The Power of Movement in Plants · Charles Darwin
CHAPTER I. THE CIRCUMNUTATING MOVEMENTS OF SEEDLING PLANTS.
Our seeds were subjected to a high temperature, and in the course of three or four days the petioles penetrated the soil perpendicularly to a depth of from 2 to 2½ inches; and not until then did the true radicle begin to grow. In one specimen which was closely observed, the petioles in 7 days after their first protrusion attained a length of 2½ inches, and the radicle by this time had also become well developed. The plumule, still enclosed within the tube, was now .3 inch in length, and was quite straight; but from having increased in thickness it had just begun to split open the lower part of the petioles on one side, along the line of their confluence. By the following morning the upper part of the plumule had arched itself into a right angle, and the convex side or elbow had thus been forced out through the slit. Here then the arching of the plumule plays the same part as in the case of the petioles of the Delphinium. As the plumule continued to grow, the tip became more arched, and in the course of six days it emerged through the 2½ inches of superincumbent soil, still retaining its arched form. After reaching the surface it straightened itself in the usual manner. In the accompanying figure (Fig. 58, A) we have a sketch of a seedling in this advanced state of development; the surface of the ground being represented by the line G...........G.
Ipomœa leptophylla.—In most of the species of this genus the hypocotyl is well developed, and breaks through the ground as an arch. But the seeds of the present species in germinating behave like those of Megarrhiza, excepting that the elongated petioles of the cotyledons are not confluent. After they have protruded from the seed, they are united at their lower ends with the undeveloped hypocotyl and undeveloped radicle, which together form a point only about .1 inch in length. They are at first highly geotropic, and penetrate the ground to a depth of rather above half an inch. The radicle then begins to grow. On four occasions after the petioles had grown for a short distance vertically downwards, they were placed in a horizontal position in damp air in the dark, and in the course of 4 hours they again became curved vertically downwards, having passed through 90° in this time. But their sensitiveness to geotropism lasts for only 2 or 3 days; and the terminal part alone, for a length of between .2 and .4 inch, is thus sensitive. Although the petioles of our specimens did not penetrate the ground to a greater depth than about ½ inch, yet they continued for some time to grow rapidly, and finally attained the great length of about 3 inches.
The upper part is apogeotropic, and therefore grows vertically upwards, excepting a short portion close to the blades, which at an early period bends downwards and becomes arched, and thus breaks through the ground. Afterwards this portion straightens itself, and the cotyledons then free themselves from the seed-coats. Thus we here have in different parts of the same organ widely different kinds of movement and of sensitiveness; for the basal part is geotropic, the upper part apogeotropic, and a portion near the blades temporarily and spontaneously arches itself. The plumule is not developed for some little time; and as it rises between the bases of the parallel and closely approximate petioles of the cotyledons, which in breaking through the ground have formed an almost open passage, it does not require to be arched and is consequently always straight. Whether the plumule remains buried and dormant for a time in its native country, and is thus protected from the cold of winter, we do not know. The radicle, like that of the Megarrhiza, grows into a tuber-like mass, which ultimately attains a great size. So it is with Ipomœa pandurata, the germination of which, as Asa Gray informs us, resembles that of I. leptophylla. The following case is interesting in connection with the root-like nature of the petioles. The radicle of a seedling was cut off, as it was completely decayed, and the two now separated cotyledons were planted. They emitted roots from their bases, and continued green and healthy for two months. The blades of both then withered, and on removing the earth the bases of the petioles (instead of the radicle) were found enlarged into little tubers. Whether these would have had the power of producing two independent plants in the following summer, we do not know.
In Quercus virens, according to Dr. Engelmann,[9] both the cotyledons and their petioles are confluent. The latter grow to a length “of an inch or even more;” and, if we understand rightly, penetrate the ground, so that they must be geotropic. The nutriment within the cotyledons is then quickly transferred to the hypocotyl or radicle, which thus becomes developed into a fusiform tuber. The fact of tubers being formed by the foregoing three widely distinct plants, makes us believe that their protection from animals at an early age and whilst tender, is one at least of the advantages gained by the remarkable elongation of the petioles of the cotyledons, together with their power of penetrating the ground like roots under the guidance of geotropism. [9] ‘Transact. St. Louis Acad. Science,’ vol. iv. p. 190.
