The UK's farm scale evaluations have shown conclusively that the herbicide regime linked with GM spring oilseed rape and beet is damaging to biodiversity. Lim Li Ching reports.
The three-year farm scale evaluations (FSEs), results of which were published on 16 October in the Royal Society's house journal, examined three spring-sown GM crops - oilseed rape, beet and maize. They were undoubtedly the largest experiments of their kind, involving over 200 plots.
The FSEs were a compromise from the start. They did not focus on the many other key questions regarding environmental safety - gene flow, transgenic contamination, creation of 'superweeds' and 'superpests', but looked only at the impact of managing GM herbicide-tolerant (GMHT) crops on farmland biodiversity.
About 60 to70 fields each were planted to beet, maize and spring oilseed rape. Each field was split, with half planted with a conventional variety managed according to the farmer's normal practice, and the other half sown with a GMHT variety. The GM beet was tolerant to glyphosate, the GM maize and oilseed rape were tolerant to glufosinate ammonium [1]. These allow farmers to indiscriminately spray the crops with herbicides, killing weeds and not the crop itself.
But killing weeds adversely affects biodiversity. Weeds provide food and habitat for countless animal species, including threatened birds. Populations of the skylark, corn bunting and other birds have declined over the past 30 years, partly due to intensive agricultural practices that suppress weeds.
The FSEs thus recorded levels of weeds and invertebrates in the fields and surrounding field margins. The researchers concentrated on the plants and more-or-less sedentary herbivores and detritivores that react rapidly to any major change in field management [2]. Selected groups of other organisms with wider foraging ranges (e.g. carabid beetles, bees, butterflies) were studied for comparison. The key question was: would the changes in management associated with GM crops exacerbate the trends perpetuated by conventional agriculture, of reduced weed levels and wider impacts on farmland biodiversity?
In general, the GMHT crops received less herbicide-active ingredient per crop, with later and fewer applications than the conventional varieties [3], and this, GM corporations have long claimed, means that GM crops could benefit the environment. But the FSEs found otherwise. Overall results showed that GMHT oilseed rape and beet would reduce farmland biodiversity, as the stronger broad-spectrum herbicides used with GM crops control a wider range of weeds more efficiently.
In beet and oilseed rape, after the first application of broad-spectrum herbicide, weed densities were lower in the GMHT crop, reversing initial higher densities [4]. The biomass (weight of weeds collected from a fixed area) in GMHT beet and oilseed rape was one-sixth and about one-third, respectively, of that in conventional plots.
The effects on weed diversity were transient and mostly small, but the researchers concurred that, "it is only a matter of time before resistant plants become widespread" [4]. Then diversity is likely to drop, as evolved herbicide tolerance increases the dominance of a few species.
While reduction or removal of the visible flora temporarily reduces the food available to farmland animals, the key to longer-term impacts is the 'seed rain' (seeds falling from weeds) and its contribution to the seedbank (weed seeds left in soil). The GMHT beet and oilseed rape fields had one-third and one-fifth, respectively, of the seed rain of conventional fields [4]. The reduced seed rains had demonstrable effects on the seedbanks in the following year: densities in GMHT fields were about 20% lower than in conventional fields.
Although in the short term, any resulting decline is buffered by existing seedbanks, and the loss of one year's seed return itself did not produce a large difference in future weed populations, relatively small differences could sum to produce a large effect if sustained over several crop rotations. The unavoidable conclusion was that GMHT crops would have a large impact on weed populations in the longer term.
When the researchers looked closely at 12 individual weed species, which are frequent and abundant in British agriculture, and important in the diet of farmland birds, they found that biomass in the GMHT fields was significantly reduced for five species in beet and oilseed rape [5]. Subsequent survival was significantly lowered for eight species in GMHT beet and six in GMHT oilseed rape. In general, reproductive rates were lower (by about 50%) for most species; and for many species (19 out of 24 cases), seed densities were lower in the seedbank after GMHT cropping.
