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Authors: Dave Goulson

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As a first step, I tried to read everything that had been published already. This was hard to do, because the work done to examine the safety of these chemicals when they were first developed is not available for scrutiny by scientists or anyone else. Various summary reports could be downloaded from European and US regulatory agencies, but these rarely gave sufficient detail to understand fully what had been done. However, there were quite a few academic studies published in the mainstream scientific literature after the chemicals became widely used, mostly carried out in the lab or with bees flying in cages. Almost all agreed that, when exposed to realistic doses of neonics such as bees might encounter on a seed-treated crop, there was little or no mortality, at least in the short term. However, some found interesting effects on bee behaviour. Neonics are, after all, neurotoxins, so it seemed plausible that sub-lethal doses might adversely affect the behaviour of bees. Studies on both honeybees and bumblebees seemed to suggest that their ability to learn and to bring food back to the nest might be impaired when fed even minute amounts of neonics. However, the effects were generally small and nothing was seen that could explain the complete collapse of honeybee colonies.

I chatted over these studies with Penelope Whitehorn and Steph O'Connor, two members of my bumblebee research group. In nature, bees travel kilometres from their nest in search of patches of flowers. They have to learn how to get pollen and nectar out of the flowers (each flower being of a different design) and then find their way home. For their nest to thrive, each worker has to do this over and over again, all day long, for days on end. Their navigational abilities are amazing. They can use the sun as a compass; they seem also able to detect the Earth's magnetic field; and they can memorise the position of various prominent landmarks such as trees and buildings. It seemed to us that what was really needed was a study of what happened to bees when exposed to neonics in a natural setting. If the exposure was impairing their mental faculties in some way, then the effects might not be at all obvious when the bees had to fly all of two metres from their nest to a dish of honey placed there for them by the experimenter. Even a very poorly, intoxicated bee could probably manage that. On the other hand, anything that interfered with their navigation or learning would be much more likely to become a problem when faced with the challenges of the real world. If no effects were found even under such natural conditions, then I felt we might finally be able to stop worrying about neonics and look elsewhere for the cause of our bees' problems.

We sat down and devised the best experiment that we could come up with. We had no funding for this, so it had to be simple and cheap. I persuaded a colleague named Felix Wackers, of Lancaster University, to provide us with native buff-tailed bumblebee nests for free, to which he had access through his association with one of the companies that rear bumblebees for commercial use. We wanted to simulate the situation in which a wild bumblebee nest finds itself near a field of oilseed rape that has been treated as a seed with imidacloprid. Oilseed rape flowers for about one month in spring, and at this time it is a magnet for bumblebees, so during flowering one might expect a lot of the nectar and pollen coming into any nest near a rape field to be from the rape itself. Ideally we would have placed our nests next to a treated and an untreated rape field and then compared the difference, but we could not find untreated fields and we had no funds to pay for them to be planted. In any case we would have had to be certain that there were no other treated crops within flight range of a worker bee, and given that they can easily fly a kilometre or two, this was never going to be a practical option. Instead we opted to expose the bees in the lab, and then put them out in the field. That way we could control exactly what they ate.

We fed one batch of nests on clean nectar and pollen, and another on nectar and pollen carefully mixed with imidacloprid, to re-create exactly the very low concentrations found in rape. After two weeks we took the nests out on to the campus at Stirling University and opened the doors. From that point on the bees were left to look after themselves; to gather food they would have to fly off and find flowers, just as they naturally would. We couldn't be certain that they wouldn't be exposed to more neonics in the gardens on the edge of Stirling, but no arable crops are grown nearby, so they weren't likely to be exposed to much; and at least any differences between our treatment groups would have to be due to what they fed on in the lab before they went out.

Every two weeks Penelope and Steph went out in the middle of the night (when all the bees should be at home) to weigh the nests – one dark night scaring themselves half to death by imagining that a coil of hosepipe dangling from a wooden post was in fact a very tall and sinister man in a large floppy hat.

