow quicker in darkness than in light.[^[9]] So it is with many aërial roots, according to Wiesner;[^[10]] but there are other opposed cases. It appears, therefore, that light does not determine the growth of apheliotropic parts in any uniform manner.

[9] Francis Darwin, ‘Über das Wachsthum negativ heliotropischer Wurzeln’: ‘Arbeiten des Bot. Inst. in Würzburg,’ B. ii., Heft iii., 1880, p. 521.

[10] ‘Sitzb. der k. Akad. der Wissensch’ (Vienna), 1880, p. 12.

We should bear in mind that the power of bending to the light is highly beneficial to most plants. There is therefore no improbability in this power having been specially acquired. In several respects light seems to act on plants in nearly the same manner as it does on animals by means of the nervous system.[^[11]] With seedlings the effect, as we have just seen, is transmitted from one part to another. An animal may be excited to move by a very small amount of light; and it has been shown that a difference in the illumination of the two sides of the cotyledons of Phalaris, which could not be distinguished by the human eye, sufficed to cause them to bend. It has also been shown that there is no close parallelism between the amount of light which acts on a plant and its degree of curvature; it was indeed hardly possible to perceive any difference in the curvature of some seedlings of Phalaris exposed to a light, which, though dim, was very much brighter than that to which others had been exposed. The retina, after being stimulated by a bright light, feels the effect for some time; and Phalaris continued to bend for nearly half an hour towards the side which had been illuminated. The retina cannot perceive a dim light after it has been exposed to a bright one; and plants which had been kept in the daylight during the previous day and morning, did not move so soon towards an obscure lateral light as did others which had been kept in complete darkness.

[11] Sachs has made some striking remarks to the same effect with respect to the various stimuli which excite movement in plants. See his paper ‘Ueber orthotrope und plagiotrope Pflanzentheile,’ ‘Arb. des Bot. Inst. in Würzburg,’ 1879, B. ii. p. 282.

Even if light does act in such a manner on the growing parts of plants as always to excite in them a tendency to bend towards the more illuminated side—a supposition contradicted by the foregoing experiments on seedlings and by all apheliotropic organs—yet the tendency differs greatly in different species, and is variable in degree in the individuals of the same species, as may be seen in almost any pot of seedlings of a long cultivated plant.[^[12]] There is therefore a basis for the modification of this tendency to almost any beneficial extent. That it has been modified, we see in many cases: thus, it is of more importance for insectivorous plants to place their leaves in the best position for catching insects than to turn their leaves to the light, and they have no such power. If the stems of twining plants were to bend towards the light, they would often be drawn away from their supports; and as we have seen they do not thus bend. As the stems of most other plants are heliotropic, we may feel almost sure that twining plants, which are distributed throughout the whole vascular series, have lost a power that their non-climbing progenitors possessed. Moreover, with Ipomœa, and probably all other twiners, the stem of the young plant, before it begins to twine, is highly heliotropic, evidently in order to expose the cotyledons or the first true leaves fully to the light. With the Ivy the stems of seedlings are moderately heliotropic, whilst those of the same plants when grown a little older are apheliotropic. Some tendrils which consist of modified leaves—organs in all ordinary cases strongly diaheliotropic—have been rendered apheliotropic, and their tips crawl into any dark crevice.

[12] Strasburger has shown in his interesting work (‘Wirkung des Lichtes...auf Schwärmsporen,’ 1878), that the movement of the swarm-spores of various lowly organised plants to a lateral light is influenced by their stage of development, by the temperature to which they are subjected, by the degree of illumination under which they have been raised, and by other unknown causes; so that the swarm-spores of the same species may move across the field of the microscope either to or from the light. Some individuals, moreover, appear to be indifferent to the light; and those of different species behave very differently. The brighter the light, the straighter is their course. They exhibit also for a short time the after-effects of light. In all these respects they resemble the higher plants. See, also, Stahl, ‘Ueber den einfluss der Lichts auf die Bewegungs-erscheinungen der Schwärmsporen’ Verh. d. phys.-med. Geselsshalft in Würzburg, B. xii. 1878.

