By Jonathan Amos
BBC News science reporter
The fourth and final test of a GM crop grown under UK farm conditions has highlighted the detrimental effects the novel plants can have on wildlife.
A measure was taken of weed seeds falling into the soil
The tests of a winter-sown oilseed rape showed the management of the biotech crop could reduce the weeds and seeds available to some insects and birds.
And scientists found these effects could linger in fields year after year.
But they also stressed the picture was complex and there were circumstances in which GM might be beneficial as well.
The results for three other types of engineered crops - a spring-sown oilseed rape, a sugar beet and a maize - were published in October 2003. Only the maize was approved for commercialisation under strict conditions.
Finding a balance
The £6m UK Farm-Scale Evaluations (FSEs) of genetically modified (GM) plants have been described as the biggest ecological experiment in the world and a model for measuring the impact of new farming techniques on the environment.
And scientists believe they have raised major questions about how we farm and manage the countryside - over and above what type of crop technology is used in the field.
"The FSEs have drawn attention to an issue of balance," said Professor Chris Pollock, the chair of the FSEs' Scientific Steering Committee.
"They've highlighted that what's good for the farmer is not always good for the population of weeds, insects and birds that share that space.
"It is the way in which different forms of agriculture affect this balance that is exposed so clearly in the FSEs."
As with the first three FSE trialists, the winter-sown oilseed rape was modified to tolerate a particular herbicide, which meant it could be sprayed and still flourish while all the competing plants (weeds) around it died off.
It was grown at 65 sites from the north of Scotland to the south of England, side by side with a conventional variety and in a standard rotation with other plants, such as barley and wheat.
Scientists said that when compared with conventional winter-sown rapeseed, the novel plant kept the same number of weeds overall but that there were differences seen between the weed types.
Intensive agriculture has put many farmland birds under pressure
GM management led to more grass weeds but fewer broad-leaved weeds, such as chickweed and fat hen. The flowers of these "pest" plants attract insects, and their seeds are also important for many bird species, such as the skylark, tree sparrow and bullfinch.
"There is a lot of knowledge about bird diets and, generally, it's fair to say for most farmland birds, broad-leaved weeds are particularly important," said Dr David Gibbons, a steering committee member from the Royal Society for the Protection of Birds (RSPB).
"I think if this crop were commercialised on a widespread basis, we would be worried about the implications that could have."
The researchers also found slightly more insects that liked to feast on decaying plant material in the GM fields, but slightly fewer butterflies and bees.
However, they emphasised that these differences arose not because the crop was genetically altered but because of the different times at which the fields were sprayed. And they argued that other environmentally friendly practices on a farm were likely to have a far greater impact on biodiversity than simply switching between a non-GM or GM crop.
"It's one of those issues where you can look down either end of the telescope," explained Dr Les Firbank, who led the consortium of FSE scientists.
"Is there an effect of [the GM] cropping system on butterflies? Yes. But if you want to conserve the butterflies, is this the effect you'd be concentrating on? No. You'd be concentrating on getting far more wild flowers in and around the fields."
This point was picked up by green lobby groups such as Friends Of The Earth. "The FSEs specifically didn't examine the impact of organic agriculture," said FOE GM campaigner Emily Diamand.
"They only looked at 'bad' and 'worse'. There are more sustainable ways of farming than intensive agriculture that could benefit the environment."
And Dr Sue Meyer, the executive director of Genewatch UK, added: "The FSEs and the whole controversy around GM have opened up, quite rightly, a much broader look at what we want from agriculture.
"We need a much more holistic approach to farming and food. There are some very beneficial new approaches and new thinking that have come out of this whole process - and that is to be welcomed."
In their reaction to the latest FSE results, the biotech industry picked up the positives from the study - the reduction in the amount of herbicide required on the GM fields and the greater flexibility in the timing of spraying which could benefit some insect species by leaving more weed material in the field for longer.
"These results confirm once again that GM crops give farmers the flexibility that they need to balance economic viability with environmental responsibility," said Tony Combes, deputy chairman of abc, an umbrella group for the agricultural biotechnology industry.
"This weed management option is delicate and precise enough to allow active management for weed and insect species.
The four-crop FSEs counted literally millions of plants and seeds
"As with all weed management systems, some weed and insect species will be positively affected while others may be negatively affected, but the vast majority are unaffected."
The results of the FSEs are intended to help government ministers decide whether or not to allow commercialisation of GM crops.
However, there are currently no applications from biotech companies in the UK or in the EU to cultivate a winter-sown oilseed rape, which in its conventional guise is planted on 300,000 hectares across the British countryside each year.
A paper detailing the scientific investigations is published in the Proceedings of the Royal Society B: Biological Sciences.