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Popular Science Monthly/Volume 73/September 1908/Modern and Early Work Upon the Question of Root Excretions



AFTER the lapse of over half a century the one-time well-known theory of De Candolle has again come into prominence. The demonstration that De Candolle was essentially correct in his deductions revives interest in a phase of plant physiology which has been comparatively unnoticed for many years. In brief, his theory was that plants excrete from their roots substances which are deleterious to continued growth. These excreted substances were believed to have a deleterious effect when absorbed from the soil by other plants belonging to the same order as the plants from which the excretions came, but according to the De Candollian theory the excretions would be harmless or even beneficial to plants belonging to a different order.

Although this theory was supported by numerous botanists and chemists of the last century, it has come to be known in the literature as "De Candolle's theory of root excretions." There is obviously a twofold reason for this: first of all, the prominence of the man himself in his own and subsequent times and, secondly, the fact that he used this theory to explain the well-known benefits of crop rotation in agriculture.

Before the work of De Candolle appeared, Brugmans had alleged that he observed drops of liquid to exude from the roots of Viola arvensis and that he had observed small fragments of material at the extremities of the roots of certain other plants which he regarded as excretions. Although his observations were made without the precautions necessary for scientific experiment, they appear to have been quite widely accepted by naturalists of the time, among them such men as von Humboldt and De Candolle. To these pioneer workers the idea that there may be noxious substances present in the soil appeared to be the most direct means of explaining many pertinent problems of plant distribution and of agriculture.

De Candolle carried his idea further and used it to explain the apparent antagonisms of certain plants and expressed his belief that they injured their neighbors by the substances exuded from their roots into the soil. He cited the case of the cockscomb, which, he said, appears to have a bad effect upon neighboring vegetation, and euphorbias, which are harmful to the growth of flax, tares to wheat, and thistles to oats.

One of De Candolle's contemporaries, Macaire-Prinsep, carried out some experiments, which for a time gave promise of firmly establishing the existence of plant (or root) excretions. Macaire-Prinsep took up a number of adolescent plants and after carefully washing their roots, placed them in vessels containing rain water. He reported that after eight days the water in which healthy specimens of Chondrilla had grown had acquired a yellow tint and a strong odor. The water had a bitter taste and gave a precipitate when added to solutions of lead acetate. The same investigator also reported that water containing the excretions from the roots of peas was fatal to other plants of the same species, but not to wheat plants.

Using these ideas and experiments as a basis, De Candolle formulated a theory to account for the well-known benefits of crop rotation. He expressed a belief that the harmful effects observed when the soil is continuously cropped with the same species are due to an accumulation of noxious excretions. According to his theory, the substances excreted by the roots of one order of plants were not usually harmful to the roots of plants belonging to other natural orders; in fact, they might be slightly beneficial. In support of this idea he cited the incontrovertible observation of every husbandman that in the majority of cases good yields of all crops are obtained from the soil when plants belonging to different natural orders are grown in succession.

De Candolle pointed out that there exist, in a state of nature, natural successions of forest trees in the course of which a given species of tree is completely replaced by another species. According to his observations the first species seemed to disappear because its excretions so filled the soil as to render it unsuitable for the longer growth of that species. It is interesting to note in passing that he published an article in the Revue française showing the harm wrought by the decree of Louis XIV. that forests should be perpetually maintained upon forested lands.

De Candolle also made the trenchant observation that when shade trees die from any cause it is very difficult to replace them with trees of the same species.

Using these observations as a foundation, he built up a theory that plants may injure each other by the matter excreted from their roots, and that the success of crop rotation lies in preventing an undue accumulation of excreted material in the soil. He went further and expressed his belief that the excretory matter of the plants of certain families, like the legumes, is not only feebly toxic to themselves, but possesses actual value as a fertilizer for the cereals.

The ideas and observations of De Candolle were not allowed to pass unchallenged, for within a few years controversial articles began to appear.

