[page 65]

Ichnos. v. 1, p. 65-71, 1990

An International Journal for Plant and Animal Traces

History of Ichnology

Darwin on worms: the advent of experimental neoichnology

S. George Pemberton' and Robert W. Frey

¹Department of Geology, University of Alberta, Edmonton, Alberta T6G 2E3, Canada

²Department of Geology, University of Georgia, Athens, Georgia 30602, USA

INTRODUCTION

On the last page of Charles Darwin's last book he noted that: "The plough is one of the most ancient and valuable of man's inventions; but long before he existed the land was in fact regularly ploughed, and still continues to be thus ploughed by earthworms. It may be doubted whether there are many other animals which have played so important a part in the history of the world, as have these lowly organized creatures" (Darwin, 1881, p. 313).

The subject of that book was of course the effects on soil by burrowing activities of earthworms. Darwin's famous "worm book"—written in his last years (Fig. 1)—has been viewed more or less as a curiosity ever since it was published in 1881. Although it sold faster than "Origin of the Species", amounting to 6,000 copies in its first year and more than 13,000 before the turn of the century, it has since been virtually ignored.

During this century, four major Darwin centennials have been observed: his birth (1909), publication of "Origin of the Species" (1958), publication of "The Descent of Man" (1971), and his death (1982). Comments and references on commemorative literature from the first three centennials were offered by Churchill (1982). The last commemorative, and by far the largest, was held in 1982 on the occasion of the centennial of Darwin's death. Wassersug and Rose (1984) reported that more than 70 publications of collected essays (encompassing more than 800 separate titles), as well as more than a hundred symposia, lecture series, special museum exhibits, and miscellaneous other events were dedicated to the Darwin Centennial in 1982. Of these, a single essay, by Gould (1982), was devoted exclusively to the "worm book". In typical Gould fashion, he presented a lucid, thought-provoking essay on the duality of Darwin's last book.

Fig. 1. The last photograph of Charles Darwin, taken just prior to his death.

Not only is it an explicit treatise on worms but it also is a dramatic example of the underlying theme in most of Darwin's work—that given enough time, the accumulation of small events will produce a significant change.

Of more direct interest here, a symposium on earthworm ecology, celebrating the centenary of publication of the "worm book", was held at Grange-over-Sands, England, in 1981. The resulting book (Satchell, 1983) contains two contributions (Ghilarov, 1983; Graff,

Photocopying permitted by license only Reprints available directly from the publisher

© 1990 Harwood Academic Publishers Inc. Printed in the United States of America

[page] 66 Pemberton and Frey

1983) that analyze the historical impact of the "worm book" on the development of ecology and soil science. Many of the other 39 articles in the book refer to aspects of earthworm ecology that were touched on by Darwin.

DARWIN AND WORMS

Darwin's fascination with earthworms can be traced back to September 1837, when his uncle and soon to be father-in-law, Josiah Wedgwood, commented on the amount of soil brought up by worms on the lawn at his home, Maer Hall, in Staffordshire (Huxley and Kettlewell, 1965). By November 1837, Darwin had read a paper "On the formation of mould" before the Geological Society in which he commented on his observations on three pastures. Darwin concluded that surface objects were being buried by the generation of worm castings that were continually brought to the surface, resulting in a layer of mold or soil. This paper was actually published twice (Darwin, 1838, 1840), although the two drafts are not identical. The first was merely a report on Darwin's lecture, evidently written by someone else. The second was written by Darwin himself and contains additional material (Barrett, 1977). Two further short contributions followed (Darwin, 1844, 1869); the first corrected some mistakes in the 1840 paper, and the second was a reply to negative comments made by a Mr. D. T Fish (1869) who doubted that worms, because of their small size, could do what Darwin claimed they could. Such statements merely strengthened Darwin's resolve that the "whole operation is due to the digestive process of the common earthworm" (Darwin, 1840, p. 507).

