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Authors: Dave Goulson

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In reality, the process usually takes a little longer – resistance is rarely absolute, and it may take the spread of several genes, each of which confers a little more resistance, while at the same time the farmer applies heavier and heavier doses of insecticide to try and achieve a good rate of control. But in the end the outcome is more or less inevitable.

Of course the evolution of resistance is not confined to flies. In the tropics, many insect pests have developed resistance to insecticides. Insect pests breed much faster in warm climates, and there is no winter to check their growth. There are some horror stories from the middle of the twentieth century in which pesticides were grossly misused and many human lives were lost as a result. The cotton farmers of Central America and the southern states of the USA provide an example. In warm climates cotton suffers from a huge range of insect pests, including various moth caterpillars. When insecticides became widely available in the late 1940s and 1950s, cotton yields went through the roof for a few short years, as the insect pests were all but wiped out. Inevitably and inexorably, the pests started to creep back, and farmers responded by applying higher and higher doses of insecticide. When this ceased to work, the farmers would switch insecticide, and for a while all would be well, until the pests became resistant to the second and then the third chemical. Farmers then resorted to mixing them together into toxic cocktails, and applying them more frequently and in ever-increasing doses; some cotton crops were being sprayed sixty times per year. Eventually even this didn't work, and the farmers reached a point where they were spending so much on chemicals that they were no longer making a profit. They were also exposing themselves and their labourers to dangerous levels of some very unpleasant compounds, leading to all sorts of chronic health problems in rural communities, and to hundreds of deaths. To make matters even worse, there was no easy way back. The years of chemical use had wiped out all of the natural enemies: the predatory insects and birds that, in the days before insecticides, had helped to keep pest populations under control. The predators tended to have smaller populations and longer generation times than the pests they ate, so they had not generally developed resistance to the chemicals.

To return once more to Jason's flies, clearly blitzing the chicken houses with insecticides was not going to be the answer. His intention was to develop a ‘lure and kill' system, whereby the flies would be attracted to a particular place, where they could be killed or trapped. There is a commercially available pheromone for house flies, a chemical known as z-9-tricosene, which is supposed to attract them, and Jason experimented with mixing this with insecticide and sugar, then painting the sticky mix on to boards that were hung from the ceiling of the chicken houses. You might question why he was using insecticides after all that I have told you about resistance, but their use in baited lures such as this seems to be much less likely to result in the evolution of resistance – flies that land on the boards consume so much pesticide that even those that have some resistance tend to die, so the resistance genes do not spread, or at least not as rapidly. Using pesticides in this way, rather than as aerial sprays, is also much better, as the amount of pesticide required is much less; and the pesticide is less likely to contaminate the chickens, their food or the farm labourers.

These boards did work – Jason would sweep up piles of flies from under each one, and count them – but there was a fundamental flaw. Most of the corpses in these mounds were males, which seemed to be preferentially attracted to the pheromone. One male fly can mate with dozens of females, so reducing the male population has a negligible impact on the size of the next generation of flies. What was really needed was something that attracted females too. Jason tried adding black spots to the boards, either evenly spaced or in clusters. Flies seem to be attracted to black spots, perhaps because they mimic flies, suggesting that there may be food or mates. In fact male flies seem to be attracted to any small dark object that is roughly the size of a female fly – they will even pounce on, and try to mate with, knots tied in a black shoelace, although they soon realise their mistake. Jason found that spotty boards worked a little bit better than boards without spots, producing slightly larger piles of dead flies beneath them, but they were still mostly males.

Just as he was coming towards the end of his PhD, I was watching the local news one evening when there was a piece about a fly outbreak on a landfill site near Portsmouth. The landfill was in close proximity to a smart marina, with expensive waterfront flats, posh restaurants, designer boutiques and moorings for very expensive yachts. A vast horde of flies had left the landfill site and infested the marina, showing a particular and understandable attraction to the restaurants, which presumably offered tastier delicacies than they were used to. The scale of the problem was such that the ceiling of one restaurant was black with flies, and of course they had to close until the problem could be solved. The residents and business owners were up in arms, threatening to sue the landfill company for compensation for their lost earnings.