They concluded, "These differences compounded over time would result in large decreases in population densities of arable weeds". And, "With a few exceptions, weed species in beet and spring oilseed rape were negatively affected by the GMHT treatment" [5].
Correspondingly, the abundance of invertebrates on the soil surface is generally lower in GMHT beet and oilseed rape [6]. Such invertebrates are food for mammals, birds and other invertebrates, and many are important for controlling pests or recycling nutrients within the soil. The distribution of invertebrates is affected by weeds in the field, and hence mirrors that of weed levels.
Specifically, there were less carabids that feed on weed seeds in GMHT beet and oilseed rape. However, collembolan detritivore counts were larger under GMHT crop management, most likely due to additional detritus produced following efficient and later application of herbicides in the GM crops [6, 7]. While Collembola are part of the diet of some farmland birds, the long-term effects are uncertain. If GMHT crops lead to long-term decline in weed abundance, there would be less biomass to produce detritus and subsequent reduction of the effect on Collembola.
The FSEs also examined epigeal (species that spend most of their life on plant and soil surfaces) and aerial (those whose main activity in the crop involves a substantial proportion of time spent in flight) species [7]. These invertebrates play important roles in pollination and recycling of detritus; many are dependent on flowering weeds and flowering crops for nectar or pollen, or have larvae that feed directly on plants.
Most taxa were insensitive to management regimes. However, actively foraging taxa, such as bees and butterflies, showed lower abundances in GM fields. The abundances of all bees, honeybees and bumblebees in GMHT beet crops were 55%, 27% and 58%, respectively, of those in conventional crops. Similarly, there were 22% less butterflies in GMHT oilseed rape than in conventional. Butterfly numbers were also lower in GMHT beet, especially in August when the abundance was 68% of that in conventional fields. These smaller counts were associated with lower abundance of flowering weeds.
Within-field findings are mirrored in the field margins [8]. Field margins can support a high diversity of plant species and are important for conservation within farmed landscapes. They are habitat for numerous invertebrates, a food resource for mammals, and a refuge for beneficial parasitoids and predators. Margins provide resources for birds and may be the only source of nectar and pollen in arable landscapes through much of the season.
However, field margins receive direct and indirect applications of chemicals. Scorching of vegetation by herbicide-spray drift was on average 1.6% on verges beside conventional crops and 3.7% beside GMHT crops [8]. Less plant cover (by 25%), which produced fewer flowers (by 44%) and less seed (by 39%), were found on tilled margins of GMHT halves of spring oilseed rape fields. The tilled margins of GMHT halves of beet also had less flowering and seeding (34% and 39% lower, respectively).
All this had pronounced knock-on effects on butterflies. There were 24% fewer butterflies in margins of GMHT oilseed rape [8]. The likely cause is the lower nectar supply. If sufficient forage is available elsewhere, then populations of this mobile group will be buffered, but not if forage reductions occur over large contiguous areas. Of the butterfly species common to arable ecosystems, those with lower dispersal ability are likely to be most vulnerable.
Similar effects may be expected for other flower- and nectar-feeding groups such as solitary bees, moths, hoverflies and other flies, as well as less frequent nectar feeders such as beetles and wasps. Effects on such a range of species groups could have implications for the pollination of arable plants.
The FSEs also looked at the effects on invertebrate trophic (or functional) groups [9]. Where the weeds were less abundant in GMHT beet and oilseed rape, there were fewer herbivores, pollinators and natural enemies (predators and parasitoids). Detritivores increased under GMHT management across all crops due to the greater input, later in the season, of dead weeds on which they feed. This shift in resources from the herbivore to the detritivore food web resulted in a general trend of greater increases in the ratio of detritivores to herbivores under GMHT than under conventional cropping. The reduced number of pollinators may influence seed production of insect-pollinated weeds, amplifying direct effects of herbicide on the weed flora.