Unger, and his pupil, Walser, showed that there had been certain flaw? in the work of Macaire-Prinsep and made objections to his results. Walser believed that, if Macaire's statements were correct, it would be possible to demonstrate the presence of organic material in the soil similar in composition to that existing within the plants which had grown upon it. Braconnot, making the same assumption, attempted to demonstrate the existence of opium-like bodies by washing the soil on which plants of the poppy family had been grown for several years. He obtained a solution of inorganic compounds, and, in addition, only traces of organic compounds, and concluded that "If organic excretions really take place in the natural state of the plant, they are, as yet, so obscure and so little known as to justify the assumption that some other explanation must be given for the general system of rotation." Working without the proper idea of the difficulties of such a task and without adequate knowledge of the organic compounds in the soil, it is little wonder that they failed to demonstrate the presence of compounds in the soil which might be regarded as excretory matter from plants. They deserve credit, however, for showing that Brugmans had entirely misinterpreted the death of the root-hairs and the decortication of the growing roots and had assumed that this material was solid excretory matter from the living root.

One of the most scientific attempts to study this question appears to have been made by Alfred Clyde, the results of whose work were published in 1846 in the Transactions of the Highland and Agricultural Society of Scotland, and which won for the author a premium of twenty sovereigns. His modus operandi was to raise plants in pots of garden soil, sand, moss or charcoal; to remove them at different times; carefully wash their roots free from all adherent material and place the root systems in vessels of distilled water. After a certain length of time had elapsed, the composition of the water in the various vessels was studied.

Mr. Gyde reported that the roots imparted to the water soluble substances, to be regarded as excretory material, and that these excretions seemed to be yielded in greater abundance by plants having coarse roots like beans than by those which had finer roots, like wheat. In some instances the water acquired an odor which was separable on the application of heat and could be distilled over when the water was placed in a retort. Plants like the bean and cabbage imparted an odor to the water similar to that which characterizes their leaves. Plants when in bloom were observed to emit more excretory material than when young or when ripening their seed; but in any case the amount of excretion obtained after evaporating the water was very small. When this small amount of organic matter was reapplied to the soil in which other plants were growing, no harmful effects were observed. Without appreciating the additional factors which would have to be considered in such an experiment, e. g., absorptive power of the soil, action of microorganisms, oxidation, etc., Mr. Gyde concluded that the excretions of plants are not harmful to their kind, but that the necessity for a rotation of crops arises from the depletion of the soil of the mineral plant food constituents. He thus appears to turn, mirabile dictu, from a proposition which was partially proved to one for which he had no proof; neither has conclusive proof been afforded by any subsequent investigator.

Professor Johnson in "How Crops Grow" has justly remarked that Mr. Gyde's results are not to be regarded as conclusive proofs for or against the existence of root excretions.

The curiously regular growth of fungi in continually widening circles, known as "fairy rings," presents many questions of scientific interest and it is not surprising to find that the theory of deleterious excretions was called in to explain this phenomenon. If one assumes that harmful excretions are left in the soil by these plants, it is easy to understand how the new and thrifty growth would continually arise on the outer edge of the ring, and thus give rise to the phenomenon observed.

The subject of "fairy rings" appears to have been studied by Way, who admitted, in a paper published in 1847, "that by far the most scientific and intelligent solution of the question is that which was based upon De Candolle's theory of the excretions of plants." But on account of objections which appeared insuperable to him, he was unable to accept it as a final satisfactory explanation.

In connection with the decadence of the De Candollian theory, special mention must be made of Liebig and of his attitude toward the question. At first he pronounced this theory of crop rotation to be the only one "resting on a firm basis." He regarded the experiment of Macaire-Prinsep as positive proof that the roots, probably of all plants, expel substances which can not be utilized in metabolism.

In addition to his extensive investigations upon the chemistry of the soil, Liebig made numerous studies upon the chemistry of the ash constituents of plants. He found that the essential elements were present in the ash of all plants, in quantities which formed a more or less definite ratio for a given plant. Reasoning from these facts, Liebig developed the idea that each plant requires a certain ratio of mineral constituents in the soil, as well as a certain minimum amount. He held firmly to the idea that plants could no more attain their maximum growth in the absence of a proper ratio of these mineral nutrients than when the total quantity was too small. This theory became known as Liebig' theory of mineral requirements.

Liebig's explanation of the benefits of crop rotation followed as a corollary to his theory of mineral requirements; since plants take their essential constituents in such established ratios they must in time destroy the necessary ratio of these elements in the soil, but when another plant drawing its ash constituents in a different ratio is substituted, it obtains a sufficient supply of nutrients and the soil is thus relieved of exhaustion.

