The Formation of Vegetable Mould Through the Action of Worms / With Observations on Their Habits

by Charles Darwin

The leaves of a foreign plant were next searched for, the blades of which were not more pointed towards the apex than towards the base. This proved to be the case with those of a laburnum (a hybrid between Cytisus alpinus and laburnum) for on doubling the terminal over the basal half, they generally fitted exactly; and when there was any difference, the basal half was a little the narrower. It might, therefore, have been expected that an almost equal number of these leaves would have been drawn in by the tip and base, or a slight excess in favour of the latter. But of 73 leaves (not included in the first lot of 227) pulled out of worm-burrows, 63 per cent. had been drawn in by the tip; 27 per cent. by the base, and 10 per cent. transversely. We here see that a far larger proportion, viz., 27 per cent. were drawn in by the base than in the case of lime leaves, the blades of which are very broad at the base, and of which only 4 per cent. had thus been drawn in. We may perhaps account for the fact of a still larger proportion of the laburnum leaves not having been drawn in by the base, by worms having acquired the habit of generally drawing in leaves by their tips and thus avoiding the foot-stalk. For the basal margin of the blade in many kinds of leaves forms a large angle with the foot-stalk; and if such a leaf were drawn in by the foot-stalk, the basal margin would come abruptly into contact with the ground on each side of the burrow, and would render the drawing in of the leaf very difficult.

Nevertheless worms break through their habit of avoiding the foot-stalk, if this part offers them the most convenient means for drawing leaves into their burrows. The leaves of the endless hybridised varieties of the Rhododendron vary much in shape; some are narrowest towards the base and others towards the apex. After they have fallen off, the blade on each side of the midrib often becomes curled up while drying, sometimes along the whole length, sometimes chiefly at the base, sometimes towards the apex. Out of 28 fallen leaves on one bed of peat in my garden, no less than 23 were narrower in the basal quarter than in the terminal quarter of their length; and this narrowness was chiefly due to the curling in of the margins. Out of 36 fallen leaves on another bed, in which different varieties of the Rhododendron grew, only 17 were narrower towards the base than towards the apex. My son William, who first called my attention to this case, picked up 237 fallen leaves in his garden (where the Rhododendron grows in the natural soil) and of these 65 per cent. could have been drawn by worms into their burrows more easily by the base or foot-stalk than by the tip; and this was partly due to the shape of the leaf and in a less degree to the curling in of the margins: 27 per cent. could have been drawn in more easily by the tip than by the base: and 8 per cent. with about equal ease by either end. The shape of a fallen leaf ought to be judged of before one end has been drawn into a burrow, for after this has happened, the free end, whether it be the base or apex, will dry more quickly than the end imbedded in the damp ground; and the exposed margins of the free end will consequently tend to become more curled inwards than they were when the leaf was first seized by the worm. My son found 91 leaves which had been dragged by worms into their burrows, though not to a great depth; of these 66 per cent. had been drawn in by the base or foot-stalk; and 34 per cent. by the tip. In this case, therefore, the worms judged with a considerable degree of correctness how best to draw the withered leaves of this foreign plant into their burrows; notwithstanding that they had to depart from their usual habit of avoiding the foot-stalk.

On the gravel-walks in my garden a very large number of leaves of three species of Pinus (P. austriaca, nigricans and sylvestris) are regularly drawn into the mouths of worm burrows. These leaves consist of two so-called needles, which are of considerable length in the two first and short in the last named species, and are united to a common base; and it is by this part that they are almost invariably drawn into the burrows. I have seen only two or at most three exceptions to this rule with worms in a state of nature. As the sharply pointed needles diverge a little, and as several leaves are drawn into the same burrow, each tuft forms a perfect chevaux de frise. On two occasions many of these tufts were pulled up in the evening, but by the following morning fresh leaves had been pulled in, and the burrows were again well protected. These leaves could not be dragged into the burrows to any depth, except by their bases, as a worm cannot seize hold of the two needles at the same time, and if one alone were seized by the apex, the other would be pressed against the ground and would resist the entry of the seized one. This was manifest in the above mentioned two or three exceptional cases. In order, therefore, that worms should do their work well, they must drag pine-leaves into their burrows by their bases, where the two needles are conjoined. But how they are guided in this work is a perplexing question.

