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Scratching the surface

Soil is a living entity that sustains all life, yet its potential - and the vast array of creatures that exist within it - remains largely untapped. Jo Anderson goes digging

The next time you are playing football on a grass pitch, or tearing up the fairway of a golf course, or simply having a leisurely stroll through the park, cast your eye over what you are walking on. More specifically, look at the soil directly beneath your feet.

In it you will find another world - one in which a single gramme of soil is so complex that, were you to unfurl all the surfaces that criss-cross within it, they would cover an area of 20 square metres. This is a world where, incredibly, most of the total number of species of life on land exist.

If that is too hard to imagine, think of the more familiar images of the African savanna, teeming with herds of zebra, wildebeest and other game.

The variety of animals there is truly spectacular, but consider this: proportionately, the combined weight of just a few species of termites is probably 10 times greater than that of all the animals living above ground.

Similarly, in productive temperate pasture, the weight of earthworms per hectare may be larger than that of the cattle or sheep found grazing above, while the amounts of fungi and bacteria will be greater by powers of 10.

The soil on which these species depend is one of the last great unexplored territories on the planet - and, paradoxically, one of the most important.

All land ecosystems, from the great boreal forests around the Arctic Circle to the massive equatorial rainforests, are maintained by what happens less than a metre beneath our feet.

Without soil, there would be nothing to eat. The creatures that live in it are invisibly and efficiently disposing of dead plants and animals, faecal material and other organic wastes, thus releasing nutrients which in turn allow plants to grow - including food crops. Similarly, oxygen-pumping trees would not exist were it not for the mind-bogglingly complex soil systems from which they spring.

This is not the only environmental role which soil plays. By breaking down pesticides, industrial compounds, oil, wood preservatives and many other man-made environmental contaminants, soil reduces pollution in lakes and rivers by acting as a natural filter. It also helps to counteract pathogens (disease-producing agents), such as coliform bacteria in animal faeces, which are potentially hazardous to human health.

Globally, soil contains twice the amount of carbon as there is in the atmosphere and vegetation combined. Small increases in the amount of carbon released from soils, which can be caused by agricultural practices or a lowering of water levels, may have major implications for global warming.

Indeed, climate change - which is probably caused by human activities - may already be increasing the amount of carbon released from the soils of the tundra regions, where there are vast peat reserves.

In short, soil is vital because it provides the food we eat, the air we breathe and the quality of the water we drink, and it can influence our climate.

The need for research

The vital role of soil has long been underestimated. Indeed, environmentalists are now voicing great concern about the ways in which land use and agricultural practices are affecting the abundance of rare species and causing an increase in the rates of extinction. On the whole, however, little recognition has been given to the losses of soil biodiversity - partly because many of the species concerned are not very apparent or charismatic, except to soil ecologists.

Indeed, when the majority of nations signed the Rio Convention on Biodiversity at the Earth Summit of 1992, the fact that most of the total number of species on land live below ground was not considered - a case of "out of sight, out of mind" if ever there was one. It is an agreement that potentially compromises soil conservation in favour of more pressing national priorities for intensified food production.

This situation is being rectified, however. A major international programme, which began on November 29 exactly a year ago, aims to promote the idea that soil is a living entity. Feeding and tending the soil correctly will benefit farmers in all areas of the world, support livelihoods and communities, and perhaps aid humankind on a previously unimagined scale.

Research into soil could launch an agricultural revolution by dramatically shifting the focus of agriculture on to what happens beneath the ground at microscopic levels. This is truly grass-roots stuff, and we are only just beginning to obtain the tools needed to identify the vast microbe community that exists in soil, let alone exploit it.

In 1993, only 1,292 species of soil bacteria had been identified using conventional methods but, with the advent of DNA sequencing, the number rose to 5,500 in 10 years, and there are frequent new discoveries. This vast undiscovered potential - particularly in tropical soils - must be conserved as a legacy for future generations.