From this humble start Darwin set out a rigorous program to document fully the activities of earthworms, which culminated in publication of the "worm book" in 1881. The subject, therefore, occupied him for some 44 years (Fig. 2). During this time interval, Darwin laid the foundations for the book by observing, devising experiments, and rallying his legion of amateur naturalists to send him notes on the distribution and habits of earthworms. During later phases of this work he became so engrossed in the subject that in a letter to a colleague, H. Johnson, dated November 14, 1880, he wrote "My heart and soul care for worms and nothing else in the world just at present" (DeBeer, 1968, p. 74).

The "worm book", like many of Darwin's lesser known botanical volumes (i.e., Darwin, 1875, 1876, 1877, 1880), is based on a firm foundation of experimentation. Huxley and Kettlewell (1965, p. 122) concluded that "Darwin is sometimes dismissed by mod-

Fig. 2. A Sambourne caricature in the October 22, 1881, issue of Punch, which appeared just after the worm book was published.

ern laboratory biologists as merely a naturalist, devoted only to the amassing of innumerable facts of observation. A naturalist he certainly was; but in his botanical studies he revealed himself as a great experimentalist, and paved the way for that combination of field study and laboratory experiment that is proving so fruitful in present-day biology". They went on to suggest that the worm book "... is also of historical importance as the first quantitative ecological study of an animal's role in nature. Indeed it may properly be claimed that through it Darwin became one of the founding fathers of ecology ..." (Huxley and Kettlewell, 1965, p. 126). This work also marks the birth of experimental neoichnology, since Darwin was able to measure bio-turbation rates accurately and to devise methodologies that are still in use today.

EXPERIMENTAL NEOICHNOLOGY

Darwin's book on worms is much more than a description of the formation of "vegetable mould" (or soil) by earthworms: it is a treatise on experimental

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neoichnology. The book can be divided into three parts; the first concerns details of the ecology, physiology, and activities of earthworms; the second deals with the effects of burrowing by earthworms on soil formation and burial of objects by those activities; and the third section deals with denudation of the land by burrowing activities of worms. What makes this work special, however, is the novel way in which Darwin set out to prove his hypothesis of 1837. In order to accomplish this task, Darwin devised numerous experiments, some of which ran for more than 30 years. He was, therefore, able to acquire quantitative data that are difficult to generate even today.

As noted by Keith (1955, p. 194), the worm book "... illustrates better than any other of his publications the persistent manner in which Darwin nursed and nourished an idea, year after year, until it reached a certain degree of maturity". Even anticipation did not shake his resolve; in the introduction to his worm book, Darwin (1881, p. 6-7) noted: "But some of my observations have been rendered almost superfluous by an admirable paper by Von Hensen; already alluded to, which appeared in 1877". However, most of Darwin's work on worms was conducted prior to 1871, and it was much more comprehensive than that by Hensen (1877).

Ecology of Worms

In order to understand fully the activities of worms, Darwin employed novel tactics: (1) he counted the number of worm tracks seen on sidewalks, (2) he observed and experimented on worms in pots that were brought into his study, (3) he made midnight excursions with his sons, on the lawn, to study the effects of light, heat, noise, vibration, and touch on worms, (4) he noted that the sound of a whistle, a bassoon, or a shout elicited no response but that a C on the bass clef, played on a piano on which a pot containing worms was placed, sent them directly into their burrows, (5) he experimented on their ability to smell by breathing on them while chewing tobacco or by placing cottonwool with a few drops of millefleurs perfume or acetic acid in his mouth before breathing on them, and (6) he tested their preference for food items by hiding different foods in pots and mixing various foodstuffs together. In all of these tests, he accurately recorded earthworm responses and was able to draw appropriate conclusions from them.

