Miners know that the surest, starkest sign of poisoned air and approaching doom is the death of a caged canary. In modern science, the surest sign of polluted soil is the fate of the humble earthworm.

Research carried out by scientists at the Institute of Evolutionary Biology at the University of Edinburgh, shows that even low levels of chemical pollutants in the soil caused fundamental changes in the lifecycle of earthworms, affecting their ability to reproduce. These findings raise fundamental questions about the effect of pollution in the soil and also raise concerns about the effect of human exposure to widely used chemicals.

“We pour things on to the soil, to kill weeds or to get rid of waste, without thinking about the long-term impact,” Mark Blaxter, who led the research, said. “The worm is the soil equivalent of a canary in a mine - it can alert us to problems before we would notice them. We have found that exposure to low levels of pollution for a long time can be harmful, and this must be having an effect on plants and crops, and entering the food chain.

“High levels of pollution are often easy to spot because they kill animals, but these results show that low levels have important, though subtle, effects,” Professor Blaxter added.

Scientists studied the worms' DNA after exposure to a variety of contaminants, including the metals copper and cadmium, together with fluoroanthene, an industrial pollutant from incinerators, and atrazine, a common weed killer.

Their study found that exposure to low levels of pollutants had significant effects that were not simply a reduced form of the effects seen at high levels of exposure. In the long term, these could be as significant as the catastrophic effect of a serious spillage.

Ironically, Charles Darwin set great store by his study of earthworms, which effectively mix and make most of the soil on Earth, but his successors in evolutionary science have tended to neglect the creatures that live beneath their feet.

Instead, Professor Blaxter said, they regard the soil as a kind of test bed - or “black box” - that there is no need to understand. He added that this project would help to redress that issue.

“Until the soil collapses, and the ecosystems dies completely, we don't know what's going on. We have to start to get inside the ‘black box' and start looking at parts of it in isolation and ask very specific questions.”

Biologists regard earthworms as the great ecosystem engineers, breaking down organic particles, mixing and mashing them up as they make soil. In test conditions they were found to be vulnerable to chemicals that are typically bi-products of industry or routinely applied as herbicide.

“None of these chemicals is put into the soils to affect the earthworms, especially not the herbicides, which are meant to tackle weeds, but they do affect them, and toxicologists find that alarming. The findings really opened their eyes to just how damaged many of our soils are,” Professor Blaxter said.

As well as offering a greater understanding of how earthworms cope with pollutants, the project has produced technological spin-offs that could be widely applied. One offers a new means of testing for poisons during soil surveys using genes extracted from earthworms. “It is potentially a new means of monitoring the environment, effectively asking the animals what they are experiencing in the soil, rather than using proxy measures of chemical analysis,” Professor Blaxter said.

All the Edinburgh research data is likely to be published online so that it could be more easily used in developing countries, where such expertise is most urgently needed, he added.

The four-year study was carried out in co-operation with scientists at Cardiff and Cambridge Universities and at Imperial College London. It appears in BMC Genomics and in Environmental Science and Technology.

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