The Plants that Cry Wolf

Friday 20th June 2014

Wheatfield (c) Paul HetheringtonPolitical developments in the last week make it more likely that the UK will start growing GM crops within a few years.  UK researchers are currently trialling a GM wheat that ‘cries wolf’, sending out a constant chemical help signal to ladybirds, parasitic wasps and other predators, a signal that is normally only produced when a plant is under attack from aphids or other herbivores.  Growing concerns that this will create a chemical smog over the landscape that will confuse herbivores and their enemies and damage ecosystems have not yet been addressed by the scientists or the regulators.

While many people are ethically opposed to genetic modification per se, in practice each genetic modification is unique, some involve minor tweaks and some are radical transpositions of significant amounts of genetic material from distantly related organisms.  Similarly the changes to plant biology that these create are hugely varied and cover a wide range of purposes and functions.  In assessing the likely effects of a modification on bugs and the environment each approach has to be considered specifically.  Some modifications appear highly risky, while others promise environmental benefits such as reductions in insecticide use – which has occurred with GM maize and cotton in some countries .  Just because one GM modification is environmentally safe, it can’t be concluded that the next is safe. 

To address the complex environmental safety assessment required to ensure that our environment is not damaged either by the GM organisms or by the farming practices associated with the GM organism the Government has established ACRE (the Advisory Committee on Releases to the Environment).  ACRE authorises the release of GM organisms for research purposes in the UK and works with EFSA (the European Food Safety Authority) who undertake the risk assessments for applications for commercial planting of GM crops. 

To-date EFSA has determined two crops to be safe, although only one – a maize containing a butterfly and moth affecting toxin – is in use, and only then in some countries.  Many other applications are still going through the risk assessment stage, for instance EFSA recently advised against the release of a GM maize crop because its pollinator safety study was unsound and there was evidence that ladybird growth rates were being reduced.

7 Spot ladybird Coccinella 7-punctata 2 (c) Denis GIn countries with pro-GM governments, like the UK , this has led to frustration.  The UK Government’s ‘A UK Strategy for Agricultural Technologies’ (2013) complains that “The EU regulatory pipeline for genetically modified (GM) crops remains blocked”.

Genetically modified crops are not currently grown in the UK, but the likelihood of this happening in the near future has been significantly increased by a decision by the European Council to allowing Member States to restrict or ban GMO cultivation in their territory.   Pro-GM states hope this will smooth the way for EC approval of GM crops.

Press coverage  has focussed on the likely approval for planting in the UK of a herbicide resistant maize plant.  This is not the only plant in the pipeline, in 2011 ACRE approved experiments by Rothamsted Research to assess a new GM aphid repellent wheat variety and these trials have been underway for the last two years.

The Rothamsted GM wheat is one of a number of initiatives or lines of research that are focussed on genetically engineering plants to produce chemicals that repel herbivores and attract predators.  There are several crop species and odours, ‘herbivore-induced volatiles’, involved, or potentially involved with this approach.

In this case the wheat produces (E)-β-farnesene, an aphid alarm pheromone that they produce to alert one another to danger. An odour also produced by some plants as a natural defence mechanism.  Not only does this chemical repel aphids, it also attracts their natural predators.

While this approach is well intentioned and the reduction of insecticide use is a laudable aim, we have profound concerns about what would happen should such a crop be effective and be authorised for general use. 

It would seem logical that the effects of introducing a field of crops that repels herbivores and attracts predators would be to increase yield in that field, but to reduce yield in the surrounding fields – which would have more herbivores and fewer predators.  This effect (perceived or real) is likely to result in the widespread and rapid uptake of the new crop. 

Giant aphid and Jet black ant (c) Dr Bernhard SeifertImagine being the farmer with the one unprotected field in the area, surrounded by fields repelling herbivores and attracting predators.  Once the use of the crop is universal it is questionable whether the same benefit will be experienced in terms of national or landscape yield as could be observed in a single field.  However repelled they are, the herbivores would need to lay their eggs somewhere and the predators in a smog of attracting pheromones would be less able to locate them.  This could reduce the overall abundance of predators more effectively than it would reduce the overall abundance of herbivores.  

A previously trusted signal chemical produced by the plant to call for help would become a false alarm, a landscape wide cry of ‘wolf’.

The unreliability of this cry is highly likely to drive an evolutionary response similar to pesticide resistance in which both herbivores and predators use alternative signals to detect their food source. 

One can envision a genetic modification arms race in which cumulative additions are made to bolster the robustness of the chemical signals to the insects.  Farmers may be drawn into this escalation with no way to retreat.  Implications for organic farming of this new warfare may be very significant.

In addition to the effects of this ecosystem manipulation on the crop habitats there is the additional consideration of the likely impacts on wildlife inhabiting hedgerows, field margins, grasslands and nature reserves in this new chemical landscape.  Many of the chemical signals are commonly produced by many plants suffering from herbivory and are therefore used by a very wide range of herbivore and predator species.  It is probable that some of, perhaps most of, the predators and parasitoids will be affected by these chemical signals.  This could result in the attraction of predators away from wildlife habitats and into the crops, reducing the abundance of these herbivore controlling insects in hedgerows, grasslands and nature reserves.  Such a shift in trophic structure in natural and semi-natural ecosystems is likely to be profound, significantly altering the balance and population dynamics that shape the niches occupied by a great many species of plants and herbivores i.e. it is likely to give some species a competitive advantage and result in the local extinction of other species.