Darwin also conducted a number of experiments to determine the "mental qualities" of worms. He observed the method by which they would drag leaves into their burrows and concluded that dragging them in

tip-first was mechanically the most advantageous way to do it. He then went about replacing the leaves with a bundle of pine needles, which were dragged in base-first, again representing the most efficient way to accomplish the task. However, modified pine needles, which could have been drawn in equally well from either end, were still manipulated from the base. Further experiments with paper triangles showed that worms consistently preferred to seize them by the tips. Darwin concluded: "We may therefore infer—improbable as is the inference—that worms are able by some means to judge which is the best end by which to draw triangles of paper into their burrows" (Darwin, 1881, p. 90). From these experiments, Darwin was able to suggest that earthworm behavior is more elaborate than a set of simple reflexes (Ghiselin, 1969).

Burrows and Burrowing Mechanics

Darwin made minute observations on both the burrowing techniques employed by worms and the morphology of their burrows. He observed the excavation of burrows in varying types of sediment and under different degrees of substrate compaction. Darwin was able to conclude that although sediment was swallowed by worms during burrowing in cohesive sediment, it was not swallowed when the substrate was loose. Regarding this contrast he stated "As doubts have been expressed by some writers whether worms ever swallow earth solely for the sake of making their burrows, some additional cases may be given. A mass of fine reddish sand, 23 inches in thickness, left on the ground for nearly two years, has been penetrated in many places by worms; and their castings consisted partly of the reddish sand and partly of black earth brought up from beneath the mass. This sand had been dug up from a considerable depth, and was of so poor a nature that weeds could not grow on it. It is therefore highly improbable that it should have been swallowed by the worms as food" (Darwin, 1881, p. 100).

On the structure of the burrows, Darwin offered excellent descriptions: "The burrows run down perpendicularly, or more commonly a little obliquely. They are sometimes said to branch, but as far as I have seen this does not occur, except in recently dug ground and near the surface. They are generally, or as I believe invariably, lined with a thin layer of fine, dark coloured earth voided by the worms; so that they must at first be made a little wider than their ultimate diameter. I have seen several burrows in undisturbed sand thus lined at a depth of 4 ft. 6 in.; and others close to the surface thus lined in recently dug ground. The walls of fresh burrows are often dotted with little globular pellets of

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voided earth, still soft and viscid; and these, as it appears, are spread out on all sides by the worm as it travels up or down its burrow. . . . The lining appears also to strengthen the walls, and perhaps saves the worm's body from being scratched" (Darwin, 1881, p. 110-111).

Similarly, Darwin was able to offer plausible explanations for the functional morphology of the burrows: "The burrows which run far down into the ground, generally, or at least often, terminate in a little enlargement or chamber. Here according to Hoffmeister, one or several worms pass the winter rolled up into a ball. These chambers contained many small bits of stones and husks of the flax seeds. . . . The sole conjecture which I can form why worms line their winter-quarters with little stones and seeds, is to prevent their closely coiled up bodies from coming into close contact with the surrounding cold soil; and such contact would perhaps interfere with their respiration which is effected by the skin alone" (Darwin, 1881, p. 114-116).

Quantitative Models of Bioturbation

One of the main facets of Darwin's earthworm research concerned the constant turnover of soil by worms through the generation of castings. This activity resulted not only in the formation of "vegetable mould" or (humus) but also in the burial and undermining of large objects. Darwin's underlying theme was to show that even relatively insignificant activities of the lowly earthworm, when aggregated over a long period of time, result in a major change. In order to prove this claim, Darwin devised a number of experiments, some of which lasted for more than 30 years.

Shortly after purchasing his home, Down House, Darwin spread chalk and cinders over a field and observed the earthworms' activities. In his book, he reported "A quantity of broken chalk was spread, on December 10, 1842, over a part of a field near my house, which had existed as pasture certainly for 30, probably for twice or thrice as many years. The chalk was laid on the land for observing at some future period to what depth it would become buried. At the end of November, 1871, that is after an interval of 29 years, a trench was dug across this part of the field; and a line of white nodules could be traced on both sides of the trench, at a depth of 7 inches from the surface. The mould, therefore, (excluding the turf) had here been thrown up at an average rate of .22 inches per acre" (Darwin, 1881, p. 138-140).