The following cases may be here given, as they bear on our present subject, though not relating to seedlings. The flower-stem of the parasitic Lathraea squamaria, which is destitute of true leaves, breaks through the ground as an arch;[10] so does the flower-stem of the parasitic and leafless Monotropa hypopitys. With Helleborus niger, the flower-stems, which rise up independently of the leaves, likewise break through the ground as arches. This is also the case with the greatly elongated flower-stems, as well as with the petioles of Epimedium pinnatum. So it is with the petioles of Ranunculus ficaria, when they have to break through the ground, but when they arise from the summit of the bulb above ground, they are from the first quite straight; and this is a fact which deserves notice. The rachis of the bracken fern (Pteris aquilina), and of some, probably many, other ferns, likewise rises above ground under the form of an arch. No doubt other analogous instances could be found by careful search. In all ordinary cases of bulbs, rhizomes, root-stocks, etc., buried beneath the ground, the surface is broken by a cone formed by the young imbricated leaves, the combined growth of which gives them force sufficient for the purpose.
With germinating monocotyledonous seeds, of which, however, we did not observe a large number, the plumules, for instance, those of Asparagus and Canna, are straight whilst breaking through the ground. With the Gramineæ, the sheath-like cotyledons are likewise straight; they, however, terminate in a sharp crest, which is white and somewhat indurated; and this structure obviously facilitates their emergence from the soil: the first true leaves escape from the sheath through a slit beneath the chisel-like apex and at right angles to it. In the case of the onion (Allium cepa) we again meet with an arch; the leaf-like cotyledon being abruptly bowed, when it breaks through the ground, with the apex still enclosed within the seed-coats. The crown of the arch, as previously described, is developed into a white conical protuberance, which we may safely believe to be a special adaptation for this office.
The fact of so many organs of different kinds—hypocotyls and epicotyls, the petioles of some cotyledons and of some first leaves, the cotyledons of the onion, the rachis of some ferns, and some flower-stems—being all arched whilst they break through the ground, shows how just are Dr. Haberlandt’s[11] remarks on the importance of the arch to seedling plants. He attributes its chief importance to the upper, young, and more tender parts of the hypocotyl or epicotyl, being thus saved from abrasion and pressure whilst breaking through the ground. But we think that some importance may be attributed to the increased force gained by the hypocotyl, epicotyl, or other organ by being at first arched; for both legs of the arch increase in length, and both have points of resistance as long as the tip remains enclosed within the seed-coats; and thus the crown of the arch is pushed up through the earth with twice as much force as that which a straight hypocotyl, etc., could exert. As soon, however, as the upper end has freed itself, all the work has to be done by the basal leg. In the case of the epicotyl of the common bean, the basal leg (the apex having freed itself from the seed-coats) grew upwards with a force sufficient to lift a thin plate of zinc, loaded with 12 ounces. Two more ounces were added, and the 14 ounces were lifted up to a very little height, and then the epicotyl yielded and bent to one side.
In some other cases the hypocotyl or epicotyl protrudes from the seed at first only slightly bowed; but the bowing afterwards increases independently of any constraint. The arch is thus made narrow, with the two legs, which are sometimes much elongated, parallel and close together, and thus it becomes well fitted for breaking through the ground. With many kinds of plants, the radicle, whilst still enclosed within the seed and likewise after its first protrusion, lies in a straight line with the future hypocotyl and with the longitudinal axis of the cotyledons. This is the case with Cucurbita ovifera: nevertheless, in whatever position the seeds were buried, the hypocotyl always came up arched in one particular direction. Seeds were planted in friable peat at a depth of about an inch in a vertical position, with the end from which the radicle protrudes downwards. Therefore all the parts occupied the same relative positions which they would ultimately hold after the seedlings had risen clear above the surface. Notwithstanding this fact, the hypocotyl arched itself; and as the arch grew upwards through the peat, the buried seeds were turned either upside down, or were laid horizontally, being afterwards dragged above the ground. Ultimately the hypocotyl straightened itself in the usual manner; and now after all these movements the several parts occupied the same position relatively to one another and to the centre of the earth, which they had done when the seeds were first buried.
