Charles Darwin's Observations on the Behaviour of Earthworms and the Evolutionary History of a Giant Endemic Species from Germany, Lumbricus Badensis (Oligochaeta: Lumbricidae)
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Hindawi Publishing Corporation Applied and Environmental Soil Science Volume 2010, Article ID 823047, 11 pages doi:10.1155/2010/823047 Review Article Charles Darwin’s Observations on the Behaviour of Earthworms and the Evolutionary History of a Giant Endemic Species from Germany, Lumbricus badensis (Oligochaeta: Lumbricidae) U. Kutschera1 and J. M. Elliott2 1 Institute of Biology, University of Kassel, Heinrich-Plett-Straße 40, D-34109 Kassel, Germany 2 Freshwater Biological Association, The Ferry Landing, Ambleside, Cumbria LA 22 0LP, UK Correspondence should be addressed to U. Kutschera, [email protected] Received 3 June 2009; Accepted 1 December 2009 Academic Editor: Mart´ın Gerardo Rodr´ıguez Copyright © 2010 U. Kutschera and J. M. Elliott. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The British naturalist Charles Darwin (1809–1882) began and ended his almost 45-year-long career with observations, experiments, and theories related to earthworms. About six months before his death, Darwin published his book on The Formation of Vegetable Mould, through the Actions of Worms, With Observations on their Habits (1881). Here we describe the origin, content, and impact of Darwin’s last publication on earthworms (subclass Oligochaeta, family Lumbricidae) and the role of these annelids as global “ecosystem reworkers” (concept of bioturbation). In addition, we summarize our current knowledge on the reproductive behaviour of the common European species Lumbricus terrestris. In the second part of our account we describe the biology and evolution of the giant endemic species L. badensis from south western Germany with reference to the principle of niche construction. Biogeographic studies have shown that the last common ancestor of L. badensis, and the much smaller sister-taxon, the Atlantic-Mediterranean L. friendi, lived less than 10 000 years ago. Allopatric speciation occurred via geographically isolated founder populations that were separated by the river Rhine so that today two earthworm species exist in different areas. 1. Introduction which can be defined as “the biological reworking of soils and sediments by all kinds of organisms, including microbes, In his Autobiography, Charles Darwin (1809–1882) briefly rooting plants and burrowing animals” [3]. These ongoing commented on his last major publication in the following activities of different soil (or sediment) organisms, which words: “I have now (May 1, 1881) sent to the printers leads to a modification of geochemical gradients and the the MS. of a little book on The Formation of Vegetable redistribution of organic substances, can be viewed as a kind MouldthroughtheActionsofWorms. This is a subject of of “ecosystem engineering.” Moreover, it is obvious that soil but small importance; and I know not whether it will textureismodifiedanddifferent soil particles are dispersed interest any readers, but it has interested me. It is the [3]. completion of a short paper read before the Geological In this article, we review the history and current status Society more than forty years ago, and has revived old of Darwin’s “earthworm research-agenda” (Figures 1 and geological thoughts” [1, page 136]. In a foot-note on the 2), summarize the significance of his classical monograph same page, Darwin’s son Francis (1848–1925), who edited [2] with respect to modern soil biology, and describe the letters as well as other documents after his father’s death, the ecology and biogeography of a rare, endemic species, remarked that “between November 1881 and February 1884, Lumbricus badensis. The last section of our account is in 8,500 copies were sold.” Charles Darwin’s “little book” [2] part based on unpublished observations on this enigmatic later gave rise to the scientific concept of “bioturbation”, annelid. 2 Applied and Environmental Soil Science Figure 1: Charles Darwin as an earthworm scientist: caricature from the journal Punch, published in the year 1882. Figure 2: Schematic drawing of common European earthworms (Lumbricus terrestris) in their natural habitat. The annelids live in self-made burrows and forage by night on rotten leaves. Applied and Environmental Soil Science 3 2. A Trivial Gardening Matter and Darwin’s texture. More recent work has shown that they also influence SpeechtotheGeologicalSocietyofLondon soil pH and enrich the soil [11]. The processes of physical and chemical decomposition occur in the earthworm gut, chiefly Darwin first indicated the importance of earthworms in in the gizzard and crop. Darwin concluded that the ingestion a lecture “On the formation of mould” to the Geological of the topsoil, and its mixing, grinding, and digestion in Society of London on 1 November 1837. This was published the gut, continually exposed rock particles to chemical in the following year [4] and does not appear to have alteration, increasing the amount of soil. This