In 1942, a century after Darwin spread chalk over his field, and 71 years after he found nodules at a depth of 7 inches, Sir Arthur Keith (1942) reexamined the field. He found that the objects had not undergone any more appreciable burial; he concluded "The main result is to prove that after a time chalk, cinders, or other foreign bodies; when spread on the turf, do not continue to be buried deeper and deeper by worm action, but reach a stationary level" (Keith, 1942, p. 716). This level is presumably the depth limit of earthworm bioturbation in Darwin's field. The resulting vertical profile, therefore, consisted of 7 to 8 inches of stone-free, fine-grained mold overlying a stony substratum resulting from bioturbation by worms. Darwin's earlier description of these phenomena (Darwin, 1840) is probably the first detailed account of biogenic graded bedding in the literature (Fig. 3).

Darwin was fascinated by the burial of objects by the burrowing activity of worms, and he went into great detail outlining the undermining of the Stone-henge monoliths and the burial of archaeological objects such as Roman ruins. He had a specially built "worm stone" installed in his lawn (Fig. 4); the design would allow him (and his son Horace) to measure accurately its rate of sinking.

Darwin concluded that this sinking was caused by the constant activity of earthworms voiding finegrained material on the surface in the form of castings. Once again, simple experiments were set up and monitored; for example, all worm castings were collected from square-yard gradients during a period of one year at four different sites. Based on this information, Darwin calculated that from 7.56 to 18.12 tons per acre were ejected annually by the worms. He then calculated that this material would result in the production of a layer ranging from 0.09612 to 0.1524 inches in

Fig. 3. Cross-section through a field left undisturbed for 15 years. Described and illustrated by Darwin in 1840, it represents the earliest report of biogenic graded bedding.

[page] History of Ichnology: Darwin 69

Fig. 4. The worm stone that was set into the lawn at Down House, used by Darwin and his sons to measure the rate at which the action of earthworms caused it to sink. (After Huxley and Ket-tlewell, 1965.)

thickness. Such experiments proved what Aristotle had said long ago about worms being the "intestines of the earth".

Disintegration and Denudation

The last part of the worm book (Chapters 5 and 6) deals with the mechanical and chemical breakdown of grains during the worm's digestive cycle and the process of landscape denudation through the activity of worms. Once more Darwin displayed his ability to see the geological significance of the accumulative effects of a relatively minor activity. He observed that "Worms, on the other hand, add largely to the organic matter in the soil by the astonishing number of half-decayed leaves which they draw into their burrows, to a depth of 2 or 3 inches. ... It is known that various kinds of acids are generated by the decay of vegetable matter; and from the contents of the intestines of worms, and from their castings being acid, it seems probable that the process of digestion induces analogous chemical change in the swallowed, triturated, and half-decayed leaves" (Darwin, 1881, p. 239-240).

In order to prove this contention Darwin devised another novel experiment, which was based on the fact that humic acid dissolves iron oxide. Darwin stated "Now I kept some worms in a pot filled with very fine reddish sand, consisting of minute particles of silex coated with the red oxide of iron; and the burrows, which the worms made through this sand, were lined or coated in the usual manner with their castings,

formed of the sand mingled with their intestinal secretions and the refuse of the digested leaves; and this sand had almost wholly lost its red colour. When small portions of it were placed under the microscope, most of the grains were seen to be transparent and colourless, owing to the dissolution of the oxide; whilst almost all the grains taken from other parts of the pot were coated with oxide" (Darwin, 1881, p. 240-241).

In addition to chemical disintegration, Darwin concluded that sediment grains were also mechanically degraded in the gut of worms. He stated that "The trituration of small particles of stone in the gizzards of worms is of more importance under a geological point of view than may at first appear to be the case; for Mr. Sorby has clearly shown that the ordinary means of disintegration, namely, running water and the waves of the sea, act with less and less power on fragments of rock the smaller they are" (Darwin, 1881, p. 257).