A bit of digging the next day revealed the name and telephone number of the company. Rather speculatively I rang them up and offered my services, suggesting that they were clearly in need of specialist fly advice, which I could provide. They enthusiastically accepted my offer and invited Jason and me to visit the site. I had never before visited a landfill, and it was an eye-opener. The scale of the operation was impressive. I can't remember the exact figure, but the site was taking thousands of tonnes of refuse every day, with a constant stream of lorries bringing it from all over Hampshire. Huge bulldozer-like machines spread and compacted the waste, which, as you can imagine, consisted of a horrendous mix of plastic bags, paper, soiled nappies, rotting food, broken toys and more or less anything else you can think of. The toys seemed particularly poignant – once-loved dolls and cuddly toys, dog-eared and moth-eaten, doomed to be buried in a sea of filth. Immense numbers of gulls and crows wheeled above the heavy machinery, swooping down and bickering over any tasty morsels that were revealed. Others, presumably replete, perched on the surrounding fences or sat amongst the rubbish. A strong sea breeze was coming in from the south-west and noisily shredded the loose flaps of plastic shopping bags and bin-liners, but thankfully it also whipped away the terrible sour stench. Oddly enough, Jason seemed to like the smell, and said it made him feel hungry.

At first sight, it seemed to be no great surprise that the landfill site was a source of large numbers of flies. People clearly throw away a lot of organic matter: kitchen scraps, chicken carcasses, and so on. Together with the used nappies, there was an awful lot of food for maggots. The only surprise to me was that there hadn't been outbreaks of flies before – the site had been in operation for a couple of years.

The staff explained how the site worked. They would excavate huge pits, line them with thick black plastic sheeting, like giant garden ponds, then fill them with waste. The traditional system of managing landfill was to periodically cover the latest layer of waste with a compacted layer of soil, which kept down the smell and stopped rubbish from blowing away. However, landfill space is in short supply, and taking up valuable space with soil was expensive, so an alternative approach had recently been adopted: instead of covering the waste with soil, a huge sheet of sacking would be rolled out over it at night, then rolled back in the morning to allow more waste to be added. The company had also recently switched to fortnightly rather than weekly waste collections. The staff speculated that the fly outbreak might have been linked to one of these changes, and we agreed to investigate. We also set up a fly-outbreak early-warning system, consisting of dozens of sticky traps on the landfill site and at ‘control' sites away from the landfill. Every week the traps would be collected and the number and species of flies carefully counted. It seemed likely that fly outbreaks might be stimulated in part by suitable weather conditions, and so we obtained weather data from the local Met Office and built mathematical models to see if we could predict how many flies there were likely to be the following week. If we could predict a major outbreak, then perhaps action could be taken to control it before it became too awful – although we weren't sure what that action might be. At the very least the landfill company could get its lawyers on standby for another rush of complaints.

We conducted an experiment to find out whether the move to fortnightly waste collections had contributed to the problem. Any organic waste in rubbish bins is likely to attract female flies looking for somewhere to lay eggs. If it is carefully bagged, or in bins with tight-fitting lids, then flies ought not to be able to get to it, but inevitably bags get ripped and bins get left open. When bins are full to overflowing it is impossible to shut the lid. The longer the waste is in the bin, the worse it is likely to smell. Thus it seemed likely that the switch to fortnightly waste collections meant there would be more maggots in the rubbish when it was collected, but we decided we had better verify that this was indeed so.