Perhaps it is also possible that the alarm pheromones will affect the behaviour of pollinators, discouraging bees from visiting plants they believe to be stressed and perhaps therefore less pollen and nectar rich, thus reducing pollination rates.

We wrote to the lead researcher at Rothamsted – Prof. John Pickett and asked if he acknowledged that these potential risks exist; if he could comment on the likely scale and level of certainty for each risk; if he could detail what research has been done that could help model landscape effects of this pest control approach on crop yield, predator and parasitoid population dynamics and pollinator behaviour; and what further research he believed would be required to allay concerns about risks to crop yield and wildlife before such an approach should be authorised for use?  Here is his response:-

“Many thanks for your interest in our work and in the general concept as expressed in the link. We are at the moment involved only at the experimental stage but for field trials we must already, and indeed most willingly, take on board some of the issues you raise. For the research itself, these and all of your other points are extremely important and have long been under our consideration. You will appreciate also that many of these aspects are also required to be addressed by the peer reviewers of our grants and papers. The latter we are publishing in open access journals as much as we can and so your own access will, by this means, be facilitated.”  John Pickett, April 2014.

Buglife also wrote to Professor Rosemary Hails, chair of ACRE asking if the committee was aware of any relevant research or policy making and if the issues had been considered by ACRE.

Ichneumon sp male (c) JaybeeWe received the following response from Dr Louise Ball, ACRE secretary at Defra:-

“The UK Government’s policy on GM crops  acknowledges the potential benefits of the technology but commits to a robust assessment of the risks. Whilst the policy applies generally to GM crops, the commitment to risk assessment applies on a case by case basis i.e. for every application to grow a GM crop, whatever the trait and whether it’s for a small scale trial or for commercial cultivation.

You asked about what has come before ACRE:

To date, ACRE has only considered one application to grow a crop that has been genetically modified to express an alarm pheromone. ACRE’s advice on Rothamsted Research’s application to trial an aphid-repellent GM wheat . This advice reflects the small scale of the trial and as such does not discuss many of the hazards you have raised. Any future applications for larger scale trials and commercial cultivation would require new assessments that take potential receiving environments and spatial scale into account. Public consultations are a mandatory part of the regulatory process and ACRE takes scientific points raised into account when formulating its advice. It would value your contribution to these consultations and encourages you to participate in the future.”

So while Rothamsted acknowledges that Buglife’s concerns are “extremely important” ACRE has not yet addressed these concerns.

We shared our concerns with the Soil Association whose organic farming members stand to be most affected by any landscape effects on herbivores and predators.  Peter Melchett SA Policy Director said:-

“GM maize has reduced the impact of what was previously the most serious pest of maize, the corn borer. However, this created an ecological vacuum, now being filled with two previously insignificant pests, which are much more difficult to kill than the corn borer, and may now become a more serious threat to maize crops than the corn borer ever was. This new proposed GM crop with alarm pheromones will certainly have its own unintended, and quite probably disastrous consequences for other species.”

We will have to wait to see the results of the Rothamsted trials, it may be that even on a small scale the approach is not effective.  However, just as we have discovered with pesticides over the years the assessment of environmental impacts before authorisation has repeatedly failed to adequately protect the environment.  Only after approval to longer term, wider scale, population level impacts on non-target animals start to become apparent.

The question should be asked – who will pay for the scale of research and modelling required to ascertain that 'cry wolf' wheat will increase yields and won’t destroy the ecological fabric of the countryside?

Delving deep into the delicate and long evolved communication between insects and plants has huge environmental and ecological ramifications.  One has to ask if this is necessary.  Indeed this was the tack taken by a coalition of (non-wildlife) NGOs under the banner of GM Freeze when commenting on the proposals for a trial in 2013:-

“Previously published long-term research, which included a substantial input from Rothamsted Research, has shown that aphid populations in cereal crops can be kept below the level at which they cause economic damage to the crop by using/encouraging native predators and parasites, such as parasitic wasps, ladybirds, lacewings, hoverflies, spiders, and beetles.

“The key to the success of this biological control strategy is to maintain populations of parasites and predators in and around arable fields so if aphids do invade the crops the controls are there ready and waiting. To ensure this happens arable fields need to be managed differently to include wild flower-rich field margins, hedgerows, and beetle banks.”

One also has to question why plants do not naturally produce ‘cry wolf’ chemicals continuously, it would surely be to an individual plants benefit if it constantly attracted defenders and repelled attackers.  The answer must be that creating the pheromones will have a cost in terms of energy and materials, a cost the plant avoids by only crying wolf when it is attacked.

Because of the cost of producing the cry wolf chemical it is likely that there will be a corresponding reduction in crop yield.  While on a single field trial this reduction of yield may be outweighed by the protection benefits of the modification, once the crop is widely planted this reduction in yield is more likely to outweigh the diminishing benefits.

Buglife will be watching this issue carefully to ensure that impacts on beneficial bugs and agricultural yields at a landscape level are addressed before there is any authorisation for release onto the market of ‘cry wolf’ wheat. 

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