Putting earthworms on the map

Abstract

Invertebrates in soil deliver valuable ecosystem services for nature and agriculture alike. Too little is known about their ecology, but recent studies have shown that large-scale trends of their diversity and distribution can be established. Michael Gross reports. Invertebrates in soil deliver valuable ecosystem services for nature and agriculture alike. Too little is known about their ecology, but recent studies have shown that large-scale trends of their diversity and distribution can be established. Michael Gross reports. Just six months before he died, Charles Darwin had his last book published, summarising his insights on a topic that had fascinated him for five decades. It sold faster than his more famous opus, On the Origin of Species, and it had a more down-to-earth subject matter. The book was called The Formation of Vegetable Mould through the Action of Worms with Observations of their Habits. In his final year, beset by illness and general gloom, Darwin was very keen to get this last book out and was well aware of the irony of obsessing about earthworms when he appeared to be on track to join them in their realm, as Adrian Desmond and James Moore note in their biography of the iconic scientist. Darwin had spent much effort on studying the behaviour of the worms he collected from his garden at Down House. He tested their intelligence by challenging their leaf-pulling behaviour with various materials, and he tested their hearing by shouting at them and by exposing them to the accomplished piano playing of his wife, Emma. Sadly, the musical merits of this entertainment will have been lost on the invertebrate audience, as Darwin established that the worms are stone deaf. While they responded to movements like his breath or the vibrations of the piano when their container was placed on top of the instrument, it became clear that they have no perception of sound waves travelling through the air. After the publication of the worms book, Darwin was left without a scientific project and thus with little motivation to keep up the fight. He died on April 19th 1882, but he did not rejoin the worms at Downe, as he had anticipated. Instead, the clamour for a state honour — to compensate for the fact that he had remained plain Mr Darwin to his death — led his remains to rest in the sandy foundations of Westminster Abbey. For most of the 20th century, most scientists showed much less interest in Lumbricus terrestris and its relatives than Mr Darwin had. As the soil invertebrates were now lacking a champion of comparable stature, they initially failed to find a place in modern biology, and their ecological role remained underappreciated by science. The fact that species described as worms due to their shape may occur in very different parts of the tree of life didn’t help either. Thus, the first worm species to rise to scientific prominence came from the phylum of nematodes (roundworms), which are not directly related to annelids such as the earthworms. In the early 1960s, many considered Sydney Brenner an eccentric when he chose the nematode worm Caenorhabditis elegans — only around a millimetre long and thus even more inconspicuous than Darwin’s earthworms — as a model for developmental genetics. The success of his project, which made C. elegans a reference system on a par with Drosophila melanogaster and Escherichia coli, must have helped to make worms in general a more respectable subject matter. Brenner received the Nobel Prize in 2002, sharing the prize with John Sulston and Robert Horvitz, who both extended his work on C. elegans into new directions, discovering important principles of apoptosis (programmed cell death) that also apply in more complex animals like ourselves. Another biological function that is common in invertebrates and has recently attracted a great deal of interest is regeneration of body parts. In this field, planarians (a group of flatworms), have emerged as an exciting model. Like earthworms, they belong to the lophotrochozoa rather than the ecdysozoa, like C. elegans, although this phylogeny is still being debated. A high proportion of stem cells, which are controlled by an inordinate number of microRNAs, appears to be the secret of regeneration in the flatworm Schmidtea mediterranea, whose genome was sequenced in 2009. Beyond the attractions of worms as simple developmental models with remarkable abilities such as regeneration, we should of course seek to understand them better because they help to keep our soils fertile. Soil invertebrates in general are credited with ecosystem services, including nutrient cycling, carbon cycling and storage, and water infiltration and purification, and supporting primary production. In times of growing demand for food in quality and quantity and diminishing availability of land, it would be useful to understand large-scale geographic trends in soil ecosystems. This could, for instance, help to predict which areas would be promising for intensification of agriculture and which might not. In Europe, for example, the task of monitoring soil biodiversity has been addressed in several EU-sponsored projects over the last two decades. The EcoFINDERS (Ecological Function and Biodiversity Indicators in European Soils) project, funded for the years 2011 to 2014 under