This is one of the main aims of the international programme. Funded by the United Nations Environment Programme (UNEP) and the Global Environment Facility (a fund set up by the World Bank to enable developing countries to achieve the same conservation goals as their industrialised counterparts), it involves teams of scientists in India, Indonesia, Kenya, Uganda, Ivory Coast, Mexico and Brazil. It is co-ordinated by the Tropical Soil Biology and Fertility Institute, based in Nairobi. It is estimated that the programme will take five years to complete, and will cost $26 million (pound;15.5 million).

The diversity of soil animals and micro-organisms in the tropical forests of these countries will be documented by the national teams in the programme. These teams will invest-igate the relationships between soil biodiversity and different agricultural systems, from traditional farming methods to modern practices, to assess the extent to which soil organisms are being lost to intensive farming, and whether ways can be found to conserve them in situ. Whether the management of soil organisms can be improved to the advantage of local farmers will also be investigated.

Empowering farmers with a greater understanding of the vital role of the processes below ground will undoubtedly benefit both them and their communities.

The vital role of earthworms in maintaining soil structure has been incorporated into organic farming and minimum-tillage practices. By releasing native earthworms in tea plantations in India, productivity has been boosted almost threefold and annual profits have been raised by $3,500 per hectare. Using the soil to regulate pests and pathogens could also save farmers huge sums by dispensing with the need to buy pesticides.

Termites also have a role: often regarded as pests, their activities can be used to restore the structure of compacted and degraded soils. They also make delicious snacks and are sold, roasted like peanuts, in little bags.

Women in some parts of Africa eat termite soil while they are pregnant - this is the natural world's equivalent of an iron and zinc-rich vitamin pill.

In the developed world, where there is a surplus in agricultural production, we have the luxury of deciding between different farming methods, but many developing countries have not yet reached this stage, so there is an urgent need for more research into soil biodiversity in tropical systems.


There are other reasons to push for the conservation of soil biodiversity - perhaps the most simple being the fact that it is there. There is a moral imperative to resist the wanton destruction of the species affected. In any case, a growing number of people are becoming sympathetic to the idea that as soils are alive and teeming with life, and are an integral part of the natural world, there is an obligation to conserve them.

It is curious to note that creatures that are smaller and arguably less important than many soil animals - some rare beetles, for instance - have the potential to bring a halt to major land development projects on account of the threat of extinction which disturbance to their habitat would pose.

But ignorance of soil-dwelling minibeasts, such as tiny pseudo-scorpions, brightly coloured millipedes, strange mites or rare springtails, means these could be lost through land development without our even being aware of their existence.

Cynics could argue that a more powerful motivation behind research into soil involves economics. We are becoming increasingly aware of the potential value of soil biodiversity for future developments in forestry, agriculture and industrial biotechnology. Soil bacteria and fungi produce immense arrays of enzymes that enable them to process the complex range of biochemical compounds found in soil - both natural and man-made. This allows for the repair or "bio-remediation" of contaminated soil. In fact, the breaking down of diesel, lubricated oil and toxic industrial contaminants such as PCBs by soil has become a major industry.

For example, research into nitrogen-fixing bacteria that associate themselves with the roots of plants such as legumes, is big business. In Brazil, inoculating soybeans with new strains of these bacteria is saving the national economy about US$1 billion a year, By stabilising nitrogen levels in the plant, the need to import artificial fertiliser has been negated.

The decomposition of the vast amounts of leaves and dead wood produced by plants every year is something we take for granted. But understanding and managing these processes has economic importance in forestry and agriculture. For example, a new approach to managing the debris of old oil-palm plantations has been shown by a Malaysian postgraduate student to make potential savings of millions of dollars by averting the need for the fertiliser normally used to re-establish young oil palms.

Other industries also stand to make greater profits from soil research. For example, the global pharmaceutical industry has invested billions of pounds in "bio-prospecting" - research into microbes and fungi. Given that only about 5 per cent of the estimated 72,000 species of soil fungi have been discovered, the potential for uncovering new antibiotics and other agents of medicinal value is jaw-droppingly huge. Creatures in soil and decomposing materials have already produced some of the world's most important antibiotics, including streptomycin, kanamycin and penicillin.

Research at Exeter's Biocatalysis Centre has discovered a soil enzyme that looks promising as the building block to synthesise a new anti-viral drug to treat HIV.