But it may be argued in this and other such cases that, as the hypocotyl grows up through the soil, the seed will almost certainly be tilted to one side; and then from the resistance which it must offer during its further elevation, the upper part of the hypocotyl will be doubled down and thus become arched. This view seems the more probable, because with Ranunculus ficaria only the petioles of the leaves which forced a passage through the earth were arched; and not those which arose from the summits of the bulbs above the ground. Nevertheless, this explanation does not apply to the Cucurbita, for when germinating seeds were suspended in damp air in various positions by pins passing through the cotyledons, fixed to the inside of the lids of jars, in which case the hypocotyls were not subjected to any friction or constraint, yet the upper part became spontaneously arched. This fact, moreover, proves that it is not the weight of the cotyledons which causes the arching. Seeds of Helianthus annuus and of two species of Ipomœa (those of ‘I. bona nox’ being for the genus large and heavy) were pinned in the same manner, and the hypocotyls became spontaneously arched; the radicles, which had been vertically dependent, assumed in consequence a horizontal position. In the case of Ipomœa leptophylla it is the petioles of the cotyledons which become arched whilst rising through the ground; and this occurred spontaneously when the seeds were fixed to the lids of jars.
It may, however, be suggested with some degree of probability that the arching was aboriginally caused by mechanical compulsion, owing to the confinement of the parts in question within the seed-coats, or to friction whilst they were being dragged upwards. But if this is so, we must admit from the cases just given, that a tendency in the upper part of the several specified organs to bend downwards and thus to become arched, has now become with many plants firmly inherited. The arching, to whatever cause it may be due, is the result of modified circumnutation, through increased growth along the convex side of the part; such growth being only temporary, for the part always straightens itself subsequently by increased growth along the concave side, as will hereafter be described. It is a curious fact that the hypocotyls of some plants, which are but little developed and which never raise their cotyledons above the ground, nevertheless inherit a slight tendency to arch themselves, although this movement is not of the least use to them. We refer to a movement observed by Sachs in the hypocotyls of the bean and some other Leguminosae, and which is shown in the accompanying figure (Fig. 59), copied from his Essay.[12] The hypocotyl and radicle at first grow perpendicularly downwards, as at A, and then bend, often in the course of 24 hours, into the position shown at B. As we shall hereafter often have to recur to this movement, we will, for brevity sake, call it “Sachs’ curvature.” At first sight it might be thought that the altered position of the radicle in B was wholly due to the outgrowth of the epicotyl (e), the petiole (p) serving as a hinge; and it is probable that this is partly the cause; but the hypocotyl and upper part of the radicle themselves become slightly curved.
Rudimentary Cotyledons.—A few remarks on this subject may be here interpolated. It is well known that some dicotyledonous plants produce only a single cotyledon; for instance, certain species of Ranunculus, Corydalis, Chaerophyllum; and we will here endeavour to show that the loss of one or both cotyledons is apparently due to a store of nutriment being laid up in some other part, as in the hypocotyl or one of the two cotyledons, or one of the secondary radicles. With the orange (Citrus aurantium) the cotyledons are hypogean, and one is larger than the other, as may be seen in A (Fig. 60). In B the inequality is rather greater, and the stem has grown between the points of insertion of the two petioles, so that they do not stand opposite to one another; in another case the separation amounted to one-fifth of an inch. The smaller cotyledon of one seedling was extremely thin, and not half the length of the larger one, so that it was clearly becoming rudimentary[14] In all these seedlings the hypocotyl was enlarged or swollen. Fig. 60. Citrus aurantium: two young seedlings: c, larger cotyledon; c’, smaller cotyledon; h, thickened hypocotyl; r, radicle. In A the epicotyl is still arched, in B it has become erect. Fig. 61. Abronia umbellata: seedling twice natural size: c cotyledon; c’, rudimentary cotyledon; h, enlarged hypocotyl, with a heel or projection (h’) at the lower end; r, radicle.