We analysed the data as they came in, eager to see if any differences emerged between the treated and untreated nests. Slowly the average weights of nests in the two groups diverged, with the untreated nests growing at a slightly faster rate. By six weeks the differences were quite marked. After eight weeks the nests were starting to senesce, losing weight and producing males and new queens as they naturally should in summer. We collected them in and dissected them, so that we could count exactly how many eggs, larvae, pupae and adult bees there were. The results were striking. In most respects the treated nests were just a little smaller, with fewer pupae and adult bees, but in the most important respect they were dramatically different. The control nests produced, on average, about thirteen new queens. The treated nests produced an average of just two – an 85 per cent reduction. These new queens are the only stage to survive the winter, and it is the queens that found new nests the following spring. All else being equal, an 85 per cent drop in queen production means 85 per cent fewer nests being founded the following spring.

Oilseed rape is a very common crop in lowland England, so few bee nests are far from a field of it. In a recent study of the Hertfordshire landscape we found that there was almost nowhere more than one kilometre from the nearest oilseed rape, which is easily within the range of foraging bumblebees. Oilseed rape attracts honeybees and a whole range of bumblebee species, particularly buff-tails, white-tails and red-tails, plus numerous hoverflies. Almost all of it is treated with neonics – I am told that it is near-impossible to get hold of untreated seed, even if a farmer wished to. These compounds are also routinely used as seed dressings on many other crops: sunflowers, sugar beet, potatoes, wheat and maize. Well over one million hectares of UK farmland are treated with them every year. Raspberries and strawberries are sprayed with neonics during the spring and summer, using much larger amounts that are used for seed dressings, and these crops are primarily pollinated by bumblebees. Garden insecticides are mostly based on neonics. For less than ten pounds your local garden centre will sell you a bottle of neonic containing sufficient active ingredient to kill instantly several million honeybees.
3
These are advertised for use on flowers, and on flowering vegetables such as beans and peas. Unlike farmers, gardeners are entirely untrained in the use of pesticides, and most probably bung on a bit extra for luck. Bees in suburban areas are playing Russian roulette every time they feed on a new patch of flowers.

Neonics are also sold as soil drenches to kill subterranean grubs that eat grass roots in lawns, golf fairways and pastures; heaven forbid that a suburban lawn should have a few brown patches where the roots of the grass have been nibbled – far better that the whole lawn (and any clover or dandelion flowers it might produce) be impregnated with nerve toxins.

In urban areas trees are sometimes injected with neonics to protect them against pests; for example, avenues of trees in suburban streets may be treated to prevent outbreaks of aphids, which could result in unsightly and sticky honeydew on the cars below. An entire tree can be made toxic to all insect herbivores for several years to come by a single injection. If these trees happen to be lime trees, then bees will feed on them, adding yet more to the dose they receive.

Extrapolate our results across the country – indeed, across the world – and the likely scale of the impact on bumblebees is breathtaking and terrifying. One way or another, almost all bumblebee nests are likely to be exposed to these compounds. Perhaps we had discovered the ‘smoking gun' at the root of bee declines. From being rather sceptical about the claims that neonics were wiping out bees, I found myself coming round to the view that this might well be true. We were, as you might imagine, very excited by this and keen to publish our work quickly and in a high-profile journal, where it would be noticed and acted upon. We submitted it to the journal
Science
, and waited with bated breath.

The peer-review process for scientific publications can be frustratingly slow, and it was many weeks before we got a reply. Even then it was not clear whether
Science
would eventually publish our work, for the anonymous referees to whom they had sent our paper had recommended various changes, and one of them didn't seem to think the work was particularly interesting. We did our best to comply, returned the manuscript and waited once more. Eventually, to our huge relief,
Science
declared that it would publish the work. It also revealed that it intended to publish a second, related paper alongside our own. I begged a copy and was fascinated.