Such possibilities are extraordinary and pharmaceutical companies are desperate for a significant slice of this largely unknown pie.

What lives in soil?

One square metre of temperate pasture soil could contain 120 million nematodes (microscopic worms), several hundred thousand mites and springtails, and a diverse abundance of flies, beetles, slugs, spiders, woodlice, centipedes and earthworm species.

Woodland soil is equally diverse, with more than 1,000 species of soil animals per square metre. There are larger and more familiar members of the soil community - such as mushrooms, earthworms and woodlice - but the majority of organisms are tiny and are capable of processing resources the size of the full stop at the end of this sentence.

A tonne of soil from your garden - enough to fill one of those big plastic sacks used by builders to supply sand and gravel - could easily contain 4 million types of bacteria. Even a few kilograms of soil will contain a greater diversity of organisms than the plants and animals living above ground in a vast tropical rainforest.

Only in recent years have we become aware of the true extent of the diversity of life in the soil. This is partly because early soil studies used somewhat antiquated techniques, such as agar plate cultures and tests on the ability of isolates to grow on different media. But new molecular methods have been much more revealing. Extracting and characterising genetic material from soil has shown that earlier methods isolated only a tiny fraction of the total microbial diversity in soil. Even now, the vast majority of bacteria are still unknown to science.

Soil has an immensely complex structure of air- and water-filled pores associated with roots, humus (decaying matter), plant cells and mineral surfaces. These form vast labyrinthine chambers and passages that are criss-crossed by fungi - like pipes in a cellar - with walls encrusted with patches of bacteria, and niches of resources that are accessible only to tiny, flexible species such as protozoa. Mites and minute insects scuttle around in the larger pores, while burrowing earthworms taking shortcuts can cause "wormquakes" that continually restructure these micro-habitats. All these creatures combine to turn the soil - nature's equivalent of a plough.

Professor Iain Young and colleagues at Abertay Dundee University are using new computer-imaging techniques to analyse the complex structure of soil habitats. They have calculated that one gramme of soil can contain about 20 square metres of surfaces. That is like taking all of the kilometres around you - the roads, parks, buildings, factories, houses and schools - and compressing them into one cubic metre.

Hence, despite being vast in numbers, the populations of fungi, bacteria and protozoa in soils occupy only about 0.0001 per cent of the surface area - about the same density as humans on the Earth's surface. It is no surprise, then, that soil provides plenty of room for many species of tiny organisms to live in its countless niches; for predators and their prey to coexist in their cycle of hide-and-seek; and for ancient troglodytes - largely unchanged for hundreds of millions of years - to delve in a timeless isolation. Collembola, or springtails, are living links to this prehistoric past - fossils found in Scotland which are about 400 million years old look almost identical to present-day collembola species.

A rich diversity

At a depth of just 10cm - and sometimes even nearer the surface - there is great variation in the properties of most undisturbed soil. In this short distance, there are steep gradients of living space, food resources, temperature and moisture levels as we move from the litter layers of decomposing leaves and twigs on the surface down to the compact mineral soil below. This variation has enabled animals from the same group to evolve species with different physical forms. Springtails, for example, are wingless insects that get their name from a forked jumping organ at the end of their abdomen. They are typically less than 3mm long but their physical form varies depending on what depth they live at.

The Symphypleona springtails have a strangely truncated body, well adapted for jumping around in grass litter and on the soil surface. Unlike the other main subdivision of springtails - the Arthropleona - they have respiratory tracheae, much like the other insects, and so the body surface has a waxy cuticle which enables them to avoid desiccation in dry-surface habitats.

The Arthropleona, on the other hand, breathe through their body surface, and are thus confined to humid micro-habitats. Typically, those living in litter are pigmented, have large eyes, long antennae (which some species can coil like a spring to go through tight spaces) and a well-developed jumping organ. When litter is disturbed, these springtails can skip away in random patterns that confuse predators such as birds. Within the soil itself, some springtails are white and blind, and have short stumpy legs and knobbly antennae packed with receptors that are ultra-sensitive to a wide range of environmental stimuli.