process, and hadagreatimpactonhiscolleagues[5]. Darwin probably the addition of faecal casts from the worms, builds up realised this because he repeated his ideas in three following the humus-rich topsoil (Figure 3(a)) and buries various publications (published in 1840, 1844, 1869) [6–8], the materials originally on the surface (e.g., seeds, pebbles, last two being aimed at gardeners. The terms “vegetable archaeological artifacts) down to depths of 2 m, depending mould” or “plant earth” were used by the Victorians to upon the depth of the earthworm burrows. Darwin estimated refer to what is called today “humus-rich topsoil” or the “A rates of topsoil deposition in the range of 0.20–0.56 cm per horizon” (Figure 3) or “mollic epipedon”. It was his 1881 year, and the mean amount of soil brought upwards by the book [2] that had the greatest impact on those who had often worms as 17–40 t per ha per year. More recent studies in regarded earthworms as pests that disfigured well-manicured Britain, France, Switzerland, and Germany have produced Victorian lawns with their casts. They were thought to similar values for grass-dominated vegetation in a temperate be useful only as fish bait or food for hens, but Darwin climate [13]. gave them a noble and useful character and even, more Earthworms are predominately saprophages and feed controversially, considered that they had intelligence. chiefly on organic detritus, usually the decomposing leaves Although the book was a great success at the time and and stems of plants together with smaller amounts of was verified by many studies soon after its publication, it roots, seeds, algae, fungi, and testate Protozoa. They prefer has become neglected in some areas of biology, especially materials rich in nitrogen and sugar, but low in polyphenols soil science. A detailed review by Johnson [9] shows how [14]. Variable amounts of mineral soil can be ingested biomechanical processes were largely ignored in models of together with organic material, and the mineral fraction landscape evolution, and how soil science became dominated reflects that of the external medium. Darwin observed that by chemical and hydrological processes. However, this review an “astonishing number of half-decayed leaves” were drawn also demonstrates how more recent models of dynamic down by the worms into their burrows (Figure 2). Here denudation incorporate bioturbation on equal terms with they were stored until they were sufficiently decomposed to other major archaeogenic, geomorphogenic, and pedogenic be eaten. He thought that the mixture of partially digested processes. Finally, it should be noted that although Darwin’s leaves and mineral soil in the faecal casts was responsible book on earthworms became neglected by the earth sciences, for the characteristic dark colour of humus-rich topsoil it has continued to be quoted in zoological texts [10–12]. (Figure 3(a)). It is now known that the darkening is a much slower process, involving primarily chemical reactions and microbial activity [15]. However, the earlier processing of the 3. Earthworms as Living Ploughs: material in the earthworm gut may facilitate this process. Darwin’s Major Conclusions Darwin was also the first scientist to state that earth- worms improved the quality of soil by improving soil texture. As there are already some lengthy reviews of the scientific Earthworm activity facilitates the physical comminution of findings in Darwin’s book on earthworms (e.g., [10, 13]), organic particles, the amelioration of soil pH, the enhance- only the more important conclusions are summarised here. ment of microbial activity, and the mixing of soil from Darwin was probably the first scientist to examine a soil different strata in the profile. They promote the formation profile and suggest factors responsible for the structure of of organomineral complexes and, by delivering faecal casts the various layers (Figures 2 and 3). This vertical soil section at the surface, they bring organo-mineral crumbs from the with a depth of about 13 cm was taken in October 1837 from deeper parts of the profile to the surface. Earthworms also a field near the family home of Darwin’s uncle, the famous facilitate the transport of certain elements to the soil surface English potter, Josiah Wedgewood. The field had been so that their faecal casts have concentrations of calcium, drained, ploughed, harrowed, and covered extensively with sodium, potassium, magnesium, available phosphorus, and burnt marl and cinders 15 years earlier. Darwin observed that molybdenum that are higher than in the surrounding soil. this layer (Figure 3(c)) was now well below the surface and Therefore, earthworms not only improve the soil texture but concluded that this was due to the actions of earthworms, also enrich the soil [3, 9, 10, 15]. a process described as bioturbation [3]. He was the first Darwin suggested that earthworms may change the naturalist to point out the importance of earthworms in the chemical composition of materials that pass through their formation of the layer of humus-rich topsoil that covers the gut.