Even in the case of ordinary heliotropic movements, it is hardly credible that they result directly from the action of the light, without any special adaptation. We may illustrate what we mean by the hygroscopic movements of plants: if the tissues on one side of an organ permit of rapid evaporation, they will dry quickly and contract, causing the part to bend to this side. Now the wonderfully complex movements of the pollinia of Orchis pyramidalis, by which they clasp the proboscis of a moth and afterwards change their position for the sake of depositing the pollen-masses on the double stigma—or again the twisting movements, by which certain seeds bury themselves in the ground[^[13]]—follow from the manner of drying of the parts in question; yet no one will suppose that these results have been gained without special adaptation. Similarly, we are led to believe in adaptation when we see the hypocotyl of a seedling, which contains chlorophyll, bending to the light; for although it thus receives less light, being now shaded by its own cotyledons, it places them—the more important organs—in the best position to be fully illuminated. The hypocotyl may therefore be said to sacrifice itself for the good of the cotyledons, or rather of the whole plant. But if it be prevented from bending, as must sometimes occur with seedlings springing up in an entangled mass of vegetation, the cotyledons themselves bend so as to face the light; the one farthest off rising up, and that nearest to the light sinking down, or both twisting laterally.[^[14]] We may, also, suspect that the extreme sensitiveness to light of the upper part of the sheath-like cotyledons of the Gramineæ, and their power of transmitting its effects to the lower part, are specialised arrangements for finding the shortest path to the light. With plants growing on a bank, or thrown prostrate by the wind, the manner in which the leaves move, even rotating on their own axes, so that their upper surfaces may be again directed to the light, is a striking phenomenon. Such facts are rendered more striking when we remember that too intense a light injures the chlorophyll, and that the leaflets of several Leguminosae when thus exposed bend upwards and present their edges to the sun, thus escaping injury. On the other hand, the leaflets of Averrhoa and Oxalis, when similarly exposed, bend downwards.

[13] Francis Darwin, ‘On the Hygroscopic Mechanism,’ etc., ‘Transactions Linn. Soc.,’ series ii. vol. i. p. 149, 1876.

[14] Wiesner has made remarks to nearly the same effect with respect to leaves: ‘Die undulirende Nutation der Internodien,’ p. 6, extracted from B. lxxvii. (1878). Sitb. der k. Akad. der Wissensch. Wien.

It was shown in the last chapter that heliotropism is a modified form of circumnutation; and as every growing part of every plant circumnutates more or less, we can understand how it is that the power of bending to the light has been acquired by such a multitude of plants throughout the vegetable kingdom. The manner in which a circumnutating movement—that is, one consisting of a succession of irregular ellipses or loops—is gradually converted into a rectilinear course towards the light, has been already explained. First, we have a succession of ellipses with their longer axes directed towards the light, each of which is described nearer and nearer to its source; then the loops are drawn out into a strongly pronounced zigzag line, with here and there a small loop still formed. At the same time that the movement towards the light is increased in extent and accelerated, that in the opposite direction is lessened and retarded, and at last stopped. The zigzag movement to either side is likewise gradually lessened, so that finally the course becomes rectilinear. Thus under the stimulus of a fairly bright light there is no useless expenditure of force.

As with plants every character is more or less variable, there seems to be no great difficulty in believing that their circumnutating movements may have been increased or modified in any beneficial manner by the preservation of varying individuals. The inheritance of habitual movements is a necessary contingent for this process of selection, or the survival of the fittest; and we have seen good reason to believe that habitual movements are inherited by plants. In the case of twining species the circumnutating movements have been increased in amplitude and rendered more circular; the stimulus being here an internal or innate one. With sleeping plants the movements have been increased in amplitude and often changed in direction; and here the stimulus is the alternation of light and darkness, aided, however, by inheritance. In the case of heliotropism, the stimulus is the unequal illumination of the two sides of the plant, and this determines, as in the foregoing cases, the modification of the circumnutating movement in such a manner that the organ bends to the light. A plant which has been rendered heliotropic by the above means, might readily lose this tendency, judging from the cases already given, as soon as it became useless or injurious. A species which has ceased to be heliotropic might also be rendered apheliotropic by the preservation of the individuals which tended to circumnutate (though the cause of this and most other variations is unknown) in a direction more or less opposed to that whence the light proceeded. In like manner a plant might be rendered diaheliotropic.

CHAPTER X.
MODIFIED CIRCUMNUTATION: MOVEMENTS EXCITED BY GRAVITATION.

Means of observation—Apogeotropism—Cytisus—Verbena—Beta—Gradual conversion of the movement of circumnutation into apogeotropism in Rubus, Lilium, Phalaris, Avena, and Brassica—Apogeotropism retarded by heliotropism—Effected by the aid of joints or pulvini—Movements of flower-peduncles of Oxalis—General remarks on apogeotropism—Geotropism—Movements of radicles—Burying of seed-capsules—Use of process—Trifolium subterraneum—Arachis—Amphicarpæa—Diageotropism—Conclusion

Our object in the present chapter is to show that geotropism, apogeotropism, and diageotropism are modified forms of circumnutation. Extremely fine filaments of glass, bearing two minute triangles of paper, were fixed to the summits of young stems, frequently to the hypocotyls of seedlings, to flower-peduncles, radicles, etc., and the movements of the parts were then traced in the manner already described on vertical and horizontal glass-plates. It should be remembered that as the stems or other parts become more and more oblique with respect to the glasses, the figures traced on them necessarily become more and more magnified. The plants were protected from light, excepting whilst each observation was being made, and then the light, which was always a dim one, was allowed to enter so as to interfere as little as possible with the movement in progress; and we did not detect any evidence of such interference.