It seemed that a French team, based in a government lab in Avignon, had also decided to conduct more realistic experiments on the impacts of neonics on free-flying bees. They had studied honeybees, exposing foraging workers to tiny doses of a neonic called thiamethoxam, mimicking them discovering and feeding upon a treated crop. They had glued miniature radio tags to their bees, so that the return to their hive was automatically detected and recorded by sensors mounted on the hive. Their results provided a beautifully simple explanation for the slow growth and poor performance of our treated bumblebee nests. They found that worker honeybees were much more likely to get lost on the way home if they were fed a neonic. The effects were more pronounced the further the bee was from home, and if the bee was in an unfamiliar location, from which finding its way back to the hive would require its navigation skills to be in tip-top condition. In my mind there is a simple human parallel: it is easy for a drunk to find his way home from his favourite pub, particularly if it is close to home, but put him in an unfamiliar pub and he is quite likely to get lost. The French team's findings provided the first clear indication of a mechanism that could explain the symptoms of CCD. CCD is not about bees dying; it is about them disappearing. If bees cannot find their way home, then a hive will quickly empty of bees, leaving no corpses behind. Lost bees are as good as dead. Without their hive they have no purpose in life and will quickly expire. So it seems that sub-lethal doses of neonics can indirectly kill bees in the real world, while having no measurable effect in the lab.

Science
correctly anticipated that these papers, published together, would cause quite a stir. They decided to organise a press conference. The external-relations staff at the University of Stirling were quite taken aback by the idea and seemed less than enthusiastic about hosting it, so the press conference was arranged to take place in Paris instead. Press releases went out at midnight on Sunday 25 March 2012, with a strict embargo on publication of media stories until the evening of Thursday 29 – it was all terribly exciting, for someone who had not been involved in such things before. The press conference was scheduled for Thursday morning. I expected all hell to break loose on Monday, but not much happened. It took a while for the media to react, perhaps because they knew they couldn't publish anything before the Thursday night, which basically meant that the story would run in the newspapers on Friday.

After the press release went out, but before the actual papers were available to read, Defra (the Department for Environment, Food & Rural Affairs) declared that all pesticides licensed for use in the UK were perfectly safe, if used properly, and that the two new studies did not change this. This struck me as a remarkably odd position for a government department to take, particularly since it had not at the time actually been able to read the new studies. Its position seemed to reflect a belief that the systems it had in place for evaluating the safety of pesticides were infallible, and therefore that no new evidence could possibly come to light which could reveal that they had made a mistake. One might expect, and even understand, such a stance from the agrochemical companies, but from a government department – paid for by taxpayers and supposedly working on our behalf – it was mystifying.

As the week went on my phone became steadily busier, with reporters from various newspapers ringing for additional detail and quotes. Penelope and I flew to Paris on the Wednesday evening. We'd had to book a hotel way out in the suburbs as there happened to be an art festival going on in the city centre and everywhere was booked up. On the Thursday we caught the metro into the centre of Paris. The press conference was in a beautiful old building just off the Champs-Elysées, in a room that seemed more suited to a masked ball than a press conference about pesticides. Penelope and I sat nervously next to the French scientists, Mickaël Henry and Axel Decourtye, facing an audience of journalists flanked by television cameras and bright spotlights, while French aristocrats gazed imperiously down from huge gilt-framed oil paintings. We both felt like fish out of water, and were worried that we might face aggressive questions from representatives of the agrochemical industry. Penelope was heavily pregnant at the time, and we joked that she should feign contractions if things weren't going well. In fact the conference was reasonably uneventful, although some of the questions were a little eccentric. One Mexican journalist suggested that we should develop a vaccine against neonic poisoning. Afterwards we did interviews for a couple of television stations and then escaped to a park by the Seine, where I spent the whole afternoon on my mobile fielding questions from journalists.

BOOK: A Buzz in the Meadow
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