the Framework 7 programme, has defined a transect across Europe with 81 sites sampled according to standardised, well-defined protocols. This project, involving 23 partners from 10 European countries and China, aims to identify all members of the soil ecosystem from bacteria and fungi through mesofauna (e.g. microarthropods) to macrofauna such as earthworms. The aims of the project included: “description of soil biodiversity and of the relations between soil biodiversity, soil functions and ecosystem services, in long-term observatories representative of soil types, climates and land uses across Europe, metadata analyses to raise a biodiversity database at the European level, and modeling to decipher relations between soil biodiversity and functions, as well as putting a value on ecosystem services” (http://bit.ly/1Y6v0eh ). Results were published in a special journal issue in January (Appl. Soil Ecol. (2016) 97, 1–134). The project was also designed to provide the scientific and technical knowledge required to define an EU policy for the sustainable management of soils with a view to adopting a legally binding Soil Framework Directive, in analogy to the ones that exist for air and water. A draft directive had been proposed in 2006, but was withdrawn in 2014 after it failed to find consensus among the member states. In a paper concluding the special issue, Jörg Römbke and colleagues discuss the policy aspects of the research and its potential use in legislation at the EU or national level (Appl. Soil Ecol. (2016) 97, 125–133). There have also been several initiatives at the national level within EU member states, including the UK’s Soil Indicators Consortium, RMQS (Réseau de Mesure de la Qualité des Sols) in France, BISQ (Biological Indicator for Soil Quality) in the Netherlands, and Edaphobase in Germany. In an effort to get a glimpse of the bigger picture, Michiel Rutgers from the National Institute for Public Health and the Environment at Bilthoven, Netherlands, and colleagues from across Europe set out to map the earthworm communities and habitats based on existing data from Denmark, France, Germany, Ireland, the Netherlands, Northern Ireland, Scotland, Slovenia, and Spain (Appl. Soil Ecol. (2016) 97, 98–111). By standardising a large number of separate datasets, many of which had not been readily accessible, the authors believe they have been able to detect robust patterns on large geographic scales. While these can still be improved with additional data, they already enabled Rutgers and colleagues to extrapolate parameters like earthworm abundance and diversity to areas not covered by existing datasets and thus to make predictions that could then be tested. They also hope that their database grows to cover larger parts of Europe, and to provide solid information for the EU to decide on environmental policies relating to soil communities. Expanding the efforts beyond Europe, the Global Soil Biodiversity Atlas (www.globalsoilbiodiversity.org) is also being published, with electronic versions of the atlas due to become available on May 20th. With 130 authors contributing, the atlas covers 25 countries and is described as “a reference publication not only for soil biodiversity researchers but also policy makers and general public”. The general public is also invited to get involved with a citizen science project recently launched by Earthwatch Institute (Europe) and the Natural History Museum (London, UK) in association with the Earthworm Society of Britain. “Earthworm Watch” was launched for a first instalment to run through April and May, but it will continue each autumn and spring, which is the time when the worms are most active, as Dr Jenny Cousins from Earthwatch Institute explains. She and her colleagues have already registered several hundred participants, and the data collected will be analysed and disseminated in a range of publications and outreach events over the next three years. The project pack provides instructions and materials for lay participants of all ages to conduct a detailed survey of worms on two small plots in their gardens — or any other place where they can get permission to dig two holes (http://earthwormwatch.org/). The instruction booklet (also downloadable as a PDF file) suggests to survey two 20 cm x 20 cm plots that either represent different types of habitat (e.g. lawn or flowerbed) or that have been treated in different ways (e.g. with and without fertiliser use). For each of these, volunteers should dig up the soil to 10 cm depth, recover the worms from the soil, and then pour in mustard water to encourage worms from deeper layers of the soil to come up. Tables and helpful advice are provided to further characterise the worms that show up and to describe their soil environment. Participants learn to distinguish between adult and juvenile worms, as well as between deep-living, surface-feeding and soil-feeding worms. A simple acid test using vinegar clarifies if the soil contains carbonates. Thus, anybody with access to a patch of land can now follow in the footsteps of Charles Darwin and contribute to our knowledge about those helpful worms that enable the soil to provide our food. Rather than taking them indoors and playing piano for them, however, Earthworm Watch suggests to return them to the hole and to fill up the soil.