When observing the gradations between circumnutation and heliotropism, we had the great advantage of being able to lessen the light; but with geotropism analogous experiments were of course impossible. We could, however, observe the movements of stems placed at first only a little from the perpendicular, in which case geotropism did not act with nearly so much power, as when the stems were horizontal and at right angles to the force. Plants, also, were selected which were but feebly geotropic or apogeotropic, or had become so from having grown rather old. Another plan was to place the stems at first so that they pointed 30 or 40° beneath the horizon, and then apogeotropism had a great amount of work to do before the stem was rendered upright; and in this case ordinary circumnutation was often not wholly obliterated. Another plan was to observe in the evening plants which during the day had become greatly curved heliotropically; for their stems under the gradually waning light very slowly became upright through the action of apogeotropism; and in this case modified circumnutation was sometimes well displayed.

Apogeotropism.—Plants were selected for observation almost by chance, excepting that they were taken from widely different families. If the stem of a plant which is even moderately sensitive to apogeotropism be placed horizontally, the upper growing part bends quickly upwards, so as to become perpendicular; and the line traced by joining the dots successively made on a glass-plate, is generally almost straight. For instance, a young Cytisus fragrans, 12 inches in height, was placed so that the stem projected 10° beneath the horizon, and its course was traced during 72 h. At first it bent a very little downwards (Fig. 182), owing no doubt to the weight of the stem, as this occurred with most of the other plants observed, though, as they were of course circumnutating, the short downward lines were often oblique. After three-quarters of an hour the stem began to curve upwards, quickly during the first two hours, but much more slowly during the afternoon and night, and on the following day. During the second night it fell a little, and circumnutated during the following day; but it also moved a short distance to the right, which was caused by a little light having been accidentally admitted on this side. The stem was now inclined 60° above the horizon, and had therefore risen 70°. With time allowed it would probably have become upright, and no doubt would have continued circumnutating. The sole remarkable feature in the figure here given is the straightness of the course pursued. The stem, however, did not move upwards at an equable rate, and it sometimes stood almost or quite still. Such periods probably represent attempts to circumnutate in a direction opposite to apogeotropism.

Fig. 182. Cytisus fragrans: apogeotropic movement of stem from 10° beneath to 60° above horizon, traced on vertical glass, from 8.30 A.M. March 12th to 10.30 P.M. 13th. The subsequent circumnutating movement is likewise shown up to 6.45 A.M. on the 15th. Nocturnal course represented, as usual, by a broken line. Movement not greatly magnified, and tracing reduced to two-thirds of original scale.

The herbaceous stem of a Verbena melindres (?) laid horizontally, rose in 7 h. so much that it could no longer be observed on the vertical glass which stood in front of the plant. The long line which was traced was almost absolutely straight. After the 7 h. it still continued to rise, but now circumnutated slightly. On the following day it stood upright, and circumnutated regularly, as shown in Fig. 82, given in the fourth chapter. The stems of several other plants which were highly sensitive to apogeotropism rose up in almost straight lines, and then suddenly began to circumnutate. A partially etiolated and somewhat old hypocotyl of a seedling cabbage (2 3/4 inches in height) was so sensitive that when placed at an angle of only 23° from the perpendicular, it became vertical in 33 minutes. As it could not have been strongly acted upon by apogeotropism in the above slightly inclined position, we expected that it would have circumnutated, or at least have moved in a zigzag course. Accordingly, dots were made every 3 minutes; but, when these were joined, the line was nearly straight. After this hypocotyl had become upright it still moved onwards for half an hour in the same general direction, but in a zigzag manner. During the succeeding 9 h. it circumnutated regularly, and described 3 large ellipses. In this case apogeotropism, although acting at a very unfavourable angle, quite overcame the ordinary circumnutating movement.

Fig. 183. Beta vulgaris: apogeotropic movement of hypocotyl from 19° beneath horizon to a vertical position, with subsequent circumnutation, traced on a vertical and on a horizontal glass-plate, from 8.28 A.M. Sept. 28th to 8.40 A.M. 29th. Figure reduced to one-third of original scale.

The hypocotyls of Beta vulgaris are highly sensitive to apogeotropism. One was placed so as to project 19° beneath the horizon; it fell at first a very little (see Fig. 183), no doubt owing to its weight; but as it was circumnutating the line was oblique. During the next 3 h. 8 m. it rose in a nearly straight line, passing through an angle of 109°, and then (at 12.3 P.M.) stood upright. It continued for 55 m. to move in the same general direction beyond the perpendicular, but in a zigzag course. It returned also in a zigzag line, and then circumnutated regularly, describing three large ellipses during the remainder of the day. It should be observed that the ellipses in this figure are exaggerated in size, relatively to the length of the upward straight line, owing to the position of the vertical and horizontal glass-plates. Another and somewhat old hypocotyl was placed so as to stand at only 31° from the perpendicular, in which position apogeotropism acted on it with little force, and its course accordingly was slightly zigzag.