Setting up the experiment was an awful job. In some areas refuse was still being collected weekly, and the landfill company directed us to a waste depot where we could obtain samples of refuse that were from either weekly or fortnightly collections. We shovelled up a tonne or so of each and sealed it in large plastic rubbish bins. Each bin we fitted with an ‘emergence trap' at the top: a clear plastic bottle into which any emerging adult flies would crawl. Every day for the following few months we collected up, counted and identified the flies emerging from the two types of rubbish. It was surprising just how many species of fly emerged from the waste – we found more than fifty different species, including bluebottles and greenbottles, which feed on rotting flesh; various small midges and gnats; and of course many house flies. Predictably, more flies emerged from the waste collected after two weeks. What was perhaps more important was that the flies emerging from the two-week-old waste started emerging much earlier, some of them almost as soon as we set up the experiment. This was not surprising – house flies have a two-week life cycle in the warm summer months, so if waste was contaminated with fly eggs as soon as it was placed in the bins, then by the time the waste was collected two weeks later the eggs would have had time to hatch and the maggots to grow to full size and pupate.

To see whether the switch from using soil to cover the waste to using sheets of sacking was likely to have made the company's fly problems worse, we carried out some simple experiments to establish how good flies were at burrowing out of the ground when they emerged from their pupae. We buried pupae under a layer of loose soil or compacted clay, and also sealed them under samples of sacking. When a fly first crawls from its pupa its cuticle is soft, and it has an expandable balloon in the middle of its face, which it uses as a hydraulic jack to burrow upwards. It is a rather freakish sight. The fly pumps liquid into the balloon and then deflates it, creating a small space. It then crawls forward into the space and repeats the process. Flies were pretty good at burrowing up through soft soil, but could not get through clay or sacking. However, since the sacking was rolled back every morning, it simply served as a blanket to keep any flies that emerged during the night warm until they were released. It was pretty clear that the old system of using a layer of clay had sealed in many of the flies in the waste, and that the switch to a sacking blanket was making life much easier for them.

We told the landfill company that their problems were largely down to the fortnightly collection and the new sacking system, but they were extremely reluctant to change. They were saving an awful lot of money – so much so that even the threat of being sued by the nearby restaurant owners was not sufficient to force a rethink. They wanted us to find an alternative solution to their fly problem.

We tried many approaches. We spent a long time analysing the smell of male and female flies, in the hope of finding a pheromone that would attract females. If such a compound could be found, perhaps it could be used on insecticide-and-sugar-painted boards, as Jason had done in the battery farms, but placed outdoors around the landfill sites. We even synthesised a blend of chemicals which contained almost all of the compounds found on a real fly – ‘fly in a bottle'. Some of these chemicals and blends did attract flies in the lab, but whenever we tried them outdoors on landfill sites, they were more or less useless. The windy conditions, the vast numbers of real flies and the background stink of the landfill itself seemed to mask any attractant effects of our chemicals.

The only aspect of our work that was really any use at all was our fly-monitoring system. Our network of sticky traps around the landfill site gave us a pretty good early-warning system. When it was combined with weather data, we were able to predict forth-coming fly outbreaks with moderate accuracy – warm, humid weather usually preceded an outbreak, while heavy rain seemed to reduce their numbers. When we warned the landfill company of an impending outbreak, they reverted to drenching the site in insecticides. Although not 100 per cent effective, and certainly not very environmentally friendly, it usually seemed to damp down the numbers of flies for a while.

As we battled for a solution, the landfill filled up with waste. Eventually the vast hole that had been excavated was full, but still the waste arrived. Such is the shortage of landfill sites that permission is often given to create hills out of the waste, and so it was here. The waste mound slowly grew and was sculpted into a rounded hillock. We were no nearer a solution to the fly problem when the landfill site was finally closed. The waste was sealed over with a plastic membrane, with pipes buried in it to allow methane gas to escape, so as to avoid the whole lot exploding. The plastic was covered in soil, then sown with grass seed and planted with shrubs. Today all that can be seen is a slightly unnatural-looking grassy knoll just to the south of the M27 near Portsmouth.

BOOK: A Buzz in the Meadow
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