This difficulty led my son Francis and myself to observe worms in confinement during several nights by the aid of a dim light, while they dragged the leaves of the above named pines into their burrows. They moved the anterior extremities of their bodies about the leaves, and on several occasions when they touched the sharp end of a needle they withdrew suddenly as if pricked. But I doubt whether they were hurt, for they are indifferent to very sharp objects, and will swallow even rose-thorns and small splinters of glass. It may also be doubted, whether the sharp ends of the needles serve to tell them that this is the wrong end to seize; for the points were cut off many leaves for a length of about one inch, and fifty-seven of them thus treated were drawn into the burrows by their bases, and not one by the cut-off ends. The worms in confinement often seized the needles near the middle and drew them towards the mouths of their burrows; and one worm tried in a senseless manner to drag them into the burrow by bending them. They sometimes collected many more leaves over the mouths of their burrows (as in the case formerly mentioned of lime-leaves) than could enter them. On other occasions, however, they behaved very differently; for as soon as they touched the base of a pine-leaf, this was seized, being sometimes completely engulfed in their mouths, or a point very near the base was seized, and the leaf was then quickly dragged or rather jerked into their burrows. It appeared both to my son and myself as if the worms instantly perceived as soon as they had seized a leaf in the proper manner. Nine such cases were observed, but in one of them the worm failed to drag the leaf into its burrow, as it was entangled by other leaves lying near. In another case a leaf stood nearly upright with the points of the needles partly inserted into a burrow, but how placed there was not seen; and then the worm reared itself up and seized the base, which was dragged into the mouth of the burrow by bowing the whole leaf. On the other hand, after a worm had seized the base of a leaf, this was on two occasions relinquished from some unknown motive.

As already remarked, the habit of plugging up the mouths of the burrows with various objects, is no doubt instinctive in worms; and a very young one, born in one of my pots, dragged for some little distance a Scotch-fir leaf, one needle of which was as long and almost as thick as its own body. No species of pine is endemic in this part of England, it is therefore incredible that the proper manner of dragging pine-leaves into the burrows can be instinctive with our worms. But as the worms on which the above observations were made, were dug up beneath or near some pines, which had been planted there about forty years, it was desirable to prove that their actions were not instinctive. Accordingly, pine-leaves were scattered on the ground in places far removed from any pine-tree, and 90 of them were drawn into the burrows by their bases. Only two were drawn in by the tips of the needles, and these were not real exceptions, as one was drawn in for a very short distance, and the two needles of the other cohered. Other pine-leaves were given to worms kept in pots in a warm room, and here the result was different; for out of 42 leaves drawn into the burrows, no less than 16 were drawn in by the tips of the needles. These worms, however, worked in a careless or slovenly manner; for the leaves were often drawn in to only a small depth; sometimes they were merely heaped over the mouths of the burrows, and sometimes none were drawn in. I believe that this carelessness may be accounted for either by the warmth of the air, or by its dampness, as the pots were covered by glass plates; the worms consequently did not care about plugging up their holes effectually. Pots tenanted by worms and covered with a net which allowed the free entrance of air, were left out of doors for several nights, and now 72 leaves were all properly drawn in by their bases.

It might perhaps be inferred from the facts as yet given, that worms somehow gain a general notion of the shape or structure of pine-leaves, and perceive that it is necessary for them to seize the base where the two needles are conjoined. But the following cases make this more than doubtful. The tips of a large number of needles of P. austriaca were cemented together with shell-lac dissolved in alcohol, and were kept for some days, until, as I believe, all odour or taste had been lost; and they were then scattered on the ground where no pine-trees grew, near burrows from which the plugging had been removed. Such leaves could have been drawn into the burrows with equal ease by either end; and judging from analogy and more especially from the case presently to be given of the petioles of Clematis montana, I expected that the apex would have been preferred. But the result was that out of 121 leaves with the tips cemented, which were drawn into burrows, 108 were drawn in by their bases, and only 13 by their tips. Thinking that the worms might possibly perceive and dislike the smell or taste of the shell-lac, though this was very improbable, especially after the leaves had been left out during several nights, the tips of the needles of many leaves were tied together with fine thread. Of leaves thus treated 150 were drawn into burrows—123 by the base and 27 by the tied tips; so that between four and five times as many were drawn in by the base as by the tip. It is possible that the short cut-off ends of the thread with which they were tied, may have tempted the worms to drag in a larger proportional number by the tips than when cement was used. Of the leaves with tied and cemented tips taken together (271 in number) 85 per cent. were drawn in by the base and 15 per cent. by the tips. We may therefore infer that it is not the divergence of the two needles which leads worms in a state of nature almost invariably to drag pine-leaves into their burrows by the base. Nor can it be the sharpness of the points of the needles which determines them; for, as we have seen, many leaves with the points cut off were drawn in by their bases. We are thus led to conclude, that with pine-leaves there must be something attractive to worms in the base, notwithstanding that few ordinary leaves are drawn in by the base or foot-stalk.

Petioles.—We will now turn to the petioles or foot-stalks of compound leaves, after the leaflets have fallen off. Those from Clematis montana, which grew over a verandah, were dragged early in January in large numbers into the burrows on an adjoining gravel-walk, lawn, and flower-bed. These petioles vary from 2½ to 4½ inches in length, are rigid and of nearly uniform thickness, except close to the base where they thicken rather abruptly, being here about twice as thick as in any other part. The apex is somewhat pointed, but soon withers and is then easily broken off. Of these petioles, 314 were pulled out of burrows in the above specified sites; and it was found that 76 per cent. had been drawn in by their tips, and 24 per cent by their bases; so that those drawn in by the tip were a little more than thrice as many as those drawn in by the base. Some of those extracted from the well-beaten gravel-walk were kept separate from the others; and of these (59 in number) nearly five times as many had been drawn in by the tip as by the base; whereas of those extracted from the lawn and flower-bed, where from the soil yielding more easily, less care would be necessary in plugging up the burrows, the proportion of those drawn in by the tip (130) to those drawn in by the base (48) was rather less than three to one. That these petioles had been dragged into the burrows for plugging them up, and not for food, was manifest, as neither end, as far as I could see, had been gnawed. As several petioles are used to plug up the same burrow, in one case as many as 10, and in another case as many as 15, the worms may perhaps at first draw in a few by the thicker end so as to save labour; but afterwards a large majority are drawn in by the pointed end, in order to plug up the hole securely.