The sheath-like cotyledons of Phalaris Canariensis are extremely sensitive to apogeotropism. One was placed so as to project 40° beneath the horizon. Although it was rather old and 1.3 inch in height, it became vertical in 4 h. 30 m., having passed through an angle of 130° in a nearly straight line. It then suddenly began to circumnutate in the ordinary manner. The cotyledons of this plant, after the first leaf has begun to protrude, are but slightly apogeotropic, though they still continue to circumnutate. One at this stage of development was placed horizontally, and did not become upright even after 13 h., and its course was slightly zigzag. So, again, a rather old hypocotyl of Cassia tora (1 1/4 inch in height) required 28 h. to become upright, and its course was distinctly zigzag; whilst younger hypocotyls moved much more quickly and in a nearly straight line.

When a horizontally placed stem or other organ rises in a zigzag line, we may infer from the many cases given in our previous chapters, that we have a modified form of circumnutation; but when the course is straight, there is no evidence of circumnutation, and any one might maintain that this latter movement had been replaced by one of a wholly distinct kind. This view seems the more probable when (as sometimes occurred with the hypocotyls of Brassica and Beta, the stems of Cucurbita, and the cotyledons of Phalaris) the part in question, after bending up in a straight course, suddenly begins to circumnutate to the full extent and in the usual manner. A fairly good instance of a sudden change of this kind—that is, from a nearly straight upward movement to one of circumnutation—is shown in Fig. 183; but more striking instances were occasionally observed with Beta, Brassica, and Phalaris.

We will now describe a few cases in which it may be seen how gradually circumnutation becomes changed into apogeotropism, under circumstances to be specified in each instance.

Rubus idæus (hybrid).—A young plant, 11 inches in height, growing in a pot, was placed horizontally; and the upward movement was traced during nearly 70 h.; but the plant, though growing vigorously, was not highly sensitive to apogeotropism, or it was not capable of quick movement, for during the above time it rose only 67°. We may see in the diagram (Fig. 184) that during the first day of 12 h. it rose in a nearly straight line. When placed horizontally, it was evidently circumnutating, for it rose at first a little, notwithstanding the weight of the stem, and then sank down; so that it did not start on its permanently upward course until 1 h. 25 m. had elapsed. On the second day, by which time it had risen considerably, and when apogeotropism acted on it with somewhat less power, its course during 15½ h. was clearly zigzag, and the rate of the upward movement was not equable. During the third day, also of 15½ h., when apogeotropism acted on it with still less power, the stem plainly circumnutated, for it moved during this day 3 times up and 3 times down, 4 times to the left and 4 to the right. But the course was so complex that it could hardly be traced on the glass. We can, however, see that the successively formed irregular ellipses rose higher and higher. Apogeotropism continued to act on the fourth morning, as the stem was still rising, though it now stood only 23° from the perpendicular. In this diagram the several stages may be followed by which an almost rectilinear, upward, apogeotropic course first becomes zigzag, and then changes into a circumnutating movement, with most of the successively formed, irregular ellipses directed upwards.

Fig 184: Rubus idæus (hybrid): apogeotropic movement of stem, traced on a vertical glass during 3 days and 3 nights, from 10.40 A.M. March 18th to 8 A.M. 21st. Figure reduced to one-half of the original scale.

Lilium auratum.—A plant 23 inches in height was placed horizontally, and the upper part of the stem rose 58° in 46 h., in the manner shown in the accompanying diagram (Fig. 185). We here see that during the whole of the second day of 15½ h., the stem plainly circumnutated whilst bending upwards through apogeotropism. It had still to rise considerably, for when the last dot in the figure was made, it stood 32° from an upright position.

Fig. 185. Lilium auratum: apogeotropic movement of stem, traced on a vertical glass during 2 days and 2 nights, from 10.40 A.M. March 18th to 8 A.M. 20th. Figure reduced to one-half of the original scale.

Phalaris Canariensis.—A cotyledon of this plant (1.3 inch in height) has already been described as rising in 4 h. 30 m. from 40° beneath the horizon into a vertical position, passing through an angle of 130° in a nearly straight line, and then abruptly beginning to circumnutate. Another somewhat old cotyledon of the same height (but from which a true leaf had not yet protruded), was similarly placed at 40° beneath the horizon. For the first 4 h. it rose in a nearly straight course (Fig. 186), so that by 1.10 P.M. it was highly inclined, and now apogeotropism acted on it with much less power than before, and it began to zigzag. At 4.15 P.M. (i.e. in 7 h. from the commencement) it stood vertically, and afterwards continued to circumnutate in the usual manner about the same spot. Here then we have a graduated change from a straight upward apogeotropic course into circumnutation, instead of an abrupt change, as in the former case.