Armed with this evidence, Darwin concluded that gently rolling hills would be denuded over time due to the accumulation of worm castings in the valleys. He stated "But the difficulty in believing that earth in any appreciable quantity can be removed from a gently inclined surface, covered with vegetation and matted with roots, is removed through the agency of worms. For the many castings which are thrown up during rain, and those thrown up some little time before heavy rain, flow for a short distance down an inclined surface. Moreover much of the finest levigated earth is washed completely away from the castings. During dry weather, castings often disintegrate into small rounded pellets, and these, from their weight often roll down any slope" (Darwin, 1881, p. 260-261).

In typical Darwin style he then presented data collected from numerous localities on the accumulation of worm castings downslope. For one such example, he explained "My son examined the surface of this hill to its base in a south-west direction. Beneath the great ditch, where the slope was about 24°, the mould was very thin, namely from l'/2 to 2'/2 inches; whilst near the base, where the slope was only 3° to 4°, it increased to between 8 and 9 inches in thickness. We may therefore conclude that on this artificially modified hill, as well as in the natural valleys of the neighbouring Chalk Downs, some fine earth, probably derived in large part from worm-castings, is washed down, and accumulates in the lower parts. ..." (Darwin, 1881, p. 303-304).

From these data Darwin concluded "When we behold a wide, turf-covered expanse, we should remember that its smoothness, on which so much of its beauty depends, is mainly due to the inequalities having been slowly levelled by worms. It is a marvellous reflection that the whole of the superficial mould over any such

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expanse has passed, and will again pass, every few years through the bodies of worms" (Darwin, 1881, p. 313).

CONCLUSION

Darwin's "worm book" has often been looked upon as "a harmless work of little importance by a great naturalist in his dotage" (Gould, 1982, p. 16). However, it has also been hailed as "one of the most interesting books on soil ever written" (Russell, 1937, p. 253). Based on this volume, Darwin has been praised as one of the founding fathers of ecology, invertebrate ethology, and soil science (Ghilarov, 1983). To this list we might now add neoichnology.

From an ichnological point of view, Darwin was able to: (1) describe in detail the burrows and burrowing mechanics of earthworms; (2) explain limiting factors controlling the activity of earthworms; (3) quantify their rate of bioturbation; (4) evaluate the geological, geochemical, and biological significance of the burrowing activities of earthworms; and (5) offer experimental methodologies. Obtaining quantitative data on rates of bioturbation remains one of the most difficult tasks to perform in ichnology. Tracer beds such as those used by Darwin are still being used today (Glass, 1969; Ruddiman and Glover, 1972; Guinasso and Schink, 1975; Boudreau, 1986).

Darwin's little book on worms, therefore, is a treatise on neoichnology and underscores one of the main tenets of ichnology: cumulative effects of the activities of organisms, be they worms, fiddler crabs, or boring sponges, can have a dramatic effect on the substrate!

THE WORM TURNS

I've despised you, old worm, for I think you'll admit

That you never were beautiful even in youth; I've impaled you on hooks, and not felt it abit;

But all's changed now that DARWIN has told us

the truth Of your diligent life, and endowed you with fame—

You begin to inspire me with kindly regard; I have friends of my own, clever worm, I could name,

Who have ne'er in their lives been at work half so hard.

It appears that we owe you our acres of soil, That the garden could never exist without you,

That from ages gone by you were patient in toil, Till a DARWIN revealed all the good that you do.

Now you've turned with a vengeance, and all must confess

Your behaviour should make poor humanity squirm, For there's many a man on this planet, I guess,

Who is not half so useful as you, Mister Worm!

(from Punch, October 22, 1881, p. 190)

REFERENCES

Barrett, P. H. 1977. The Collected Papers of Charles Darwin. University of Chicago Press, Chicago and London, vol. 1, 277 p., vol. 2, 326 p.