Under the domination of Liebig's theory of mineral requirements, the theory of De Candolle was practically abandoned. Subsequent to his time the mineral matter of both soil and plant claimed paramount attention, and the biological factors connected with soil problems were almost entirely neglected. Unscientific as it now appears, it must be admitted that for several decades Liebig's dictum had more weight than any amount of experimental evidence. It would even appear that his word has been regarded so infallible in certain quarters that further scientific research has been regarded as unnecessary.

The inadequacy of the theory of mineral requirements alone to explain the productivity of soils has been aptly set forth by Coleman in an essay "On the Causes of Fertility or Barrenness of Soils," presented to the Royal Agricultural Society of England. This essay, although written fifty years ago, expresses the status of the problems of the mineral requirements theory as well now as at the time it was written. He says:

The causes which operate in producing the fertility or barrenness of soils have hitherto to a great extent been shrouded in mystery, not from any want of study, but owing to the difficulties which meet the inquirer at every step, and the fact that most important results frequently depend upon causes which have eluded the search of the experimenter. The science of chemistry it was hoped would afford the key wherewith to unlock the mysteries of nature, but though its discoveries have conferred much practical benefit on the agriculturist, it has up to a very recent period effected comparatively little toward settling the causes of fertility or sterility. The theories of scientific men led us to expect that fertility depended upon the presence of certain mineral substances which were found invariably present in the ashes of plants, and the analysis of a soil it was believed would confirm the practical experience of the farmer; these hopes have been falsified except in the few cases of almost simple soils, such as pure clays and sands. In all other instances the analysis presented the existence in varying proportions of those substances supposed to induce fertility equally in the barren as the fertile soil. The proportion of the various ingredients was next proposed as a sign of quality, but researches into the amount of inorganic matter abstracted by each crop have demonstrated that soils of a mixed character contain abundant supplies of mineral food for numerous crops.

From the time of Liebig and the establishment of his theory of the mineral requirements of plants, there appears to have been no serious discussion of the subject of root excretion until recent years. The reports of the Woburn Experimental Fruit Farm of the Royal Agricultural Society of England for the past few years contain a series of significant articles by the Duke of Bedford and Dr. Pickering upon the mutual effect of plants upon each other. These authors observed that the growth of young apple and pear trees was severely retarded when grass was allowed to grow about their roots. The harmful effects were much more pronounced in the case of grass than in the case of weeds. Young trees planted in a pasture, with all the sod replaced around them, died during the first season, but when a small circle of sod was permanently removed, they lived. The first supposition was that the injury was due to the removal of plant nutrients, and experiments were accordingly inaugurated to ascertain whether this was the case, but all the experiments answered the question in the negative. Experiments were also conducted to determine whether the removal of water by the grass was the cause of the injury, but again a negative answer was obtained. The results of other experiments showed that the injury could not be ascribed to the presence of an excessive amount of carbon dioxide, or to the lack of oxygen, since the characteristic injury was only observed when grass was growing around the tree roots. The authors finally concluded that the injurious effect of the grass could be due only to some action on the tree roots akin to that of direct poisoning, leaving the question open as to whether this action is due to excretions from the grass or to the changed bacterial action in the soil induced by the presence of grass.

Jones and Morse, of the Vermont Agricultural Experiment Station, have reported observations which indicate that a somewhat similar antagonism exists between butternut trees and the shrubby cinquefoil. They found that the cinquefoil, which grows abundantly in certain localities, was not found under or around butternut trees on a circle fully twice the diameter of the tree-top. Their observations showed that the "dead line" for the cinquefoil is pushed outward year by year as the butternut tree expands, so that the trees may be surrounded by a circle of dead and dying cinquefoil plants bordering the clean grass plot under the tree. Upon closer examination the roots of dead and dying cinquefoil plants were found always to be in close proximity to. those of the butternut trees. That the injury was not due to shade or the removal of water is very improbable, since other species of deciduous trees in the same locality were closely surrounded by cinquefoil plants.

The antagonistic effect of roots is also shown by an instructive experiment recently published by Hunt and Gates in a bulletin of the Cornell Agricultural Experiment Station: Rectangular boxes of soil were planted with corn in one end and with common weeds in the opposite end. Where the roots of the two kinds of plants were allowed to intermingle, the corn made less growth than where a partition in the middle of the boxes kept the roots of the weeds separate from those of the corn. When the partition was present, each sort of plant was confined to half the soil in the box, but, where lacking, one sort of roots appeared to exercise a noxious influence upon the other.