Avena sativa.—The sheath-like cotyledons, whilst young, are strongly apogeotropic; and some which were placed at 45° beneath the horizon rose 90° in 7 or 8 h. in lines almost absolutely straight. An oldish cotyledon, from which the first leaf began to protrude whilst the following observations were being made, was placed at 10° beneath the horizon, and it rose only 59° in 24h. It behaved rather differently from any other plant, observed by us, for during the first 4½ h. it rose in a line not far from straight; during the next 6½ h. it circumnutated, that is, it descended and again ascended in a strongly marked zigzag course; it then resumed its upward movement in a moderately straight line, and, with time allowed, no doubt would have become upright. In this case, after the first 4½ h., ordinary circumnutation almost completely conquered for a time apogeotropism.

Fig 186. Phalaris Canariensis: apogeotropic movement of cotyledon, traced on a vertical and horizontal glass, from 9.10 A.M. Sept. 19th to 9 A.M. 20th. Figure here reduced to one-fifth of original scale.

Brassica oleracea.—The hypocotyls of several young seedlings placed horizontally, rose up vertically in the course of 6 or 7 h. in nearly straight lines. A seedling which had grown in darkness to a height of 2 1/4 inches, and was therefore rather old and not highly sensitive, was placed so that the hypocotyl projected at between 30° and 40° beneath the horizon. The upper part alone became curved upwards, and rose during the first 3 h. 10 m. in a nearly straight line (Fig. 187); but it was not possible to trace the upward movement on the vertical glass for the first 1 h. 10 m., so that the nearly straight line in the diagram ought to have been much longer. During the next 11 h. the hypocotyl circumnutated, describing irregular figures, each of which rose a little above the one previously formed. During the night and following early morning it continued to rise in a zigzag course, so that apogeotropism was still acting. At the close of our observations, after 23 h. (represented by the highest dot in the diagram) the hypocotyl was still 32° from the perpendicular. There can be little doubt that it would ultimately have become upright by describing an additional number of irregular ellipses, one above the other.

Fig 187. Brassica oleracea: apogeotropic movement of hypocotyl, traced on vertical glass, from 9.20 A.M., Sept. 12th to 8.30 A.M. 13th. The upper part of the figure is more magnified than the lower part. If the whole course had been traced, the straight upright line would have been much longer. Figure here reduced to one-third of the original scale.

Apogeotropism retarded by Heliotropism.—When the stem of any plant bends during the day towards a lateral light, the movement is opposed by apogeotropism; but as the light gradually wanes in the evening the latter power slowly gains the upper hand, and draws the stem back into a vertical position. Here then we have a good opportunity for observing how apogeotropism acts when very nearly balanced by an opposing force. For instance, the plumule of Tropaeolum majus (see former Fig. 175) moved towards the dim evening light in a slightly zigzag line until 6.45 P.M., it then returned on its course until 10.40 P.M., during which time it zigzagged and described an ellipse of considerable size. The hypocotyl of Brassica oleracea (see former Fig. 173) moved in a straight line to the light until 5.15 P.M., and then from the light, making in its backward course a great rectangular bend, and then returned for a short distance towards the former source of the light; no observations were made after 7.10 P.M., but during the night it recovered its vertical position. A hypocotyl of Cassia tora moved in the evening in a somewhat zigzag line towards the failing light until 6 P.M., and was now bowed 20° from the perpendicular; it then returned on its course, making before 10.30 P.M. four great, nearly rectangular bends and almost completing an ellipse. Several other analogous cases were casually observed, and in all of them the apogeotropic movement could be seen to consist of modified circumnutation.

Apogeotropic Movements effected by the aid of joints or pulvini.—Movements of this kind are well known to occur in the Gramineæ, and are effected by means of the thickened bases of their sheathing leaves; the stem within being in this part thinner than elsewhere.[^[1]] According to the analogy of all other pulvini, such joints ought to continue circumnutating for a long period, after the adjoining parts have ceased to grow. We therefore wished to ascertain whether this was the case with the Gramineæ; for if so, the upward curvature of their stems, when extended horizontally or laid prostrate, would be explained in accordance with our view—namely, that apogeotropism results from modified circumnutation. After these joints have curved upwards, they are fixed in their new position by increased growth along their lower sides.

[1] This structure has been recently described by De Vries in an interesting article, ‘Ueber die Aufrichtung des gelagerten Getreides,’ in ‘Landwirthschaftliche Jahrbücher,’ 1880, p. 473.