All these negative impacts of GMHT beet and oilseed rape on biodiversity are so conclusive that several NGOs demanded an immediate ban on GM crops. The Royal Society for the Protection of Birds agreed that the risks are too great for wildlife and called for the two GM crops to be banned. Many farmland birds rely on seeds from weeds for their survival and GMHT beet and oilseed rape may be the final nail in the coffin for some species.
In trying to downplay the negative impacts, some alleged that the effects are not due to the GM crops per se, but to the herbicide regime, and hence can be somehow 'managed' away. However, the GM crops are inextricably linked with the proprietary herbicides they are engineered to tolerate, and it is the GMHT practice - the modified plant and the herbicide as a package - that has been damaging to the environment. Moreover, the FSEs' herbicide regime was recommended by the GM seed companies, so presumably is realistic under commercial conditions.
The effect of growing the third GMHT crop - maize - seemed to be positive, with higher weed density throughout the season, as well as higher late-season biomass and seed rain [4, 5]. This had a corresponding effect on invertebrates, with higher abundance on the soil surface, specifically of carabids [6], and more butterflies during some months [7]. There was greater plant cover and flowering in field margins of the GMHT field, but no butterfly differences were observed [8].
However, the apparent harmlessness of the GMHT maize is primarily accounted for by the relative toxicity of the herbicide atrazine used on most of the conventional maize, which resulted in lower weed densities. In contrast, the GMHT maize allowed farmers to spray with a different, albeit weaker, herbicide, leading to more weeds. Compared to the conventional, the biodiversity measurements in GMHT maize thus looked relatively good.
A week before the publication of the FSE results, the EU announced a ban on atrazine in agriculture. This means that atrazine would have to be phased out in Britain within 18 months and that it would probably be withdrawn from use before GM maize - if it mustered approval - was grown commercially. This effectively invalidates the maize trails, which no longer reflect the real conditions under which non-GM crops will be grown.
The researchers were only confident that their findings represent what would actually happen "unless the management regimes altered somewhat, for example if... atrazine was no longer allowed on maize crops...". They acknowledged that the results might need to be 'recalibrated' and that extra field research might be needed to gather new data on whatever regime replaces atrazine in conventional maize.
But, there's more to this story than has been alluded to by the media or admitted by the researchers (see "Cynical & dishonest science" in GM maize trials).
The Advisory Committee on Releases to the Environment (ACRE) will now consider the FSE results and advise the UK government on their implications. ACRE will likely suffer some well-deserved embarrassment, as it had blithely approved, in 1997, the GM oilseed rape tested in the FSEs, saying that it "did not pose a risk in terms of human health and environmental safety for the United Kingdom". On their recommendation, the UK Government had agreed to marketing of the oilseed rape, but this was prevented because other European countries opposed it.
If ACRE's advice had been followed, farmers could have been growing this damaging crop for the last five years. It was only public opposition that forced more research on environmental effects.
And the public have made their opinion on GM crops clear. The GM Nation? debate found widespread unease about GM crops and scepticism about its benefits. An overwhelming 86% of the 37 000 people who responded said they would not be happy to eat GM food, and 54% said they never want to see GM crops grown in the UK.
Additionally, a report into the economics of GM crops by the Prime Minister's Strategy Unit forecast found that the overall economic benefit to the UK, at least in the short term, was "likely to be limited".
The GM Science Review report, flawed as it is, also failed to give blanket approval for GM crops and instead highlighted the gaps and uncertainties in our knowledge.
Moreover, while the FSEs showed up the damaging effects of GMHT crops, they were still narrow, and say nothing about impacts on human or animal health or agronomic performance. They also failed to ask any questions about the transgenic nature of the crops, choosing instead to focus only on a secondary effect, the impact of changing patterns of herbicide use. But neither did the FSEs compare the GMHT crops with ecologically-managed crops that use no herbicides, nor did they study effects on below-ground biodiversity (and thus soil fertility). They say nothing about gene flow, coexistence with other forms of agriculture and liability if anything goes wrong.
The UK government simply has no case for approving the commercial growing of GM crops.
Article first published 8/11/03
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