These species mate and reproduce without physical contact: females wander through total blackness, seeking out pheromones from packets of sperm deposited by males. Living within these confined spaces, these springtails are more at risk of death by flooding than drying out like the surface-dwelling Symphypleona. Consequently, their bodies are covered with tiny water-repellent papillae that retain a film of air as a respiratory surface. An easy way to find these springtails is to stir up some soil in a bucket so that they bob up on to the water surface.

But be sure to take it easy on these little creatures. They, along with the thousands of other species scuttling around in the centimetres of soil beneath our feet, are tirelessly maintaining the function and health of the planet. Recognising their role and treating them with respect is something our species would do well to understand.

Jonathan Anderson is professor of ecology at the University of Exeter. He is consultant to the UNEPGEFTSBF soil biodiversity programme and an adviser to the Food and Agriculture Organisation of the UN, the Rockefeller Foundation and other international agricultural development agencies. He is also a director of an organisation that develops food security among farmers in Kenya through sustainable management of soils.

Captions for microscopic mites provided by Dr David Walter, adjunct professor of the University of Alberta, Canada

* A Immature cepheid oribatid mite (0.75 mm long): hides under an umbrella of cast skin and hairs

B Sellnickia mite (0.6 mm long): an armoured predator that ambushes passing springtails and mites, pouncing with its pincer-like front legs

C Gozmanyina mite (1mm long): lives in leaf litter and feeds on fungi

D Athiasella (0.7 mm long) with acarids (0.13 mm): a fast-moving predator that covers long distances. Acarid mites disperse by hitching a ride

E Proturan (body 0.6mm long): these primitive relatives of springtails are a soil enigma - no one has identified their role in the soil

F Entomobrid springtail (1.3mm long): escapes predators by springing away on its 'tail', and by shedding slippery purple scales

G Phtiracaroid mite (0.5 mm long): known as box mites because they can close the two ends of their body over their legs and mouthparts in self-defence

* Cosmochthonius mite (0.45 mm): feeds on fungi and defends itself from predators with porcupine-like erectile setae (bristles)

* Terpnacarus (0.26 mm long): jumping mites that consist entirely of females, reproducing by parthenogenesis; related to 400-million-year-old fossilised mites

* Zerconid mite (0.5 mm long): a blind predator whose club-shaped setae act like a cat's whiskers to feel its surroundings

* Tuckerella mite (1.1 mm long): defends itself by sweeping its tail hairs over its body and flicking away attackers


It happened in 1992. It was one of those events in which something so incredible is discovered in an obscure corner of the scientific world that it expands beyond the boundaries of laboratories and academic papers and into the global media spotlight.

Myron Smith and colleagues at the University of Toronto were studying a stretch of woodland in Crystal Falls, Michigan. In particular, they were studying a mushroom-like, wood-decomposing fungus called Armillaria bulbosa, also known as the Honey Fungus.

By using molecular methods similar to forensic "fingerprinting" now in general use, the team discovered that this fungus covering 15 hectares of woodland was a single genetic entity that weighed nearly 10 tonnes - close to the mass of an adult blue whale. It was also ancient, having begun its life before AD500.

The fungus has survived for so long by forming a network of root-like structures that enable it to attack living trees and shrubs, using energy and nutrients gained from decomposing the last victim to overcome the next host's defences. Details of this astonishing discovery were published in the scientific magazine Nature, and the resulting publicity was as frenzied as it was unexpected.

News of one of the oldest living organisms on the planet filtered to all parts of the globe. The enterprising Crystal Falls community even turned the discovery into a tourist attraction, and now holds an annual Fungus Fest every September, at which participants can buy a Humungous Fungus burger (not made with Armillaria, despite it being a delicious edible mushroom) or some Fungus Fudge. Humungous Fungus T-shirts are also available.

Armillaria bulbosa even made David Letterman's Top 10 list. The final word, however, should perhaps rest not with David Letterman - not renowned for his knowledge of mycology - but rather with Myron Smith and his team. Their paper concludes by stating: "This is the first report estimating the minimum size, mass and age of an unambiguously defined fungal individual.

"Although the number of observations for plants and animals is much greater, members of the fungal kingdom should now be recognised as among the oldest and largest organisms on Earth."

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