In studying the general question of soil fertility, the laboratories of the Bureau of Soils in the United States Department of Agriculture have obtained some instructive evidence bearing upon this problem of plant excretions. The data obtained from different lines of experimentation all go to prove the truth of the general assumption that plants do excrete substances which may have a toxic action on the species of plants producing them.

The Bureau of Soils has recently published the outcome of some experiments in which several sets of wheat plants were grown in rapid succession on the same soil. The soil was kept in pots and each set of wheat plants was smaller than the one immediately preceding, as might have been predicted, since it is well known that the continuous culture of a given crop on a soil "exhausts" it more rapidly than the culture of diversified crops. In the experiments cited, the growth of the fourth set of plants was in some cases only 30 per cent, of the growth of the first set.

Such cases of apparent exhaustion have generally been assumed to be due to the removal of plant nutrients from the soil by previous crops. Accordingly, experiments were made in which mineral plant nutrients in the form of pure chemicals were added to the soil at the time of planting the successive crops in amounts equal or greater than those removed by the preceding crop. The addition of these supplies of plant food constituents failed, however, to produce a growth of plants equal to the first crop, although they helped the growth of the plants. This possibility of soil exhaustion is still further rendered improbable by the fact that the wheat plants grew only three weeks and during that time they derived much of their food supply from the reserve nutrients stored in the seed; hence the amounts taken from the soil were very small.

To emphasize the action of root excretions upon the soil, experiments were made in which the first set of wheat plants was allowed to grow for only five days, or until the plumules were just beginning to appear above the surface of the soil in the pots, a length of time obviously insufficient to "exhaust" the soil. All the plants were carefully removed and the soil again planted with wheat, simultaneously with the same number of pots of fresh soil. The plants following the five-day crop made only 80 per cent, of the growth of the plants in fresh soil.

The outcome of these experiments is quite strong proof that the cause of these decreased yields is not the depletion of mineral nutrients, but lies rather in the production of unfavorable soil conditions by the excretion of substances from the roots of preceding crops of plants.

The effect of root excretions is strikingly shown by some experiments in which wheat was grown in pure quartz sand. The sand contained a very insignificant amount of plant nutrients, but the young wheat seedlings were able to draw sufficient nourishment from the seed to maintain growth during the time of the experiment. Pots of fresh quartz sand were planted with wheat simultaneously with an equal number of pots containing quartz sand which had previously grown wheat for twenty-one days. The growth of the wheat in the "exhausted" sand was only about 45 per cent, of that in the fresh sand, in spite of the fact that both sets of plants were supplied with nutrients from the seeds. It would be obviously incorrect to ascribe the "exhaustion" of the sand to a depletion of plant nutrients at the outset. The harmful effects following a previous crop appear to be more probably due to the presence of deleterious substances arising in the sand during the growth of that crop.

Evidence from another experiment showed that the roots leave substances in the soil which may be removed by proper treatment. Three crops of wheat seedlings were grown in pots and showed decreasing yields. When the last crop was removed, an aqueous extract of the soil was prepared and used as a nutrient solution in which a fourth set of wheat plants was grown. A portion of the soil extract was shaken with carbon black, which acts as a strong absorbing agent, and filtered free from carbon black at the end of a half hour. When a soil extract possessing deleterious properties is given this treatment with an absorbing agent, it is almost invariably improved, on account of the removal of the harmful substances. In this "exhausted" soil the same results of the carbon black treatment were noticed as in the case of deleterious soil extracts. The extract of the "exhausted" soil produced as good plants, after treatment with carbon black, as the extract of fresh soil treated in the same way.