The fallen petioles of our native ash-tree were next observed, and the rule with most objects, viz., that a large majority are dragged into the burrows by the more pointed end, had not here been followed; and this fact much surprised me at first. These petioles vary in length from 5 to 8½ inches; they are thick and fleshy towards the base, whence they taper gently towards the apex, which is a little enlarged and truncated where the terminal leaflet had been originally attached. Under some ash-trees growing in a grass-field, 229 petioles were pulled out of worm burrows early in January, and of these 51.5 per cent. had been drawn in by the base, and 48.5 per cent. by the apex. This anomaly was however readily explained as soon as the thick basal part was examined; for in 78 out of 103 petioles, this part had been gnawed by worms, just above the horse-shoe shaped articulation. In most cases there could be no mistake about the gnawing; for ungnawed petioles which were examined after being exposed to the weather for eight additional weeks had not become more disintegrated or decayed near the base than elsewhere. It is thus evident that the thick basal end of the petiole is drawn in not solely for the sake of plugging up the mouths of the burrows, but as food. Even the narrow truncated tips of some few petioles had been gnawed; and this was the case in 6 out of 37 which were examined for this purpose. Worms, after having drawn in and gnawed the basal end, often push the petioles out of their burrows; and then drag in fresh ones, either by the base for food, or by the apex for plugging up the mouth more effectually. Thus, out of 37 petioles inserted by their tips, 5 had been previously drawn in by the base, for this part had been gnawed. Again, I collected a handful of petioles lying loose on the ground close to some plugged-up burrows, where the surface was thickly strewed with other petioles which apparently had never been touched by worms; and 14 out of 47 (i.e. nearly one-third), after having had their bases gnawed had been pushed out of the burrows and were now lying on the ground. From these several facts we may conclude that worms draw in some petioles of the ash by the base to serve as food, and others by the tip to plug up the mouths of their burrows in the most efficient manner.

The petioles of Robinia pseudo-acacia vary from 4 or 5 to nearly 12 inches in length; they are thick close to the base before the softer parts have rotted off, and taper much towards the upper end. They are so flexible that I have seen some few doubled up and thus drawn into the burrows of worms. Unfortunately these petioles were not examined until February, by which time the softer parts had completely rotted off, so that it was impossible to ascertain whether worms had gnawed the bases, though this is in itself probable. Out of 121 petioles extracted from burrows early in February, 68 were imbedded by the base, and 53 by the apex. On February 5 all the petioles which had been drawn into the burrows beneath a Robinia, were pulled up; and after an interval of eleven days, 35 petioles had been again dragged in, 19 by the base, and 16 by the apex. Taking these two lots together, 56 per cent. were drawn in by the base, and 44 per cent. by the apex. As all the softer parts had long ago rotted off, we may feel sure, especially in the latter case, that none had been drawn in as food. At this season, therefore, worms drag these petioles into their burrows indifferently by either end, a slight preference being given to the base. This latter fact may be accounted for by the difficulty of plugging up a burrow with objects so extremely thin as are the upper ends. In support of this view, it may be stated that out of the 16 petioles which had been drawn in by their upper ends, the more attenuated terminal portion of 7 had been previously broken off by some accident.

Triangles of paper.—Elongated triangles were cut out of moderately stiff writing-paper, which was rubbed with raw fat on both sides, so as to prevent their becoming excessively limp when exposed at night to rain and dew. The sides of all the triangles were three inches in length, with the bases of 120 one inch, and of the other 183 half an inch in length. These latter triangles were very narrow or much acuminated. [79] As a check on the observations presently to be given, similar triangles in a damp state were seized by a very narrow pair of pincers at different points and at all inclinations with reference to the margins, and were then drawn into a short tube of the diameter of a worm-burrow. If seized by the apex, the triangle was drawn straight into the tube, with its margins infolded; if seized at some little distance from the apex, for instance at half an inch, this much was doubled back within the tube. So it was with the base and basal angles, though in this case the triangles offered, as might have been expected, much more resistance to being drawn in. If seized near the middle the triangle was doubled up, with the apex and base left sticking out of the tube. As the sides of the triangles were three inches in length, the result of their being drawn into a tube or into a burrow in different ways, may be conveniently divided into three groups: those drawn in by the apex or within an inch of it; those drawn in by the base or within an inch of it; and those drawn in by any point in the middle inch.