In _Cyclamen Persicum_ the hypocotyl, even whilst still within the seed, is enlarged into a regular corm,[15] and only a single cotyledon is at first developed (see former Fig. 57). With _Ranunculus ficaria_ two cotyledons are never produced, and here one of the secondary radicles is developed at an early age into a so-called bulb.[16] Again, certain species of Chaerophyllum and Corydalis produce only a single cotyledon;[17] in the former the hypocotyl, and in the latter the radicle is enlarged, according to Irmisch, into a bulb. [15] Dr. H. Gressner, ‘Bot. Zeitung,’ 1874, p. 824. [16] Irmisch, ‘Beiträge zur Morphologie der Pflanzen,’ 1854, pp. 11, 12; ‘Bot. Zeitung,’ 1874, p. 805. [17] Delpino, ‘Rivista Botanica,’ 1877, p. 21. It is evident from Vaucher’s account (‘Hist. Phys. des Plantes d’Europe,’ tom. i. 1841, p. 149) of the germination of the seeds of several species of Corydalis, that the bulb or tubercule begins to be formed at an extremely early age.
In the several foregoing cases one of the cotyledons is delayed in its development, or reduced in size, or rendered rudimentary, or quite aborted; but in other cases both cotyledons are represented by mere rudiments. With Opuntia basilaris this is not the case, for both cotyledons are thick and large, and the hypocotyl shows at first no signs of enlargement; but afterwards, when the cotyledons have withered and disarticulated themselves, it becomes thickened, and from its tapering form, together with its smooth, tough, brown skin, appears, when ultimately drawn down to some depth into the soil, like a root. On the other hand, with several other Cacteæ, the hypocotyl is from the first much enlarged, and both cotyledons are almost or quite rudimentary. Thus with Cereus Landbeckii two little triangular projections, representing the cotyledons, are narrower than the hypocotyl, which is pear-shaped, with the point downwards. In Rhipsalis cassytha the cotyledons are represented by mere points on the enlarged hypocotyl. In Echinocactus viridescens the hypocotyl is globular, with two little prominences on its summit. In Pilocereus Houlletii the hypocotyl, much swollen in the upper part, is merely notched on the summit; and each side of the notch evidently represents a cotyledon. Stapelia sarpedon, a member of the very distinct family of the Asclepiadeae, is fleshy like a cactus; and here again the upper part of the flattened hypocotyl is much thickened and bears two minute cotyledons, which, measured internally, were only .15 inch in length, and in breadth not equal to one-fourth of the diameter of the hypocotyl in its narrow axis; yet these minute cotyledons are probably not quite useless, for when the hypocotyl breaks through the ground in the form of an arch, they are closed or pressed against one another, and thus protect the plumule. They afterwards open.
From the several cases now given, which refer to widely distinct plants, we may infer that there is some close connection between the reduced size of one or both cotyledons and the formation, by the enlargement of the hypocotyl or of the radicle, of a so-called bulb. But it may be asked, did the cotyledons first tend to abort, or did a bulb first begin to be formed? As all dicotyledons naturally produce two well-developed cotyledons, whilst the thickness of the hypocotyl and of the radicle differs much in different plants, it seems probable that these latter organs first became from some cause thickened—in several instances apparently in correlation with the fleshy nature of the mature plant—so as to contain a store of nutriment sufficient for the seedling, and then that one or both cotyledons, from being superfluous, decreased in size. It is not surprising that one cotyledon alone should sometimes have been thus affected, for with certain plants, for instance the cabbage, the cotyledons are at first of unequal size, owing apparently to the manner in which they are packed within the seed. It does not, however, follow from the above connection, that whenever a bulb is formed at an early age, one or both cotyledons will necessarily become superfluous, and consequently more or less rudimentary. Finally, these cases offer a good illustration of the principle of compensation or balancement of growth, or, as Goethe expresses it, “in order to spend on one side, Nature is forced to economise on the other side.”