Lolium perenne.—A young stem, 7 inches in height, consisting of 3 internodes, with the flower-head not yet protruded, was selected for observation. A long and very thin glass filament was cemented horizontally to the stem close above the second joint, 3 inches above the ground. This joint was subsequently proved to be in an active condition, as its lower side swelled much through the action of apogeotropism (in the manner described by De Vries) after the haulm had been fastened down for 24 h. in a horizontal position. The pot was so placed that the end of the filament stood beneath the 2-inch object glass of a microscope with an eye-piece micrometer, each division of which equalled 1/500 of an inch. The end of the filament was repeatedly observed during 6 h., and was seen to be in constant movement; and it crossed 5 divisions of the micrometer (1/100 inch) in 2 h. Occasionally it moved forwards by jerks, some of which were 1/1000 inch in length, and then slowly retreated a little, afterwards again jerking forwards. These oscillations were exactly like those described under Brassica and Dionaea, but they occurred only occasionally. We may therefore conclude that this moderately old joint was continually circumnutating on a small scale.

Alopecurus pratensis.—A young plant, 11 inches in height, with the flower-head protruded, but with the florets not yet expanded, had a glass filament fixed close above the second joint, at a height of only 2 inches above the ground. The basal internode, 2 inches in length, was cemented to a stick to prevent any possibility of its circumnutating. The extremity of the filament, which projected about 50° above the horizon, was often observed during 24 h. in the same manner as in the last case. Whenever looked at, it was always in movement, and it crossed 30 divisions of the micrometer (3/50 inch) in 3½ h.; but it sometimes moved at a quicker rate, for at one time it crossed 5 divisions in 1½ h. The pot had to be moved occasionally, as the end of the filament travelled beyond the field of vision; but as far as we could judge it followed during the daytime a semicircular course; and it certainly travelled in two different directions at right angles to one another. It sometimes oscillated in the same manner as in the last species, some of the jerks forwards being as much as 1/1000 of an inch. We may therefore conclude that the joints in this and the last species of grass long continue to circumnutate; so that this movement would be ready to be converted into an apogeotropic movement, whenever the stem was placed in an inclined or horizontal position.

Movements of the Flower-peduncles of Oxalis carnosa, due to apogeotropism and other forces.—The movements of the main peduncle, and of the three or four sub-peduncles which each main peduncle of this plant bears, are extremely complex, and are determined by several distinct causes. Whilst the flowers are expanded, both kinds of peduncles circumnutate about the same spot, as we have seen (Fig. 91) in the fourth chapter. But soon after the flowers have begun to wither the sub-peduncles bend downwards, and this is due to epinasty; for on two occasions when pots were laid horizontally, the sub-peduncles assumed the same position relatively to the main peduncle, as would have been the case if they had remained upright; that is, each of them formed with it an angle of about 40°. If they had been acted on by geotropism or apheliotropism (for the plant was illuminated from above), they would have directed themselves to the centre of the earth. A main peduncle was secured to a stick in an upright position, and one of the upright sub-peduncles which had been observed circumnutating whilst the flower was expanded, continued to do so for at least 24 h. after it had withered. It then began to bend downwards, and after 36 h. pointed a little beneath the horizon. A new figure was now begun (A, Fig. 188), and the sub-peduncle was traced descending in a zigzag line from 7.20 P.M. on the 19th to 9 A.M. on the 22nd. It now pointed almost perpendicularly downwards, and the glass filament had to be removed and fastened transversely across the base of the young capsule. We expected that the sub-peduncle would have been motionless in its new position; but it continued slowly to swing, like a pendulum, from side to side, that is, in a plane at right angles to that in which it had descended. This circumnutating movement was observed from 9 A.M. on 22nd to 9 A.M. 24th, as shown at B in the diagram. We were not able to observe this particular sub-peduncle any longer; but it would certainly have gone on circumnutating until the capsule was nearly ripe (which requires only a short time), and it would then have moved upwards.

The upward movement (C, Fig. 188) is effected in part by the whole sub-peduncle rising in the same manner as it had previously descended through epinasty—namely, at the joint where united to the main peduncle. As this upward movement occurred with plants kept in the dark and in whatever position the main peduncle was fastened, it could not have been caused by heliotropism or apogeotropism, but by hyponasty. Besides this movement at the joint, there is another of a very different kind, for the sub-peduncle becomes upwardly bent in the middle part. If the sub-peduncle happens at the time to be inclined much downwards, the upward curvature is so great that the whole forms a hook. The upper end bearing the capsule, thus always places itself upright, and as this occurs in darkness, and in whatever position the main peduncle may have been secured, the upward curvature cannot be due to heliotropism or hyponasty, but to apogeotropism.

Fig. 188. Oxalis carnosa: movements of flower-peduncle, traced on a vertical glass: A, epinastic downward movement; B, circumnutation whilst depending vertically; C, subsequent upward movement, due to apogeotropism and hyponasty combined.

