It looked like such a good idea: take the pressure off wild fish stocks by growing GM oilseeds that produce health-enhancing long-chain omega-3 fatty acids, writes Claire Robinson. But as a new study has established, those fish oils, novel in terrestrial ecosystems, cause wing deformities in cabbage white butterflies. Yet a third open field trial of these GM crops could soon be under way
In humans, long-chain omega-3 fatty acids are important for heart health, brain development and function, and the immune system.
They are naturally found in oily fish and algae. Many people take supplements of omega-3 oils produced in algae to boost their health status and alleviate allergies, arthritis and other diseases.
Recently, scientists have genetically engineered GM canola and camelina (also known as 'false flax') to contain long-chain omega-3 fatty acids.
Rothamsted Research in the UK has applied for approval to conduct a third open field trial of the GM camelina this year. The crop is being promoted both as a health supplement for humans and for feeding farmed fish in the aquaculture industry.
Like humans, fish need omega-3 fatty acids for healthy development. Currently, farmed fish are fed fish oils to provide them with enough omega-3 fatty acids to keep them as healthy as their wild counterparts, which enjoy a diet naturally rich in these oils.
But as fish stocks become more limited, Rothamsted is developing and promoting crops genetically engineered to produce long chain omega-3 fatty acids as a way of providing "new and sustainable sources of healthy omega-3 fish oils for the fish feed industry to reduce the burden on marine fish oil stocks".
Can we conclude that these are the healthy and sustainable GMOs that we've been promised for two decades? A shocking new study suggests they may be anything but, when the wider ecological context is considered.
Butterflies' unexpected wing deformities
Researchers found that when the long chain omega-3 fatty acids found in fish oil – eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) – were fed to an insect, the cabbage white butterfly, the insects grew into heavier adults and had a higher frequency of wing deformities.
The team was careful to test realistic doses that might be expressed in GM omega-3-producing crops and ingested by butterflies feeding on them.
The researchers, most of whom are based at Ryerson University in Ontario, Canada, concluded that "further research on the environmental impacts of EPA and DHA production on terrestrial biota is advisable."
The problem with GM omega-3-producing crops lies in the fact that genetic engineers have introduced a compound from the sea into a terrestrial environment. Neither this butterfly nor any other invertebrates that feed on these plants have ever been exposed to these molecules in their diets.
Some might rejoice that such GM omega-3-producing crops will have the unexpected added benefit of harming a butterfly that is considered to be crop pest. But that would be to ignore the potential effects on beneficial insects such as non-pest butterflies, bees, and other pollinators. It is also not known what effects may occur further up the food chain, such as on predators that consume such insects.
In an objection to the field trial of the GM camelina – filed before these findings were published – campaigners warned of a high risk that the plant could spread into the environment:
"Pollen and seeds could escape from the trial site through dispersal by wind, wildlife or machinery. Human error and mix ups could also result in accidental releases, not only to the environment but also to the human food chain or even directly to humans."
GM crop developers fail to consider ecological risk
Amid the claims of sustainability surrounding the UK omega-3 camelina trial, it seems that no one considered the potential side-effects on the fauna of terrestrial ecosystems. And that includes the genetic engineers who developed the crop.
Professor Johnathan Napier, who led the GM camelina programme at Rothamsted Research, hailed the crop as "a landmark moment in the effort to develop truly sustainable sources of feed for fish farms".
Napier has published scientific studies (here, here, here and here) focusing on the successful genetic engineering of the crop and its suitability as fish feed. But none of these papers so much as mention the possibility of unforeseen harmful consequences to ecosystems.
Dr Angelika Hilbeck, senior scientist at the Institute of Integrative Biology at ETH Zurich, Switzerland, has researched the risks of GM Bt insecticidal crops on beneficial and non-target insects. She commented on the surprise nature of the new findings:
"The fact that these compounds [long-chain omega-3 fatty acids] are novel in terrestrial systems has been entirely overlooked until this study. I congratulate the authors for having raised the issue of this important ecological risk before these crops are planted on a significant scale."
New organisms, new toxicologies
Dr Hilbeck cautions that one uncertainty remains to be clarified. The new study did not test the omega-3 fatty acids as they are expressed in the actual GM plants. Instead the researchers used omega-3 fatty acids derived from non-GM algae, which will not be identical to the omega-3 fatty acids produced in the GM crops.