Circumnutation and other movements of Hypocotyls and Epicotyls, whilst still arched and buried beneath the ground, and whilst breaking through it.—According to the position in which a seed may chance to have been buried, the arched hypocotyl or epicotyl will begin to protrude in a horizontal, a more or less inclined, or in a vertical plane. Except when already standing vertically upwards, both legs of the arch are acted on from the earliest period by apogeotropism. Consequently they both bend upwards until the arch becomes vertical. During the whole of this process, even before the arch has broken through the ground, it is continually trying to circumnutate to a slight extent; as it likewise does if it happens at first to stand vertically up,—all which cases have been observed and described, more or less fully, in the last chapter. After the arch has grown to some height upwards the basal part ceases to circumnutate, whilst the upper part continues to do so.
That an arched hypocotyl or epicotyl, with the two legs fixed in the ground, should be able to circumnutate, seemed to us, until we had read Prof. Wiesner’s observations, an inexplicable fact. He has shown[18] in the case of certain seedlings, whose tips are bent downwards (or which nutate), that whilst the posterior side of the upper or dependent portion grows quickest, the anterior and opposite side of the basal portion of the same internode grows quickest; these two portions being separated by an indifferent zone, where the growth is equal on all sides. There may be even more than one indifferent zone in the same internode; and the opposite sides of the parts above and below each such zone grow quickest. This peculiar manner of growth is called by Wiesner “undulatory nutation.” Circumnutation depends on one side of an organ growing quickest (probably preceded by increased turgescence), and then another side, generally almost the opposite one, growing quickest. Now if we look at an arch like this [upside down U] and suppose the whole of one side—we will say the whole convex side of both legs—to increase in length, this would not cause the arch to bend to either side. But if the outer side or surface of the left leg were to increase in length the arch would be pushed over to the right, and this would be aided by the inner side of the right leg increasing in length. If afterwards the process were reversed, the arch would be pushed over to the opposite or left side, and so on alternately,—that is, it would circumnutate. As an arched hypocotyl, with the two legs fixed in the ground, certainly circumnutates, and as it consists of a single internode, we may conclude that it grows in the manner described by Wiesner. It may be added, that the crown of the arch does not grow, or grows very slowly, for it does not increase much in breadth, whilst the arch itself increases greatly in height.
As long as an arched hypocotyl or epicotyl remains buried beneath the ground, the two legs cannot separate from one another, except to a slight extent from the yielding of the soil; but as soon as the arch rises above the ground, or at an earlier period if the pressure of the surrounding earth be artificially removed, the arch immediately begins to straighten itself. This no doubt is due to growth along the whole inner surface of both legs of the arch; such growth being checked or prevented, as long as the two legs of the arch are firmly pressed together. When the earth is removed all round an arch and the two legs are tied together at their bases, the growth on the under side of the crown causes it after a time to become much flatter and broader than naturally occurs. The straightening process consists of a modified form of circumnutation, for the lines described during this process (as with the hypocotyl of Brassica, and the epicotyls of Vicia and Corylus) were often plainly zigzag and sometimes looped. After hypocotyls or epicotyls have emerged from the ground, they quickly become perfectly straight. No trace is left of their former abrupt curvature, excepting in the case of Allium cepa, in which the cotyledon rarely becomes quite straight, owing to the protuberance developed on the crown of the arch.
The increased growth along the inner surface of the arch which renders it straight, apparently begins in the basal leg or that which is united to the radicle; for this leg, as we often observed, is first bowed backwards from the other leg. This movement facilitates the withdrawal of the tip of the epicotyl or of the cotyledons, as the case may be, from within the seed-coats and from the ground. But the cotyledons often emerge from the ground still tightly enclosed within the seed-coats, which apparently serve to protect them. The seed-coats are afterwards ruptured and cast off by the swelling of the closely conjoined cotyledons, and not by any movement or their separation from one another. Nevertheless, in some few cases, especially with the Cucurbitaceæ, the seed-coats are ruptured by a curious contrivance, described by M. Flahault.[19] A heel or peg is developed on one side of the summit of the radicle or base of the hypocotyl; and this holds down the lower half of the seed-coats (the radicle being fixed into the ground) whilst the continued growth of the arched hypocotyl forced upwards the upper half, and tears asunder the seed-coats at one end, and the cotyledons are then easily withdrawn. [19] ‘Bull. Soc. Bot. de France,’ tom. xxiv. 1877, p. 201.
Text from Project Gutenberg, public domain in the United States.