The antagonistic action of one plant upon another was shown by the harmful effect of trees upon wheat. Small trees were transplanted into paraffine wire pots and kept growing in a greenhouse where optimum conditions of light and moisture could be obtained. Wheat was also planted in each pot and allowed to grow about three weeks. As soon as the first set of wheat plants had been cut and weighed, a second set was planted and this was repeated at intervals of about three weeks, until nine successive crops had been grown, always growing control crops in pots without trees. The growth of the wheat in the pots containing trees was poorer than the controls during the summer while the trees were actively growing, "but when autumn came and the trees entered their resting period, the growth of wheat in the pots became better. It does not seem possible that the harmful effects of the trees could have been due to the removal of plant food; if so, there would have been no increase in the yield in autumn. It seems, therefore, that the presence of the roots must have had some other effect upon the growth of the wheat, as the size of the pots made it necessary for the two kinds of roots to be in close physical relation. That the retarding effect is due to substances excreted by the tree roots seems probable. It was also noted that tree pots that produced as much wheat growth in November as the controls were the ones in which the trees showed the earliest signs of winter rest. These results seem to be conclusive, therefore, in showing that the injurious effect of the trees was due to the excretion of toxic substances from the roots.

These experiments, which may be regarded as furnishing negative evidence upon the problem, were supplemented by others which furnish more direct and conclusive evidence of a positive sort. By taking advantage of the chemotropic sensitiveness of the roots of seedlings, it is possible to employ them as indicators of the presence of their own harmful excretions. It is well known that roots, like other perceptive organs, will curve and grow towards substances possessing beneficial properties, but will curve away from other bodies possessing deleterious properties. Advantage was taken of this reaction to chemical stimuli for showing the presence of deleterious excretions.

Without going into lengthy details of the experiments in this place, it may be said that the method consisted essentially in growing roots in small glass tubes, from which they might escape at suitable openings if any stimulus caused them to turn aside from their normal downward course of growth. In this case there was a stimulus, and it was the deleterious matter excreted from the roots during growth. It was unmistakably shown that the growing roots of healthy plants do excrete deleterious substances in amounts sufficient to exercise an influence upon plant growth. It was shown that roots of wheat are indifferent to substances excreted by plants of another sort, like maize or cowpeas. The excretions from roots of a more closely related plant, like oats, were not as harmful to wheat as excretions from wheat, but more harmful than excretions from the more distantly related plants.

Eecent work in the laboratories of the Bureau of Soils has resulted in obtaining organic compounds from "wheat-sick" and "cowpeasick" soils. At the late meeting of the American Association for the Advancement of Science, held in Chicago, Schreiner and Sullivan reported the results of this work.

Wheat seedlings were grown continuously upon a soil until it became "wheat-sick," and its productiveness for wheat was quite small. This soil when carefully distilled yielded a small quantity of a line organic compound which, when dissolved in pure water, exhibited a toxic action upon wheat plants, but was relatively harmless to cow-peas. Crystals were similarly obtained from a "cowpea-sick" soil and were found to be harmful to cowpeas, but relatively harmless to wheat plants. Since the same soil in which neither plant was grown yielded none of these substances, it seems only logical to conclude that these substances were formed as a result of the plant growth in that soil.

Data like those briefly presented above have given strong proof of the existence of excretions from the roots of plants, and show that they may exert a harmful effect upon the growth of succeeding crops of the same kind. Without too liberally interpreting these facts, it may be said that the demonstration of root excretions throws a new light upon the interrelation of soils and plants and promises to afford a solution to some important questions. De Candolle and his contemporaries failed to appreciate the agencies in the soil which effect the destruction of deleterious organic substances, and maintained that, once a crop had been grown, the soil would for a long time be unsuitable to that crop. When the majority of soils are kept in what is ordinarily known as "good tilth" by cultivation and continued rotation of crops, it is improbable that root excretions will accumulate to an extent which would be harmful. Processes of oxidation, brought about by proper cultivation, the oxidizing power of roots, and the action of microorganisms in the soil are important factors in destroying these deleterious substances. It has also been shown that substances ordinarily employed as fertilizers have a destructive action upon toxic substances, especially when aided by the action of plant roots.

It is more than probable that the consideration of the existence of root excretions will also throw considerable light upon the problem of association and migration of species and individuals in the vegetable kingdom. The reasons for the association of certain species in nature have often been studied, but never satisfactorily explained. The same applies to questions of migration and natural succession. It has been shown that such physical factors as light and water play important parts, but they have not been found sufficient to give a satisfactory explanation for all the phenomena.

It would seem that the methods of soil fertility investigations might be applied with profit to the study of plant ecology. The effect of the root excretions from one species upon another might in certain cases prove to be the controlling factor in association. From the evidence already at hand, it would seem that the biological factors play a definite and considerable role in these phenomena.