Boudreau, B. P. 1986. Mathematics of tracer mixing in sediments, 1. Spatially-dependent, diffuse mixing. American Journal of Science, 286:161-198.

Churchill, F. B. 1982. Darwin and the historian. Biological Journal of the Linnean Society, 17:45-68.

Darwin, C. 1838. On the formation of mould. Proceedings of the Geological Society, 2:574-576.

Darwin, C. 1840. On the formation of mould. Transactions of the Geological Society of London, 5:505-509.

Darwin, C. 1844. On the origin of mould. Gardener's Chronicle and Agricultural Gazette, 14:218.

Darwin, C. 1869. The formation of mould by worms. Gardener's Chronicle and Agricultural Gazette, 20:530.

Darwin, C. 1875. Insectivorous Plants. John Murray, London, 462p.

Darwin, C. 1876. The Effects of Cross and Self Fertilization in the Vegetable Kingdom. John Murray, London, 482 p.

Darwin, C. 1877. The Different Forms of Flowers on Plants of the Same Species. John Murray, London, 352 p.

Darwin, C. 1880. The Power of Movement in Plants. John Murray, London, 592 p.

Darwin, C. 1881. The Formation of Vegetable Mould, Through the Action of Worms. John Murray, London, 326 p.

DeBeer, G. 1968. The Darwin letters at Shrewsbury School. Notes and Records Royal Society of London, 23:68-85.

Fish, D. T. 1869. A chapter on worms. Gardener's Chronicle and Agricultural Gazette, 20:417-418.

Ghilarov, M. S. 1983. Darwin's "Formation of Vegetable Mould"—its philosophical basis. In Satchell, J. E. (ed.), Earthworm Ecology from Darwin to Vermiculture. Chapman and Hall, London, p. 1-4.

Ghiselin, M. T. 1969. The Triumph of the Darwinian Method. University of California Press, Berkeley and Los Angeles, 287 p.

Glass, B. P. 1969. Reworking of deep-sea sediments as indicated by the vertical dispersion of the Australasian and Ivory Coast mi-crotektite horizons. Earth and Planetary Science Letters, 6: 265-278.

Gould, S. J. 1982. The importance of trifles. Natural History, 91(4): 16-23.

Graff, O. 1983. Darwin on earthworms—the contemporary background and what the critics thought. In Satchell, J. E. (ed.), Earthworm Ecology from Darwin to Vermiculture. Chapman and Hall, London, p. 5-18.

Guinasso, N. L., Jr., and Schink, D. R. 1975. Quantitative estimates of biological mixing rates in abyssal sediments. Journal of Geophysical Research, 80: 3032-3043.

Hensen, V. 1877. Die Tatigkett des Regenwurms (L. terrestris) fur die Fruchtbarkeit des Erdbodens. Zeitschrift fur Wissenschaft, Zo-ologie, 28: 354-364.

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Huxley, J., and Kettlewell, H. B. D. 1965. Charles Darwin and His World. Viking Press, New York, 144 p.

Keith, A. 1942. A postscript to Darwin's Formation of Vegetable Mould through the Action of Worms. Nature, 149: 716-720.

Keith, A. 1955. Darwin Revalued. Watts and Company, London, 294 p.

Ruddiman, W F, and Glover, L. K. 1972. Vertical mixing of ice-rafted volcanic ash in North Atlantic sediments. Geological Society of America, Bulletin, 83:2817-2835.

Russell, E. J. 1937. Soil Conditions and Plant Growth (7th ed.). Longmans Green and Company, London, 655 p.

Satchell, J. E. (ed.) 1983. Earthworm Ecology from Darwin to Vermiculture. Chapman and Hall, London, 495 p.

Wassersug, R. J., and Rose, M. R. 1984. A reader's guide and retrospective to the 1982 Darwin Centennial. Quarterly Review of Biology, 59:417-437.