Likewise the GMO industry, when safety testing its products for regulatory authorizations, often does not test the new protein as produced in the actual GM plant. Instead it tests a surrogate protein produced in microbes genetically engineered with the same GM gene construct as is used to transform the plant. Yet the protein may have different toxicological properties when expressed in GM microbes than when expressed in the GM plant. The context of the GM gene construct is crucial.
Thus when assessing the risks of GM omega-3-producing crops, Dr Hilbeck points out, generically sourced omega-3 fatty acids "can only serve as a proxy for the real thing – the GM plant." Nonetheless, Dr Hilbeck says the new study's findings clearly show that GM omega-3 crops must be thoroughly tested for ecological effects before commercialisation:
"Mandatory extensive testing should be carried out with the actual GM plant, not only on pest herbivores, but also on beneficial insects, butterflies, pest predators, parasites, bees, and pollinators. Concerned scientists like myself have been calling for such testing for decades."
In other words, the burden is now firmly on GMO crop developers to show that what these researchers found with non-GM omega-3 oil will not happen with the transgenic omega-3 oil in GM plants. And for that, they have to test the actual GM plants.
Remaining questions over human safety
The new study does not imply a health risk for humans or other mammals, for whom omega-3 fatty acids are generally accepted to be beneficial, says Dr Michael Antoniou, a London-based molecular biologist:
"Although these findings have a clear implication for the well-being of insect populations that feed on GM oilseed crops that produce high levels of omega-3/omega-6 long chain fatty acids, these same fats are essential nutrients for mammals, including humans. Thus they do not pose any risk, but rather contribute to health."
But Dr Antoniou, who uses genetic engineering in his work on gene therapies, says that other questions remain over the potential effects on human health of omega-3-producing GM crops:
"The GM transformation process can produce unexpected outcomes, leading to the production of novel toxins. That's especially the case when the genetic engineering process alters the core biochemistry of the GM plant, as in the case of omega-3-producing GM crops.
"Thus all GM crops producing omega-3/omega-6 long chain fatty acids that are earmarked for direct use as human food supplements as well as in farmed fish feed must be generically evaluated for toxicity in long-term laboratory animal toxicity studies. This could help ensure that no unexpected toxins have been produced, which may be present in the final marketed product."
Beware the hyperbolic claims
The lesson to be learned from the new study seems to be that we should be wary of the claims of genetic engineers that their products are safe and sustainable when those claims are not substantiated through rigorous testing.
In making such claims, they often restrict their framework to narrow and self-serving considerations, such as whether the GM crop expresses the desired trait and delivers an acceptable product when fed to livestock – in this case, farmed fish. They ignore the wider context in which the GM crop is grown and consumed. In this way, the genetic engineer's claimed 'sustainability' success can turn out to be a hazard for ecosystems.
The study also raises a major question over whether the GM camelina field trial application should be immediately rejected. According to the scientists, "the next step in risk assessment should involve using the actual plants (both in laboratory and in fully contained field trials) engineered to produce EPA and DHA to validate our findings." (my emphasis).
They also warn, "we do not know the full scope of potential effects that access to dietary EPA and DHA during the larval period might have on post-emerged adults; for example, how these FA [fatty acids] may affect adult lifespan, flying ability, sensory ability, and/or overwintering and reproductive success ...
"We suggest that, in order to make informed decisions with respect to agricultural and environmental policies and management of genetically engineered oilseeds ... studies similar to ours (as well as contained field studies) need to be conducted in order to understand more completely the potential global environmental impacts of widespread commercial production of these novel crops on agroecosystems."
I could not agree more!
Claire Robinson is managing editor at GMWatch, a public news and information service on issues surrounding GM crops and foods. GMWatch is one of the UK-based NGOs that objected this year to the GM camelina trials at Rothamsted.
The paper: 'Long-Chain Omega-3 Polyunsaturated Fatty Acids Have Developmental Effects on the Crop Pest, the Cabbage White Butterfly Pieris rapae' by Stefanie M. Hixson , Kruti Shukla, Lesley G. Campbell, Rebecca H. Hallett, Sandy M. Smith, Laurence Packer, Michael T. Arts is published in PLOS One.
This article was first published in The Ecologist, 18 April 2016.
Image: Left: cabbage white butterfly with deformed wings (pinned to an insect board) that was fed an experimental diet enriched with long chain omega-3 fatty acids, 48 hours after emergence. Right: Control butterfly. Photo: PLOS One.