In order to trace this upward movement, a filament was fixed to a sub-peduncle bearing a capsule nearly ripe, which was beginning to bend upwards by the two means just described. Its course was traced (see C, Fig 188) during 53 h., by which time it had become nearly upright. The course is seen to be strongly zigzag, together with some little loops. We may therefore conclude that the movement consists of modified circumnutation.

The several species of Oxalis probably profit in the following manner by their sub-peduncles first bending downwards and then upwards. They are known to scatter their seeds by the bursting of the capsule; the walls of which are so extremely thin, like silver paper, that they would easily be permeated by rain. But as soon as the petals wither, the sepals rise up and enclose the young capsule, forming a perfect roof over it as soon as the sub-peduncle has bent itself downwards. By its subsequent upward movement, the capsule stands when ripe at a greater height above the ground by twice the length of the sub-peduncle, than it did when dependent, and is thus able to scatter its seeds to a greater distance. The sepals, which enclose the ovarium whilst it is young, present an additional adaptation by expanding widely when the seeds are ripe, so as not to interfere with their dispersal. In the case of Oxalis acetosella, the capsules are said sometimes to bury themselves under loose leaves or moss on the ground, but this cannot occur with those of O. carnosa, as the woody stem is too high.

Oxalis acetosella.—The peduncles are furnished with a joint in the middle, so that the lower part answers to the main peduncle, and the upper part to one of the sub-peduncles of O. carnosa. The upper part bends downwards, after the flower has begun to wither, and the whole peduncle then forms a hook; that this bending is due to epinasty we may infer from the case of O. carnosa. When the pod is nearly ripe, the upper part straightens itself and becomes erect; and this is due to hyponasty or apogeotropism, or both combined, and not to heliotropism, for it occurred in darkness. The short, hooked part of the peduncle of a cleistogamic flower, bearing a pod nearly ripe, was observed in the dark during three days. The apex of the pod at first pointed perpendicularly down, but in the course of three days rose 90°, so that it now projected horizontally. The course during the two latter days is shown in Fig. 189; and it may be seen how greatly the peduncle, whilst rising, circumnutated. The lines of chief movement were at right angles to the plane of the originally hooked part. The tracing was not continued any longer; but after two additional days, the peduncle with its capsule had become straight and stood upright.

Fig. 189. Oxalis acetosella: course pursued by the upper part of a peduncle, whilst rising, traced from 11 A.M. June 1st to 9 A.M. 3rd. Figure here reduced to one-half of the original scale.

Concluding Remarks on Apogeotropism.—When apogeotropism is rendered by any means feeble, it acts, as shown in the several foregoing cases, by increasing the always present circumnutating movement in a direction opposed to gravity, and by diminishing that in the direction of gravity, as well as that to either side. The upward movement thus becomes unequal in rate, and is sometimes interrupted by stationary periods. Whenever irregular ellipses or loops are still formed, their longer axes are almost always directed in the line of gravity, in an analogous manner as occurred with heliotropic movements in reference to the light. As apogeotropism acts more and more energetically, ellipses or loops cease to be formed, and the course becomes at first strongly, and then less and less zigzag, and finally rectilinear. From this gradation in the nature of the movement, and more especially from all growing parts, which alone (except when pulvini are present) are acted on by apogeotropism, continually circumnutating, we may conclude that even a rectilinear course is merely an extremely modified form of circumnutation. It is remarkable that a stem or other organ which is highly sensitive to apogeotropism, and which has bowed itself rapidly upwards in a straight line, is often carried beyond the vertical, as if by momentum. It then bends a little backwards to a point round which it finally circumnutates. Two instances of this were observed with the hypocotyls of Beta vulgaris, one of which is shown in Fig. 183, and two other instances with the hypocotyls of Brassica. This momentum-like movement probably results from the accumulated effects of apogeotropism. For the sake of observing how long such after-effects lasted, a pot with seedlings of Beta was laid on its side in the dark, and the hypocotyls in 3 h. 15 m. became highly inclined. The pot, still in the dark, was then placed upright, and the movements of the two hypocotyls were traced; one continued to bend in its former direction, now in opposition to apogeotropism, for about 37 m., perhaps for 48 m.; but after 61 m. it moved in an opposite direction. The other hypocotyl continued to move in its former course, after being placed upright, for at least 37 m.

Different species and different parts of the same species are acted on by apogeotropism in very different degrees. Young seedlings, most of which circumnutate quickly and largely, bend upwards and become vertical in much less time than do any older plants observed by us; but whether this is due to their greater sensitiveness to apogeotropism, or merely to their greater flexibility we do not know. A hypocotyl of Beta traversed an angle of 109° in 3 h. 8 m., and a cotyledon of Phalaris an angle of 130° in 4 h. 30 m. On the other hand, the stem of a herbaceous Verbena rose 90° in about 24 h.; that of Rubus 67°, in 70 h.; that of Cytisus 70°, in 72 h.; that of a young American Oak only 37°, in 72 h. The stem of a young Cyperus alternifolius rose only 11° in 96 h.; the bending being confined to near its base. Though the sheath-like cotyledons of Phalaris are so extremely sensitive to apogeotropism, the first true leaves which protrude from them exhibited only a trace of this action. Two fronds of a fern, Nephrodium molle, both of them young and one with the tip still inwardly curled, were kept in a horizontal position for 46 h., and during this time they rose so little that it was doubtful whether there was any true apogeotropic movement.

The most curious case known to us of a difference in sensitiveness to gravitation, and consequently of movement, in different parts of the same organ, is that offered by the petioles of the cotyledons of Ipomœa leptophylla. The basal part for a short length where united to the undeveloped hypocotyl and radicle is strongly geotropic, whilst the whole upper part is strongly apogeotropic. But a portion near the blades of the cotyledons is after a time acted on by epinasty and curves downwards, for the sake of emerging in the form of an arch from the ground; it subsequently straightens itself, and is then again acted on by apogeotropism.

A branch of Cucurbita ovifera, placed horizontally, moved upwards during 7 h. in a straight line, until it stood at 40° above the horizon; it then began to circumnutate, as if owing to its trailing nature it had no tendency to rise any higher. Another upright branch was secured to a stick, close to the base of a tendril, and the pot was then laid horizontally in the dark. In this position the tendril circumnutated and made several large ellipses during 14 h., as it likewise did on the following day; but during this whole time it was not in the least affected by apogeotropism. On the other hand, when branches of another Cucurbitaceous plant, Echinocytis lobata, were fixed in the dark so that the tendrils depended beneath the horizon, these began immediately to bend upwards, and whilst thus moving they ceased to circumnutate in any plain manner; but as soon as they had become horizontal they recommenced to revolve conspicuously.[^[2]] The tendrils of Passiflora gracilis are likewise apogeotropic. Two branches were tied down so that their tendrils pointed many degrees beneath the horizon. One was observed for 8 h., during which time it rose, describing two circles, one above the other. The other tendril rose in a moderately straight line during the first 4 h., making however one small loop in its course; it then stood at about 45° above the horizon, where it circumnutated during the remaining 8 h. of observation.

[2] For details see ‘The Movements and Habits of Climbing Plants,’ 1875, p. 131.

A part or organ which whilst young is extremely sensitive to apogeotropism ceases to be so as it grows old; and it is remarkable, as showing the independence of this sensitiveness and of the circumnutating movement, that the latter sometimes continues for a time after all power of bending from the centre of the earth has been lost. Thus a seedling Orange bearing only 3 young leaves, with a rather stiff stem, did not curve in the least upwards during 24 h. whilst extended horizontally; yet it circumnutated all the time over a small space. The hypocotyl of a young seedling of Cassia tora, similarly placed, became vertical in 12 h.; that of an older seedling, 1 1/4 inch in height, became so in 28 h.; and that of another still older one, 1½ inch in height, remained horizontal during two days, but distinctly circumnutated during this whole time.

When the cotyledons of Phalaris or Avena are laid horizontally, the uppermost part first bends upwards, and then the lower part; consequently, after the lower part has become much curved upwards, the upper part is compelled to curve backwards in an opposite direction, in order to straighten itself and to stand vertically; and this subsequent straightening process is likewise due to apogeotropism. The upper part of 8 young cotyledons of Phalaris were made rigid by being cemented to thin glass rods, so that this part could not bend in the least; nevertheless, the basal part was not prevented from curving upward. A stem or other organ which bends upwards through apogeotropism exerts considerable force; its own weight, which has of course to be lifted, was sufficient in almost every instance to cause the part at first to bend a little downwards; but the downward course was often rendered oblique by the simultaneous circumnutating movement. The cotyledons of Avena placed horizontally, besides lifting their own weight, were able to furrow the soft sand above them, so as to leave little crescentic open spaces on the lower sides of their bases; and this is a remarkable proof of the force exerted.

As the tips of the cotyledons of Phalaris and Avena bend upwards through the action of apogeotropism before the basal part, and as these same tips when excited by a lateral light transmit some influence to the lower part, causing it to bend, we thought that the same rule might hold good with apogeotropism. Consequently, the tips of 7 cotyledons of Phalaris were cut off for a length in three cases of .2 inch and in the four other cases of .14, .12, .1, and .07 inch. But these cotyledons, after being extended horizontally, bowed themselves upwards as effectually as the unmutilated specimens in the same pots, showing that sensitiveness to gravitation is not confined to their tips.